issn 1305–3124 journal perinatal · ahmet yal›nkaya,diyarbak›r, turkey jun yoshimatsu, osaka,...

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The Official Publication of Perinatal Medicine Foundation Turkish Perinatology Society Turkish Society of Ultrasound in Obstetrics and Gynecology ISSN 1305–3124 PERINATAL JOURNAL www.perinataljournal.com Volume 27 | Issue 2 | August 2019 P E R I N A T A L J O U R N A L P E R I N A T A L J O U R N A L

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Page 1: ISSN 1305–3124 JOURNAL PERINATAL · Ahmet Yal›nkaya,Diyarbak›r, Turkey Jun Yoshimatsu, Osaka, Japan Emre Zafer, Ayd›n, Turkey Yaron Zalel, Tel Aviv, Israel Ivica Zalud, Honolulu,

The Official Publication of

Perinatal Medicine Foundation

Turkish Perinatology Society

Turkish Society of Ultrasound in Obstetrics and Gynecology

ISSN 1305–3124

PERINATALJOURNAL

w w w . p e r i n a t a l j o u r n a l . c o m

Volume 27 | Issue 2 | August 2019

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I NA T A L J O U R

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Page 2: ISSN 1305–3124 JOURNAL PERINATAL · Ahmet Yal›nkaya,Diyarbak›r, Turkey Jun Yoshimatsu, Osaka, Japan Emre Zafer, Ayd›n, Turkey Yaron Zalel, Tel Aviv, Israel Ivica Zalud, Honolulu,

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Description

Perinatal Journal, the Official Publication of Perinatal MedicineFoundation, Turkish Perinatology Society and Turkish Society ofUltrasound in Obstetrics and Gynecology, is an international onlineopen access peer-reviewed scientific journal (e-ISSN: 1305-3124)published triannually in English. The manuscripts which are accept-ed for publication in the Perinatal Journal are published as a parallelpublication of Turkish version in “Perinatoloji Dergisi” (p-ISSN:1300-5251, e-ISSN:1305-3132). Translation into Turkish language is pro-vided by the publisher as free of charge for authors. This is automat-ically accepted by the authors of manuscripts at the time of submis-sion.

The journal mainly includes original clinical and experimentalresearch articles, case reports, reviews, editorial and opinion articles,and a letters column. Perinatal Journal can be read by perinatolo-gists, obstetricians, gynecologists, radiologists, pediatricians, sonog-raphers, midwives, radiographers, and scientific members of otherrelated areas.

Aim and Scope

Perinatal Journal aims to create an interdisciplinary scientific plat-form for sharing and discussing topics on perinatal medicine and toshare its experience with international scientific community.

Copyright

Periantal Journal does not officially agree with the ideas of manu-scripts published in the journal and does not guarantee for any prod-uct or service advertisements in its content. Scientific and legal respon-sibilities of published articles belong to their authors. Materials such aspictures, figures, tables etc. sent with manuscripts should be originalor if they were published before written approval of copyright holdershould be sent with manuscript for publishing together.

All published materials will become the sole property of, and willbe copyrighted by Perinatal Journal. Therefore, "Acknowledgementof Authorship and Transfer of Copyright Agreement" presented bymanuscript submission system should be approved by the authorsduring the submission process. No payment is done for manuscripts

under the name of copyright or others approved for publishing inthe journal and no publication cost is charged.

To promote the development of global open access to scientificinformation and research, the journal provides copyrights of allonline published papers (except where otherwise noted) for free useof readers, scientists, and institutions (such as link to the content orpermission for its download, distribution, printing, copying, andreproduction in any medium, without any changing and except thecommercial purpose), under the terms of CC BY-NC-ND 3.0 License(www.creativecommons.org/licenses/by-nc-nd/3.0), provided theoriginal work is cited. To get permission for commercial purposeplease contact the publisher.

Conflicts of Interest

The authors should disclose all issues concerning financial relation-ship, conflicts of interest, and competing interest that may potential-ly influence the results of the research or scientific judgment. Allfinancial contributions or sponsorship, financial relations, and areasof conflicts of interest should be clearly explained in the relevantstep of the submission process, with full assurance that any relateddocument will be submitted to the journal when requested.

Publication Ethics and Malpractice Statement

For the details of journal's “Publication Ethics and Malpractice Statement”please visit www.perinataljournal.com.

Publication Info

Ownership: On behalf of the Perinatal Medicine Foundation,Cihat fien

Managing Editor: Murat Yayla

Administrative Office: Cumhuriyet Cad. 30/5 Elmada¤, Taksim34367 ‹stanbul

Due the Press Law of Turkish Republic dated as June 26, 2004 andnumbered as 5187, this publication is classified as a local periodi-cal. Perinatal Journal is published by Deomed Publishing (Copyright© 2019, Perinatal Medicine Foundation).

Publication Coordinator: ‹lknur Demirel

English Editor: Fikret Yeflilyurt

Graphic Design: Tolga Erbay

The Official Publication of Perinatal Medicine Foundation, Turkish Perinatology Society and Turkish Society of Ultrasound in Obstetrics and Gynecology

Deomed PublishingGür Sok., No: 7BKad›köy 34720 Istanbul, TurkeyTelefon: +90 216 414 83 43 (Pbx) Faks: +90 216 414 83 42e-posta: [email protected] • www.deomed.com

www.perinataljournal.com

Page 3: ISSN 1305–3124 JOURNAL PERINATAL · Ahmet Yal›nkaya,Diyarbak›r, Turkey Jun Yoshimatsu, Osaka, Japan Emre Zafer, Ayd›n, Turkey Yaron Zalel, Tel Aviv, Israel Ivica Zalud, Honolulu,

Editor-in-ChiefCihat fien, Perinatal Medicine Center,Taksim, Istanbul; Memorial Bahçelievler Hospital,Istanbul, Turkey

EditorsMurat Yayla Clinics of Obstetrics &Gynecology, Ac›bademInternational Hospital,Istanbul, Turkey

Olufl ApiPerinatology Clinic, Istanbul American Hospital,Istanbul, Turkey

Advisory BoardAbdallah Adra, Beirut, LebanonArif Akflit, Eskiflehir, TurkeySaadet Arsan, Ankara, TurkeyAhmet Baschat, Baltimore, MD, USAChristoph Berg, Bonn, GermanyJulene Carvalho, London, UKRabih Chaoui, Berlin, GermanyFrank Chervenak, New York, NY, USAFiliz Çayan, Mersin, TurkeyNur Daniflmend, Istanbul, TurkeyJan Deprest, Leuven, BelgiumJoachim Dudenhausen, Berlin, GermanyAlaa Ebrashy, Cairo, EgyptHakan Erenel, Istanbul, TurkeySertaç Esin, Adana, TurkeyElif Gül Yapar Eyi, Ankara, TurkeyAli Gedikbafl›, Istanbul, TurkeyUlrich Gembruch, Bonn, GermanyAnne Greenough, London, UKGökhan Göynümer, Istanbul, TurkeyArif Güngören, Hatay, TurkeyMelih A. Güven, Istanbul, TurkeyJoseph Haddad, Tours, FranceOliver Kagan, Tübingen, GermanyBurçin Kavak, Elaz›¤, TurkeyU¤ur Keskin, Ankara, TurkeyAsma Khalil, London, UKEsin Koç, Ankara, TurkeyÖzge Korkmaz, ‹stanbul, TurkeySelahattin Kumru, Antalya, TurkeyAs›m Kurjak, Zagreb, CroatiaNilgün Kültürsay, Izmir, TurkeyNarendra Malhotra, Agra, IndiaAlexandra Matias, Porto, Portugal

Mohammed Momtaz, Cairo, EgyptGiovanni Monni, Cagliari, ItalyLütfü Öndero¤lu, Ankara, TurkeySoner R. Öner, Izmir, TurkeyOkan Özkaya, Isparta, TurkeyHalil Gürsoy Pala, ‹zmir, TurkeyAlexander Papitashvilli, Tbilisi, GeorgiaOiu Yan Pei, Shanghai, PRC‹brahim Polat, Istanbul, TurkeyRitsuko Pooh, Osaka, JapanRuben Quintero, Miami, FL, USANebojsa Radunovic, Belgrade, SerbiaGuiseppe Rizzo, Rome, ItalyStephen Robson, Newcastle, UKRoberto Romero, Detroit, MI, USALevent Salt›k, Istanbul, TurkeyHaluk Sayman, Istanbul, TurkeyMekin Sezik, Isparta, TurkeyJiri Sonek, Dayton, OH, USAMilan Stanojevic, Zagreb, CroatiaFlorin Stomatian, Cluj, RomaniaTurgay fiener, Eskiflehir, TurkeyAlper Tanr›verdi, Ayd›n, TurkeyEbru Tar›m, Adana, TurkeyBasky Thilaganathan, London, UKIlan Timor-Tritsch, New York, NY, USALiliana Voto, Buenos Aires, ArgentinaSimcha Yagel, Jerusalem, IsraelAhmet Yal›nkaya, Diyarbak›r, Turkey

Jun Yoshimatsu, Osaka, JapanEmre Zafer, Ayd›n, TurkeyYaron Zalel, Tel Aviv, IsraelIvica Zalud, Honolulu, HI, USA

The Official Publication of Perinatal Medicine Foundation, Turkish Perinatology Society and Turkish Society of Ultrasound in Obstetrics and Gynecology

Correspondence: Perinatal Journal, Perinatal Medicine Foundation,Cumhuriyet Cad. 30/5 Elmada¤, Taksim 34367 ‹stanbul, TurkeyPhone: (0212) 225 52 15 • Fax: (0212) 225 23 22 e-mail: [email protected]

Names are in alphabetical order. For the institutional details of the Advisory Board Members please see EditorialBoard link which is available under the Information tab on the home page (www.perinataljournal.com).

Statistical AdvisorMurat Api, Istanbul, Turkey

Volume 27 | Issue 2 | August 2019

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www.perinataljournal.com

Perinatal Journal is currently indexed in the following abstractingand indexing services: TÜB‹TAKULAKB‹M TR Index Health SciencesDatabase, EBSCOhost, EBSCO(Academic Search Complete), and Google Scholar.

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Perinatal Journalii

Coverage

The manuscripts should be prepared for one of the following article categorieswhich are peer-reviewed:

• Original Article

• Case Report

• Technical Note

• Letter to the Editor

In addition, the journal includes article categories which do not require a peerreview process but are prepared by the Editorial Board or consist of invited articles,titled as:

• Editorial• Opinion• Review• Report• Clinical Guidelines• Abstracts• Announcements• Erratum

Manuscript Evaluation

All submissions to Perinatal Journal must be original, unpublished, and not underthe review of any other publication. This is recorded by the system automaticallywith the IP number, the date and time of submission. On behalf of all authors thecorresponding author should state that all authors are responsible for the manu-scripts. The name, date, and place of the relevant meeting should be stated if thesubmission is a work that was previously presented at a scientific meeting.

Following the initial review, manuscripts which have been accepted forconsideration are reviewed by at least three referees under double-blind peerreview process. The Editors of the journal decide to accept or reject the manu-script considering the comments of the reviewers. They are authorized to rejector revise the manuscript, to suggest required corrections and changes upon thecomments and suggestions of reviewers, and/or to correct or condense the textby permission of the corresponding author. They may send the manuscript forthe statistical evaluation to Statistical Advisor if necessary as well. They have alsothe right to reject a manuscript after authors’ revision. Author(s) should provideadditional relevant data, documents, or information upon the editorial requestif necessary.

Ethical Issues

All manuscripts presenting data obtained from studies involving human subjectsmust include a statement that the written informed consent of the participantswas obtained and that the study was approved by an institutional ethics boardor an equivalent body. This institutional approval should be submitted with themanuscript. Authors of case reports must submit the written informed consentof the subject(s) of the report or of the patient’s legal representatives for thepublication of the manuscript. All studies should be carried out in accordancewith the World Medical Association Declaration of Helsinki, covering the latestrevision date. Patient confidentiality must be protected according to the univer-sally accepted guidelines and rules. Manuscripts reporting the results of experi-mental studies on animals must include a statement that the study protocol wasapproved by the animal ethics committee of the institution and that the studywas conducted in accordance with the internationally accepted guidelines,including the Universal Declaration of Animal Rights, European Convention forthe Protection of Vertebrate Animals Used for Experimental and Other ScientificPurposes, Principles of Laboratory Animal Science, and the Handbook for theCare and Utilization of Laboratory Animals. The authors are strongly requestedto send the approval of the ethics committee together with the manuscript. Inaddition, manuscripts on human and animal studies should describe proceduresindicating the steps taken to eliminate pain and suffering.

The authors should also disclose all issues concerning financial relationship,conflicts of interest, and competing interest that may potentially influence theresults of the research or scientific judgment. All financial contributions or spon-

sorship, financial relations, and areas of conflicts of interest should be clearlyexplained in the relevant step of the submission process, with full assurance thatany related document will be submitted to the journal when requested.

Perinatal Journal is committed to upholding the highest standards of pub-lication ethics and observes the following principles of Publication Ethics andMalpractice Statement which is based on the recommendations and guidelinesfor journal editors developed by the Committee on Publication Ethics (COPE),Council of Science Editors (CSE), World Association of Medical Editors (WAME)and International Committee of Medical Journal Editors (ICMJE). For the detailsof journal's "Publication Ethics and Malpractice Statement" please visitwww.perinataljournal.com.

Manuscript Preparation

In addition to the rules listed below, manuscripts to be published in PerinatalJournal should be in compliance with the Uniform Requirements forManuscripts Submitted to Biomedical Journals published by InternationalCommittee of Medical Journal Editors (ICMJE) of which latest version is availableat www.icmje.org.

Authors are requested to ensure that their manuscript follows the appro-priate guidelines such as CONSORT for randomized controlled trials, STROBE forobservational studies, STARD for diagnostic accuracy studies, and PRISMA forsystematic reviews and meta-analyses, for the study design and reporting ifapplicable.

Authorship and Length of TextsThe author(s) must declare that they were involved in at least 3 of the 5 stages ofthe study stated in the “Acknowledgement of Authorship and Transfer ofCopyright Agreement” as “designing the study”, “collecting the data”, “analyz-ing the data”, “writing the manuscript” and “confirming the accuracy of the dataand the analyses”. Those who do not fulfill this prerequisite should not be statedas an author. Every author should also declare their ORCID ID (www.orcid.org) aswell as the standard personal data such as affiliation.

Original Research Articles base on clinical or experimental studies. Themain text should not exceed 2500 words (max. 16 pages), and a maximum ofsix authors is advisable.

Case Reports should illustrate interesting cases including their treatmentoptions. The main text should not exceed 2000 words (max. 8 pages), and amaximum of five authors is advisable.

Opinion Articles: Only by invitation and should be no more than 2000words long (max. 8 pages).

Review Articles: Only by invitation and should be no more than 4000–5000 words long (max. 20 pages).

Technical Notes aims to present a newly diagnostic or therapeuticmethod. They should not exceed 2000 words (max. 8 pages) and include a max-imum of 10 references.

Letters to the Editor should be no more than 500 words long (max. 2pages) and include a maximum of 10 references.

Sections in the Manuscripts

Manuscripts should be designed in the following order: title, abstract, main text,references, and appendix (tables, figures, drawings, pictures, videos, patientforms, surveys etc.).

Title

The title of the manuscript should be carefully chosen to better reflect the con-tents of the study. No anusual abbreviations should be used in the title of themanuscript.

Abstract

Abstracts should not contain any abbreviation and references. They should beprepared under following designs.

— Abstracts of Original Research Articles should be max. 250 wordsand structured in four paragraphs using the following subtitles: Objective,

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Volume 27 | Issue 2 | August 2019 iii

Information for the Authorswww.perinataljournal.com

Methods, Results, and Conclusion. Following the abstract, each abstract shouldinclude max. 5 key words separated with comma and written in lower cases.

— Abstracts of Case Reports should be max. 125 words and structuredin three paragraphs using the following subtitles: Objective, Case, Conclusion.Following the abstract, each abstract should include max. 3 key words separat-ed with comma and written in lower cases.

— Abstracts of Review Articles should be max. 300 words and present-ed not structured in one paragraph. Following the abstract, each abstract shouldinclude max. 5 key words separated with comma and written in lower cases.

— Abstracts of Technical Notes should be max. 125 words and struc-tured in three paragraphs using the following subtitles: Objective, Technique,Conclusion. Following the abstract, each abstract should include max. 3 keywords separated with comma and written in lower cases.

Main text

The sections in main text are defined according to the manuscript type.

— In Original Research Articles, main text should consist of sectionstitled as "Introduction, Methods, Results, Discussion and Conclusion". Each titlemay have subtitles. The categories of subtitles should be clearly defined.

The Introduction section should include a brief summary of the base of thework and clearly states the purpose of the study.

The Methods section should contain a detailed description of the material,the study design and clinical and laboratory tests, and statistical methods used.A statement regarding the ethical issues should also be given in this section.

The Results section should provide the main findings of the study. Datashould be concisely presented, preferably in tables or graphs.

The Discussion section should mainly rely on the results derived from thestudy, with relevant citations from the most recent literature.

The Conclusion section should briefly and claearly present the conclusionsderived from the results of the study. It should be in compliance with the aim ofthe work and and point out its application in clinical practice.

— In Case Reports, main text should be divided with the titles"Introduction, Case(s), Discussion". Reported case(s) should be introducedclearly including the case story, and the results of laboratory tests should begiven in table format as far as possible.

— The text of the Review Articles should follow the "Introduction" andbe organized under subtitles which should clearly define the text's context cat-egorization. The reviews are expected to include wide surveying of literature andreflect the author's personal experiences as far as possible.

— The text of the Technical Note type of articles should be divided into"Introduction, Technic, Discussion". The presented technic should be definedbriefly under the related title, and include illustrations or figures as soon aspossible.

— Letters to the Editor should not have titled sections. If there is a cita-tion about a formerly published article within the text, reference(s) should beprovided.

References

References used in the text should be directly related to the topic, as recent aspossible and in enough numbers. They should be numbered in square bracketsin the order in which they are mentioned in the text including Tables andFigures. Citation order should be checked carefully.

Only published articles or articles in press can be used in references.Unpublished data including conference papers or personal communicationsshould not be used. Papers published in only electronic journals or in thepreprint or online first issues of the electronic versions of conventional periodi-cals should be absolutely presented with DOI (digital object identifier) numbers.

Journal titles should be abbreviated according to the Index Medicus. Allauthors if six or fewer should be listed; otherwise, the first six and “et al.”should be written.

Direct use of references is strongly recommended and the authors may beasked to provide the first and last pages of certain references. Publication of themanuscript will be suspended until this request is fulfilled by the author(s).

The style and punctuation should follow the formats outlined below:

— Standard journal article: Hammerman C, Bin-Nun A, Kaplan M.Managing the patent ductus arteriosus in the premature neonate: a new lookat what we thought we knew. Semin Perinatol 2012;36:130–8.

— Article published in an only electronic journal: Lee J, Romero R, XuY, Kim JS, Topping V, Yoo W, et al. A signature of maternal anti-fetal rejectionin spontaneous preterm birth: chronic chorioamnionitis, anti-human leukocyteantigen antibodies, and C4d. PLoS One 2011;6:e16806. doi:10.1371/journal.pone.0011846

— Book: Jones KL. Practical perinatology. New York, NY: Springer; 1990.p. 112–9.

— Chapter in a book: Moore TR, Hauguel-De Mouzon S, Catalano P.Diabetes in pregnancy. In: Creasy RK, Resnik R, Greene MF, Iams JD, LockwoodCJ, Moore TR, editors. Creasy and Resnik’s maternal-fetal medicine: principlesand practice. 7th ed. Philadelphia, PA: Saunders-Elsevier; 2014. p. 988–1021.

Figures and tables

All illustrations (photographs, graphics, drawings, etc.) accompanying the man-uscript should be referred to as “figure”. All figures should be numbered con-secutively and mentioned in the text. Figure legends should be added at the endof the text as a separate section. Each figure should be prepared as a separatedigital file in “jpeg” format, with a minimum 300 dpi or better resolution. Allillustrations should be original. Illustrations published elsewhere should be sub-mitted with the written permission of the original copyright holder. For recog-nizable photographs of human subjects, written permission signed by thepatient or his/her legal representative should be submitted; otherwise, patientnames or eyes must be blocked out to prevent identification. Microscopic pho-tographs should include information on staining and magnification.

Each table should be prepared on a separate page with table heading ontop of the table. Table heading should be added to the main text file on a sep-arate page when a table is submitted as a supplementary file.

Submission

For a swift peer review, Perinatal Journal operates a web-based submission, peerreview and manuscript tracking system. Authors are required to submit theirarticles online. Details of how to submit online can be found at www.perina-taljournal.com.

Submission Checklist

The following list will be useful during the final check of a manuscript beforesubmission:

1. Manuscript length (max. 4000 words for original research articles)

2. Number of authors (max. 6 authors for original research articles)

3. Title (no anusual abbreviations)

4. Abstracts (max. 250 words for original research articles)

5. Key words (max. 5 keys for original research articles)

6. Main text (subtitles)

7. References (listed according to the rules of ICMJE)

8. Appendices such as tables, figures, drawings, pictures, videos, patientforms, surveys etc. (numbering; legends and headings; copyrightinfo/permission)

9. Acknowledgement of Authorship and Transfer of CopyrightAgreement

10. Conflicts of Interest Disclosure Statement (if necessary)

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Perinatal Journaliv

ContentsVolume 27, Issue 2, August 2019

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Original ArticleThe impact of distress experienced during pregnancy on prenatal attachment 49

Gebelikte distres durumunun prenatal ba¤lanmaya etkisi Anayit Margirit Coflkun, Gülflen Okcu, Sedef Arslan

The management of persistent adnexal masses in cesarean section 56Sezaryen do¤umda persistan adneksiyal kitlelerin yönetimi Aflk›n Evren Güler, Zeliha Çi¤dem Demirel Güler, Özge fiehirli Kinci

The role of systemic inflammatory indexes in predicting preeclampsia and its severity 62Sistemik inflamatuar indekslerin preeklampsiyi ve ciddiyetini öngörmedeki yeri Onur Bektafl, K›v›lc›m Bektafl, Cuma Tafl›n

Determination of median values of triple screening test hormones for Kayseri region and their cross-regional comparisons 68

Kayseri bölgesi için üçlü tarama testi hormonlar›n›n ortanca de¤erlerinin belirlenmesi ve bunlar›n bölgeleraras› karfl›laflt›rmalar› Nahide Ekici Günay

The knowledge, attitude and behavior levels of midwifery students for the non-pharmacological methods used in the management of labor pain 77

Ebelik ö¤rencilerinin do¤um a¤r›s›n›n yönetiminde kullan›lan nonfarmakolojik yöntemlere iliflkin bilgi, tutum ve davran›fllar›Ayfer Arslan, Gamze Temiz

The evaluation of cesarean section rates in accordance with Robson Ten-Group Classification System and the data of perinatology (tertiary center) 89

Sezaryen oranlar›n› Robson On Gruplu S›n›fland›rma Sistemi ve perinatoloji (tersiyer merkez) verileri do¤rultusunda konuflmak Hüseyin K›yak, Gökhan Bolluk, Emel Canaz, Semra Yüksel, Ali Gedikbafl›

Seasonal change of the prevalence of hypertensive disorders of pregnancy 101Gebeli¤in hipertansif bozukluklar›n›n prevalans›n›n mevsimsel de¤iflimiCuma Tafl›n, K›v›lc›m Bektafl

Anthropometric differences in the newborns with brachial plexus palsy, clavicle fracture in pregnancies without risk factor 105

Risk faktörü olmayan gebeliklerde brakiyal pleksus felci ve klavikula k›r›¤› olgular›nda yenido¤anda antropometrik farkl›l›klarHüseyin K›yak, Alev At›fl Ayd›n, Gökhan Bolluk, Emel Canaz, Zemzem Ulaflk›n, Ali Gedikbafl›

Fetal conotruncal heart anomalies: is four-chamber view sufficient in the prenatal screening? 113Fetal konotrunkal kalp anomalileri: Prenatal taramada dört oda görünümü yeterli mi?Baflak Kaya, Deniz Kanber Açar, Ahmet Tayyar, Helen Bornaun, Pelin Ayy›ld›z, ‹brahim Polat

Case Report A case achieved at 28 weeks of gestation by cervical cerclage with retained placenta after expulsion of nonviable fetus underwent selective termination in multifetal pregnancy 119

Ço¤ul gebelikte selektif terminasyon uygulanan nonviyabl fetüsün tahliyesinden sonra plasentaretansiyonlu servikal serklaj ile 28. gebelik haftas›na ulaflan olgu P›nar Özcan, Mehmet Serdar Kütük, Taha Takmaz, Havva Sevde ‹fllek

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The impact of distress experienced during pregnancyon prenatal attachment

Anayit Margirit Coflkun , Gülflen Okcu , Sedef ArslanNursing Department, Faculty of Health Sciences, Bezmialem Vak›f University, ‹stanbul, Turkey

İDİDİD

IntroductionPregnancy is a significant period that requires physiolog-ical, psychological and social changes in the lives ofwomen. Women go through an adaptation process topregnancy first and then the motherhood. While thisprocess varies for every woman and her family, the prob-lems related with adaptation to pregnancy, reactions andperceptions are also different.[1,2]

The communication between expectant mother andbaby during pregnancy is called “prenatal attachment”.Today, the importance of prenatal attachment process isemphasized for establishing the attachment betweenmother and newborn in a short time at postpartum peri-od. Accepting physical changes and transferring positivefeelings to fetus is the first foundation of the attachment.The process of attachment between pregnant woman and

Özet: Gebelikte distres durumunun prenatal ba¤lanmaya etkisiAmaç: Gebelikte yaflanan distres durumunun prenatal ba¤lanma-ya etkisini belirlemektir. Yöntem: Tan›mlay›c› ve kesitsel türde gerçeklefltirilen çal›flma,Mart–Temmuz 2018 aras›nda bir Vak›f Üniversitesi T›p Fakülte-si Hastanesi Kad›n Hastal›klar› ve Do¤um Poliklini¤ine baflvuran370 gebe ile gerçeklefltirildi. Veriler, tan›t›c› bilgi formu, prenatalba¤lanma ölçe¤i ve prenatal distres ölçe¤i kullan›larak elde edildi.Verilerin analizinde, frekans ve yüzde da¤›l›m, ortalama, Kruskal-Wallis ve Mann-Whitney U testi ve Spearman korelasyon analizikullan›ld›. Bulgular: Gebelerin %82.9’u 18–35 yafl aral›¤›nda, %36.8’i primi-gravida idi ve %68.3’ü planlayarak gebe kalm›fl, %52.2’si efli ile herzaman uyumlu, %70.8’i bu gebeli¤inde aile deste¤i alm›fl ve%30.2’si bu gebeli¤inde problem yaflam›flt›. Gebelerin prenatal ba¤-lanma ölçek puan ortalamas› 62.35±11.28, prenatal distres ölçek pu-an ortalamas› 10.26 ± 5.18 idi. Her iki puan ortalamalar› aras›ndanegatif yönde zay›f ve ileri düzeyde anlaml› bir iliflki saptand›. Sonuç: Gebelikte yaflanan distres durumu, prenatal ba¤lanmay›olumsuz yönde etkilemifltir. Planlayarak gebe kalan ve ilk gebeli¤iolan, gebelikte sorun yaflamayan ve efli ile her zaman uyumlu olankad›nlar›n prenatal distres düzeyi anlaml› derecede düflük bulun-mufltur. Prenatal ba¤lanma düzeyine, planl› gebe kalma ve efli ileuyumlu olma durumu olumlu yönde etkili olmufltur.

Anahtar sözcükler: Prenatal ba¤lanma, distres, gebelik.

Correspondence: Anayit Margirit Coflkun, PhD. Nursing Department, Faculty of Health Sciences, Bezmialem Vak›f University, Fatih, Istanbul, e-mail: [email protected] / Received: May 31, 2019; Accepted: July 10, 2019Please cite this article as: Coflkun AM, Okcu G, Arslan S. The impact of distress experienced during pregnancy on prenatal attachment. PerinatalJournal 2019;27(2):49–55. doi:10.2399/prn.19.0272001

Original Article

Perinatal Journal 2019;27(2):49–55©2019 Perinatal Medicine Foundation

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Abstract

Objective: To determine the impact of distress experienced dur-ing pregnancy on prenatal attachment. Methods: This descriptive and cross-sectional study was conductedwith 370 pregnant women who admitted to the Clinic ofGynecology and Obstetrics of Faculty of Medicine of a FoundationUniversity between March and July 2018. The data were obtained byusing introductory information form, prenatal attachment scale andprenatal distress scale. Frequency and percentage distribution, meanvalues, Kruskal-Wallis and Mann-Whitney U tests and Spearman’scorrelation analysis were used for the analysis of the data. Results: Of the pregnant women, 82.9% were in the age group of18–35, 36.8% were primigravida, 52.2% were always compatible withtheir partners, 70.8% got family support during this pregnancy and30.2% had problems during this pregnancy. Mean scores of pregnantwomen in prenatal attachment scale and prenatal distress scale were62.35±11.28 and 10.26 ± 5.18, respectively. There was negatively weakand significantly advanced correlation between two mean scores. Conclusion: Distress experienced during pregnancy affects pre-natal attachment negatively. Prenatal distress level is significantlylow in women who conceive intentionally and it is their first preg-nancy, do not experience any problem and are always compatiblewith their partners. Planned pregnancy and compatibility withpartner have a positive impact on prenatal attachment level.

Keywords: Prenatal attachment, distress, pregnancy.

ORCID ID: A. M. Coflkun 0000-0001-9155-3783; G. Okcu 0000-0002-6375-3718; S. Arslan 0000-0002-7672-1424

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fetus begins as of the moment when woman responds topregnancy positively. Mother perceiving fetus as an indi-vidual, interacting with fetus and interpreting fetal char-acteristics are the most important points in the develop-ment of mother-fetus attachment. Supporting the adap-tation of pregnant woman to her new role during thisperiod, raising awareness on maternal-fetal attachmentand noticing potential issue early will increase the lifequality of expectant mother significantly.[3,4]

Although pregnancy is a condition giving happinessto woman and her family, it can be a great burden andthe source of stress for female body. The diseases ofwomen which already exist or develop during pregnancyand stressful conditions such as hospitalization compli-cate pregnancy process further. It is affected by manyfactors such as the adaptation of individual to the riskyconditions during pregnancy, reactions from the imme-diate surroundings, her feelings, thoughts, impulses anddesires, hospitalization and treatment processes, fetalhealth condition and the requirement of bed rest.During pregnancy, fetus is affected by the changes inmaternal organism as well as pregnant woman. It isreported that risky pregnancies, problems such as stress-ful conditions during pregnancy, fetal health and growthaffect the development negatively.[3,5]

In the literature, desiring and planning pregnancy,socioeconomic and cultural status of family, social sup-port systems, health issues and stressful conditions dur-ing pregnancy, maternal age, educational and employ-ment status, family type and the status of participating inchildbirth classes etc. are highlighted among the factorsaffecting prenatal attachment level.[1,6] In the studies con-ducted, it was found that the processes of adaptation tomotherhood and attachment to newborn were rapid andpostpartum depression levels were low in pregnantwomen who participated in childbirth class and activelyparticipated in their own deliveries. It was also reportedthat working pregnant women have low levels of stressand anxiety and pregnant women with elementary fami-ly structure have higher attachment levels.[2,7–9] Prenatalattachment levels were higher in primiparous pregnantwomen than multiparous pregnant women.[10] In a studyinvestigating prenatal attachment level and affecting fac-tors in pregnant women with high risk, it was found thatattachment level of pregnant women were moderatelylow, and educational status affected attachment in adirect proportion while age affected it in an inverse pro-portion. Furthermore, it was found that primigravidacases have higher prenatal attachment levels compared

to multiparous cases and there was an inverse correlationbetween the number of children and prenatal attach-ment.[6] Positive conditions such as compatible marriagerelationship, desired and planned pregnancy and receiv-ing social support from partner, family members andimmediate surroundings facilitate the processes ofattachment and adaptation to changes caused by preg-nancy and risky conditions in particular. The studiesshow that the use of harmful substances such as cigarette,alcohol and drugs and the status of experiencing stressand depression related with parenthood are at a highlevel and mother-baby attachment is insufficient inunplanned and unintended pregnancies.[10–13]

Participating in antenatal training and childbirthclasses may be effective for expectant mothers and fathersto have a healthy and happy pregnancy process. In thisway, the process of adaptation to pregnancy and con-scious preparation for parenthood become smooth and itis easier to manage negative conditions experienced dur-ing pregnancy and causing distress. Therefore, it is possi-ble to support prenatal attachment process of pregnantwoman and her partner. It is important to evaluate notonly physical health needs but also psychosocial condi-tion of pregnant woman and her family, raise awarenessabout parenthood and support maternal attachmentprocess in the training programs managed by nurses andmidwives. Some studies reported that extensive nursingcare and training programs given through a holisticapproach during prenatal period decrease the distress ofpregnant woman and improve prenatal attachment.[1,2,14,15]

We conducted this study to determine the impact ofdistress experienced during pregnancy on prenatalattachment. We believe that the results obtained willenrich and support the nursing care and the content ofantenatal training programs.

In line with this purpose, we sought answers for thequestions below:• What is the level of prenatal distress of pregnant

women?• Does the stress experienced during pregnancy affect

prenatal attachment?• Do some sociodemographic and obstetric character-

istics causing stress during pregnancy affect prenatalattachment?

MethodsThe population of this descriptive and cross-sectionalstudy consisted of 10,000 pregnant women who were 18

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years old and above and who admitted to the Clinic ofGynecology and Obstetrics of Faculty of Medicine of aFoundation University between March and July 2018.

The sample of the research consisted of a total of 397pregnant women who admitted to the clinic during thesame period and were selected by random samplingmethod according to the following criteria. The numberof samples was determined as 370 pregnant women con-sidering the sample size table with 95% CI and ±0.05margin of error.

The inclusion criteria were as below:• Willingness to participate in the research• Not having a psychiatric disease• Speaking Turkish • Data collection tools

Introductory information form developed accord-ing to the literature, prenatal attachment inventory andprenatal distress scale were used to collect researchdata. The consents of the participants were obtainedfor the use of scales.Introductory information form: Sociodemographicand obstetric characteristics of the pregnant womenwere obtained by the form consisting of 21 questionsprepared according to the literature.[16–20]

Prenatal attachment inventory (PAI): The scale,which was developed by Mary Muller in 1993 in orderto describe thoughts, emotions and conditions ofwoman throughout the pregnancy and to determinefetal attachment level during prenatal period, consistsof 21 items. In this four-point Likert type scale, theminimum and maximum scores are 21 and 84, relative-ly. As the score increases, the level of attachment levelof pregnant woman increases as well. Y›lmaz and Beji[3]

performed the validation and confidence check of thescale and they reported the coefficient of internal con-sistence 0.84. In our study, we found the coefficient ofinternal consistence 0.77.Prenatal distress scale (PDS): The scale, which wasdeveloped in order to evaluate gestational stress, anxietyor concerns, was reorganized by Lobel in 2008 and a newversion with 17 items was created. It was adapted intoTurkish by Yüksel, Ak›n and Durnal[11] in 2011 and itscontent validity was found 96% and Cronbach’s alphainternal consistency coefficient was found 0.85. In ourstudy, Cronbach’s alpha internal consistency coefficientwas 0.80. The Likert-type scale containing 17 items hasoptions “None” (0), “Slightly” (1) and “Highly” (2) forbeing distressed, sorry or concerned at the time for each

item. The distress score specific to the pregnancy experi-enced during gestational period is determined by com-bining the scores of each scale item, and minimum scoreis 0 while maximum score is 34 in the scale. The increasein the total score of the respondents is interpreted as theincrease in the prenatal distress level perceived by preg-nant women. The scale does not have a cutoff score.

For the ethic approval of the research, writtenapproval was obtained from Ethics Committee ofBezmialem Vak›f University (Ethic approval no. 5-32;Date: 27.02.2018) and the institution that the study willbe conducted. Informed consents were obtained fromthe pregnant women participating in the research byinforming them about the purpose of the research.

SPSS version 24.0 (SPSS Inc., Chicago, IL, USA)was used for the evaluation of the data. Frequency, per-centage and mean values, Kruskal-Wallis and Mann-Whitney U tests and Spearman’s correlation analysiswere used for the analysis of the data. p<0.05 was con-sidered as significant.

Limitations

Since the sample was limited with a single center inIstanbul, we think that the results cannot be generalizedand that conducting the research by descriptive methodmakes it impossible to make causative inferences.

ResultsAs seen in Table 1, the majority (82.9%) of the preg-nant women who participated in the research were inthe age group of 18–35, 81.4% of them had elementaryfamily structure, 36.8% of them were primigravida,68.3% of them had a planned pregnancy, 69.8% ofthem did not have any problem in this pregnancy and70.8% got family support during this pregnancy. Of120 pregnant women who had problems during thepregnancy, 42.5% (51 pregnant women) had gestation-al complications such as hyperemesis and the threats ofmiscarriage and premature birth, partial placenta pre-via, and mild preeclampsia etc., 22.5% (27 pregnantwomen) had health issues which complicate the preg-nancy such as anemia, gestational diabetes, influenza,and Rh incompatibility etc., and 35% (42 pregnantwomen) had both conditions (Table 1).

As seen in Table 2, mean scores of pregnant womenfor PAI and PDS were 62.35±11.28 (range: 21–84) and10.26±5.18 (range: 0–26), respectively. According to thisresult, it was found that prenatal attachment perceived by

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the pregnant women was “at a high level” and stress levelof pregnant women was “slightly lower than moderatelevel”.

It was shown in Table 3 that there was a negativelyweak correlation between the mean scores of PAI andPDS (r<1). According to this result, as mean score of

prenatal distress scale increased, in other words, as theirstress levels increased, their mean scores of prenatalattachment decreased significantly.

It is shown in Table 4 that age did not affect PDSscore but PAI scores of the pregnant women in the agegroup of 18–35 were much higher than the pregnantwomen who were above 35 years old and this was statisti-cally significant at a higher level. This result was con-firmed by intragroup comparisons. In terms of the num-ber of children, mean PDS scores were significantly high-er in primigravida women than those with 1–2 childrenand higher in those with 3 and more children than thosein two other groups. Mean PDS scores were significantlyhigher in women with unplanned pregnancy than thosewith planned pregnancy and in women who had problemsin this pregnancy than those who did not have any prob-lem. It was found that mean PAI scores of women withplanned pregnancy were significantly higher than thosewith unplanned pregnancy. In terms of compatibility withpartner, mean PDS scores were lower in pregnant womenin the group of “always compatible” compared to twoother groups. The highest mean PDS score was seen inthe pregnant women in the “incompatible” group. MeanPAI scores were higher in a statistically significant way infavor of the “always compatible” group.

DiscussionIssues experienced during pregnancy such asunplanned pregnancy, multiparity, pregnancy at anadvanced age, partner incompatibility and not receiv-ing support from the immediate surroundings, currenthealth problems during pregnancy, hospitalizationand/or bed rest need may be a stress reason and it alsoaffects prenatal attachment process of the expectantmother negatively.[1–4]

In the post-graduate thesis study of Çobanlar Akkaflentitled “Compatibility between partners during preg-nancy”, the author reported that 80% of the pregnantwomen received support from their partners and fami-lies, and 73.3% of them had planned pregnancy.[17] In thestudies investigating similar issues, planned pregnancyrate exhibits a difference interval ranging from 68% to80%.[5–7] Our results for partner and family supports andplanned pregnancy rate are consistent with the literature.

In parallel with our study, 2013 data of TurkeyDemographic and Health Survey (TDHS) reportedthat the highest fertility rate according to the age is inthe age group of 20–30.[8]

Table 1. Some sociodemographic and obstetric characteristics ofthe pregnant women (n=397).

Sociodemographic and obstetric characteristics Number %

Age 18–26 119 30.027–35 210 52.936 years old and above 68 17.1

Educational level Literate 10 2.5Primary school 56 14.1Secondary school 83 20.9High school 137 34.5University and above 111 28.0

Family type Elementary 323 81.4Extended 71 17.9Fragmented 3 0.7

Having problem during Available 120 30.2this pregnancy Not available 277 69.8

Partner compatibility Always compatible 207 52.2Compatible 184 46.3Incompatible 6 1.5

Number of children None (primigravida) 146 36.81–2 194 48.93 and more 57 14.3

Planning status of Planned 271 68.3this pregnancy Unplanned 126 31.7

Receiving family support Available 281 70.8during pregnancy Not available 116 29.2

Table 2. Mean scores of prenatal attachment inventory (PAI) andprenatal distress scale (PDS) of the pregnant women.

Scales Minimum Maximum χχ±SD*

PAI 21 84 62.35±11.28

PDS 0 26 10.26±5.18

*χ±SD=Mean ± standard deviation.

Table 3. The correlation between the mean scores of prenatal attach-ment inventory (PAI) and prenatal distress scale (PDS) of thepregnant women.

PDS PAI

PDÖ r=-0.002*PBÖ r=-0.002*

*p<0.001.

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In the study of Alan Dikmen and Çankaya, entitledas “The impact of maternal obesity on prenatal attach-ment”, the authors reported that 46.6% of the womenhad problems during pregnancy and in parallel withthis result, they stated that prenatal attachment ratewas significantly low.[9] The study of Erkal Aksoy et al.,entitled as “Prenatal attachment in risky pregnanciesand social support”, reported similar results. In theirstudy, the authors reported the rate of having a prob-lem during pregnancy 48.8%.[1] Unlike these two stud-ies, we found this rate 30.2% in our study and this dif-ference can be explained by the fact that those studieswere conducted on obese and risky pregnant groups.

In our study, the mean PAI and PDS scores were62.35±11.28 and 10.26±5.18, relatively (Table 2). In thestudy of Y›lmaz and Beji (2010), entitled as “Adaptingprenatal attachment inventory into Turkish”, mean PAIscores of 210 pregnant women who participated in theresearch was 60.7±10.1.[3] In similar studies reflecting oursocial characteristics, mean PAI scores of pregnantwomen were close to each other. In their study conduct-ed on pregnancies with high risk, Bak›r et al.[2] found thisrate 61.96±9.24, Erkal Aksoy et al.[1] found it 56.76±9.23in their study conducted on risky pregnancies, and AlanDikmen and Çankaya[9] found it 61.24±0.49 in theirstudy about the impact of maternal obesity on prenatal

attachment. In our study which was consistent with theliterature, we found high level of prenatal attachmentperceived by the pregnant women who participated inour research.[1–3,9]

As an answer to our first research question, we foundin our study that the prenatal distress level of pregnantwomen was slightly lower than moderate level. In thestudy of Alt›nçelep,[10] entitled as “Determining prenataldistress level of pregnant women”, mean PDS scores of522 pregnant women who participated in the researchwere at a low level (9.88±4.79). This different rate mayresult from the characteristics of pregnant women, whoparticipated in the relevant study, from the group whichhad fewer problems during the pregnancy (10.26±5.18).Conversely, Yüksel et al.[11] conducted a study, entitled“Adaptation of prenatal distress scale into Turkish andfactor analysis”, with 233 pregnant women, and theyfound mean PDS scores 12.03±5.61. The distress levelfound in this study conducted with 370 pregnantwomen, who admitted to the clinic for routine antenatalchecks and only 30.2% of whom expressed some smallproblems related with pregnancy, is consistent with theliterature.[10,11]

Our second research question is answered in Table 3,and we found a negatively weak correlation between themean scores of PAI and PDS (r<1). According to this

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Table 4. The comparison of the mean scores of prenatal attachment inventory (PAI) and prenatal distress scale (PDS) with the sociodemographicand obstetric characteristics of the pregnant women.

PDS KW†/z‡ and PAI KW†/z‡ and Characteristics (9±SS) p value (9±SS) p value

Age 18–26 (n=119) 10.08±4.99 63.18±1.0427–35 (n=210) 10.59±5.37 1.931†/0.381 63.50±11.09 17.415†/0.000***36 years old and above (n=68) 9.58±4.89 57.35±11.07

Educational level Graduated from the primary school at least (n=66) 10.48±5.850.007‡/0.994

61.31±11.370.737‡/0.461Graduated from the elementary school or above (n=331) 10.22±5.04 62.56±11.26

Family type Elementary (n=323) 10.14±5.04 62.24±11.53Extended (n=71) 10.56±5.73

4.066†/0.13163.25±10.00

2.957†/0.228Fragmented (n=3) 16.00±3.60 52.66±10.50

Number of children None (n=142) 9.90±5.04 63.85±11.631–2 (n=197) 9.83±4.85

10.384†/0.006**61.75±10.88

4.810†/0.0903 and more (n=58) 12.62±5.99 60.74±11.51

Planning status of Planned (n=271) 9.39±4.634.285‡/0.000***

63.40±11.247.031‡/0.008*this pregnancy Unplanned (n=126) 12.14±5.79 60.20±11.07

Partner compatibility Always compatible (n=207) 9.38± 5.02 64.19±11.58Compatible (n=184) 11.12 ±5.13 14.269†/0.001** 60.44±10.67 15.442†/0.000***Incompatible (n=6) 14.33± 6.53 57.50±8.96

Having problem during Available (n=120) 11.82 ±4.984.179‡/0.000***

62.80±11.360.670‡/0.503this pregnancy Not available (n=277) 9.59 ±5.13 62.15±11.25

Receiving family support Available (n=281) 10.37± 5.200.802‡/0.423

62.92±10.871.149‡/0.251during pregnancy Yok (n=116) 10.01± 5.13 60.97±12.15

9±SD=Mean ± standard deviation. KW††: Kruskal-Wallis test; z‡: Mann-Whitney U test; *p<0.05; **p<0.01; ***p<0.001.

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finding, the perception of pregnancy and prenatal attach-ment of pregnant women, who experienced stress due tovarious reasons during pregnancy, were affected nega-tively. In their study, Abasi et al.[12] found a correlationsimilar to our study and reported that there is a negative-ly significant correlation between gestational anxiety andprenatal attachment. Unlike our results, Topaç Tunçeland Kahyao¤lu Süt[13] evaluated the prenatal depressionand prenatal attachment during all three trimesters of 319pregnant women that they monitored in their study.Within the scope of their data, they found that meanPDS scores of the participants decreased as the trimestersadvanced although they were not at a significant level (1sttrimester: 9.7±5.7; 2nd trimester: 9.2±5.2; 3rd trimester:9.2±4.8) while their mean PAI scores increased(54.9±13.9, 61.3±10.9 and 64.1±11.1, respectively), andthe correlation was highly significant. Our study resultswere consistent with these data and we found that thereis a negative correlation between stress level and prenatalattachment of pregnant women.[12,13]

We evaluated the answer of our last research ques-tion, “Do some sociodemographic and obstetric charac-teristics causing stress during pregnancy affect prenatalattachment?”, in Table 4. In this regards, we found thatage, fertility status, partner compatibility, planning preg-nancy and having problems during pregnancy affectPDS and PAI scores. In harmony with our research data,Y›lmaz and Beji[3] reported in their study that primi-parous pregnant women have higher levels of prenatalattachment. In the same study, the authors found thatwomen who conceived without any plan and being pre-pared have lower mean prenatal attachment scores butsignificantly higher mean prenatal distress scores.

In our study, we found that age did not affect PDSscore but PAI scores of the pregnant women in the agegroup of 18–35 were much higher than the pregnantwomen who were above 35 years old and this was statis-tically significant at a higher level. Similar to our results,Elkin[14] found in their study investigating prenatalattachment level of pregnant women and the factorsaffecting this level that 77.5% of the pregnant womenwere between 18 and 30 years old and their prenatalattachment scores were significantly higher than otherage groups. Similarly, Bak›r et al.[2] found that mean pre-natal attachment scores of the pregnant women, 55.6%of which were in the same age group (18–30) were high-er at a statistically significant level than the advanced agegroup. In the study of Y›lmaz and Beji,[3] the authors

reported that prenatal attachment level of the pregnantwomen in the age group of 18–34 was significantly high-er than those who are 35 years old and above. Literaturefindings also support the results of our study. There arealso other studies showing that there is an inverse corre-lation between maternal age and prenatal attach-ment.[12,14,15] This result can be interpreted by the fact thatexpectant mothers from younger age groups are ready tohave children.

Alan Dikmen and Çankaya[9] found in their study thatthe prenatal attachment level of pregnant women withelementary family type is significantly higher than thosewith extended or fragmented family type. On the otherhand, Kartal and Karaman[16] reported in their study,entitled “The impact of childbirth classes on prenatalattachment and depression risk in pregnant women”,that the prenatal attachment scores of pregnant womenwith extended family types are higher than those withelementary family type. Although we found higher PAIscores in elementary and extended family types com-pared to the fragmented family type in our study, thecorrelation between them was not significant. This situ-ation which is different than the literature may be asso-ciated with the characteristics of study groups.

It is stated in the literature that having problemduring pregnancy affects prenatal attachment processnegatively.[2,9,12] Having problem during pregnancy, orrisky pregnancy in other words, affects partner com-patibility negatively, increases stress level during pre-natal period and even leads up to postpartum depres-sion. Therefore, it is indicated that having stress dur-ing pregnancy is a risk factor for postpartum depres-sion.[17,18]

In our study, we found significantly higher meanPDS scores in those who had problems during preg-nancy than those who did not have any problem. Whilemean PDS scores of pregnant women who are alwayscompatible with their partners were significantly lowerthan other groups, their mean PAI scores were higher.Our study result is consistent with the literature.

Öztürk[19] reported in their study, entitled “Theimpact of perceived social support on prenatal attach-ment and anxiety experienced during pregnancy”, thatmean PAI scores of pregnant women who receivedsocial and family support were significantly higher.Although we did not find any significant correlationbetween family support and mean PAI scores, meanPAI scores of the group which receive family support

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were higher. We had a similar result related with thenumber of children. Although it was not statisticallysignificant, PDS scores of primiparous pregnantwomen were higher than the groups with 1–2 childrenand more than 3 children. Çap›k et al.[20] reported intheir study that there was a significant correlationbetween the number of children and mean PDS scoresin favor of primiparous pregnant women.

ConclusionIn conclusion, mean prenatal attachment inventoryscores were higher (62.35±11.28) and mean prenatal dis-tress scale scores were slightly lower than moderate level(10.26±5.18). There was a negatively week correlationbetween the mean scores of prenatal distress and prena-tal attachment scales. Accordingly, prenatal attachmentlevels of pregnant women significantly decreased as theirstress levels increased. We found that age, number ofchildren, the status of planning pregnancy, partner com-patibility and having problem during pregnancy affectedprenatal distress level and therefore prenatal attachment.

Conflicts of Interest: No conflicts declared.

References1. Erkal Aksoy Y, Dereli Y›lmaz S, Aslantekin F. Riskli gebelerde

prenatal ba¤lanma ve sosyal destek. Türkiye Klinikleri Journalof Health Sciences 2016;1:163–9.

2. Bak›r N, Ölçer Z, Oskay Ü. Yüksek riskli gebelerin prenatalba¤lanma düzeyi ve etkileyen faktörler. Uluslararas› HakemliKad›n Hastal›klar› ve Anne Çocuk Sa¤l›¤› Dergisi (JACSD)2014;1:25–37.

3. Y›lmaz SD, Beji NK. Gebelerin stresle bafla ç›kma, depresyonve prenatal ba¤lanma düzeyleri ve bunlar› etkileyen faktörlerGenel T›p Dergisi 2010;20:100–8.

4. Özorhan EY, Ejder Apay S, Düzyurt M. Riskli olan ve olma-yan gebelerin prenatal ba¤lanma düzeylerinin karfl›laflt›r›lmas›.Uluslararas› Hakemli Kad›n Hastal›klar› ve Anne Çocuk Sa¤-l›¤› Dergisi (JACSD) 2015;3:1–15.

5. Özkan A, Arslan H. Gebeli¤e karar verme, fizyolojik yak›nma-lar› alg›lama ve e¤itim gereksinimleri. Zeynep Kamil T›p Bül-teni 2007;38:155–61.

6. Uçar H. Gebelerin psikososyal sa¤l›k durumlar› ile annelik ro-lü aras›ndaki iliflki. Yüksek lisans tezi, Atatürk ÜniversitesiSa¤l›k Bilimleri Enstitüsü, Erzurum, 2014.

7. Babacan Gümüfl A, Çevik N, Hataf Hyusni S, Biçen fi, KeskinG, Tuna Malak A. Gebelikte benlik sayg›s› ve beden imaj› ileiliflkili özellikler. Anatolian Journal of Clinical Investigation2011;5:7–14.

8. Hacettepe Üniversitesi Nüfus Etüdleri Enstitüsü. TürkiyeNüfus ve Sa¤l›k Araflt›rmas› (TNSA) 2013. Retrieved from:www.hips.hacettepe.edu.tr/tnsa2013/rapor/TNSA_2013_ana_rapor.pdf

9. Alan Dikmen H, Çankaya S. Maternal obezitenin prenatalba¤lanma üzerine etkisi. Ac›badem Üniversitesi Sa¤l›k BilimleriDergisi 2018;9:118–23.

10. Alt›nçelep F. Gebelerdeki prenatal distres düzeyinin belirlen-mesi. Yüksek lisans tezi, ‹stanbul Bilim Üniversitesi Sa¤l›kBilimleri Enstitüsü, ‹stanbul, 2011.

11. Yüksel F, Ak›n S, Durna Z. Prenatal distres ölçe¤inin Türkçe’yeuyarlanmas› ve faktör analizi. Hemflirelikte E¤itim ve Araflt›rmaDergisi 2011;8:43–51.

12. Abasi E, Tahmasebi H, Zafari M, Nairi Takami G. Assessmenton effective factors of maternal-fetal attachment in pregnantwomen. Life Science Journal 2012;9:68–75.

13. Topaç Tunçel N, Kahyao¤lu Süt H. Gebelikte yaflanan anksi-yete, depresyon ve prenatal distres düzeyinin do¤um öncesi be-be¤e ba¤lanmaya etkisi. Jinekoloji - Obstetrik ve NeonatolojiT›p Dergisi 2019;16:9–17.

14. Elkin N. Gebelerin prenatal ba¤lanma düzeyleri ve bunlar› et-kileyen faktörler. Sürekli T›p E¤itimi Dergisi 2015;24:230–6.

15. Lindgren K. Relationships among maternal-fetal attachment,prenatal depression, and health practices in pregnancy. ResNurs Health 2001;24:203–17.

16. Kartal YA, Karaman T. Do¤uma haz›rl›k e¤itiminin gebelerdeprenatal ba¤lanma ve depresyon riski üzerine. Zeynep KamilT›p Bülteni 2018;49:85–91.

17. Çobanlar Akkafl S. Gebelik döneminde efller aras› uyum. Yükseklisans tezi, Ayd›n Adnan Menderes Üniversitesi Sa¤l›k BilimleriEnstitüsü, Ayd›n, 2014.

18. Ayvaz S, Hocao¤lu Ç, Tiryaki A, Ak ‹. Incidence of postpar-tum depression in Trabzon province and risk factors at gesta-tion. [Article in Turkish] Turk Psikiyatri Derg 2006;17:243–51.

19. Öztürk E. Alg›lanan sosyal deste¤in prenatal ba¤lanma vegebelikte yaflanan anksiyete üzerine etkisi. Yüksek lisans tezi,Manisa Celal Bayar Üniversitesi Sa¤l›k Bilimleri Enstitüsü,Manisa, 2018.

20. Çap›k A, Ejder Apay S, Sakar T. Gebelerde distres düzeyininbelirlenmesi. Anadolu Hemflirelik ve Sa¤l›k Bilimleri Dergisi2015;18:196–203.

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The management of persistent adnexal masses incesarean section

Aflk›n Evren Güler1 , Zeliha Çi¤dem Demirel Güler1 , Özge fiehirli Kinci2

1Obstetrics and Gynecology Clinic, Koru Ankara Hospital, Ankara, Turkey2Department of Obstetrics and Gynecology, Mu¤la S›tk› Koçman University Training and Research Hospital, Mu¤la, Turkey

İDİDİD

Özet: Sezaryen do¤umda persistan adneksiyalkitlelerin yönetimi

Amaç: Amac›m›z, antenatal dönemde veya sezaryen do¤um esnas›n-da adneksiyal kitleleri oldu¤u tespit edilen gebelerin antenatal dö-nemdeki veya sezaryen do¤um esnas›ndaki yönetimini ortaya koymakve literatür bulgular› ›fl›¤›nda bunlar›n sonuçlar›n› tart›flmakt›r.

Yöntem: Haziran 2013 ile Aral›k 2018 tarihleri aras›nda Koru An-kara Hastanesi Kad›n Hastal›klar› ve Do¤um Klini¤inde sezaryendo¤umu planlanm›fl veya acil sezaryen do¤um gerçeklefltirmifl2364 hastan›n verileri retrospektif olarak incelenmifltir. Patolojisonuçlar›nda ölçülen en büyük çap, kitlelerin çap› kabul edilmifltir.

Bulgular: Yirmi alt› (%1.09) hastada adneksiyal kitle bulundu.Hastalar›n hiçbirinde gebelik öncesinde bilinen adneksiyal kitleyoktu. Tüm fibroid olgular› çal›flma d›fl› b›rak›ld›. On sekiz hastaantenatal dönemde ortalama 10.5±1.2 gebelik haftas›nda (%69) ta-n› al›rken, gebelik esnas›nda kitlelerde hiçbir de¤ifliklik gözlemlen-medi. Ancak 8 (%31) olguda adneksiyal kitleler sezaryen do¤umesnas›nda tesadüfen tespit edildi. Yirmi alt› hastan›n 5’inde(%19.2) bulunan kitleler paraovaryen veya paratubal iken, kalan 21hastada ovaryen kitleler bulundu. Bu ovaryen kitlelerin histolojiktipleri, prevalanslar› temel al›narak afla¤›daki gibi listelenebildi:matür kistik teratom (%34.6), seröz kistadenom (%15.4) ve endo-metriyom (%15.4), müsinöz kist (%11.5) ve fibrom (%3.9). Büyükboyutlu olma e¤ilimindeki kitleler, ortalama 62.64±22.18 mm bo-yut ile ciddi kistadenomlar olarak saptand›.

Sonuç: Gebelikte adneksiyal kitleler, hastan›n klinik bulgular› vemalignite flüphesinin varl›¤› dikkate al›narak takip edilebilir ve uy-gun trimesterde opere edilebilir. Sezaryen do¤um esnas›nda göz-lemlenen kitleler al›narak, cerrah›n karar›na ba¤l› olarak patolojikincelemeye gönderilebilir.

Anahtar sözcükler: Adneksiyal kitle, gebelik, kistektomi.

Correspondence: Özge fiehirli Kinci, MD. Department of Obstetrics and Gynecology, Mu¤la S›tk› Koçman University Training and Research Hospital,Mu¤la, Turkey. e-mail: [email protected] / Received: May 25, 2019; Accepted: August 31, 2019Please cite this article as: Güler AE, Demirel Güler ZÇ, fiehirli Kinci Ö. The management of persistent adnexal masses in cesarean section. PerinatalJournal 2019;27(2):56–61. doi:10.2399/prn.19.0272002

Original Article

Perinatal Journal 2019;27(2):56–61©2019 Perinatal Medicine Foundation

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Abstract

Objective: Our aim is to reveal the management of pregnantwomen in the antenatal period or during cesarean section (CS) whoare found to have adnexal masses during antenatal period or CS anddiscuss the consequences thereof based on the literature findings.

Methods: The data of 2364 patients with scheduled or emergencyCS performed at Koru Ankara Hospital Obstetrics andGynecology Clinic between June 2013 and December 2018 wereretrospectively reviewed. The largest diameter measured in thepathology results was taken as the diameter of the masses.

Results: Twenty-six (1.09%) patients were found to have adnexalmasses. None of the patients had an adnexal mass known beforepregnancy. All cases of fibroids are excluded. Eighteen patients werediagnosed in the antenatal period, in the pregnancy week 10.5±1.2on average (69%), and no changes were observed in the masses dur-ing pregnancy. In 8 cases, however, adnexal masses were detectedincidentally during CS (31%). Masses found in 5 out of 26 patientswere paraovarian or paratubal (19.2%) whereas the remaining 21patients were identified to have ovarian masses. The histologicaltypes of these ovarian masses can be listed based on their prevalenceas follows: mature cystic teratoma (34.6%), serous cystadenoma(15.4%) and endometrioma (15.4%), mucinous cyst (11.5%), andfibroma (3.9%). The masses, which tend to be the largest in size, areserous cystadenomas having an average size of 62.64±22.18 mm.

Conclusion: Adnexal masses in pregnancy can be monitored con-sidering the patient’s clinical findings and the presence of a malig-nancy suspicion or can be operated in the appropriate trimester.Masses observed during cesarean section may be removed and sentfor a pathological examination, depending on the surgeon’s decision.

Keywords: Adnexal mass, pregnancy, cystectomy.

ORCID ID: A. E. Güler 0000-0002-2281-2347; Z. Ç. Demirel Güler 0000-0002-9300-7329; Ö. fiehirli Kinci 0000-0001-6439-0798

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IntroductionThe incidence of adnexal masses in pregnancy rangesbetween 1/41 and 1/1500.[1] Only 3% of those masses aremalignant.[2] Mature cystic teratoma is the most preva-lent type, with an incidence rate of 50%.[3] Due to themore widespread use of ultrasonography and otherimaging methods as well as the increasing rate of cesare-an section (CS), adnexal masses are now detected morefrequently during pregnancy.[4,5]

However, management of persistent ovarian cystsdetected in pregnancy and incidental adnexal massesencountered during cesarean section is debated.Conditions such as torsions, ruptures, or progress oftumor stage in malignant masses which may potentiallycause both maternal and fetal complications may occurthroughout pregnancy, especially in the advancing weeksof pregnancy.[6] Surgeons, on the other hand, are con-cerned that surgical interventions may lead to manycomplications, in particular, preterm delivery.[1]

Our aim with this retrospective study is to reveal themanagement of pregnant women in the antenatal periodor during CS who were found to have adnexal massesduring antenatal period or CS and discuss the conse-quences thereof based on the literature findings.

MethodsThe data of 2364 patients with scheduled or emer-gency CS performed at Koru Ankara HospitalObstetrics and Gynecology Clinic between June 2013and December 2018 were retrospectively reviewed.Ethical approval for the study was obtained from theEthics Committee, Koru Ankara Hospital (EthicsCommittee protocol code: 13/03/2019-38). The studywas conducted in accordance with the Helsinki decla-ration. CSs were performed under spinal or generalanesthesia by several obstetricians in a single center.All CS and cystectomy/oophorectomy procedureswere performed by obstetrics and gynecology special-ists. Exclusion criterion for the study was the presenceof adnexal mass before the pregnancy period. Thelargest diameter measured in the pathology results wastaken as the diameter of the masses.

After the CS was completed, cystectomy/oophorec-tomy decision was made, considering the experience ofthe surgeon, for patients who were found to have

adnexal masses. Cystectomy was carried out by strip-ping the cyst capsule off from the healthy ovarian tis-sue after a dissection was made on the ovarian tissuethrough cautery. Oophorectomy was performed byclamping, cutting and then suturing with 0 Vicryl® thesuspensory ligament of ovary and ligament of ovary, ingiven order. Due to the risk of malignancy, cystecto-my/oophorectomy procedures were performed with-out rupturing the cysts. Pathologic examination(frozen section) was not performed in any case. Finalpathological examination expected for other surgeries.

Age, gravidity, parity, week of delivery, CS indica-tions, the period when mass was detected (antenatal,intra-cesarean), and mass removal technique (cystecto-my/oophorectomy) were evaluated for all patients ret-rospectively. Sizes of cysts/ovaries and histopathologi-cal examination results were followed up throughpathology reports. Cysts/ovaries were evaluated by thesame pathologist.

All analyses were conducted using SPSS 22.0 (SPSSInc., Chicago, IL, USA).

ResultsBetween June 2013 and December 2018, 2364 patientsunderwent CS at Koru Ankara Hospital, in 26 (1.09%)of whom adnexal masses were detected. None of thepatients had an adnexal mass known before pregnancy.Diagnosis was made during the antenatal period in 18patients (69%), at gestational Week 10.5±1.2, on aver-age, who had no changes in their masses during the restof pregnancy. In 8 cases (31%), however, adnexal mass-es were detected incidentally during CS. Mean age ofdelivery of the pregnant women who were found to haveadnexal masses were 30.2, mean parity were 2, and meanweek were 38 weeks and 3/7 days, respectively.

Indications for CS included 15 past CS (57.7%), 2fetal distress (7.7%), 3 breech presentation (11.5%), 3cephalopelvic disproportion (11.5%), 1 placenta previa(3.9%), and 2 multiple pregnancy cases (Table 1). Onlyone of 26 patients underwent oophorectomy (3.9%)whereas 25 patients (96.1%) had cystectomy surgery(Table 2).

Masses found in 5 (19.2%) out of 26 patients wereparaovarian or paratubal whereas the remaining 21patients were identified to have ovarian masses. The his-tological types of these ovarian masses, in order of fre-

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quency, were as follows: mature cystic teratoma (34.6%)(Fig. 1 and 2), serous cystadenoma (15.4%) (Fig. 3) andendometrioma (15.4%), mucinous cyst (11.5%), andfibroma (3.9%). The masses, which tend to be thelargest in size, are serous cystadenomas having an aver-age size of 62.64±22.18 mm. Endometrioma was theonly case treated with oophorectomy (Table 2).

DiscussionThe incidence of adnexal masses in pregnancy rangesbetween 1/41 and 1/1500.[1] The most common types aremature cystic teratoma, cystadenoma, and functionalcysts.[3] The incidence and histological types identified inour study were comparable to those available in the lit-erature. In our case series, the incidence was around 1%with mature cystic teratoma being the most commonhistological type (34.6%). Adnexal masses in pregnancyusually have an asymptomatic course. Complicationssuch as torsion and cyst rupture may occur in cysts larg-er than 5 cm.[7,8] In fact, the majority of the adnexal cystsin pregnancy get resorbed before the 16th week.Technological advancements in imaging methods notonly made the detection of adnexal masses easier but alsoincreased the dilemmas associated with the managementof such masses.[4] In their study, Lee et al. supported theconservative management of adnexal masses in pregnan-cy.[9] Risk of malignancy in masses with unchanging orgrowing sizes should be noted: 0.6% of such masses areknown to have malignancy risk.[10] Malignancy was notdetected in our patients. Sherard et al. found a 13%malignancy incidence in persistent adnexal masses asso-ciated with pregnancy and the malignancy rate to be1/4741.[11]

MRI and ultrasonography have an important placein the imaging of adnexal masses during pregnancy.[4]

Ultrasonography is very helpful in understanding thecontent and nature of the mass in the first-stage evalu-ation. It helps elaborating as to whether the mass issolid or cystic, whether or not it has a septum, and pro-vides further information about the structure of thecyst wall, and content of the cyst. MRI may be usedwhen ultrasonography is inadequate. For all of ourpatients, the evaluation was performed through ultra-sonography. Adnexal masses were detected in 18patients during antenatal monitoring, and during fol-low-up, likewise, ultrasonography was employed whileMRI was not needed.

Intervention to the adnexal masses detected inpregnancy should be considered during pregnancyonly in the presence of suspicion of malignancy, symp-tomatic mass, and persistent adnexal mass greater than8–10 cm.[12] In our study, none of the patients was oper-ated during pregnancy since none of them met theforegoing criteria. Small ovarian cysts are usually man-aged conservatively. Conventionally, laparotomy is

Table 1. Distribution of the indications for cesarean section.

Indication for cesarean section Number (n) Percentage (%)

Previous caesarean delivery 15 57.7

Fetal distress 2 7.7

Breech presentation 3 11.5

Cephalopelvic disproportion 3 11.5

Placenta previa 1 3.9

Multiple pregnancy 2 7.7

Total 36 100

Table 2. Distribution of the histological types of cysts.

Treatment Time of detection

Cyst size Cystectomy Oophorectomy Antenatal Intra-cesarean Histological type n (%) (mm) n (%) n (%) n (%) n (%)

Mature cystic teratoma 9 (34.6) 41.24±12.1 9 (34.61) 0 (0) 5 (19.23) 4 (15.38)

Serous cystadenoma 4 (15.4) 62.64±22.18 4 (15.38) 0 (0) 4 (15.38) 0 (0)

Mucinous cystadenoma 3 (11.5) 32.56±18.21 3 (11.53) 0 (0) 2 (7.69) 1 (3.84)

Endometrioma 4 (15.4) 51.92±10.62 3 (11.53) 1 (3.84) 3 (11.53) 1 (3.84)

Paratubal-paraovarian cyst 5 (19.2) 44.18±11.26 5 (19.23) 0 (0) 4 (15.38) 1 (3.84)

Fibroma 1 (3.9) 24 1 (3.84) 0 (0) 0 (0) 1 (3.84)

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recommended if the mass is greater than 6 cm, is solidand bilateral or persists in the second trimester.[3,12]

Elective surgery is usually planned in the secondtrimester, after week 18, in order to reduce the risk ofabortus.[13] In the event of incidentally detected masses,removal is recommended, especially for those greater

than 5 cm, during CS which already involves a laparo-tomy and is suggested to have no undesired effects onmortality or morbidity.[14] In our study, we performedcystectomy/oophorectomy in order to obtain ahistopathological result (risk of malignancy) in allcases, regardless of the size of the masses.

Fig. 1. 16-weeks pregnancy + mature cystic teratoma (MRI scan).

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Fig. 2. Mature cystic teratoma in cesarean section.

Fig. 3. 13-weeks pregnancy + serous cystadenoma (MRI scan).

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ConclusionIn adnexal masses during pregnancy, close follow up isa way of management, but patient’s clinical findingsand symptoms or suspicion of malignancy are indica-tions of surgery. Masses observed during CS may beremoved and sent for a pathological examination,depending on the surgeon’s decision.

Conflicts of Interest: No conflicts declared.

References

1. Ye P, Zhao N, Shu J, Shen H, Wang Y, Chen L, et al.Laparoscopy versus open surgery for adnexal masses in preg-nancy: a meta-analytic review. Arch Gynecol Obstet 2019;299:625–34.

2. Hermans RH, Fischer DC, van der Putten HW, Van De PutteG, Einzmann T, Vos MC, et al. Adnexal masses in pregnancy.Onkologie 2003;26:167–72.

3. Whitecar MP, Turner S, Higby MK. Adnexal masses in preg-nancy: a review of 130 cases undergoing surgical management.Am J Obstet Gynecol 1999;181:19–24.

4. Chiang G, Levine D. Imaging of adnexal masses in pregnancy.J Ultrasound Med 2004;23:805–19.

5. Ulubay M, Öztürk M, Fidan U, Keskin U, F›ratl›gil FB, K›nc›M F, et al. Skin incision lengths in caesarean section. ÇukurovaMedical Journal 2016;41:82–6.

6. Roberts, JA. Management of gynecologic tumors during preg-nancy. Clin Perinatol 1983;10:369–82.

7. Munnell EW. Primary ovarian cancer associated with preg-nancy. Clin Obstet Gynecol 1963;30:983–93.

8. Grimes WH, Jr, Bartholomew RA, Colvin ED, Fish JS,Lester WM. Ovarian cyst complicating pregnancy. Am JObstet Gynecol 1954;68:594–605.

9. Lee GS, Hur SY, Shin JC, Kim SP, Kim SJ. Elective vs. con-servative management of ovarian tumors in pregnancy. Int JGynaecol Obstet 2004;85:250–4.

10. Duic Z, Kukura V, Ciglar S, Podobnik M, Podgajski M.Adnexal masses in pregnancy: a review of eight cases undergo-ing surgical management. Eur J Gynaecol Oncol 2002;23:133–4.

11. Sherard GB, 3rd, Hodson CA, Williams HJ, Semer DA, HadiHA, Tait DL. Adnexal masses and pregnancy: a 12-year experi-ence. Am J Obstet Gynecol 2003;189:358–62; discussion 62–3.

12. Schmeler KM, Mayo-Smith WW, Peipert JF, Weitzen S,Manuel MD, Gordinier ME. Adnexal masses in pregnancy:surgery compared with observation. Obstet Gynecol 2005;105:1098–103.

13. Platek DN, Henderson CE, Goldberg GL. The managementof a persistent adnexal mass in pregnancy. Am J Obstet Gynecol1995;173:1236–40.

14. Dede M, Yenen MC, Yilmaz A, Goktolga U, Baser I.Treatment of incidental adnexal masses at cesarean section:a retrospective study. Int J Gynaecol Obstet 2007;17:339–41.

Bu makalenin kullan›m izni Creative Commons Attribution-NoCommercial-NoDerivs 3.0 Unported (CC BY-NC-ND3.0) lisans› arac›l›¤›yla bedelsizsunulmaktad›r. / This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported (CC BY-NC-ND3.0)License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ or send a letter to Creative Commons, PO Box 1866,Mountain View, CA 94042, USA.

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The role of systemic inflammatory indexes in predictingpreeclampsia and its severityOnur Bektafl , K›v›lc›m Bektafl , Cuma Tafl›n

Department of Obstetrics and Gynecology, Faculty of Medicine, Mersin University, Mersin, Turkey

İDİDİD

Özet: Sistemik inflamatuar indekslerin preeklampsiyive ciddiyetini öngörmedeki yeriAmaç: ‹mmün arac›l› inflamasyondaki anormal de¤ifliklikler pre-eklampsinin (PE) patogenezine katk›da bulunur. Bu çal›flmadaamac›m›z sistemik inflamatuar indekslerini [nötrofil/lenfosit oran›(NLO), trombosit/lenfosit oran› (TLO), monosit/lenfosit oran›(MLO), trombosit /nötrofil oran› (TNO)] hastal›k göstergeleriolarak ve ayn› zamanda erken tan› imkân›, hastal›¤›n fliddetinin de-¤erlendirilmesi ve PE’nin prognozu için teorik bir temel olarakaraflt›rmakt›r.

Yöntem: Retrospektif olgu kontrollü olarak planlanan bu çal›flma-da 573 gebenin klinik kay›tlar› tarand›. Yirmi sekiz hasta eklamp-tik nöbet geçirmesi, 50 hasta HELLP sendromu (hemoliz, trom-bositopeni ve yüksek karaci¤er transaminaz), 20 hasta süperempo-ze preeklampsi, 19 hasta kronik hipertansiyon, 25 hasta gestasyo-nel hipertansiyonu olmas› nedeniyle çal›flma d›fl›na al›nd›. Yüzdoksan hasta PE, 119 hasta fliddetli PE ve 122 sa¤l›kl› tekil gebekontrol grubuna al›narak 3 grup oluflturuldu. Tüm gruplar›n he-moglobin, trombosit say›s›, nötrofil, monosit, lenfosit de¤erleri ilebirlikte sistemik inflamatuar yan›t belirteçleri olan NLO, TLO,MLO, TNO oranlar› kay›t alt›na al›nd› ve birbirleriyle karfl›laflt›-r›ld›.

Bulgular: PE ve fliddetli PE gruplar› aras›nda anlaml› farkl›l›k tes-pit edilmezken, her iki PE grubu kontrol grubuyla ayr› ayr› karfl›-laflt›r›ld›¤›nda, trombosit, nötrofil, lenfosit ve monosit say›lar› ileNLO, TLO, MLO ve TNO de¤erleri istatistiksel olarak anlaml›farkl›l›k gösterdi. Kontrol ve PE gruplar› için NLO>3.497 olarakal›nd›¤›nda %51.5 sensitivite, %50.8 spesifisite, %71.9 pozitif pre-diktif de¤er, %71.4 negatif prediktif de¤er elde edilmektedir.

Sonuç: Tam kan say›m› parametrelerinin sekonder analizleri sis-temik inflamasyon ve ba¤›fl›kl›k durumunu etkin bir flekilde de¤er-lendirmektedir. NLO ve TLO mutlak beyaz kan hücresi say›mla-r›na göre klinik de¤erlendirme, PE fliddetinin de¤erlendirilmesi vePE’nin prognozunun de¤erlendirilmesi aç›s›ndan daha etkili gös-tergeler sunar. Ancak hâlihaz›rdaki bulgularla sistemik inflamatu-ar indeksler preeklampsi tan›s› koymada ve fliddetini öngörmedeyeterli de¤ildirler.

Anahtar sözcükler: Preeklampsi, TLO, NLO, MLO, TNO.

Correspondence: Onur Bektafl, MD. Department of Obstetrics and Gynecology, Faculty of Medicine, Mersin University, Mersin, Turkey.e-mail: [email protected] / Received: May 24, 2019; Accepted: September 2, 2019Please cite this article as: Bektafl O, Bektafl K, Tafl›n C. The role of systemic inflammatory indexes in predicting preeclampsia and its severity. Perinatal Journal 2019;27(2):62–67. doi:10.2399/prn.19.0272003

Original Article

Perinatal Journal 2019;27(2):62–67©2019 Perinatal Medicine Foundation

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Abstract

Objective: Abnormal changes in immune-mediated inflammationcontribute to the pathogenesis of preeclampsia (PE). In our study, weaimed to investigate systemic inflammatory indexes [neutrophil/lym-phocyte rate (NLR), platelet/lymphocyte rate (PLR), monocyte/lymphocyte rate (MLR), platelet/neutrophil rate (PNR)] as diseasemarkers as well as a theoretical basis for early diagnosis opportunity,evaluation of disease severity and prognosis of PE.

Methods: The records of 573 pregnant women were evaluated inthis retrospective case-controlled study. Twenty-eight patients wereexcluded from the study as they suffered eclamptic seizure while 50patients were excluded from the study due to HELLP syndrome(hemolysis, thrombocytopenia and elevated liver transaminases), 20patients due to superimposed preeclampsia, 19 patients due tochronic hypertension and 25 patients due to gestational hyperten-sion. Three groups were established where 190 patients were includ-ed in PE group, 119 patients in severe PE group and 122 healthysingleton pregnant women in the control group. Platelet numbers,neutrophil, monocyte and lymphocyte values as well as NLR, PLR,MLR and PNR values which are systemic inflammatory responsemarkers of all groups were recorded and compared with each other.

Results: While no significant difference was found between PE andsevere PE group, there was statistically significant difference in termsof the numbers of platelet, neutrophil, monocyte and lymphocytenumbers and NLR, PLR, MLR and PNR values when both PEgroups were compared to the control group. When NLR is consid-ered >3.497 for the control and PE groups, sensitivity is 51.5%, speci-ficity is 50.8%, positive predictive value is 71.9%, and negative predic-tive value is 71.4%.

Conclusion: Secondary analyses of complete blood count parame-ters evaluate systemic inflammation and immunity effectively.According to the absolute leukocyte counts, NLR and PLR providemore effective markers in terms of clinical evaluation, and evaluationof PE severity and PE prognosis. However, with current findings,systemic inflammatory indexes are insufficient to establishpreeclampsia diagnosis and to predict its severity.

Keywords: Preeclampsia, PLR, NLR, MLR, PNR.

ORCID ID: O. Bektafl 0000-0002-7089-8480; K. Bektafl 0000-0002-5628-9929; C. Tafl›n 0000-0002-9315-4791

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IntroductionHypertensive diseases complicate 5–11% of all pregnan-cies. Preeclampsia (PE) is an idiopathic multisystemic dis-ease with unknown etiology affecting approximately2–8% of pregnancies.[1] It usually appear after 20 weeks ofgestation and affects both mother and fetus which causesan increase in the rates of maternal and neonatal mortal-ity and morbidity. PE is defined as the hypertension andproteinuria in a pregnant woman. In severe cases, PE maylead to maternal organ dysfunction, a systemic diseasesuch as HELLP syndrome (hemolysis, thrombocytope-nia and elevated liver transaminases), poor maternal out-comes and poor perinatal outcomes such as early and lateintrauterine growth retardation.[2] The main reasons ofPE are not clear; however, recent studies have confirmedthat PE is associated with extreme inflammation andabnormal immune responses.[3]

Hyperactivation of inflammatory and immunologicresponses in preeclampsia causes a significant increase inneutrophil number and modulation of neutrophil func-tion, and it leads to more superoxide production com-pared to nitric oxide, resulting in endothelial injury anddysfunction.[4–6] Systemic immune inflammation indexesderived from peripheral blood cells have drawn attentionrecently because they are measured easily and practical.These combined indexes are calculated based on basicparameters such as platelet/lymphocyte rate (PLR), neu-trophil/lymphocyte rate (NLR) and monocyte/lympho-cyte rate (MLR). It is stated that they are diagnosticallysignificant in many systemic and local inflammatory dis-eases such as coronary artery disease, diabetes mellitus,arthritis and ulcerative colitis, and that platelet/lympho-cyte rate (PLR) in particular can be used as a marker forovarian, colon and breast cancers.[7–12] In PE, abnormalchanges were also observed in leukocytes;[13] however, therole of these systemic inflammatory markers remainsuncertain in clinical evaluation, differential diagnosis andprognosis evaluation in PE.

PE is a progressive, unpredictable and untreatabledisease, and its only treatment currently is the comple-tion of pregnant in due course. Therefore, early diagno-sis of PE is useful for the close clinical follow-up of thepatients. In our study, we aimed to investigate systemicinflammatory indexes (NLR, PLR and MLR) as diseasemarkers and also a theoretical basis for early diagnosisopportunity, evaluation of disease severity and the prog-nosis of PE.

MethodsAfter obtaining approval from Mersin University’sEthics Committee of Clinic Researches, 122 healthypregnant women and 573 cases of whom 451 had hyper-tensive disease, who delivered in Department ofObstetrics and Gynecology, Faculty of Medicine, MersinUniversity which was a tertiary center between January2010 and January 2019, were evaluated retrospectively.Twenty-eight patients were excluded from the study asthey suffered eclamptic seizure while 50 patients wereexcluded from the study due to HELLP syndrome, 20patients due to superimposed preeclampsia, 19 patientsdue to chronic hypertension and 25 patients due to ges-tational hypertension. The control group consisted of122 (28.3%) pregnant women who did not have mater-nal medical complication or autoimmune disease historyand had normotensive singleton pregnancy during thesame period. A total of 309 preeclampsia patients wereseparated into 2 groups as PE [190 (44.0%)] and severePE [119 (27.6%)]. Complete blood count results of thecases sent as a routine practice before delivery, andhemoglobin (Hb) (mg/dl), neutrophil (103/μL), lympho-cyte (103/μL), monocyte (103/μL) and platelet (103/μL)values were recorded. Thereafter, neutrophil/lympho-cyte rate (NLR), platelet/lymphocyte rate (PLR), mono-cyte/lymphocyte rate (MLR) and platelet/neutrophil rate(PNR) were calculated and recorded.

Gestational age was calculated by evaluating lastmenstrual period and/or first trimester obstetric ultra-sonography and the measurement of crown-rumplength. Preeclamptic patient selection and classificationwere done according to the criteria of the study groupestablished by American Congress of Obstetricians andGynecologists in 2013. Accordingly, the diagnosis ofpreeclampsia was established through 2 measurements atleast with 4-hour interval after 20 weeks of gestationwhere systolic blood pressure is 140 mmHg, diastolicblood pressure is 90 mmHg and there is 300 mg proteinin 24-hour urine or the rate of protein (mg/dL) / creati-nine (mg/dL) is ≥0.3 or it is at least +1 by dipstick whilethe case is normotensive before pregnancy. The diagno-sis of severe preeclampsia was established by the pres-ence of any of the following conditions: systolic bloodpressure is ≥160 mmHg and/or diastolic blood pressureis ≥110 mmHg, serum creatinine level is >1.1 mg/dL orthe concentration of serum creatinine is doubled withoutany renal disease or presence of new cerebral or visualdisorders, pulmonary edema or thrombocytopenia

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(thrombocyte count <100,000/μL) or liver dysfunction(normal limits of liver enzyme levels doubling or elevat-ing more than double), chronic severe right upper quad-rant pain which cannot be explained by another diagno-sis or presence of epigastric pain non-responsive to thetreatment or presence of both conditions.

Data analysis was carried out by using IBM SPSS v25.0 (Armonk, NY, USA). Conformity of the data tonormal distribution was checked by Kolmogorov–Smirnov test. The data were presented as mean ± stan-dard deviation (SD) for continuous variable and aspatient number (n) and percentage (%) or median (min-imum–maximum) for categorical variables. Chi-squaretest was used for the comparisons of categorical variables.Mann-Whitney test was performed to compare the non-parametric data between two groups and Kruskal-Wallistest was used to compare the data among three groups.ROC curves were created in PE group and the areaunder curve (AUC) was calculated for each marker (Fig.1). Sensitivity, specificity and likelihood ratio were calcu-lated according to the cut-off point determined by ROCcurves. p<0.05 was defined as statistically significant level.

ResultsThe cases included in the study were separated intothree groups which were preeclampsia group (n=190;44.0%), severe preeclampsia group (n=119; 27.6%), andthe control group (n=122; 28.3%); the ages of the casesvaried between 18 and 46, and the mean age was30.6±6.25. The demographics of mothers and newbornsare given in Table 1.

Statistically significant difference was found betweenthe groups in terms of parity, number of living children,birth weights of newborns, week of gestation at delivery,and 1-minute and 5-minute Apgar scores (p<0.01). Insevere preeclampsia group, 1-minute and 5-minuteApgar scores were significantly lower than the cases inboth the control group and the preeclampsia group(p≤0.01, p=0.022; p≤0.01, p=0.007). Compared to thecontrol group, birth weights of newborns were signifi-cantly low in PE and severe PE groups (p=0.001,

Table 1. Demographic information.

PE Severe PE Control (n=190; (n=119; (n=122; p p p%44.0) %27.6) %28.3) PE- Severe PE- PE-

Mean±SD Mean±SD Mean±SD Control Control Severe PE p

Maternal age (year) 31.1±6.1 30.5±6.8 29.9±5.8 0.223 0.003 0.364 0.372

Gravida (median) 2 2 2 0,191 <0.01 0.224 0.010

Parity (median) 1 0 1 0.164 <0.01 0.081 <0.01

Living children (median) 1 0 1 0.093 <0.01 0.134 <0.01

Birth weight (g) 2352±886 1897±857 3318±440 0.001 <0.01 0.461 <0.01

Week of gestation at delivery 35.0±3.3 33.3±3.6 38.6±0.8 <0.01 <0.01 0.442 <0.01

1-minute Apgar 7.05±1.61 6.16±2.19 7.67±1.22 0.002 <0.01 0.022 <0.01

5-minute Apgar 8.46±1.41 7.72±2.06 9.18±0.88 <0.01 <0.01 0.007 <0.01

Fig. 1. ROC curves.

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p<0.01). Compared to the control group, delivery weekwas also significantly low in PE and severe PE groups(p=0.001, p<0.01).

Blood count parameters are shown in Table 2.There was no significant difference between the groupsin terms of hemoglobin values (p=0.1). Compared to thecontrol group, platelet (p=0.001, p=0.018), neutrophil(p=0.01, p=0.006), monocyte (p=0.03, p=0.017) and lym-phocyte (p=0.022, p=0.021) values, and PLR (p=0.005,p=0.001), NLR (p=0.005, p=0.001), MLR (p=0.004,p=0.002) and PNR (p=0.006, p=0.001) were different ina statistically significant way in preeclampsia and severepreeclampsia groups, respectively. All these values werenot statistically significant between preeclampsia andsevere preeclampsia groups.

When all preeclamptic patients (n=309) were com-pared to the control group (n=122), the area under curveobtained for PLR is 0.435; when the limit value is104.269, it was calculated that sensitivity was 44.7%,specificity was 42.6%, likelihood ratio for positive testwas 0.778, positive predictive value was 72.6%, likeli-

hood ratio for negative test was 1.298, and negative pre-dictive value was 71.0% (p=0.035).

The area under curve obtained for NLR is 0.548;when the limit value is 3.497, it was calculated that sen-sitivity was 51.5%, specificity was 50.8%, likelihoodratio for positive test was 1.046, positive predictive valuewas 71.9%, likelihood ratio for negative test was 0.955,and negative predictive value was 71.4% (p=0.120).

The area under curve obtained for MLR is 0.420;when the limit value is 0.325, it was calculated that sen-sitivity was 44.7%, specificity was 44.3%, likelihoodratio for positive test was 0.801, positive predictive valuewas 71.9%, likelihood ratio for negative test was 1.250,and negative predictive value was 71.5% (p=0.010).

The area under curve obtained for PNR is 0.394;when the limit value is 29.765, it was calculated that sen-sitivity was 41.4%, specificity was 42.6%, likelihoodratio for positive test was 0.721, positive predictive valuewas 71.1%, likelihood ratio for negative test was 1.374,and negative predictive value was 72.1% (p≤0.001). Therates are summarized in Table 3.

Table 2. Blood count parameters of preeclamptic pregnant women and the control group.

PE Severe PE Control p p p(n=190; (n=119; (n=122; PE- Severe PE- PE-%44.0) %27.6) %28.3) Control Control Severe PE p

Hemoglobin 11.50±1.71 11.63±1.53 11.84±1.28 0.079 0.111 0.419 0.100

Platelet 21.6215.79±76.593.00 194.655.46±80.980.48 222.639.34±60.740.07 0.001 0.018 0.570 0.004

Neutrophil 7923.13±2963.92 8893.51±4788.85 7210.49±1682.06 0.010 0.006 0.535 0.005

Monocyte 692.25±312.44 678.16±433.83 703.44±162.54 0.030 0.017 0.688 0.257

Lymphocyte 2297.42±1492.94 1986.22±792.60 2071.97±53.55 0.022 0.021 0.655 0.036

PLR 111.09±59.73 113.61±77.05 111.18±3.11 0.005 0.001 0.430 0.107

NLR 4.28±2.99 5.38±3.75 3.66±1.19 0.005 0.001 0.410 0.004

MLR 0.34±0.23 0.37±0.24 0.36±0.10 0.004 0.002 0.475 0.010

PNR 133.17±1411.35 119.70±1029.04 32.37±11.26 0.006 0.001 0.443 <0.01

Table 3. Diagnostic performance of systemic inflammatory indexes to distinguish preeclampsia from the control cases.

LR for Positive LR for Negative AUC Limit Sensitivity Specificity positive predictive negative predictive

Parameter (95%CI) p value % % test value % test value %

PLR 0.435 (0.380–0.490) 0.035 104.269 44.7 42.6 0.778 72.6 1.298 71.0

NLR 0.548 (0.494–0.602) 0.120 3.497 51.5 50.8 1.046 71.9 0.955 71.4

MLR 0.420 (0.366–0.475) 0.010 0.325 44.7 44.3 0.801 71.9 1.250 71.5

PNR 0.394 (0.340–0.449) <0.001 29.765 41.4 42.6 0.721 71.1 1.374 72.1

AUC: Area under curve; 95%CI: 95% confidence interval; LR: Likelihood ratio. *AUC and cut-off value were created by using ROC curve (Fig. 1).

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DiscussionPreeclampsia is a progressive disease severely compro-mising the health of pregnant women and fetuses. In clin-ical follow-up, early diagnosis may be helpful in order toprolong pregnancy, improve gestational outcomes andkeep disease under control. In recent years, some mater-nal plasma biomarkers such as plasma placental protein13(PP13),[15] soluble tyrosine kinase 1(sFlt-1)[16] and pla-cental growth factor (PGF)[17] have been defined as themarkers of PE. In a study, the success rate of populationscreening was increased from 26% to 40% by combiningPP13 with pregnancy-associated plasma protein A(PAPPA) and free leptine index.[15] In another study, sen-sitivity/specificity rates of sFlt-1 and PGF to predictpreeclampsia were 85/66% and 96/94%, but these ratesincreased up to 96/97% when sFlt-1 and PGF were pro-portioned (sFlt-1/PGF).[18] However, these biomarkersare very expensive and they still need confirmation.Simple, widespread and inexpensive laboratory findingsare needed to establish the diagnosis of preeclampsia andto determine its severity. In Turkey, the parameters ofcomplete blood count are obtained easily and their resultsare reached rapidly in almost all health institutions, andthey are the most appropriate laboratory examination forthese criteria. When hematologic parameters were evalu-ated, it was observed in some studies that hemoglobinvalues elevated, platelet numbers decreased in leukocytenumbers increased in preeclamptic pregnant women.[19,20]

Some studies asserted that the numbers of hemoglobinand thrombocyte might be associated with geographiclocation, dietary habits and ethnic origin.[21] Although dif-ferent results were reported in various studies, some stud-ies reported that there was no difference betweenpreeclamptic and healthy pregnant women in terms ofhemoglobin, platelet, lymphocyte and neutrophil num-bers.[19,22] In our study, we did not find any differencebetween preeclampsia, severe preeclampsia and the con-trol groups in terms of hemoglobin values but there wassignificant difference in preeclampsia and severepreeclampsia groups compared to the control group interms of platelet, neutrophil, monocyte and lymphocytevalues; however, there was no difference betweenpreeclampsia and severe preeclampsia groups. When weevaluated inflammatory markers, we found a difference inpreeclampsia group compared to the control group interms of platelet/lymphocyte, platelet/neutrophil, neu-trophil/lymphocyte and monocyte/lymphocyte rates butthere was no difference between preeclampsia and severepreeclampsia groups. Mannaerts et al. also observed in

their study that NLR increased and PLR decreased inpreeclampsia group compared to the control group.[23]

Systemic inflammatory indexes are the ratio indexesconsidered as active markers of systemic inflammationand immune balance, and calculated by platelet, inflam-matory activators (neutrophils/monocytes) and inflam-matory regulators (lymphocytes) which play a significantrole in diagnosis, prognosis and therapeutic evaluation ofvarious diseases. In our study, we found that PE patientshad significantly different NLR, MLR, PNR and PLRvalues compared to the control group and noticed thatdifferentiated leukocyte number changed significantly inPE. Previous studies show that increased numbers ofmonocytes and neutrophils and surface marker activationand medium level systemic immune response in a normalpregnancy is very important to maintain a successfulpregnancy.[24] On the other hand, immune responsebecomes stronger in PE, it may explain clinical character-istics of PE since neutrophil and monocyte cells activatedby inflammatory cytokines which are produced by pla-centa cells (stromal and trophoblast cells) have abnormalbiological functions.[25] Thus, the sensitivity and specifici-ty rates for NLR, PLR, MLR and PNR to detectpreeclampsia are not even close to 95% in our study, andthey are not appropriate for practical use; therefore, weconcluded that they are insufficient to diagnosepreeclampsia and predict the severity of the disease byusing them only. However, these rates and prediction val-ues can be increased by combining them with practicaland inexpensive methods such as uterine artery Doppler.

ConclusionAlthough leukocyte count is a traditional method to fol-low up inflammatory diseases clinically, NLR, PLR,MLR and PNR are secondary analyses to interpret thebalance between inflammation and immune regulationmore effectively. Our results show that NLR, PLR,MLR, PNR values as inflammation markers are morevaluable than absolute leukocyte count for the early diag-nosis and prognostic evaluation of PE. On the otherhand, the sensitivity and specificity values of NLR, PLR,MLR, PNR indexes are not appropriate for practical usealthough they have advantages in terms of convenience,simplicity, sensitivity, versatility and speed, and they areinsufficient alone to diagnose preeclampsia and predicttheir severity.

Conflicts of Interest: No conflicts declared.

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References1. Wong TY, Groen H, Faas MM, van Pampus MG. Clinical

risk factors for gestational hypertensive disorders in preg-nant women at high risk for developing preeclampsia.Pregnancy Hypertens 2013;3:248–53.

2. Milosevic-Stevanovic J, Krstic M, Radovic-Janosevic D,Stefanovic M, Antic V, Djordjevic I. Preeclampsia with andwithout intrauterine growth restriction – two pathogeneti-cally different entities? Hypertens Pregnancy 2016;35:573–82.

3. Visser N, van Rijn BB, Rijkers GT, Franx A, Bruinse HW.Inflammatory changes in preeclampsia: current understand-ing of the maternal innate and adaptive immune response.Obstet Gynecol Surv 2007;62:191–201.

4. Laresgoiti-Servitje E, Gómez-López N, Olson DM. Animmunological insight into the origins of pre-eclampsia.Hum Reprod Update 2010;16:510–24.

5. Laresgoiti-Servitje E. A leading role for the immune systemin the pathophysiology of preeclampsia. J Leukoc Biol 2013;94:247–57.

6. Gu Y, Lewis DF, Deere K, Groome LJ, Wang Y. Elevatedmaternal IL-16 levels, enhanced IL-16 expressions inendothelium and leukocytes, and increased IL-16 produc-tion by placental trophoblasts in women with preeclampsia.J Immunol 2008;181:4418–22.

7. Taylor RN, Roberts JM. Endothelial cell dysfunction. In:Lindheimer MD, Roberts JM, Cunningham FG, editors.Hypertensive disorders in pregnancy. 2nd ed. Stamford, CT:Appleton & Lange; 1999. p. 395–429.

8. Celikbilek M, Dogan S, Ozbak›r O, Zarars›z G, Kücük H,Gürsoy S, et al. Neutrophil-lymphocyte ratio as a predictorof disease severity in ulcerative colitis. J Clin Lab Anal2013;27:72–6.

9. Imtiaz F, Shafique K, Mirza SS, Ayoob Z, Vart P, Rao S.Neutrophil lymphocyte ratio as a measure of systemicinflammation in prevalent chronic diseases in Asian popula-tion. Int Arch Med 2012;5:2.

10. Tousoulis D, Antoniades C, Koumallos N, Stefanadis C.Pro-inflammatory cytokines in acute coronary syndromes:from bench to bedside. Cytokine Growth Factor Rev 2006;17:225–33.

11. Zahorec R. Ratio of neutrophil to lymphocyte counts –Rapid and simple parameter of systemic inflammation andstress in critically ill. Bratisl Lek Listy 2001;102:5–14.

12. Proctor MJ, Morrison DS, Talwar D, Balmer SM, FletcherCD, O’Reilly DS, et al. A comparison of inflammation-basedprognostic scores in patients with cancer. A GlasgowInflammation Outcome Study. Eur J Cancer 2011;47:2633–41.

13. Elgari MM, Khabour OF, Alhag SM. Correlations betweenchanges in hematological indices of mothers with preeclamp-

sia and umbilical cord blood of newborns. Clin Exp Hypertens2018;41:58–61.

14. American College of Obstetricians and Gynecologists; TaskForce on Hypertension in Pregnancy. Hypertension in preg-nancy. Report of the American College of Obstetricians andGynecologists’ Task Force on Hypertension in Pregnancy.Obstet Gynecol 2013;122:1122–31.

15. De Villiers CP, Hedley PL, Placing S, Wøjdemann KR,Shalmi AC, Carlsen AL, et al. Placental protein-13 (PP13) incombination with PAPP-A and free leptin index (fLI) in firsttrimester maternal serum screening for severe and earlypreeclampsia. Clin Chem Lab Med 2017;56: 65–74.

16. Burke SD, Zsengellér ZK, Khankin EV, Lo AS, RajakumarA, DuPont JJ, et al. Soluble fms-like tyrosine kinase 1 pro-motes angiotensin II sensitivity in preeclampsia. J Clin Invest2016;126:2561–74.

17. Lecarpentier É, Vieillefosse S, Haddad B, Fournier T, LeguyMC, Guibourdenche J, et al. Placental growth factor (PlGF)and sFlt-1 during pregnancy: physiology, assay and interest inpreeclampsia. Ann Biol Clin (Paris) 2016;74:259– 67.

18. Taraseviãienò V, Grybauskienò R, Maãiuleviãienò R. sFlt-1,PlGF, sFlt-1/PlGF ratio and uterine artery Doppler forpreeclampsia diagnostics. Medicina (Kaunas) 2016;52:349–53.

19. Canzoneri BJ, Lewis DF, Groome L, Wang Y. Increasedneutrophil numbers account for leukocytosis in women withpreeclampsia. Am J Perinatol 2009;26:729–32.

20. Yavuzcan A, Ca¤lar M, Ustün Y, Dilbaz S, Ozdemir I, YildizE, et al. Mean platelet volume, neutrophil-lymphocyte ratioand platelet-lymphocyteratio in severe preeclampsia. GinekolPol 2014;85:197–203.

21. Järemo P, Lindahl TL, Lennmarken C, Forsgren H. Theuse of platelet density and volume measurements to estimatethe severity of pre-eclampsia. Eur J Clin Invest 2000;30:1113–8.

22. Ramma W , Buhimschi IA, Zhao G, Dulay AT, Nayeri UA,Buhimschi CS, et al. The elevation in circulating anti-angio-genic factors is independent of markers of neutrophil activa-tion in preeclampsia. Angiogenesis 2012;15:333–40.

23. Mannaerts D, Heyvaert S, De Cordt C, Macken C, Loos C,Jacquemyn Y. Are neutrophil/lymphocyte ratio (NLR),platelet/lymphocyte ratio (PLR), and/or mean platelet volume(MPV) clinically useful as predictive parameters forpreeclampsia? J Matern Fetal Neonatal Med 2019;32:1412–9.

24. Palm M, Axelsson O, Wernroth L, Larsson A, Basu S.Involvement of inflammation in normal pregnancy. Acta ObstetGynecol Scand 2013;92:601–5.

25. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, RedmanCW. Systemic inflammatory priming in normal pregnancyand preeclampsia: the role of circulating syncytiotrophoblastmicroparticles. J Immunol 2007;178:5949–96.

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Determination of median values of triple screeningtest hormones for Kayseri region and their

cross-regional comparisonsNahide Ekici Günay

Department of Medical Biochemistry, University of Health Sciences, Kayseri City Hospital, Kayseri, Turkey

İD

Özet: Kayseri bölgesi için üçlü tarama testi hormonlar›n›n ortanca de¤erlerinin belirlenmesi vebunlar›n bölgeleraras› karfl›laflt›rmalar›Amaç: Kayseri bölgesi için ikinci trimester serum tarama testindekullan›lan hormon parametrelerinin ortanca de¤erlerini belirle-mek ve ortanca de¤erleri tarama raporunda bildirilen de¤erlerlekarfl›laflt›rmak, yeni ortanca de¤erlere sahip olgular›n risk durumu-nu de¤erlendirmek ve Kayseri bölgesinin güncel ortanca de¤erle-rini di¤er bölgelerle karfl›laflt›rmak.

Yöntem: fiubat 2018 ve May›s 2018 tarihleri aras›nda art ardaKayseri Do¤um Klini¤i’ne baflvuran ve üçlü tarama testi yapt›ran1481 gebenin (gestasyonel yafl: 15–20 hafta) verilerini retrospektifolarak kaydettik.

Bulgular: Toplam beta-insan koryonik gonadotropini (tβ-hCG),serbest östriol (uE3) ve alfa-fetoprotein (AFP) için gerçek ortancade¤erlerin, Prisca program›nda önerilen de¤erlerden daha düflükoldu¤u bulundu (p<0.001). Prisca program› taraf›ndan risksiz ola-rak bildirilen 29 gebe gerçek ortanca de¤erleriyle tekrar de¤erlen-dirildi¤inde, tβ-hCG MoM kesme de¤eri Down sendromu için ar-tan risk ile >2.5 olarak bulundu. Risksiz olarak bildirilen 12 gebe,nöral tüp defekti (NTD) için risk içermeyerek AFP için >2.5 MoMde¤erine sahipti. Kayseri bölgesi için ortanca tβ-hCG de¤erleri-nin, di¤er bölgelerden daha düflük oldu¤u bulundu (p<0.01).

Sonuç: Test amac›m›za uygun olarak, testin risksiz gebeliklerdegereksiz invazif prosedürleri önermemesi ve gerçek yüksek riskligebelikleri tespit etmesi önemlidir. Popülasyona ve laboratuvaraözgü ortanca de¤erlerin tespiti, test performans›n› iyilefltirecek-tir.

Anahtar sözcükler: Prenatal, tan›, risk, alfa-fetoprotein, insankoryonik gonadotropini, serbest östriol.

Correspondence: Nahide Ekici Günay, MD. Department of Medical Biochemistry, University of Health Sciences, Kayseri City Hospital, Kayseri, Turkey.e-mail: [email protected] / Received: May 31, 2019; Accepted: September 3, 2019Please cite this article as: Ekici Günay N. Determination of median values of triple screening test hormones for Kayseri region and their cross-regional comparisons. Perinatal Journal 2019;27(2):68–76. doi:10.2399/prn.19.0272004

Original Article

Perinatal Journal 2019;27(2):68–76©2019 Perinatal Medicine Foundation

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Abstract

Objective: To determine median values of hormone parametersused in second trimester serum screening test for Kayseri region andto compare the median values with those given in screen report, toassess risk status of cases with new median values, and to compareup-to-date median values for Kayseri region with those from otherregions.

Methods: We retrospectively recorded data from 1481 pregnantwomen (gestational age: 15–20 weeks) who consecutively presentedto Kayseri Obstetrics Clinic between February, 2018 and May, 2018and had triple screen test.

Results: Actual median values for total beta-human chorionicgonadotropin (tβ-hCG), unconjugated estriol (uE3) and alpha-feto-protein (AFP) were found to be lower than those recommended inPrisca software (p<0.001). When 29 pregnant women reported asrisk-free by Prisca software were re-assessed by actual median val-ues, tβ-hCG MoM cut-off value was found as >2.5 with increasedrisk for Down syndrome. It was found that 12 pregnant womenreported as risk-free had >2.5 MoM for AFP with risk for NTD.Median tβ-hCG values for Kayseri region were found to be lowerthan those in other regions (p<0.01).

Conclusion: In accordance with the purpose of the test, it is impor-tant that the test should not recommend unnecessary invasive pro-cedures in risk-free pregnancies and should detect true high-riskpregnancies. The identification of population-and laboratory-specif-ic medians will improve test performance.

Keywords: Prenatal, diagnosis, risk, alpha-fetoprotein, humanchorionic gonadotropin, unconjugated estriol.

ORCID ID: N. Ekici Günay 0000-0002-3041-7427

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IntroductionThe triple screen test is one of the major tests thatinform whether infant has congenital anomalies such asDown syndrome (trisomy 21), Edwards syndrome (tri-somy 18), Patau syndrome (trisomy 13), Smith-Lemli-Opitz syndrome (SLOS) and neural tube defect(NTD).[1,2] The test (also known as second trimesterscreen test) includes serum biochemistry screening per-formed between 14 and 20 gestational weeks and is basedon generating a congenital disease-specific risk ratio by aprogram using maternal serum total beta-human chori-onic gonadotropin (tβ-hCG), unconjugated estriol(uE3), alpha-fetoprotein (AFP) values and maternal ageas input.[3–5]

As with other biochemical parameters, it is needed tomeasure the parameters accurately in accordance toterms of laboratory carrying out analyses for reliability ofrisk results reported in triple screen test. The medianvalues used for calculation can be affected by several fac-tors including population, geographic region, ethnicity,age or smoking.[6] The “multiples of median” (MoM)based on regional median values are used for more accu-rate risk calculation. The MoM is obtained by dividingtest result of a certain pregnant women to median valueof population, which indicates how far is the result ofcertain pregnant women from average value of normalpopulation.[7]

The aim of present study was to determine medianvalues of hormone parameters used in second trimesterserum screening test for Kayseri region and to comparethe median values with values given in screen report, toassess risk status of cases with new median values, and tocompare up-to-date median values for Kayseri regionwith those from other regions.

MethodsThe study included women with singleton pregnancy(gestational age: 15–20 weeks) who consecutively pre-sented to Kayseri Obstetrics Clinic between February,2018 and May, 2018 and underwent triple screen test.The tβ-hCG, uE3 and AFP were measured byIMMULITE® 2000 XPi system (Siemens HealthcareDiagnostics, Los Angeles, CA, USA) using chemilumi-nescence immunoassay technique.

In the assays, the analytic sensitivity is approximately0.24 ng/mL for AFP, 0.4 mIU/mL for tβ-hCG, and 0.01

ng/mL for uE3. The within-run coefficient of variation(CV) is around 2.5%, 7%, and 8%, respectively.

The gestational age was determined by sonograph-ic measurements of biparietal diameter (BPD) andfemur length (FL) based on Hadlock II method.[8] Thepatients reported as high-risk pregnancy by Prisca soft-ware, those with tβ-hCG level ≥2.5 MoM, and thosewith tβ-hCG, uE3 and AFP<0.5 MoM were excluded.In addition, patients with history of gestational dia-betes mellitus, those with newly diagnosed diabetesmellitus, IVF pregnancies, twin pregnancies and smok-ers were excluded. In all pregnant women included,data regarding diabetes mellitus, smoking status, age,weight, gestational age, BPD measurement and triplescreen test parameters including tβ-hCG, uE3 andAFP values were entered into PRISCA 5.0 software(Prenatal Risk Estimation Typology Software GmBH,Hamburg, Germany).

The tβ-hCG, uE3 and AFP values were recordedaccording to ultrasonographic gestational ages deter-mined via BDP and FL measurements together withdemographic data for each pregnant woman and MoMvalues were determined according to median values ofnormal population in Prisca software.

Then, actual median value for each parameter wascalculated in the pregnant population. A new MoMvalue was calculated via dividing test value by actualmedian value. Median values and MoM values for eachpatient were compared to actual median and MoM val-ues and percent difference was calculated.

The actual median values for Kayseri region werecompared to those obtained for ‹stanbul, Erzurum,Antalya, Van, Bingöl and Eskiflehir provinces byIMMULITE 2000 analyzer and same software in sim-ilar studies and percent bias values were calculated.[9–14]

Statistical analyses were performed by IBM® SPSS®

24.0 (Armonk, NY, USA). Normal distribution wasassessed by Shapiro-Wilk test. Descriptive statistics aresummarized as median, minimum–maximum andinterquartile range (IQR). Median values were calcu-lated for each gestational week and new MoM valueswere calculated. Wilcoxon signed-rank test was used tocompare pregnancy MoM values. Non-parametric signtest was used to compare median values in Prisca soft-ware with those obtained for other regions. Inter-regional percent differences were calculated by

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Windows Excel (Redmond, Washington, USA) soft-ware. A p-value <0.05 was considered as statisticallysignificant in all analyses.

ResultsTable 1 presents demographic data according to gesta-tional week in 1481 pregnant women included. We cal-culated new median values for tβ-hCG, uE3 and AFPbetween gestational weeks 15 (15 weeks 0 days) and 20(20 weeks 6 days) and compared these new values withmedian values in Prisca software (Table 2). In the com-parison it was found that all median values for all param-eters in Prisca software other than tβ-hCG on gestation-al week 20 and AFP on gestational week 15 were signif-icantly higher than regional median values. The highestpercent difference was detected in tβ-hCG (23.3%)while lowest percent difference was detected in AFP(11.8%).

For gestational weeks 15–20, new MoM values werecalculated for each patient and compared with those inPrisca software (Table 3). For tβ-hCG, MoM values inPrisca software was significantly higher than newly cal-culated MoM values on gestational weeks 15, 18 and 19(p<0.001) while they were significantly lower on gesta-tional weeks 16, 17 and 20 (p<0.001). For uE3 and AFP,MoM values in Prisca software were significantly lowerthan actual MoM values on all weeks (p<0.001). Whenactual MoM values for tβ-hCG were considered, it wasfound that MoM value was above cut-off value (2.5) in 3pregnant women on week 15, 5 pregnant women onweek 16, 10 pregnant women on week 17, 7 pregnantwomen on week 18 and 4 pregnant women on week 20,and these patients were considered to have increased riskfor Down syndrome, all of which were reported as risk-free previously (overall 29 pregnant women). tβ-hCGMoM values calculated for gestational week 19 did notcause change in risk stratification for Down syndrome.There were 8 pregnant women reported as high-risk forNTD according to Prisca software; however, 12 addi-tional pregnant women had >2.5 MoM according toactual MoM values for AFP, all which were reported asrisk-free previously (overall 20 pregnant women). Twopatients were considered as risk-free according to actualMoM values, who were previously reported to be high-risk for SLOS and have <0.5 MoM value for uE3.Median tβ-hCG values for Kayseri region were com-pared to other regions’ values (Table 4 and Figs. 1a–c).

DiscussionAlthough it is well-known that triple test is a screeningtool and does not draw definitive conclusions about fetalproblems, reported results play important role in themanagement of pregnancy for both patient and clini-cian. There is a strong interest on prenatal triple screentests given that the diseases associated with chromoso-mal defect have serious consequences and that onlysymptomatic benefit can be achieved in such disease cur-rently.

The expression of tβ-hCG, a triple test analyte,reflects somatic genotypes, and its production is affectedby genetic variation. CGB5 is one of six genes that reg-ulate hCG expression. It was shown that CGB5 varia-tion play role in recurrent spontaneous abortions andthe gene exhibits region- and population-based varia-tions.[15–17] As a matter of fact, due to the low levels weobserved in our region, we suggests that descriptivestudies could be carried out on this gene regulating hCGexpression.

The AFP, one parameter of triple screen test, is aprotein that resembles to fetal-derived albumin in phys-ical and chemical manner. It was shown that AFP playsrole in production of osmotic pressure and immunolog-ical development of fetus.[18] Maternal serum AFP level isincreased in NTD as well as presence of some anomaliesand other adverse outcomes including congenitalnephrosis, renal agenesis, gastrointestinal atresia, oligo-hydramnios, threatened abortion, Turner syndrome,triploidy, low birth weight and risk for preeclampsia.[19]

Undoubtedly, the diagnostic value of sonographic meas-urements is higher for NTD when compared to elevat-ed serum APF level. However, elevated AFP MoM val-ues are important in pregnancies without NTD on rou-tine sonographic examination regarding presence ofother fetal anomalies and referral to detailed sonograph-ic examination for pregnancy-related complications aswell as monitoring for potential complications duringdelivery.[20] According to our results of the region, calcu-lated AFP median values were evaluated as babies withoverlooked probable problems. In other words, becauseof the standard median data used by the software pro-gram, MoM values could not be calculated accuratelyand true high fetal risks could not be reported to theobstetrician. In the triple screen test using maternal tβ-hCG, uE3 and AFP values, the detection rates are about

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Table 1. Demographic data of pregnants.

Median±SE IQR Min–max

15th week (n=230) Age (year) 25.6±0.42 9.2 18.1–42.1

Weight (kg) 65.3±0.95 8.6 45–103

β-hCG (mIU/mL) 23,214±2156 14,820 5584–98,249

β-hCG (MoM) 0.87±0.09 0.64 0.24–4.23

uE3 (ng/mL) 0.45±0.03 0.292 0.127–1.07

uE3 (MoM) 1.09±0.07 0.65 0.44–2.23

AFP (IU/ml) 25.4±3.8 15.1 10–225

AFP (MoM) 0.96±0.02 0.53 0.47–5.25

16th week (n=277) Age (year) 25.3±0.58 8.2 15.2–48

Weight (kg) 65.9±1.52 18 44–108

β-hCG (mIU/mL) 21,647±1388 11,709 4876–56,571

β-hCG (MoM) 1.04±0.05 0.4 0.2–2.08

uE3 (ng/mL) 0.55±0.03 0.27 0.16–1.46

uE3 (MoM) 0.81±0.06 0.45 0.28–1.81

AFP (IU/ml) 26.05±2.4 15.4 0.8–121

AFP (MoM) 0.93±0.06 0.4 0.20–2.08

17th week (n=284) Age (year)) 25.56±0.68 9.5 17.1–43.5

Weight (kg) 66.1±0.8 11 46–108

β-hCG (mIU/mL) 15,785±1129 11,611 1774–95,408

β-hCG (MoM) 1.20±0.08 0.59 0.20–3.44

uE3 (ng/mL) 0.72±0.26 0.34 0.19–1.71

uE3 (MoM) 0.89±0.05 0.35 0.23–1.94

AFP (IU/ml) 30.20±2.29 16.8 11.9–103

AFP (MoM) 0.99±0.06 0.59 0.20–3.44

18th week (n=253) Age (year) 24.9±0.92 12 16.5–41.8

Weight (kg) 67.1±0.6 9.6 45–113

β-hCG (mIU/mL) 14,295±1156 10631 1509–86,067

β-hCG (MoM) 1.01±0.06 0.47 0.16–2.09

uE3 (ng/mL) 0.91±0.40 0.41 0.33–3.94

uE3 (MoM) 1.00±0.04 0.36 0.29–1.65

AFP (IU/ml) 35.35±2.56 17.3 12.9–110

AFP (MoM) 0.94±0.07 0.37 0.33–2.96

19th week (n=288) Age (year) 26.8±0.9 9.6 17.2–41.8

Weight (kg) 68±0.9 11 48–110

β-hCG (mIU/mL) 15,190±1084 9557 4233–38,505

β-hCG (MoM) 1.0±0.05 0.62 0.31–1.63

uE3 (ng/mL) 1.11±0.03 0.53 0.144–3.45

uE3 (MoM) 0.96±0.04 1.44 0.42–1.86

AFP (IU/ml) 40±2.49 21.4 9.8–116

AFP (MoM) 0.96±0.05 0.45 0.29–1.69

20th week (n=149) Age (year) 25.4±0.7 8.8 17.8–40.8

Weight (kg) 70.1±1.2 8.5 46–108

β-hCG (mIU/mL) 14,501±1415 14493 3984–38,442

β-hCG (MoM) 1.03±0.08 0.77 0.26–2.47

uE3 (ng/mL) 1.31±0.04 0.793 0.618–2.59

uE3 (MoM) 0.99±0.04 0.48 0.42–1.45

AFP (IU/ml) 45.30±4.20 22.6 21.6–187

AFP (MoM) 1.01±0.07 0.36 0.46–3.36

ββ-hCG: human chorionic gonadotrophin; AFP: alpha-fetoprotein; IQR: interquartile range; SE: standard error; uE3: unconjugated estriol.

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60–65% for trisomy 21 and 18, and 75–80% for neuraltube defects.[21] Again, it measures AFP, uE3 and tβ-hCG with a sensitivity of 60% and false-positive rate of5%.[22] Although the triple screening test result is not adiagnostic, it is important in terms of referral to detailedultrasonographic test request and decision of amniocen-tesis. By the reporting laboratory, failure to use analyti-cal median values obtained from the regional pregnantcommunity is an important factor that may affect theclinician’s performance in patient follow-up and man-agement (such as the request for advanced ultrasono-graphic examination or decision of amniocentesis).

As with other biochemical parameters, factors suchas ethnicity, age and smoking used in risk calculation in

triple screen test can alter median values in the centercarrying out studies. In this context, concordancebetween regional median values and those used in thesoftware is an important requirement which influenceson performance regarding accurate risk identificationand decision-making process in the pregnancy.

Triple test result aids preparation of parent for deliv-ery. If all test results are normal, parents are assured thatlikelihood of infant with genetic disorder is low.However, early recognition of high-risk pregnancies willadd advantage to parents for better management ofdelivery and to attending clinician for management ofpotential complications.

Table 2. Comparison of the triple test parameters in the newly calculated median values and Prisca program.

Total ββ-hCG (mIU/mL)

Gestational week n Current median Prisca median p bias %

15 230 23,214 34,820 <0.001 33.33

16 277 21,647 26,783 <0.001 19.18

17 284 15,785 22,865 <0.001 30.96

18 253 14,295 19,931 <0.001 28.28

19 288 15,190 18,057 <0.001 15.88

20 149 14,501 16,528 0.846 12.26

Unconjugated estriol (ng/mL)

Gestational week n Current median Prisca median p bias %

15 230 0.45 0.53 0.023 15.09

16 277 0.55 0.74 <0.001 25.68

17 284 0.72 0.87 <0.001 17.24

18 253 0.91 1.17 <0.001 22.22

19 288 1.11 1.38 <0.001 19.57

20 149 1.31 1.87 <0.001 29.95

Alpha-fetoprotein (IU/ml)

Gestational week n Current median Prisca median p bias %

15 230 25.40 26.60 0.911 4.51

16 277 26.05 30.30 0.004 14.03

17 284 30.20 34.45 0.004 12.34

18 253 35.35 40.60 0.016 12.93

19 288 40.00 46.55 <0.001 14.07

20 149 45.30 52.10 0.033 13.05

Sign test for medians. ββ-hCG: β-human chorionic gonadotrophin.

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Among other reasons, strong interest to triple screentest in prenatal diagnosis is due to higher costs and lim-ited access to laboratory technologies despite being non-invasive and high diagnostic values.[23]

When median values obtained for Kayseri regionwere compared to those obtained for ‹stanbul, Erzurum,Antalya, Van, Bingöl and Eskiflehir by similar studies, itwas found that there was no significant difference inmedian tβ-hCG values on weeks 19 and 20 while mediantβ-hCG values on week 17 and 28 were found to be sig-nificantly lower than those obtained for all regions(p<0.001).

Actual median uE3 values on all weeks were found tobe significantly lower than those for Erzurum province

(p<0.001). There was no significant difference in actualmedian uE3 values on all weeks other than week 18between Van and Kayseri region.

Regarding AFP, there was no significant differencein actual median values on all weeks between Kayseriand ‹stanbul, Erzurum and Van provinces. Inter-regional bias was found to be significantly higher onthe weeks 16–18 (considered as optimal timing fortriple screen test) when compared to remainingweeks.

Strong immigration dynamics is remarkable inKayseri region. It is essential to perform similar studiesand to keep median value pools up-to-date in geo-graphic regions which have high potential for changes

Table 3. Comparison of triple test parameters with MoM values calculated according to currently and Prisca program medians.

Total ββ-hCG (mIU/mL)

Gestation week n Current MoM (mean) Prisca MoM (mean) p bias %

15 230 1.09 0.97 <0.001 -12.4

16 277 1.11 0.93 <0.001 -19.4

17 284 1.19 1.12 <0.001 -6.2

18 253 1.14 0.81 <0.001 -40.7

19 288 1.02 0.91 <0.001 -12.1

20 149 1.17 1.07 <0.001 -9.3

Unconjugated estriol (ng/mL)

Gestation week n Current MoM (mean) Prisca MoM (mean) p bias %

15 230 1.12 0.98 <0.001 -14.3

16 277 1.04 0.83 <0.001 -25.3

17 284 1.03 0.80 <0.001 -28.8

18 253 1.06 0.84 <0.001 -26.2

19 288 1.09 0.86 <0.001 -26.7

20 149 1.06 0.85 <0.001 -14.3

Alpha-fetoprotein (IU/ml)

Gestation week n Current MoM (mean) Prisca MoM (mean) p bias %

15 230 1.20 1.04 <0.001 -15.4

16 277 1.11 0.87 <0.001 -27.6

17 284 1.08 0.89 <0.001 -21.3

18 253 1.09 0.94 <0.001 -16.0

19 288 1.07 0.88 <0.001 -21.6

20 149 1.11 0.93 <0.001 -19.4

Wilcoxon signed-rank test. ββ-hCG: human β chorionic gonadotrophin.

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in population characteristics (age, weight, and ethnici-ty) over time and high pregnancy rate. In fact, 16% ofconsecutive subjects included to our study were movedto our region within prior years, reflecting monthlyaverage in 2018 in the study center.

In our study, lower median tβ-hCG values whencompared to those in Prisca software and thoseobtained for other geographic regions may promotegenetic sequence analyses that regulate the hormoneknown to be affected by genetic variation.

Due to retrospective design, the study is limited bylack of detailed sonographic reports and pregnancy

outcomes in patients who were reported to be risk-freepreviously but found to be at risk according to actualmedian values.

ConclusionIn accordance with the purpose of the triple screeningtest, it is important that the test should not produce rec-ommendation of unnecessary invasive procedures inrisk-free pregnancies and should detect true risky preg-nancies. The test performance will be improved bydetermination of population-specific regional medianvalues. The knowledge of regional variation in different

Table 4. Comparison of median values of Kayseri region with median values of some regions.

15th gestational 16th gestational 17th gestational 18th gestational 19th gestational 20th gestational week week week week week week

(RQ2=23.214) (RQ2=21.647) (RQ2=15.785) (RQ2=14.295) (RQ2=15.190) (RQ2=14.501)n=230 n=277 n=284 n=253 n=288 n=149

Q2 p diff. % Q2 p diff. % Q2 P diff. % Q2 P diff. % Q2 p diff. % Q2 p diff. %

‹stanbul - - - 26,772 <.001 19.1 21,446 <.001 26.40 19,533 <.001 26.82 17,140 .004 11.38 - - -

Erzurum 30,134 <.001 22.96 26,296 <.001 17.7 23,508 <.001 32.85 19,342 <.001 26.09 19,213 <.001 20.94 17,884 .317 18.9

Antalya - - - 25,000 <.001 13.4 20,803 <.001 24.12 18,026 <.001 20.70 16,340 .139 7.04 - -

Van 24,391.5 .694 4.82 22,219.5 .954 2.6 20,436 <.001 22.76 17,167 <.005 16.73 14,403 .125 -5.46 14,971 .363 3.1

Bingöl 27,603 <.001 15.90 22,645 .588 4.4 20,199 <.001 21.85 19,631.5 <.001 27.18 18,565 <.001 18.18 - - -

Eskiflehir 26,402 .016 12.07 26,604 <.001 18.6 24,267 <.001 34.95 24,362 <.001 41.32 24,213 <.001 37.27 15,766 .762 8

(RQ2=0.448) (RQ2=0.551) (RQ2=0.72) (RQ2=0.91) (RQ2=1.11) (RQ2=1.31)

‹stanbul - - - 0.58 .220 5.2 0.76 .039 5.26 0.97 .015 6.19 1.18 .079 5.93 - - -

Erzurum* 0.60 <.001 25.3 0.76 <.001 27.6 1.02 <.001 29.41 1.35 <.001 32.59 1.68 <.001 33.93 1.90 <.001 31.1

Antalya - - - 0.61 .003 9.8 0.82 <.001 12.20 0.92 .627 1.09 1.21 .016 8.26 - -

Van 0.45 .237 0.4 0.56 .933 1.8 0.72 .931 0 0.88 .036 -3.41 1.07 .188 -3.74 1.54 .056 14.9

Bingöl 0.451 .269 0.4 0.66 <.001 16.7 0.87 <.001 17.24 1.65 <.001 44.85 1.31 <.001 15.27 - - -

Eskiflehir 0.35 <.001 -28 0.56 .933 1.8 0.87 <.001 17.24 1.28 <.001 28.91 1.66 <.001 33.13 2.10 <.001 37.6

(RQ2=25.40) (RQ2=26.05) (RQ2=30.20) (RQ2=35.35) (RQ2=40.0) (RQ2=45.30)

‹stanbul - - - 28.4 .231 8.27 33.3 .081 9.31 36.5 .361 3.15 43.4 .188 7.83 - - -

Erzurum 24.6 .133 -3.25 27.31 .872 4.61 31.11 .653 2.93 35.62 .113 0.76 41.9 .781 4.42 46.80 .505 3.2

Antalya - - - 30.10 .006 13.46 31.80 .777 5.03 38.10 .621 7.22 44.4 .019 9.91 - - -

Van 27.2 .486 6.62 28.3 .274 7.95 32.1 .566 5.92 33.3 .193 -6.16 42.1 .628 4.99 48.1 .325 5.8

Bingöl 31.5 <.001 19.37 28.1 .371 7.30 34.6 .003 12.72 35.6 .109 0.70 44.3 .0.4 9.71 - - -

Eskiflehir 29.20 .021 13.01 31 <.001 15.97 32.30 .448 6.50 34.00 .685 -3.97 36 .004 -11.11 35.90 <.001 -26.2

Sign test for medians, diff.: difference; Q2: median; RQ2: regional median of Kayseri. Estriol median values for Erzurum region were divided into 3.47 and converted fromnmol/L to ng/mL. -: no data.

Tota

l ββ-h

CG

(m

IU/m

L)Es

trio

l (n

g/m

L)A

lpha

-fet

o pr

otei

n(IU

/ml)

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Determination of median values of triple screening test hormones for Kayseri region and their cross-regional comparisons

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gestational weeks will be helpful to report and interpretresults. In fact, MoM values are used for standardizationof results. However, MoM performance will be affectedunless they are actual or region-specific. It is an analyti-cal requirement that the central immunoassay laborato-ry determine the prenatal screening tests’ hormonemedians for the population it serves. Identification ofregional current median values of hormones used in pre-

natal screening tests will contribute to map median val-ues in our country, to ensure standardization among dif-ferent laboratories and to create software used in riskestimation.

Conflicts of Interest: No conflicts declared.

References1. Palomaki GE, Haddow JE, Knight GJ, Wald NJ, Kennard

A, Canick JA, et al. Risk-based prenatal screening for trisomy18 using alpha-fetoprotein, unconjugated oestriol andhuman chorionic gonadotropin. Prenat Diagn 1995;15:713–23.

2. Craig WY, Haddow JE, Palomaki GE, Roberson M. Majorfetal abnormalities associated with positive screening testsfor Smith-Lemli-Opitz syndrome (SLOS). Prenat Diagn2007;27:409–14.

3. Reynolds T. The triple test as a screening technique forDown syndrome: reliability and relevance. Int J WomensHealth 2010;2:83–8.

4. Onrat ST, Seyman H, Konuk M. Incidence of neural tubedefects in Afyonkarahisar, Western Turkey. Genet Mol Res2009;8:154–61.

5. Acikbas I, Tomatir AG, Akdag B, Koksal A. Retrospectiveanalysis of live birth prevalence of children with Down syn-drome in Denizli, Turkey. Genet Mol Res 2012;11:4640–5.

6. Peter AB, Jonathan M, Colins C. Medians for secondtrimester maternal serum alpha-fetoprotein, human chori-onic gonadotropin and unconjugated estriol; differencesbetween races or ethnic groups. Clin Chem 1997;43:333–7.

7. Burtis CA, Ashwood ER, Bruns DE. Tietz textbook of clin-ical chemistry and molecular diagnostics. Philadelphia, PA:Elsevier Saunders; 2006. p. 2168.

8. Hadlock FP, Deter RL, Harrist RB, Park SK. Estimatingfetal age: computer-assisted analysis of multiple fetal growthparameters. Radiology 1984;152:497–501.

9. Sucu V, Y›ld›rmak S, Vardar M, Mihmanl› V. Determinationof the median levels of double and triple screening testparameters in our hospital. [Article in Turkish] AbantMedical Journal 2018;7:35–40.

10. Y›lmaz A. Determination of the median values of triple testscreening parameters in Erzurum region. [Article inTurkish] Türk Klinik Biyokimya Dergisi 2009;7:37–41.

11. Akal›n N, Ar›kan S. Determination of the median levels oftriple test screening parameters in our region. PerinatalJournal 2007;15:12–9.

12. Alp HH, Huyut Z, Çokluk E, fiekero¤lu MR. Median valuesof double and triple prenatal screening tests: a van scale restro-spective study. [Article in Turkish] Türk Klinik BiyokimyaDergisi 2018;16:17–24.

13. Duran ‹. Determination of the median values of triple testscreening parameters in Bingol region. [Article in Turkish]Türk Klinik Biyokimya Dergisi 2017;15:37–44.

14. fianl› DB, Kartkaya K. Determination of the median levels oftriple test screening parameters in Eskiflehir region. [Articlein Turkish] Turkish Journal of Biochemistry 2011;36;50–4.

Fig. 1. Median values by regions for (a) total β-human chorionicgonadotrophin (tβ-hCG), (b) for unconjugated estriol (uE3)and (c) for alpha-fetoprotein (AFP).

a

b

c

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15. Policastro PF, Daniels-McQueen S, Carle G, Boime I. Amap of the hCG beta-LH beta gene cluster. J Biol Chem1986;261:5907–16.

16. Rull K, Christiansen OB, Nagirnaja L, Steffensen R, MargusT, Laan M. A modest but significant effect of CGB5 genepromoter polymorphisms in modulating the risk of recurrentmiscarriage. Fertil Steril 2013;99:1930–6.

17. Rull K, Nagirnaja L, Ulander V-M, Kelgo P, Margus T,Kaare M, et al. Chorionic gonadotropin beta-gene variantsare associated with recurrent miscarriage in two Europeanpopulations. J Clin Endocrinol Metab 2008;93:4697–706.

18. Nicholas NS. Human fetal allograft survival. In: Studd J, edi-tor. Progress in Obstetrics and Gynecology. Edinburgh:Churchill Livingstone; 1983. p. 97:12.

19. Spaggiari E, Ruas M, Dreux S, Valat AS, Czerkiewicz I,Guimiot F, et al. Management strategy in pregnancies withelevated second-trimester maternal serum alpha-fetoprotein

based on a second assay. Am J Obstet Gynecol 2013;208:303.e1–7.

20. Ghi T, Pilu G, Falco P, Segata M, Carletti A, Cocchi G, etal. Prenatal diagnosis of open and closed spina bifida.Ultrasound Obstet Gynecol 2006;28:899–903.

21. Moghadam MN, Davoodi M, Behzadmehr R. Prenatal diag-nosis. Journal of Medical Practice and Review 2018;2:119–22.

22. Lao MR, Calhoun BC, Bracero LA, Wang Y, Seybold DJ,Broce M, et al. The ability of the quadruple test to predictadverse perinatal outcomes in a high-risk obstetric popula-tion. J Med Screen 2009;16:55–9.

23. García-Pérez L, Linertová R, Álvarez-de-la-Rosa M, BayónJC, Imaz-Iglesia I, Ferrer-Rodríguez J, et al. Cost-effective-ness of cell-free DNA in maternal blood testing for prenataldetection of trisomy 21, 18 and 13: a systematic review. EurJ Health Econ 2018;19:979–91.

Bu makalenin kullan›m izni Creative Commons Attribution-NoCommercial-NoDerivs 3.0 Unported (CC BY-NC-ND3.0) lisans› arac›l›¤›yla bedelsizsunulmaktad›r. / This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported (CC BY-NC-ND3.0)License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ or send a letter to Creative Commons, PO Box 1866,Mountain View, CA 94042, USA.

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The knowledge, attitude and behavior levels of midwifery students for the non-pharmacologicalmethods used in the management of labor pain

Ayfer Arslan1 , Gamze Temiz2

1Koç University Hospital, ‹stanbul, Turkey 2Hamidiye Midwifery Faculty, University of Health Sciences, ‹stanbul, Turkey

İDİD

Özet: Ebelik ö¤rencilerinin do¤um a¤r›s›n›n yöneti-minde kullan›lan nonfarmakolojik yöntemlere iliflkinbilgi, tutum ve davran›fllar›Amaç: Bu çal›flma ebelik ö¤rencilerinin do¤um a¤r›s›n›n yönetimin-de kullan›lan nonfarmakolojik yöntemler konusundaki bilgi düzey-lerinin belirlenmesi ve fark›ndal›klar›n›n artt›r›lmas› amac›yla plan-land› ve uyguland›.

Yöntem: Araflt›rma ‹stanbul Bilim Üniversitesi Sa¤l›k Yükseko-kulu Ebelik bölümünde okuyan ve araflt›rmaya kat›lmay› kabuleden 60 ö¤renci ile tan›mlay›c› olarak yürütüldü. Veriler kurumizni ve etik kurul onay› al›narak anket formu ile topland›. Anket-ler SPSS versiyon 22 (SPSS Inc., Chicago, IL, ABD) program›kullan›larak de¤erlendirildi.

Bulgular: Araflt›rmaya göre ebelik ö¤rencilerinin %43.3’ünün(n=26) nonfarmakolojik yöntemler hakk›nda bilgi sahibi oldu¤u vebu yöntemlerden en az bir tanesini gebeye uygulad›¤› saptand›.Ö¤renim gördükleri s›n›fa göre karfl›laflt›r›ld›¤›nda; 2. s›n›flar›ndo¤um a¤r›s›n›n yönetiminde kullan›lan nonfarmakolojik yön-temlere iliflkin tutumlar›n› belirlemeye yönelik sorulara verdiklericevaplar›n toplam puanlar›n›n, 4. s›n›flar›n puanlar›na göre istatis-tiksel olarak anlaml› derecede yüksek oldu¤u; yafllar› karfl›laflt›r›l-d›¤›nda ise 18–19, 22–23 ve 24 yafl ve üzeri ö¤renci ebelerin dav-ran›fllar›n› belirlemeye yönelik sorulara verdikleri cevaplar›n top-lam puanlar›n›n, 20–21 yafl grubundaki ö¤renci ebelerin puanlar›-na göre istatistiksel olarak anlaml› derecede yüksek oldu¤u bulun-du.

Sonuç: Ö¤rencilerin do¤um a¤r›s›n›n yönetiminde kullan›lannonfarmakolojik yöntemler konusunda bilgilerinin art›r›lmas›nagereksinim vard›r. Bunun için konu ile ilgili teorik e¤itimlerin ya-n› s›ra, görsel ö¤renme teknikleri ve simülasyon uygulama yön-temleri de kullan›larak ö¤rencilerin bilgileri pekifltirilmelidir.

Anahtar sözcükler: Ö¤renci ebe, gebe, do¤um, do¤um a¤r›s›,nonfarmakolojik.

Correspondence: Ayfer Arslan. Koç University Hospital, ‹stanbul, Turkey.e-mail: [email protected] / Received: August 2, 2019; Accepted: September 20, 2019Please cite this article as: Arslan A, Temiz G. The knowledge, attitude and behavior levels of midwifery students for the non-pharmacological methodsused in the management of labor pain. Perinatal Journal 2019;27(2):77–88. doi:10.2399/prn.19.0272006

Original Article

Perinatal Journal 2019;27(2):77–88©2019 Perinatal Medicine Foundation

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Abstract

Objective: We planned and conducted this study to determinethe knowledge levels of midwifery students for the non-pharma-cological methods used in the management of labor pain and toraise awareness on this topic.

Methods: This descriptive study was conducted with 60 students whoattend the Department of Midwifery, Health College, ‹stanbul BilimUniversity and accepted to participate in the research. The data werecollected by the questionnaire forms upon obtaining the approvals ofthe institution and the ethics committee. The questionnaires wereassessed by SPSS version 22 (SPSS Inc., Chicago, IL, USA).

Results: We found that 43.3% (n=26) of the midwifery studentshave knowledge on the non-pharmacological methods and applyat least one of these methods to the pregnant women. When thestudents were compared according to their grades, it was foundthat the total scores of responses given by students in 2nd gradefor the questions to determine their attitudes for the non-pharma-cological methods used in the management of labor pain werehigher in a statistically significant way than the scores of studentsin 4th grade, and when they were compared in terms of their ages,it was seen that the total scores of the responses given by the stu-dents who are 1–19, 22–23 and 24 years old and above for thequestions to determine their behaviors were higher in a statistical-ly significant way than the students who are 20–21 years old.

Conclusion: It is needed to increase the knowledge level of the stu-dents on the non-pharmacological methods used in the managementof labor pain. In order to do this, the knowledge level of the studentsshould be reinforced by using visual learning techniques and simu-lation practice methods in addition to their theoretical education.

Keywords: Midwifery student, pregnant woman, delivery, laborpain, non-pharmacological.

ORCID ID: A. Arslan 0000-0001-8288-4812; G. Temiz 0000-0002-0681-0595

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IntroductionThe labor is a clinical process starting with the cervicaldilation and resulting in the expulsion of placenta and itsmembers, and it is one of the reasons for the most intensepain types known and defined so far.[1–3] The pain devel-oped by labor’s nature affects the perception of pregnantwomen towards labor. Uncontrolled pain may causepregnant women to perceive labor negatively, to havenegative experiences about and dissatisfy with the labor,and may lead to postpartum depression, posttraumaticstress disorder, sexual dysfunction, insufficient attach-ment between mother and newborn, breastfeeding issuesand situations such as mother neglecting newborn.[4–8]

Labor pain is a part of the natural process. Whileother pain types indicate a disease or disorder, labor painis the sign of a good outcome expected. Each labor painhas certainly a preparation period and a particular timespan. It does not last for days or months. It is not contin-uous, but intermittent. As the labor progresses, theintensity and duration of the pain increase.[1,2,5,9,10]

Labor pain is affected by many factors such as theduration of delivery, the duration and dosage ofepidural analgesia, use of oxytocin or misoprostol,amniotomy, size and position of fetus, maternal psy-chology, delivery position, number of delivery andpelvic anatomy.[3,5,6,11,12]

The failure of pain control eliminated the ideas thatlabor pain is acceptable or necessary, and the presence ofpain was considered to be an indication for treatment.Although many studies have been conducted and manydifferent methods have been tried, it has been found outthat labor pain still cannot be managed by pregnantwomen. The pain felt causes stress response and thismaternal change affects fetus negatively. Fear, stress andpain may prolong labor duration by decreasing uterineactivity. This has led both pregnant women and caretak-ers to seek different approaches for pain manage-ment.[2,4,6,8,13,14]

Relieving the labor pain has become a mystery forresearchers for many years, and therefore many pharma-cological and non-pharmacological methods have beendeveloped. The purpose of the methods used to relievelabor pain is to reduce or regulate labor pain directlywithout causing any effect on mother and fetus.Pharmacological methods are based on the use of variousanalgesic and anesthetic substances via different meth-ods. In recent years, non-pharmacological methods have

been developed alternatively due to the fact that pharma-cological methods are expensive and have potential sideeffects. These methods are preferred as they are ease touse and have less side effects as well as being economic.Also, the pregnant women who use the method expresshigher level of satisfaction as they feel that they have thecontrol.[1–7,9,11]

The non-pharmacological methods used in pain con-trol include various techniques not only reduce the phys-ical effects of the pain but also to reinforce the psychoe-motional and spiritual condition of pregnant women.The most common methods are massage, therapeutictouch, applying pressure on sacrum, superficial heat andcold application, hydrotherapy, effleurage, focus, dis-traction, feedback relaxation, respiration techniques,hypnosis, music, aquatic therapy/water birth, transcuta-neous electrical nerve stimulation (TENS), imagination,yoga, biofeedback, aromatherapy, phytotherapy, antena-tal training, acupressure (Shiatsu), acupuncture, sophrol-ogy (the relaxation technique based on yoga), and move-ment and position changes. These non-pharmacologicalmethods used to relieve labor pain are the part of mid-wifery/nursing applications and can be used in laborsafely. Therefore, healthcare professionals should guidefor the use of these methods in order to reduce the per-ceived labor pain, help labor to progress and increase theself-confidence of mother.[14–16]

The management of labor pain will contribute to theproblem-free completion of the labor, immediate start ofmother-newborn relationship and the happiness ofmother for the process. Informing healthcare profes-sionals about this matter beginning from their schoollives will make these methods to be used more actively.For the control of the labor pain and using non-pharma-cological methods more during labor, detailed studiesare needed.

We believe that the results of this research will pro-vide significant contribution to the evaluation of knowl-edge, attitude and behavior levels of the midwifery stu-dents for the non-pharmacological methods used in themanagement of labor pain and for raising their aware-ness.

Following questions were the questions of thisresearch:• What are the knowledge levels of midwifery students

for the non-pharmacological methods used in themanagement of labor pain?

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• What are the attitude and behavior levels of mid-wifery students for the non-pharmacological meth-ods used in the management of labor pain?

• Is there a difference between the grades that the stu-dents attend and the knowledge, attitude and behav-ior levels for the non-pharmacological methods usedin the management of labor pain?

MethodsThe study is a descriptive research, and it was conduct-ed to determine the knowledge, attitudes and behaviorsof students, who attend to the midwifery department ofhealth sciences faculty of a foundation university in‹stanbul, for the non-pharmacological methods used inthe management of labor pain.

The population of the research consisted of the stu-dents attending 1st, 2nd, 3rd and 4th grades of mid-wifery department. The sample was consisted of mid-wifery students who were attending 2nd, 3rd and 4thgrades and meeting the sampling criteria. Attendanceto 2nd, 3rd and 4th grades of midwifery department,completing the class of basic principles and applica-tions, having the experience of clinical practice, andwilling to participate in the research were the inclusioncriteria for the research sampling. In this regard, 60midwifery students, 25 of whom were in 2nd grade, 16of them in 3rd grade and 19 of them in 4th gradebetween 15.11.2017 and 30.11.2017 were the sample ofthe study.

Before the research, the approval of the EthicsCommittee of Health Sciences Institute, ‹stanbul BilimUniversity was obtained. Institutional approval wasobtained for the application. The informed consents ofthe volunteer students were obtained by informingthem about the purpose of the study, and explainingthat the results of the evaluation would be kept anony-mous and that they can withdraw their consents at anytime.

The data were collected by face-to-face interviewby the interviewer between 15.11.2017 and30.11.2017. Each interview took about 15–20 minutes.The data were obtained by “The Student InformationForm and The Evaluation Form for Non-pharmaco-logical Methods Used in the Management of LaborPain”.

Data collection tools

• Student Information Form: This form includesquestions to determine socio-demographic charac-teristics, employment status and knowledge level ofstudents for the non-pharmacological methodsused in the management of labor pain (Table 1).

• Evaluation Form for Non-pharmacologicalMethods Used in the Management of Labor Pain:This form was prepared by the researches by utilizingthe relevant sources. This form includes questions todetermine attitudes and behaviors. The form consistsof two parts, which are Part A answered as “Yes” or“No”, and Part B answered as “True” or “False”.In the questionnaire, each correct answer was

awarded 1 point and each wrong answer was awarded 0point. In the questionnaire, the answer “Yes” for thestatements 5, 8, 9, 10, 12, 13, 14, 15, 17, 18, and 19 andthe answer “No” for the statements 6, 7, 11, and 16 ofthe Part A, and the answer “Correct” for the state-ments 1, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, and 16 andthe answer “False” for the statements 3, 15, and 17 ofthe Part B were considered correct (Table 1).

The minimum score is 0 and the maximum score is31 in the Evaluation Form for Non-pharmacologicalMethods Used in the Management of Labor Pain. Theincrease in the questionnaire score was interpreted asthe increased knowledge level.

Statistical analysis

The data obtained were analyzed by using SPSS 22(Statistical Program for Social Sciences; IBM,Chicago, IL, USA). The data were analyzed by usingstatistical tests such as frequency distribution, arith-metic mean, standard deviation, Kruskal-Wallis test,and Mann-Whitney U test.

ResultsOf the students, 18.3% were in the age group of 18–19,35% in 20–21, 30% in 22–23 and 16.7% in 24 and abovewhile 41.7% were in 2nd grade, 26.7% in 3rd grade and31.7% in 4th grade. While 83.3% of the group has anuclear family, only 5% of them are working and 98.3%of them are having paid education. Also, 96.7% of thestudents were graduated from regular high school and3.3% of them were graduated from vocational highschool of health (Table 2).

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Table 1. The questionnaire form to evaluate the knowledge level of midwifery students on the non-pharmacological methods used in the manage-ment of labor pain.

Student Information Form

1. How old are you? 1. 18–19 � 2. 20–21 � 3. 22–23 � 4. 24–25 � 5. 26 and above �

2. Your grade 2nd grade � 3rd grade � 4th grade �

3. What is your family type? 1. Nuclear � 2. Extended family �

4. Do you work? 1. Yes � 2. No �

5. Your education type 1. Scholarship � 2. Paid �

6. The high school type you graduated 1. Regular high school � 2. Vocational high school of health � 3. Other, please specify…….........

7. Have you ever acquired knowledge on the management of labor pain? 1. Yes � 2. No �

8. If yes, where did you acquire your 1. From my current school �knowledge from? 2. From scientific activities (congress, seminar, conference, etc.) �

3. By reading in Internet, books, or journals �

4. From the hospital that I work / do internship �

9. Do you know anything about the non-pharmacological methods used for the labor pain?

1. Yes � 2. No �

10. If yes, where did you acquire your knowledge from? (You may select multiple options)

1. From the school that I graduated �

2. From my current school �

3. From scientific activities (congress, seminar, conference, etc.) �

4. From the hospital that I work / do internship �

5. From a physician �

6. From a midwife �

7. From a nurse �

8. From books/journals �

9. From scientific publications �

10. From Internet/social networks �

11. Which of the following methods do you know? (You may select multiple options)

12. Have you ever applied these methods to a pregnant woman? Yes � No �

13. If “Yes”, which of the methods did you apply? (You may select multiple options)

1. Massage �

2. Therapeutic touch �

3. Applying pressure on sacrum �

4. Superficial heat and cold application �

5. Hydrotherapy �

6. Focus �

7. Distraction �

8. Feedback relaxation �

9. Respiration techniques �

10. Hypnosis �

11. Music �

12. Aquatic therapy / water birth �

13. Transcutaneous electrical nerve stimulation (TENS) �

14. Imagination �

15. Yoga �

16. Biofeedback �

17. Aromatherapy �

18. Phytotherapy �

19. Antenatal training �

20. Acupressure (Shiatsu) �

21. Acupuncture �

22. Sophrology (the relaxation technique based on yoga) �

23. Movement and position changes �

11. Music �

12. Aquatic therapy / water birth �

13. Transcutaneous electrical nerve stimulation (TENS) �

14. Imagination �

15. Yoga �

16. Biofeedback �

17. Aromatherapy �

18. Phytotherapy �

19. Antenatal training �

20. Movement and position changes

1. Massage �

2. Therapeutic touch �

3. Applying pressure on sacrum �

4. Superficial heat and cold application �

5. Hydrotherapy �

6. Focus �

7. Distraction �

8. Feedback relaxation �

9. Respiration techniques �

10. Hypnosis �

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Table 1. [Continuation] The questionnaire form to evaluate the knowledge level of midwifery students on the non-pharmacological methods usedin the management of labor pain.

Evaluation Form for the Knowledge Level on Non-pharmacological Methods Used in the Management of Labor Pain

A- Please read the following statements carefully. Please select either “Yes” or “No” for each statement. Yes No

1. I had education about the physiology of labor pain. � �

2. I have knowledge of pain theories about the management of labor pain. � �

3. I have knowledge of evaluating labor pain. � �

4. I had education about the impact of labor pain on labor. � �

5. Controlling the labor pain is important in the management of labor pain. � �

6. The methods used are not effective on labor pain. Therefore, it is not necessary to use a non-pharmacological method. � �

7. Any uneducated person can apply non-pharmacological methods used to relieve labor pain. � �

8. Any educated person can apply non-pharmacological methods used to relieve labor pain. � �

9. There are non-pharmacological methods with similar or different application technique. � �

10. Different methods may be applied according the needs of each pregnant woman. � �

11. In case of a labor pain, a single method is started and ended. No other method is needed. � �

12. Non-pharmacological methods used for labor pain help pregnant woman to relax. � �

13. Providing training to pregnant women for non-pharmacological methods helps their participation in labor positively. � �

14. Biofeedback, movement/position change, hypnosis, acupuncture, acupressure, music, sophrology, haptonomy and � �making noise are among the relaxation methods.

15. Appropriate non-pharmacological methods according to the phases of the labor should be applied upon the consent of pregnant woman. � �

16. It is not necessary to record the method used for labor pain. � �

17. The respiratory techniques are applied through 4 levels of respiration. � �

18. Applying non-pharmacological methods increases the confidence of pregnant woman towards healthcare professional. � �

19. Physical application methods are performed by TENS, intradermal fluid injection, superficial heat-cold application, � �hydrotherapy/bath/shower, massage and aromatherapy.

B- Please read the following statements carefully. Indicate your attitude about the methods by writing (T) if it is true or (F) if it is false on the blank part before each statement.

� 1. This is a team work. Education is required before practice.

� 2. I am not interested on this subject, I do not want to do anything.

� 3. If I have the opportunity, I initiate the application on my own.

� 4. I consult to my trainer for the methods.

� 5. I choose the method according to the pregnant woman by considering the setting.

� 6. I can use many methods together.

� 7. I inform the pregnant woman and her family in advance about the non-pharmacological method.

� 8. When I fail about the method, I try to improve my weaknesses with the help of my trainer.

� 9. I investigate if the method used is effective or not by using a pain scale.

� 10. I continue to use the method when I see the effects of the method used.

� 11. I involve the family of pregnant woman into the process while applying the methods.

� 12. It is useful to increase the number of training classes for the application of these methods.

� 13. It should be taught in school how these methods are applied.

� 14. The physical setting to apply methods should be arranged in delivery rooms.

� 15. I believe that I do not have sufficient knowledge to apply the method.

� 16. I record every application performed, and share the results with other team members.

� 17. These applications are not practiced in delivery rooms, I do not find it necessary.

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Of the midwifery students, 63.3% had knowledge ofthe management of labor pain. Accordingly, it was foundthat 56.7% of the students acquired their knowledge onthe management of labor pain from their current school,3.3% of them from Internet, 3.3% of them from the hos-pital they work, and 70% of them had knowledge of thenon-pharmacological methods used in the managementof the labor pain, and 63.3% of them acquired theirknowledge on the non-pharmacological methods used inthe management of the labor pain from their currentschool, 1.7% of them from scientific activities such ascongresses or seminars, 41.7% of them from the hospi-tal, 1.7% of them from a physician, 43.3% of them froma midwife, 13.3% of them from a nurse, 5% of themfrom books and journals, 35% of them from scientificpublications, and 41.7% of them from Internet and socialnetworks.

When the midwifery students were asked the non-pharmacological methods used for labor pain, the groupstated that massage, movement and position change andtherapeutic palpation were the methods they know themost, and aromatherapy, sophrology, acupressure andphytotherapy were the methods they know the least,respectively. It was found that 43.3% of the studentsapplied these methods to a pregnant woman previously.Accordingly, it was found that the most common meth-ods used by the students were movement and positionchanges, massage and focus, respectively (Table 3).

When the answers of midwifery students given forthe Attitude scale of the knowledge evaluation form forthe non-pharmacological methods used in the manage-ment of labor pain were analyzed, it was found that theygave correct answer for the statement “Applying non-pharmacological methods increases the confidence ofpregnant woman towards healthcare professional”. Thisstatement was followed by the statements “Appropriatenon-pharmacological methods according to the phases ofthe labor should be applied upon the consent of pregnantwoman” and “Non-pharmacological methods used forlabor pain help pregnant woman to relax”. On the otherhand, the statement that was given wrong answer themost was “It is not necessary to record the method usedfor labor pain”. The other statements that were givenwrong answer the most were “I had education about thephysiology of labor pain” and “I have knowledge of paintheories about the management of labor pain” (Table 4).

When the answers of midwifery students participat-ed in the research given for the Behavior scale of theknowledge evaluation form for the non-pharmacologicalmethods used in the management of labor pain wereanalyzed, it was seen that the students gave correctanswer for the statements “This is a team work.Education is required before practice”, “I inform thepregnant woman and her family in advance about thenon-pharmacological method” and “These applicationsare not practiced in delivery rooms, I do not find it nec-essary”. On the other hand, the statement that was givenwrong answer the most was “I record every applicationperformed, and share the results with other team mem-bers” which was followed by the statements “If I have theopportunity, I initiate the application on my own”, and“I believe that I do not have sufficient knowledge toapply the method” (Table 5).

It was seen that the Attitude sub-scale scores of themidwifery students in the knowledge evaluation form forthe non-pharmacological methods used in the manage-ment of labor pain ranged from 10 to 19, and the meanscore was 13.35±1.999, the Behavior sub-scale scoresranged from 0 to 17, and the mean score was13.00±1.426 (Table 6).

The significant socio-demographic characteristicsand the characteristics regarding the management oflabor pain of the midwifery students who participated inthis research were compared to their scores in theknowledge evaluation form for the non-pharmacologicalmethods used in the management of labor pain.

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Table 2. The distribution of the students according to their socio-demographic characteristics (n=60).

Characteristics Category n %

Age 18–19 11 18.320–21 21 35.022–23 18 30.024 and above 10 16.7

Grade 2nd grade 25 41.73rd grade 16 26.74th grade 19 31.7

Family type Nuclear family 50 83.3Extended family 10 16.7

Employment Yes 3 5.0status No 57 95.0

Education type Scholarship 1 1.7Paid 59 98.3

The high school Regular high school 58 96.7type graduated Vocational high school of health 2 3.3

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Table 3. The distribution of midwifery students according to their characteristics regarding to the management of labor pain (n=60).

Characteristics Category n %

Acquiring knowledge on the management of Yes 38 63.3labor pain previously No 22 36.7

The source for acquiring knowledge From my current school 34 56.7on the management of labor pain From Internet 2 3.3

From the hospital I work 2 3.3

Having knowledge of the non-pharmacological Yes 42 70.0methods used for labor pain No 18 30.0

The source where the knowledge of the From the school that I graduated 2 3.3non-pharmacological methods used for From my current school 38 63.3labor pain is acquired Scientific activities (congress, etc.) 1 1.7

From the hospital that I work / do internship 25 41.7From a physician 1 1.7From a midwife 26 43.3From a nurse 8 13.3From books/journals 3 5.0From scientific publications 21 35.0From Internet/social networks 25 41.7

The methods known Massage 47 78.3Therapeutic touch 33 55.0Applying pressure on sacrum 32 53.3Superficial heat and cold application 32 53.3Hydrotherapy 10 16.7Focus 28 46.7Distraction 27 45.0Feedback relaxation 15 25.0Respiration techniques 28 46.7Hypnosis 7 11.7Music 32 53.3Aquatic therapy/water birth 7 11.7Transcutaneous electrical nerve stimulation 3 5.0Imagination 15 25.0Yoga 6 10.0Biofeedback 3 5.0Aromatherapy 1 1.7Phytotherapy 2 3.3Antenatal training 31 51.7Acupressure 2 3.3Acupuncture 6 10.0Sophrology 2 3.3Movement and position changes 43 71.7

Application of known methods to a pregnant woman Yes 26 43.3No 33 55.0

The method applied Massage 24 40.0Therapeutic touch 18 30.0Applying pressure on sacrum 19 31.7Superficial heat and cold application 15 25.0Hydrotherapy 0 -Focus 20 33.3Distraction 17 28.3Feedback relaxation 5 8.3Respiration techniques 8 13.3Hypnosis 0 -Music 19 31.7Aquatic therapy/water birth 0 -Transcutaneous electrical nerve stimulation 0 -Imagination 9 15.0Yoga 0 -Biofeedback 0 -Aromatherapy 0 -Phytotherapy 0 -Antenatal training 1 1.7Movement and position changes 25 41.7

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Table 4. The distribution of the responses of midwifery students given for the Attitude sub-scale items of the Evaluation Form for the KnowledgeLevel on Non-pharmacological Methods Used in the Management of Labor Pain (n=60).

Yes No

Attitude sub-scale items n % n %

1. I had education about the physiology of labor pain. 44 73.3 16 26.7

2. I have knowledge of pain theories about the management of labor pain. 44 73.3 16 26.7

3. I have knowledge of evaluating labor pain. 42 70.0 18 30.0

4. I had education about the impact of labor pain on labor. 41 68.3 19 31.7

5. Controlling the labor pain is important in the management of labor pain. 53 88.3 7 11.7

6. The methods used are not effective on labor pain. Therefore, it is not necessary to use a non-pharmacological method. 10 16.7 50 83.3

7. Any uneducated person can apply non-pharmacological methods used to relieve labor pain. 17 28.3 43 71.7

8. Any educated person can apply non-pharmacological methods used to relieve labor pain. 40 66.7 20 33.3

9. There are non-pharmacological methods with similar or different application technique. 55 91.7 5 8.3

10. Different methods may be applied according the needs of each pregnant woman. 54 90.0 6 10.0

11. In case of a labor pain, a single method is started and ended. No other method is needed. 35 58.3 25 41.7

12. Non-pharmacological methods used for labor pain help pregnant woman to relax. 58 96.7 2 3.3

13. Providing training to pregnant women for non-pharmacological methods helps their participation in labor positively. 56 93.3 4 6.7

14. Biofeedback, movement/position change, hypnosis, acupuncture, acupressure, music, sophrology, haptonomy andmaking noise are among the relaxation methods.

56 93.3 4 6.7

15. Appropriate non-pharmacological methods according to the phases of the labor should be applied upon 59 98.3 1 1.7the consent of pregnant woman.

16. It is not necessary to record the method used for labor pain. 49 81.7 11 18.3

17. The respiratory techniques are applied through 4 levels of respiration. 57 95.0 3 5.0

18. Applying non-pharmacological methods increases the confidence of pregnant woman towards healthcare professional. 60 100 0 -

19. Physical application methods are performed by TENS, intradermal fluid injection, superficial heat-cold application, hydrotherapy/bath/shower, massage and aromatherapy.

55 91.7 5 8.3

Table 5. The distribution of the responses of midwifery students given for the Behavior sub-scale items of the Evaluation Form for the KnowledgeLevel on Non-pharmacological Methods Used in the Management of Labor Pain (n=60).

True False

Behavior sub-scale items n % n %

1. This is a team work. Education is required before practice. 59 98.3 1 1.7

2. I am not interested on this subject, I do not want to do anything. 10 16.7 50 83.3

3. If I have the opportunity, I initiate the application on my own. 51 85.0 9 15.0

4. I consult to my trainer for the methods. 55 91.7 5 8.3

5. I choose the method according to the pregnant woman by considering the setting. 52 86.7 8 13.3

6. I can use many methods together. 54 90.0 6 10.0

7. I inform the pregnant woman and her family in advance about the non-pharmacological method. 59 98.3 1 1.7

8. When I fail about the method, I try to improve my weaknesses with the help of my trainer. 57 95.0 3 5.0

9. I investigate if the method used is effective or not by using a pain scale. 52 86.7 8 13.3

10. I continue to use the method when I see the effects of the method used. 52 86.7 8 13.3

11. I involve the family of pregnant woman into the process while applying the methods. 48 80.0 12 20.0

12. It is useful to increase the number of training classes for the application of these methods. 52 86.7 8 13.3

13. It should be taught in school how these methods are applied. 50 83.3 10 16.7

14. The physical setting to apply methods should be arranged in delivery rooms. 56 93.3 4 6.7

15. I believe that I do not have sufficient knowledge to apply the method. 49 81.7 11 18.3

16. I record every application performed, and share the results with other team members. 55 91.7 5 8.3

17. These applications are not practiced in delivery rooms, I do not find it necessary. 1 1.7 59 98.3

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Accordingly, the Behavior sub-scale scores of themidwifery students in the age groups of 18–19, 22–23and 24 and above (13.45±0.688; 13.22±1.263 and13.40±0.699, respectively) were higher than the studentsin the age group of 20–21 (12.19±2.015), and the differ-ence was statistically significant (p<0.05) (Table 7).

The Attitude sub-scale scores of the 2nd grademidwifery students (14.24±2.368) were higher than thescores of the 4th grade students (12.47±1.124) (p<0.05)(Table 8), and the Attitude sub-scale scores of themidwifery students who did not acquire knowledge onthe management of labor pain previously (14.36±2.441) were higher than the students who acquiredtheir knowledge on the management of labor pain pre-viously (12.76±1.422), and the difference in both com-parisons were statistically significant (p<0.05) (Table9).

The Attitude sub-scale scores of the midwifery stu-dents who do not have knowledge of the non-pharmaco-logical methods used for labor pain (14.61±2.279) andthe Attitude sub-scale scores of the midwifery studentswho did not apply the methods they know to a pregnantwoman (14.21±2.103) were high which was statisticallysignificant (p<0.05) (Table 10).

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Table 6. The distribution of the scores of the Evaluation Form forthe Knowledge Level on Non-pharmacological MethodsUsed in the Management of Labor Pain (n=60).

Sub-scale Potential distribution 9 ±SS Min Max

Attitude sub-scale 0–19 13.35 1.999 10 19

Behavior sub-scale 0–17 13.00 1.426 6 15

Table 7. The comparison of the scores of the Evaluation Form forthe Knowledge Level on Non-pharmacological MethodsUsed in the Management of Labor Pain according to theage groups of the midwifery students (n=60).

Sub-scale Age group n 9 ±SS χχ2kw p

Attitude sub-scale 18–19 11 14.55 2.06720–21 21 13.05 2.012

5.935 0.11522–23 18 13.06 1.955

24 and above 10 13.20 1.751

Behavior sub-scale 18–19 11 13.45 0.68820–21 21 12.19 2.015

8.803 0.03222–23 18 13.22 1.263

24 and above 10 13.40 0.699

χχ2kw: Kruskal-Wallis test.

Table 8. The comparison of the scores of the Evaluation Form for theKnowledge Level on Non-pharmacological Methods Used inthe Management of Labor Pain according to the grades ofthe midwifery students (n=60).

Sub-scale Grade n 9 ±SS χχ2kw p

Attitude sub-scale 2nd grade 25 14.24 2.368

3rd grade 16 13.00 1.673 9.385 0.009

4th grade 19 12.47 1.124

Behavior sub-scale 2nd grade 25 12.68 1.952

3rd grade 16 12.81 1.377 2.056 0.358

4th grade 19 13.37 0.761

χχ2kw: Kruskal-Wallis test.

Table 10. The comparison of the scores of the Evaluation Form forthe Knowledge Level on Non-pharmacological MethodsUsed in the Management of Labor Pain with the status ofknowledge of non-pharmacological methods used in themanagement of labor pain and application of the knownmethods to a pregnant woman (n=60).

Having Sub-scale knowledge n 9 ±SS Zmwu p

Attitude sub-scale Yes 42 12.81 1.612-3.320 0.001

No 18 14.61 2.279

Behavior sub-scale Yes 42 13.17 1.248-1.802 0.072

No 18 12,39 1,944

Application of known methods

to a pregnantSub-scale woman n 9 ±SS Zmwu p

Attitude sub-scale Yes 26 12.27 1.251-3.908 0.000

No 33 14.21 2.103

Behavior sub-scale Yes 26 13.35 0.797-1.633 0.103

No 33 12.58 1.855

Zmwu: Mann-Whitney U testi.

Table 9. The comparison of the scores of the Evaluation Form for theKnowledge Level on Non-pharmacological Methods Used inthe Management of Labor Pain according to acquiringknowledge on the management of labor pain previously bymidwifery students (n=60).

Acquiring knowledge on

the management of labor pain

Sub-scale previously n 9 ±SS Zmwu p

Attitude sub-scale Yes 38 12.76 1.422-2.862 0.004

No 22 14.36 2.441

Behavior sub-scale Yes 38 13.26 1.083-1.939 0.053

No 22 12.36 1.965

Zmwu: Mann-Whitney U test.

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DiscussionIn the research, it was found that 63.3% of the midwiferystudents have knowledge of the management of laborpain and 56.7% of them learnt it in their current school.Of these students, 43.3% stated that they have knowl-edge of non-pharmacological methods and applied atleast one of these methods to at least one pregnantwoman. The most common methods used by the stu-dents are massage, listening to music, distraction andimagination, respectively. In the study conducted byAyd›n, Turan and Malkoç,[16] it was found that 86.1% ofthe students have knowledge of the non-pharmacologicalmethods and learnt these methods during their universi-ty education, and the methods they know are respiratorytechniques, superficial heat and cold application, andreflexology.

In a study conducted with a different sample group, itwas reported that midwifery students had education onthe nature of pain and pain-relief methods, 92.6% ofthem believed that pharmacological and non-pharmaco-logical methods should be used together to relieve pain,and that the most common methods were distraction,massage, listening to music and imagination.[17] When wecompared the midwifery students who participated inour research and the nursing students participated in thestudy of Özveren and Uçar[17] in terms of non-pharmaco-logical method applications, we found that 6.5% of thenursing students apply non-pharmacological methodswhile this rate is 43.3% for the midwifery students, andthis result show that midwifery students are more activein dealing with labor pain and reducing labor painbecause of the profession’s nature.

The professional support given throughout the laborimproves the capability of women to cope with pain andto keep it under control, and it prevents pregnant womento have negative experience. The non-pharmacologicalmethods applied during labor aim to provide active sup-port to the women having labor, meet their emotionalneeds and requests, make them feel comfortable,improve labor outcomes, boost self-esteem, ensure themto have positive labor experience and facilitate the transi-tion to the motherhood role. In this way, non-pharmaco-logical methods applied upon the consent of pregnantwoman help her to relax, participate in the labor andcomplete the process positively.[18] In our research, all ofthe midwifery students expressed that the application ofnon-pharmacological methods increases the confidenceof pregnant woman towards healthcare professional,

98.6% of them stated that “the appropriate non-pharma-cological methods according to the phases of the laborshould be applied upon the consent of pregnant woman”,96.7% of them said that “non-pharmacological methodsused for labor pain help pregnant woman to relax”, 95%of them stated expressed that “the respiratory techniquesare applied through 4 levels of respiration”, 93.3% ofthem stated that “providing training to pregnant womenfor non-pharmacological methods helps their participa-tion in labor positively” and said that “biofeedback,movement/position change, hypnosis, acupuncture, acu-pressure, music, sophrology, haptonomy and makingnoise are among the relaxation methods”.

According to the research results, the knowledge levelof the students regarding the concept of pain is good ingeneral; however, the non-pharmacological methodsused for labor pain, its evaluation and control did notprovide expected change in students. Aksoy et al.[10]

reported that the theoretical knowledge of 51.1% of thestudents on labor pain and its management and practiceskills of 56.9% of the students were partially sufficient,and for more active participation in labor, the expecta-tions of the students from the department were activeacademician support (25.9%) and the increased numberof internship in delivery room (28.2%) while their expec-tation from clinics was active professional communica-tion (44.8%). These results indicate that the course sub-jects regarding pain management are limited in the cur-riculum and the clinical field is insufficient in terms ofpracticing.

In our research, we found that the trainings, labora-tory practices and clinical experiences during school termexpand the awareness of the students. Similarly, the atti-tude sub-scale scores of the 2nd grade midwifery studentswere higher than other classes, which is statistically sig-nificant. This result is inconsistent with the literature.The expected result is that the knowledge levels of 3rdand 4th grades midwifery students should be higher thanthe 2nd grade midwifery students in terms of labor, laborpain physiopathology, pain control and non-pharmaco-logical methods. This difference of the students who arein 2nd grade and the age group of 18–19 results from themidwives who graduated from vocational high schools ofhealth and work actively. Midwifery education ensuresthe integration of theoretical training and clinical appli-cation, and helps students to learn by practicing and liv-ing in a real setting. The aim of the education is to devel-op the psychomotor skills of students and establish per-

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manent behavior changes by integrating their theoreticalknowledge into their technical skills. As their ages andgrades progress and their theoretical knowledge getsenriched, their awareness levels also raise. The clinicalfields enable students to observe role models, to performapplications by themselves, and to think about thoseseen, heard, felt and done. The curriculum provided dur-ing education is created by considering the cognitive,behavioral and psychomotor skills, and the targetsexpected from students in all grades are developedaccordingly.[19]

We found that the Attitude sub-scale scores of themidwifery students who did not acquire the knowledgeon the management of labor pain (14.36±2.441) werehigher than the scores of the students who acquired theknowledge on the management of labor (12.76±1.422),and this difference was statistically significant. However,we found out that 63.3% (n=38) of the students in ourstudy had education on the management of labor pain intheir current school. This result indicates that the educa-tion on the methods used for the management of laborpain did not lead to any change in the attitudes andbehaviors. It is necessary to increase the efficiency ofeducation and the number of applied trainings as well astheoretical knowledge in order to create permanent atti-tude and behavior changes.

One of the limitations of the research is that the studywas carried out with 60 students attending midwiferydepartment of a foundation university in ‹stanbul. Thefindings can be generalized to the midwifery studentsreached in 2017–2018 academic year. Acquiring theknowledge level of the sample for the non-pharmacolog-ical methods used in the management of labor pain bythe self-report of the students, the research design beingin the descriptive type, and being unable to observe therelevant methods applied by the students in the clinicalfield are the other limitations of the study.

ConclusionIt is needed to increase the knowledge level of the mid-wifery students on the non-pharmacological methodsused in the management of labor pain. In order to dothis, the knowledge level of the students should be rein-forced by using visual learning techniques and simulationpractice methods in addition to their theoretical educa-tion. For that purpose, we suggest to include the meth-ods that may be used for the labor pain in the curriculum

programs, organizing planned trainings and expandingthe learning process throughout the entire educationperiod, creating application fields that the students maypractice what they learnt, and to ensure integrationbetween school and hospital to that end. In order to beable to apply non-pharmacological methods, the mid-wifery students should know the nature, anatomy andphysiology of women and normal labor process, and theyshould be able to transfer this knowledge into their atti-tudes and behaviors. Therefore, revisions should bemade with frequent intervals and the topics that studentsfeel themselves insufficient should be completed by sim-ulations. The models that will increase the activity of stu-dents for the non-pharmacological methods in clinicalapplication should be developed, implemented, and theresults should be evaluated. Regular evaluation meetingsshould be held in order to enable the students to discusstheir challenges they face in the clinical setting about thelabor physiology, labor pain and its management duringthe labor follow-ups in delivery rooms. In all applica-tions, maternal and fetal health should be taken into con-sideration, and the students should be taught how theycan use the non-pharmacological methods for the man-agement of labor pain according to the phases of thelabor. Beginning from the 2nd grade vocational classes,non-pharmacological methods should be explained in allapplied classes and the subject should be reinforced bysimulations. When teaching psychomotor skills to mid-wifery students in vocational training laboratories, thepractices that will help students to solve problems, makedecisions and gain skills to associate their knowledge withthe clinical setting should be conducted. The importanceof involving the families of pregnant women into allapplications should be highlighted during the education.

Conflicts of Interest: No conflicts declared.

References1. Taflk›n L. Do¤um ve kad›n sa¤l›¤› hemflireli¤i. 8. bas›m.

Ankara: Sistem Ofset Matbaac›l›k; 2004. p. 312–23.2. fiirin A, Kavlak O. Kad›n sa¤l›¤›. ‹stanbul: Bedray Bas›m

Yay›nc›l›k; 2008. p. 664–8.3. Kömürcü N, Ergin A. Do¤um a¤r›s›nda farmakolojik olmayan

yöntemlerin kullan›m›. Hemflirelikte E¤itim ve Araflt›rmaDergisi 2009;6:29–35.

4. Berkiten A. Do¤umun I. ve II. evresinde gebeye uygulat›lanpozisyonlar›n do¤um sürecine etkisi. Doktora Tezi, MarmaraÜniversitesi Sa¤l›k Bilimleri Enstitüsü, ‹stanbul, 2005.

5. Taflç› E, Sevil Ü. Do¤um a¤r›s›na yönelik farmakolojikolmayan yaklafl›mlar. Genel T›p Dergisi 2007;17:181–6.

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6. Coflkun A. Kad›n sa¤l›¤› ve hastal›klar› hemflireli¤i el kitab›.‹stanbul: Koç Üniversitesi Yay›nlar›; 2012. p. 195–206

7. Erdine S. A¤r› mekanizmalar› ve a¤r›ya genel yaklafl›m. In:Erdine S, editör. A¤r›. 3. bask›. ‹stanbul: Nobel T›p Kitabevleri;2007. p. 37–49.

8. Kannan S, Jamison RN, Dattla S. Maternal satisfaction andpain control in women electing natural child birth. RegAnesth Pain Med 2001;26:468–72.

9. Mete S, Uluda¤ E. Do¤um eyleminde destekleyici bak›m.Cumhuriyet Hemflirelik Dergisi 2014;3:22–9.

10. Aksoy Ö, P›nar fi, Yurtsal Z, Uçuk S, fiahin T, Y›lan H. Do-¤um eylemine aktif olarak kat›lan ebelik ö¤rencilerinin kayg›ve öz-güven düzeylerinin incelenmesi. Gümüflhane Üniversi-tesi Sa¤l›k Bilimleri Dergisi 2017;6:2.

11. Eti Aslan F, Karadakovan A. Dahili ve cerrahi hastalardabak›m. Adana: Nobel Kitabevi, Adana, 2011.

12. ‹pek A, Ery›lmaz G. Do¤um eyleminde alt s›rt bölgesineuygulanan derisel terapi yöntemlerinin do¤um a¤r›s› alg›s›nave do¤umun süresine etkisi. Yüksek lisans tezi, AtatürkÜniversitesi Sa¤l›k Bilimleri Enstitüsü, Erzurum, 2014.

13. Phumdoung S, Good M. Music reduces sensation and distressof labor pain. Pain Manag Nurs 2003;4:54–61.

14. Anderson FWJ, Johnson CT. Complementary and alternativemedicine in obstetrics. Int J Gynaecol Obstet 2005;91:116–24.

15. Avc›bay B, Alan S. Do¤um a¤r›s›nda kullan›lan nonfarmakolojikyöntemler. Mersin Üniversitesi Sa¤l›k Bilimleri Dergisi 2011;4:18–24.

16. Ayd›n Y, Turan Z, Malkoç ÖÖ. Ebelik intörn ö¤rencilerinindo¤um a¤r›s›n›n kontrolünde uygulanan non-farmakolojikyöntemler hakk›nda bilgi düzeylerinin belirlenmesi. EbelikteGüncel Yaklafl›mlar Sempozyumu, Sakarya Üniversitesi, 30Nisan 2015.

17. Özveren H, Uçar H. Ö¤renci hemflirelerin a¤r› kontrolündekullan›lan farmakolojik olmayan baz› yöntemlere iliflkin bilgi-leri. Hacettepe Üniversitesi Sa¤l›k Bilimleri Fakültesi Hemfli-relik Dergisi 2009;16:59–72.

18. Karaçam Z, Akyüz EÖ. Do¤um eyleminde destekleyici bak›mve ebe/hemflirenin rolü. ‹stanbul Üniversitesi FlorenceNightingale Hemflirelik Dergisi 2011;19:45–53.

19. Titrek O, Hakkakul MA, Varl› S. Hemflirelik bölümü stajuygulamalar›n›n etkililik düzeyine iliflkin ö¤renci ve rehberhemflirelerin görüflleri. Abant ‹zzet Baysal Üniversitesi E¤itimFakültesi Dergisi 2015;15:264–80.

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The evaluation of cesarean section rates in accordancewith Robson Ten-Group Classification System and the

data of perinatology (tertiary center)Hüseyin K›yak1 , Gökhan Bolluk2 , Emel Canaz3 , Semra Yüksel4 , Ali Gedikbafl›2

1Gynecology and Obstetrics Clinic, ‹stanbul Kanuni Sultan Süleyman Training and Research Hospital, ‹stanbul, Turkey2Perinatology Department, Gynecology and Obstetrics Clinic, ‹stanbul Kanuni Sultan Süleyman Training and Research Hospital, ‹stanbul, Turkey

3Department of Obstetrics and Gynecology, Faculty of Medicine, ‹stanbul Bilim University, ‹stanbul, Turkey 4Gynecology and Obstetrics Clinic, ‹stanbul Taksim GOP Training and Research Hospital, ‹stanbul, Turkey

İDİDİDİDİD

Özet: Sezaryen oranlar›n› Robson On GrupluS›n›fland›rma Sistemi ve perinatoloji (tersiyermerkez) verileri do¤rultusunda konuflmakAmaç: Hastanemizde gebe ve perinatoloji klinik verilerinin RobsonOn Gruplu S›n›fland›rma Sistemi (ROGSS) üzerine etkilerini ayr›ayr› de¤erlendirmek. Yöntem: 2015–2019 verileri dijital olarak ç›kar›l›p sistem üzerin-den gebe ve perinatoloji sonuçlar› ay›rt edildikten sonra, bütüngruplar Dünya Sa¤l›k Örgütü önerileri do¤rultusunda karfl›laflt›r›-larak incelendi. Bulgular: Toplam 57.402 do¤umun 24.240 tanesi (%42.2) sezar-yen ile do¤urtulmufltur. Gebe grubunu oluflturan 42.500 gebenin(tüm do¤umlar›n %74’ü) 15.025 tanesi sezaryen ile (%35.4) do-¤urtulmufltur. Perinatoloji klini¤inde takip edilen 14.902 gebenin(tüm do¤umlar›n %26’s›) de 9215 tanesi sezaryen (%61.8) ile do-¤urmufltur. Hastaneye yüksek oranda multipar baflvurusu gerçek-leflmektedir (%39.2). Eski sezaryen tan›l› hastalara %99.8 oran›n-da sezaryen uygulanmaktad›r. Makat prezantasyon ile gelen gebe-lerin oran› beklenenden daha düflük olup, nullipar makat gelifllerde%96.8 ve multipar makat gelifllerde %88.6’lik sezaryen oran› gö-rülmüfltür. Ço¤ul gebelik nedeniyle baflvuran gebelerin oran›%6.1 ve sezaryen oran› %90.1 olarak saptanm›flt›r. Perinatolojiklini¤inde takip edilen baflta preeklampsi olmak üzere farkl› ne-denlerle baflvuran ve preterm do¤um gerçeklefltirilen gebelerinoran› %25.1 ve sezaryen oran› %66.1 olarak gerçekleflmifltir. Sonuç: Perinatoloji klini¤i/tersiyer merkeze ba¤l› sezaryen oran-lar› çok daha yüksek düzeydedir. Primer sezaryen oranlar›n› uygundüzeylerde tutmak için ›srarc› do¤um indüksiyonu uygulamalar›n-dan kaç›nmal›, tüp ligasyon ifllemi için sezaryeni önermemeli veuygun hastalarda makat gelifli durumlar›nda eksternal sefalik versi-yon denenmelidir.

Anahtar sözcükler: Robson On Gruplu S›n›fland›rma Sistemi,perinatoloji/tersiyer klini¤i.

Correspondence: Ali Gedikbafl›, MD. Perinatology Department, Gynecology and Obstetrics Clinic, ‹stanbul Kanuni Sultan Süleyman Training and ResearchHospital, ‹stanbul, Turkey. e-mail: [email protected] / Received: August 15, 2019; Accepted: September 23, 2019Please cite this article as: K›yak H, Bolluk G, Canaz E, Yüksel S, Gedikbafl› A. The evaluation of cesarean section rates in accordance with RobsonTen-Group Classification System and the data of perinatology (tertiary center). Perinatal Journal 2019;27(2):89–100. doi:10.2399/prn.19.0272007

Original Article

Perinatal Journal 2019;27(2):89–100©2019 Perinatal Medicine Foundation

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Abstract

Objective: To evaluate separately the impacts of clinical data ofpregnant women and perinatology on Robson Ten-GroupClassification System in our hospital. Methods: After the data of pregnant women and perinatology out-comes between 2015 and 2019 were obtained digitally from the sys-tem and distinguished from each other, all groups were evaluated bycomparing them in accordance with the suggestions of the WHO. Results: A total of 24,240 (42.2%) out of 57,402 labors were carriedout by cesarean section. Of 42,500 (74% of all labors) pregnantwomen composing the pregnant women group, 15,025 (35.4%)delivered by cesarean section. Of 14,902 (26% of all labors) pregnantwomen who were followed up in the perinatology clinic, 9215(61.8%) delivered by cesarean section. The hospital receives a highrate of multiparous case application (39.2%). The cesarean section isperformed in 99.8% of the patients with previous history of cesareansection. The rate of pregnant women who admitted for breech pres-entation was lower than expected, and the rate of cesarean section was96.8% for nulliparous breech presentations and 88.6% for multi-parous breech presentations. The rate of pregnant women whoadmitted for multiple pregnancy was 6.1%, and the rate of cesareansection for these cases was 90.1%. The rate of pregnant women whowere followed up in the perinatology clinic, admitted for various rea-sons, particularly for preeclampsia, and had preterm labor was 25.1%,and the rate of cesarean section for these cases was 66.1%. Conclusion: The cesarean rates associated with perinatology clin-ic/tertiary center are much higher. In order to keep the rates of pri-mary cesarean section within reasonable levels, the practices of per-sistent labor induction should be avoided, cesarean section shouldnot be recommended for tubal ligation procedure, and externalcephalic version should be tried in breech presentation cases inappropriate patients.

Keywords: Robson Ten-Group Classification System, perinatol-ogy/tertiary clinic.

ORCID ID: H. K›yak 0000-0001-7580-9179; G. Bolluk 0000-0002-3506-6806; E. Canaz 0000-0002-2047-548X; S. Yüksel 0000-0003-3773-4107; A. Gedikbafl› 0000-0002-4727-0310

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IntroductionThe cesarean section is defined as the delivery of fetuswith the help of abdominal and uterine incisions, and itsapplication is recommended only when there areincreased morbidity and mortality risks for mother and/orfetus during vaginal delivery.[1,2] The World HealthOrganization (WHO) indicated ideal rate of cesarean sec-tion as 10–15% in 1985; however, cesarean section is oneof the most common surgical procedures in the world.[3,4]

According to the data of the WHO, Turkey is among thecountries which have the highest rates of cesarean sectionin the world, and the rates of cesarean section increasedfrom 7% to 53% between 1993 and 2015.[5,6]

Repeating cesarean section, dystocia, fetal distress andabnormal fetal presentation have been reported as themost common indications for cesarean section.[7]

Moreover, increased labor induction, the use of electron-ic fetal monitor becoming prevalent and the suboptimalevaluation, first labors being at more advanced ages,decreased practice of labor induction in preeclampticpregnant women, increased use of assisted reproductiontechnologies and the multiple pregnancies accordingly,performing cesarean section in all breech presentationcases, not preferring vaginal delivery after cesarean sec-tion and the difficulty of follow-up, fear of vaginal deliv-ery in young pregnant women as a social indication,decreased use of forceps and vacuum, the pressure creat-ed on obstetricians due to medicolegal issues that mayarise in association with the operative labor are amongthe other reasons contributing to the increased rates ofindications and cesarean section.[2,5,7–9]

With the proposal of the Turkish Ministry of Health,“Robson Ten-Group Classification System” (Robson’sTGCS) has being used in obstetrics clinics since May2012.[10] In this system, the women are classified in tendifferent groups based on 5 basic labor characteristicsindependent of each other: parity (nulliparous, multi-parous, previous history of cesarean section), onset of thelabor (spontaneous, induced, cesarean section before thelabor), duration of pregnancy (preterm, term), numberof fetus (singleton, multiple), and fetal presentation(head, breech, transverse). While this classificationenables the simple, safe and clinically significant evalua-tion of every woman who admits for labor, it also makesit possible to inter- and intra-group comparisons of therates of cesarean section.[11] With the current version,Robson’s TGCS is a clinical obstetric evaluation, and thegroups are evaluated independent from each other.

On the other hand, when clinical experience andpatient variety are evaluated together, differences can beobserved among various hospitals and clinics, and it isalso possible to see various clinical practices due to thedifferent approaches of different clinics in the samedepartment. Despite the idealized labor rates, the inclu-sion of high risk pregnancies in the patient cohort withthe presence of a separate perinatology clinic within thedepartment leads to the expectation of an increase in therates of cesarean section. There are a limited number ofliterature findings on Robson data associated with differ-ent clinic and patient groups. Our purpose in this studyis to evaluate the impact of differences between obstet-rics clinics and perinatology clinics on Robson’s TGCSas well as the data of obstetrics training clinic in our hos-pital which provides intensive service, and to see itsreflection on labor outcomes.

MethodsAlthough Robson criteria have been recorded in our hos-pital since 2012 upon the instructions of the Ministry ofHealth, relevant data have been recorded regularly since2015 after the digitalization of these records in 2014 andtraining the personnel who were responsible for record-ing procedures (Table 1). For the procurement of digitaldata, the pregnant women in the data system of the hos-

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Table 1. Robson’s Classification System.

Groups Description

Group 1 Nulliparous women with a single cephalic pregnancy, ≥37 weeks of gestation in spontaneous labor

Group 2 Nulliparous women with a single cephalic pregnancy at term who either had labor induced or were delivered by cesarean section before labor

Group 3 Multiparous women without a previous uterine scar, with a single cephalic pregnancy, ≥37 weeks of gestation in spontaneous labor

Group 4 Multiparous women without a previous uterine scar, with a single cephalic pregnancy, ≥37 weeks of gestation who either had labor induced or were delivered by cesarean section before labor

Group 5 Multiparous women with at least one previous uterine scar, with a single cephalic pregnancy, ≥37 weeks of gestation

Group 6 Nulliparous women with a single breech pregnancy

Group 7 Multiparous women with a single breech pregnancy, including women with previous uterine scars

Group 8 All multiple pregnancies, including those with previous uterine scars

Group 9 All women with a single pregnancy with a transverse or oblique presentation, including women with previous uterine scars

Group 10 All women with a single cephalic pregnancy, <37 weeks of gestation, including women with previous scars

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pital were classified in two groups according to the outpa-tient clinics that they were followed up and the clinic theywere hospitalized (Pregnancy group and Perinatologygroup), and their clinic origins were reviewed. In this way,all data of obstetrics clinic, Pregnancy group andPerinatology group were obtained separately and in anaggregated form for each year (2015–2019).

This study is the retrospective review of the hospitaldata, and the records for the labors carried out in theobstetrics and perinatology clinics of the hospitalbetween 01.01.2015 and 30.06.2019 were reviewed. Theassessment of the study protocol and the approval wereconducted by the local ethics committee of the hospital.

The WHO published Robson Classification:Implementation Manual in 2017, and provided somerecommendations about the implementation.[12] Theserecommendations about cesarean section and popula-tion data were applied to the sub-groups of Robsonand given in Table 2.

While problem-free pregnancies were followed upin obstetrics clinic, high risk pregnancies were followedup in perinatology outpatient clinics of the perinatol-ogy clinic and the perinatology service when necessary.However, the hospitalization for labor and the deliver-ies of all these patients were carried out in the samedelivery rooms and operating rooms. Accordingly, theadmission and hospitalization of pregnant women wereconducted in two ways:• The pregnant women who were monitored in preg-

nancy outpatient clinics and hospitalized afteractive labor or referred to the hospital for the firsttime under emergency conditions due to differentreasons; the hospitalization of both groups are con-ducted through emergency obstetrics clinic.

• The pregnant women with perinatology record;they are the pregnant women for whom delivery isdecided due to maternal or fetal indications whenthey are hospitalized in the perinatology unit orthose followed up in perinatology outpatient clinicand delivered in the hospital in due course.In line with the recommendations of the WHO and

FIGO in 2016, the rates of the data were recalculatedto see their contribution on their own weightings andthe rates of cesarean section.[12,13] In accordance withthe recommendations, the groups, the numbers ofcesarean section in the group, the total number ofwomen who gave birth in the group, size of thesegroups compared to the available population, intra-

group cesarean section rates, and actual and relativecontributions of the group to the total rate of cesareansection were determined for the patients of Robson’sTGCS in 7 separate columns. After the total data ofobstetrics clinic were obtained, the data of the preg-nancy group and perinatology group were also deter-mined as indicated above. These data were evaluatedfor all patients of obstetrics clinic and pregnancy andperinatology groups in accordance with the recom-mendations and comments given in Table 2.

Unfortunately, primary cesarean section rates,which are one of the data requested by the Ministry ofHealth, cannot be calculated by these tables establishedaccording to the Robson’s TGCS. Since nulliparousand multiparous pregnancy groups are different thaneach other, both groups cannot be evaluated togetherin Robson’s TGCS. We calculated them separatelyand presented their results.

We paid attention to the confidentiality of the per-sonal data of the patients during pre-investigationalstudy. In the data analysis, the qualitative variableswere summarized in numbers and percentages.

ResultsDuring the review of the data system, it was found thata total of 57,402 deliveries were carried out in ‹stanbulKanuni Sultan Süleyman Training and ResearchHospital between 01.01.2015 and 30.06.2019. In termsof the data record by years, a proper classification couldnot be made for 40 pregnant women in 2015, 4 pregnantwomen in 2016, 1 pregnant woman in 2017, and 2 preg-nant women in 2018. The classification of these patientswas not taken into consideration during the calculations.Similarly, it was reported that the failure of classificationmight occur.[12]

A total of 24,240 (42.2%) out of 57,402 labors werecarried out by cesarean section in the hospital during therelevant period. All data and cesarean section rates of thegroups of entire obstetrics clinic are given by years inTable 3. After pregnancy clinic / outpatient clinic andperinatology clinic were distinguished, it was seen that15,025 (35.4%) of 42,500 deliveries (74% of all deliver-ies) in pregnancy outpatient clinic were carried out bycesarean section (the rates of relevant group were given inTable 4), and 9215 (61.8%) of 14,902 pregnant women(26% of all deliveries) who were hospitalized throughperinatology clinic delivered by cesarean section (therates of relevant group were given in Table 5).

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Table 2. WHO’s Robson recommendations – Population interpretations and recommendations for the rates of cesarean section (Summarizedand edited according to the reference 12).

Type of population

Groups Recommendation Interpretation CS recommendation (Column 5)

Group 1: nulliparous normal It represents 35–42% A lower ratio indicates high Rates under 10% are achievablelabor, ≥37 of the pregnancies induction / cesarean section This rate can be interpreted properly

before labor starts; it shows when size rates of Groups 1 and increased rate of cesarean 2 are considered. section due to the presence of high risk population

Group 2: nulliparous ind/cs The ratio of Group 1/ If it is high, it means that we did Consistently around 20–35%Group 2 should be 2:1 not induced sufficiently.

Group 3: multiparous It represents 30% of the The reason for low rates of Groups Not higher than 3% normally normal labor, ≥37 total pregnancies 3 and 4 may be the high rates in In units with higher rates, this may

Group 5 and the accompanying be due to poor data collection or high rates of cesarean section. requesting tubal ligation.

Group 4: multiparous The ratio of Group 3/ A lower rate may indicate the It is rarely higher than 15% ind/cs, ≥37 Group 4 should be higher cesarean section before labor in A high rate of cesarean section in

than the ratio of Group 1/ multiparous women, or the cesarean Group 4 may reflect a high maternal Group 2 section before labor due to tubal request for cesarean section even

ligation. if these women have delivered their first pregnancy vaginally, or being able to do tubal ligation.

Group 5: cs, ≥37 The size is roughly half of If the Group is big, it means that Rates of 50–60% are considered the total cesarean section Groups 1 and 2 in particular have appropriate provided you have rate in general high rates of cesarean section good maternal and perinatal

in previous years. outcomes.

The size of this group may be >15% If the rates are higher, this is possiblyin settings with high rates of due to a larger group of women with cesarean section. 2 or more previous cesarean section

or due to a policy of scheduling pre-labor cesarean section for all women with 1 previous scar without attempting a trial of labor.

Group 6: nulliparous breech The total should be 3–4% If the total is over 4%, the reason is presentation usually a high rate of preterm deliveries

or a higher proportion of nulliparous women. If the size of Group 10 is above 4–5%, then this hypothesis is correct.

Group 7: multiparous breech The ratio of Group 6/Group If the rate is different, there is an presentation, cs 7 should be 2:1 unexpected ratio of nulliparous/mu

ltiparous women.

Group 8: multiple It should be 1.5–2% If it is higher, the hospital is probably It is usually around 60%.pregnancy, cs a tertiary center. The variations will depend on the type

If it is lower, probably the majority of the of twin pregnancy, previous history

twin pregnancies twins are referred out of cesarean section and the ratioof nulliparous/multiparous women

Group 9: Transverse, cs It should be less than 1% It should be 100%; if the woman gives birth vaginally by internal version, it should be classified as either cephalic or breech presentation

Group 10: preterm labor, It should be less than 5% If it is higher, the hospital is It is usually around 30% in the <37, cs in normal risky settings probably a tertiary center. most populations

If the rate of cesarean section is high, If it is higher than 30%, it is usually dueit may suggest pre-labor cesarean to the cases of high risk pregnanciessection due to fetal growth restriction (e.g. fetal growth restriction,or preeclampsia and other complications. preeclampsia) that will need preterm

pre-labor cesarean section

cs: Including previous cesarean section; ind: including those underwent induction; ≥≥37: 37 weeks of gestation and above; <<37: less than 37 weeks of gestation

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Table 3. The labor data of all Obstetrics Clinic (Pregnancy Outpatient Clinics and Perinatology Clinic) according to the Robson’s Ten-Group Classi-fication System.

Column 1 Column 2 Column 3 Column 4 Column 5 Column 6 Column 7

CS Number of women Group size The actual contribution The relative contributionRobson number who delivered in according to the Intra-group of the group to the of the group to the

Year groups of group the group population (%) CS rate (%) total rate of CS (%) total rate of CS (%)

2015 1 579 2944 21.4 19.7 4.1 10.12 325 542 3.9 60.0 2.3 5.53 619 4810 34.9 12.9 4.4 10.74 168 280 2.0 60.0 1.2 2.85 2263 2266 16.6 99.9 16.4 39.56 147 150 1.0 98.0 1.1 2.47 152 159 1.1 95.6 1.1 2.58 302 336 2.4 89.9 2.1 5.19 15 16 0.1 93.8 0.1 0.210 1218 2266 16.6 53.8 8.8 21.2

Total 5728 13,769 100.0 41.6 41.6 100.0

2016 1 778 3268 22.9 23.8 5.4 12.92 45 188 1.3 23.9 0.3 0.73 665 5150 36.0 12.9 4.7 11.14 25 124 0.9 20.2 0.2 0.45 2825 2827 19.8 99.9 19.8 47.06 143 151 1.1 94.7 1.0 2.47 91 97 0.7 93.8 0.6 1.58 310 357 2.5 86.8 2.2 5.29 5 5 0.1 100.0 0.0 0.110 1121 2129 14.9 52.7 7.8 18.7

Total 6008 14,296 100.0 42.0 42.0 100.0

2017 1 536 2536 20.6 21.1 4.4 10.62 33 67 0.5 49.3 0.3 0.63 612 4988 40.6 12.3 5.0 12.14 4 32 0.3 12.5 0.1 0.15 2329 2332 19.0 99.9 18.9 46.16 78 83 0.7 94.0 0.6 1.57 66 89 0.7 74.2 0.5 1.38 273 335 2.7 81.5 2.2 5.49 2 2 0.1 100.0 0.0 0.110 1119 1830 14.9 61.1 9.1 22.2

Total 5052 12,294 100.0 41.1 41.1 100.0

2018 1 668 2456 20.9 27.2 5.7 13.42 29 45 0.4 64.4 0.2 0.63 504 4838 41.1 10.4 4.3 10.14 21 52 0.4 40.4 0.2 0.45 2611 2619 22.2 99.7 22.2 52.56 117 119 1.0 98.3 1.0 2.47 61 71 0.6 85.9 0.5 1.28 291 337 2.9 86.4 2.5 5.99 13 13 0.1 100.0 0.1 0.310 655 1225 10.4 53.5 5.6 13.2

Total 4970 11,775 100.0 42.2 42.2 100.0

2019 1 418 1196 22.7 34.9 8.0 17.22 1 7 0.1 14.3 0.0 0.03 317 2193 41.6 14.5 6.0 13.14 0 6 0.1 0.0 0.0 0.05 1225 1226 23.3 99.9 23.3 50.66 51 51 1.0 100.0 1.0 2.17 36 42 0.8 85.7 0.7 1.58 157 175 3.3 89.7 3.0 6.59 9 9 0.2 100.0 0.2 0.410 208 363 6.9 57.3 3.9 8.6

Total 2422 5268 100.0 46.0 46.0 100.0

The period 1 2979 12,400 21.6 24.0 5.2 12.3between 2 433 849 1.5 51.0 0.8 1.801.01.2015 3 2717 21,979 38.3 12.4 4.7 11.2and 4 218 494 0.9 44.1 0.4 0.930.06.2019 5 11,253 11,270 19.6 99.8 19.6 46.4

6 536 554 1.0 96.8 0.9 2.27 406 458 0.8 88.6 0.7 1.78 1333 1540 2.7 86.6 2.3 5.59 44 45 0.1 97.8 0.1 0.210 4321 7813 13.6 55.3 7.5 17.8

Total 24,240 57,402 100.0 42.2 42.2 100.0

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Table 4. The labor data of Pregnancy clinics according to the Robson’s Ten-Group Classification System.

Column 1 Column 2 Column 3 Column 4 Column 5 Column 6 Column 7

CS Number of women Group size The actual contribution The relative contribution Robson number who delivered according to the Intra-group of the group to the of the group to the

Year groups of group in the group population (%) CS rate (%) total rate of CS (%) total rate of CS (%)

2015 1 380 2430 23.8 15.6 3.8 10.62 155 291 2.8 53.3 1.5 4.33 377 4038 39.5 9.3 3.7 10.54 89 122 1.2 73.0 0.9 2.55 1691 1694 16.6 99.8 16.5 47.16 109 110 1.1 99.1 1.1 3.07 105 112 1.1 93.8 1.0 2.98 90 103 1.0 87.4 0.9 2.59 10 11 0.1 90.9 0.1 0.310 586 1319 12.9 44.4 5.7 16.3

Total 3592 10,230 100.0 35.1 35.1 100.0

2016 1 519 2762 25.0 18.8 4.7 13.22 16 99 0.9 16.2 0.1 0.43 427 4436 40.2 9.6 3.9 10.84 8 61 0.6 13.1 0.1 0.25 2183 2185 19.8 99.9 19.8 55.46 84 88 0.8 95.5 0.8 2.17 58 63 0.6 92.1 0.5 1.58 145 174 1.6 83.3 1.3 3.79 4 4 0.0 100.0 0.0 0.110 498 1172 10.6 42.5 4.6 12.6

Total 3942 11,044 100.0 35.7 35.7 100.0

2017 1 334 2045 22.4 16.3 3.6 10.62 12 25 0.3 48.0 0.1 0.43 381 4145 45.4 9.2 4.1 12.14 1 7 0.1 0.1 0.0 0.05 1741 1744 19.1 99.8 19.1 55.46 48 50 0.5 96.0 0.5 1.57 50 69 0.8 72.5 0.5 1.68 102 140 1.5 72.9 1.1 3.39 2 2 0.0 100.0 0.2 0.010 475 905 9.9 52.5 5.2 15.1

Total 3146 9132 100.0 34.5 34.5 100.0

2018 1 391 1818 21.7 21.5 4.6 13.22 20 31 0.4 64.5 0.2 0.73 303 3951 47.0 7.7 3.6 10.34 15 37 0.4 40.5 0.2 0.55 1763 1771 21.1 99.5 21.0 59.66 62 63 0.7 98.4 0.7 2.17 46 52 0.6 88.5 0.5 1.68 115 143 1.7 80.4 1.4 3.99 8 8 0.1 100.0 0.1 0.310 233 538 6.4 43.3 2.8 7.8

Total 2956 8412 100.0 35.1 35.1 100.0

2019 1 224 849 23.1 26.4 6.1 16.12 1 6 0.2 16.7 0.0 0.03 178 1742 47.3 10.2 4.8 12.84 0 2 0.1 0.0 0.0 0.05 802 803 21.8 99.9 21.8 57.76 30 30 0.8 100.0 0.8 2.27 24 28 0.8 85.7 0.7 1.88 65 74 2.0 87.8 1.8 4.79 8 8 0.2 100.0 0.2 0.610 57 140 3.8 40.7 1.5 4.1

Total 1389 3682 100.0 37.7 37.7 100.0

The period 1 1848 9904 23.3 18.7 4.4 12.3between 2 204 452 1.1 45.1 0.5 1.401.01.2015 3 1666 18,312 43.1 9.1 3.9 11.1and 4 113 229 0.5 49.3 0.3 0.830.06.2019 5 8180 8197 19.3 99.8 19.2 54.4

6 333 341 0.8 97.7 0.8 2.27 283 324 0.8 87.3 0.7 1.98 517 634 1.5 81.5 1.2 3.49 32 33 0.1 97.0 0.1 0.210 1849 4074 9.6 45.4 4.4 12.3

Total 15,025 42,500 100.0 35.4 35.4 100.0

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Tablo 5. The labor data of Perinatology patients according to the Robson’s Ten-Group Classification System.

Column 1 Column 2 Column 3 Column 4 Column 5 Column 6 Column 7

CS Number of women Group size The actual contribution The relative contribution Robson number who delivered according to the Intra-group of the group to the of the group to the

Year groups of group in the group population (%) CS rate (%) total rate of CS (%) total rate of CS (%)

2015 1 199 514 14.5 38.7 5.7 9.12 170 251 7.1 67.7 4.8 7.73 242 772 21.8 31.3 6.8 11.04 79 158 4.5 50.0 2.2 3.65 572 572 16.2 100.0 16.2 26.16 38 40 1.1 95.0 1.1 1.77 47 47 1.3 100.0 1.3 2.18 212 233 6.6 91.0 6.0 9.79 5 5 0.1 100.0 0.1 0.210 632 947 26.8 66.7 17.9 28.8

Total 2196 3539 100.0 62.1 62.1 100.0

2016 1 259 506 15.6 51.2 8.0 12.52 29 89 2.8 32.6 0.9 1.43 238 714 22.0 33.3 7.3 11.54 17 63 1.9 27.0 0.5 0.85 642 642 19.7 100.0 19.7 31.16 59 63 1.9 93.7 1.8 2.97 33 34 1.0 97.1 1.0 1.68 165 183 5.6 90.2 5.1 8.09 1 1 0.0 100.0 0.0 0.010 623 957 29.4 65.1 19.2 30.2

Total 2066 3252 100.0 63.5 63.5 100.0

2017 1 202 491 15.5 41.1 6.4 10.62 21 42 1.3 50.0 0.7 1.13 231 843 26.7 27.4 7.3 12.14 3 25 0.8 12.0 0.1 0.25 588 588 18.6 100.0 18.6 30.86 30 33 1.0 90.9 0.9 1.67 16 20 0.6 80.0 0.5 0.88 171 195 6.2 87.7 5.5 9.09 0 0 0.0 0.0 0.0 0.010 644 925 29.3 69.6 20.4 33.8

Total 1906 3162 100.0 60.3 60.3 100.0

2018 1 277 638 19.0 43.4 8.2 13.82 9 14 0.4 64.3 0.3 0.43 201 887 26.4 22.7 6.0 10.04 6 15 0.4 40.0 0.2 0.35 848 848 25.3 100.0 25.2 42.16 55 56 1.7 98.2 1.6 2.77 15 19 0.6 78.9 0.4 0.78 176 194 5.8 90.7 5.2 8.89 5 5 0.1 100.0 0.1 0.210 422 687 20.4 61.4 12.6 21.0

Total 2014 3363 100.0 59.9 59.9 100.0

2019 1 194 347 21.9 55.9 12.2 18.82 0 1 0.1 0.0 0.0 0.03 139 451 28.4 30.8 8.8 13.54 0 4 0.3 0.0 0.0 0.05 423 423 26.7 100.0 26.7 40.96 21 21 1.3 100.0 1.3 2.07 12 14 0.9 85.7 0.8 1.28 92 101 6.4 91.1 5.8 8.99 1 1 0.1 100.0 0.1 0.110 151 223 14.1 67.7 9.5 14.6

Total 1033 1586 100.0 65.1 65.1 100.0

The period 1 1131 2496 16.8 45.3 7.6 12.3between 2 229 397 2.7 57.7 1.5 2.501.01.2015 3 1051 3667 24.6 28.7 7.1 11.4and 4 105 265 1.8 39.6 0.7 1.130.06.2019 5 3073 3073 20.6 100.0 20.6 33.3

6 203 213 1.4 95.3 1.4 2.27 123 134 0.9 91.8 0.8 1.38 816 906 6.1 90.1 5.5 8.99 12 12 0.1 100.0 0.1 0.110 2472 3739 25.1 66.1 16.6 26.9

Total 9215 14,902 100.0 61.8 61.8 100.0

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These total data for 4.5 years were evaluated sepa-rately and in an aggregated form, and the data and calcu-lated rates of total, Pregnancy group and PerinatologyGroup of the obstetrics clinic were compared with thesummarized rates and the data given in Table 2 for theWHO’s Robson’s TGCS (Table 6).

However, the primary cesarean section rates (per-forming cesarean section to pregnant women for the firsttime regardless of nulliparous or multiparous pregnan-cy), which are requested from the hospitals regularly bythe Turkish Health Ministry, cannot be calculatedaccording to the Robson’s TGCS. According to the dataobtained from the statistics unit of the hospital for theyears 2015, 2016, 2017, 2018 and first 6 months of 2019,the primary cesarean section rates of the hospital were20.1%, 19.0%, 16.2%, 16.7% and 20.0%, respectively.

As seen in Table 6, it was found that more multi-parous pregnant women admitted to the hospital thanthe expected rates of nulliparous/multiparous pregnantwomen. It is seen for each group that the rates of Group1 and Group 2 involving nulliparous pregnancies arehighly above the ratio of 2:1 by years. The results of thecesarean section rates in Group 1 and Group 2 for allpregnant women of Obstetrics clinic, Pregnancy clinic

and Perinatology clinic were 24.0% and 51.0%, 18.7%and 45.1%, and 45.3% and 57.7%, respectively.

It is seen in the Obstetrics and Pregnancy groups thatthe rates of Group 3 and Group 4 patients involvingmultigravida pregnancies are higher than the expected.On the other hand, the admission rate of 26.4% wasachieved in the Perinatology group, which is below thetotal rate of 30% expected from these two groups. It wasseen in all groups that the cesarean rates were highlyabove the targeted rates which were 3% for Group 3 and15% for Group 4.

It is understood through the data that the rates ofpatients who constitute Group 5 and had cesarean sec-tion or uterine incision previously are about 19–20% forall groups and that the cesarean section was performed inalmost all pregnant women who admitted with the histo-ry of previous cesarean section.

However, the admission rates of Group 6 constitutedby breech presentation cases and involving nulliparouscases and Group 7 involving multiparous cases were farbelow the recommended rate of 3–4% and the ratio ofthese groups was lower than 2:1. It was found that therates of cesarean section were 96.8%, 97.7% and 95.3%

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Table 6. The results of Obstetrics, Pregnancy and Perinatology groups according to the recommendations.

WHO Total data of Pregnancy Perinatology Criteria recommendations Obstetrics Clinic clinic clinic

Group 1 / Group 2 Total 35–42% 23.1% 24.4% 19.4%Ratio 2:1 14.6 21.9 6.3

Group 1 CS rate 10% 24.0% 18.7% 45.3%

Group 2 CS rate 20–35% 51.0% 45.1% 57.7%

Group 3 / Group 4 Total 30% 39.2% 43.6% 26.4%Ratio >2:1 44.5 80 13.8

Group 3 CS rate <3% 12.4% 9.1% 28.7%

Group 4 CS rate <15% 44.1% 49.3% 39.6%

Group 5 Size 15% 19.6% 19.3% 20.6%CS rate 50–60% 99.8% 99.8% 100%

Group 6 / Group 7 Total 3–4% 1.8% 1.6% 2.3%Ratio 2:1 1.2 1.1 1.6

Group 6 CS rate 4% 96.8% 97.7% 95.3%

Group 7 CS rate 4% 88.6% 87.3% 91.8%

Group 8 Size 1.5–2% 2.7% 1.5% 6.1%CS rate 60% 86.6% 81.5% 90.1%

Group 9 Size <1% 0.1% 0.1% 0.1%CS rate 100% 97.8% 97.0% 100%

Group 10 Size <5% 13.6% 9.6% 25.1%CS rate 30% 55.3% 45.4% 66.1%

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for Group 6 and 88.6%, 87.3% and 91.8% for Group 7,respectively.

Group 8 involves multiple pregnancies and the ratesin Pregnancy group are consistent with those recom-mended by the WHO; however, it is seen that the rate of6.1% in the Perinatology group impacts the total rate andtotal group rate is 2.7%. Again, all groups have higherrates of cesarean section than the desired cesarean sectionrate of 60%, and it was 86.6%, 81.5% and 90.1% forObstetrics, Pregnancy and Perinatology groups, respec-tively.

The rates of cesarean section for all three groupswere found 97.8%, 97% and 100% due to the rates givenin the data of 2015, which was the first year when Group9 was evaluated in terms of transverse presentation. Theresults are as they should be except the data of 2015, andall rates of other years are 100%.

Although targeted group size was <5% in Group 10which has admission difference due to high risk pregnan-cies and in which preterm pregnant women that causedeviations from the recommendations of the WHO ingeneral are evaluated, the admission rates for Obstetrics,Pregnancy and Perinatology groups were 13.6%, 9.6%and 25.1%, respectively. Also, the rates of 55.3%, 45.4%and 66.1% were found for these groups which werehighly above the targeted rate of 30% for cesarean sec-tion. With these data, it was seen that the hospital doesnot only serve to the pregnant women who need to havepreterm labor through Perinatology clinic, but alsothrough the delivery room where many pregnant womenneed to have preterm labor due to various reasons.

DiscussionRobson’s TGCS helps to classify every pregnant womanwho admits for labor in one of the 10 groups which arecompletely inclusive in a way not involving in two differ-ent but correct conditions simultaneously. This uniformcoding system provides a strict quality control system forcomplications by determining specific and diagnosticcriteria for the complications.[12] Our study is the secondstudy in Turkey about a tertiary center.[14] Yet, in our lit-erature review, we found a limited number of data onthe use of Robson’s TGCS in the tertiary centers in theworld.[15–22] We found only 2 of these studies[15,16] that thelabor data between tertiary centers and secondary deliv-ery units were evaluated in terms of Robson’s TGCS.

The study data and the relevant results are affectedhighly by the population and clinical variety of the preg-nant women who admitted to the hospital. Therefore, afollow-up systematic has been developed by a perinatol-ogy clinic or tertiary center for high risk pregnancies interms of both fetal and maternal aspects. In this way, theneed of finalizing pregnancy by vaginal delivery as a nat-ural method or by cesarean section due to compulsoryreasons varies depending on the clinical condition and itis seen that cesarean section is performed more fre-quently in tertiary centers having perinatology units.[15,16]

The perinatology unit of our hospital serves as an inten-sive care unit, and approximately one fourth of all cases(26%) are treated and deliver in this unit. When wereviewed the study results, we found differences amongthe groups in terms of Robson’s TGCS; the general rateof cesarean section in the perinatology unit of our hos-pital was 61.8% while it was 35.4% in the Pregnancygroup, and the mean of our total clinic data which wasthe common result of these two groups was 42.2%.

We also found that the numbers and rates of nulli-parous and multiparous pregnant women who admittedto the hospital were different than the values providedby the WHO. While the mean values given by theWHO as example were 35–42% for primigravida casesand 30% for multigravida cases, they were quite theopposite for our hospital data, and it was 23.1% forprimigravida cases and 39.2% for multigravida cases. Inthe sub-group analysis, the mean admission rates forprimigravida and multigravida cases were 24.4% and43.6% in the Pregnancy group and 19.4% and 26.4% inthe Perinatology group, respectively. With these rates,the rate of multigravida patients admitting to the perina-tology unit is at an acceptable level. However, in twoprevious studies evaluating Robson’s TGCS data inTurkey reported that the rates were consistent withthose recommended by the WHO.[14,23] In this respect, itcan be thought that many primigravida pregnant womenwould like to have their labors in private centers due tomany social factors in Turkey or in the region that thehospital is located in a narrow perspective.[24,25] However,it is seen that the rates of cesarean section are high inGroups 1–4 which involve primigravida and multigravi-da cases. WHO motions report that the decision forcesarean section instead of induction is made more easi-ly in primigravida cases, and therefore induction proce-dures should be focused on much more, and the decisionfor cesarean section is made more easily in multigravida

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cases due to the families’ request of tubal ligation.[12] TheWHO recommends evaluating the relative contribu-tions of Groups 1, 2 and 5 to general rate of cesareansection, because these three groups are responsible for2/3 (66%) of the cesarean section procedures in hospi-tals, and the focus should be on these three groups forthe efforts of decreasing general rate of cesarean sectionin hospitals. In fact, the higher the general rate ofcesarean rate is, the more focus should be on Group 1.[26]

The group of pregnant women with the history ofprevious cesarean section (Group 5) is the group whichis an opportunity to decrease the rates of cesarean sec-tion in this regard. From this aspect, the WHO predictsthe rate of cesarean section 50–60% in a group with asize of 15% approximately. However, some factors suchas the number of previous cesarean section, the type ofuterine incision performed previously, week of gesta-tion, the presence of multiple pregnancy and maternalobesity are the significant limitations for the vaginallabor after cesarean section. Taking these factors intoconsideration and following up the labor under appro-priate conditions and in the environments prepared inadvance are the important necessities.[27] With regard toour study, the lack of relevant practices in the obstetricsunit and delivery room can be expressed as a significantissue; however, it is important that the patients haveappropriate conditions and the pregnant women arewilling to participate. Besides, a majority of the pregnantwomen who admit to the hospital having two or morecesarean section and the hospital being a referral centerfor placenta previa and placenta percreta cases can beshown as the reasons for the cesarean section rate of99% for Pregnancy group and 100% for Perinatologygroup which are 19–20% in Group 5.

Interestingly, in consistent with our data, two otherstudies from Turkey[14,23] reported the admission rates ofpregnancies with breech presentation 3–4% lower thanthe recommended rates. Group 9, which had transverseand oblique presentations, had similar low rate.Cochrane reviews report that the pregnancies withbreech presentation have lower rates of perinatal/neona-tal mortality and morbidity by cesarean section.[28] Thismay explain the low rate of admission of the patients inthis group; pregnant women with breech presentationare delivered by a planned labor decision.[25] However,the societies in many countries recommend vaginaldelivery or cesarean section for the pregnancies withbreech presentation after trying external cephalic ver-

sion.[29] Eliminating the lack of this practice by trainingsthrough the societies can be a potential precaution.

In the hospital which is a reference center for multi-ple pregnancies constituting Group 8 and for Group 10involving preterm labors due to gestational complica-tions, the mean rate of hospital is 2.7% and it is 6.1% inthe perinatology unit for multiple pregnancies, and theyare 13.5% and 25.1% for preterm labors, respectively,which are higher than the rates recommended by theWHO. Similar high rates in both groups are also report-ed by other studies evaluating tertiary centers.[15,19,21]

However, we associated the high rates of Group 8 andGroup 10 with the rates of primary cesarean sectionwhich involve the cases with previous cesarean sectionand already high.

One of the limitations of our study is shift order inour hospital. Delivery room is a common area, andPregnancy and Perinatology groups do not have sepa-rate delivery rooms. One of the reasons for the highrates in the pregnancy group is considered that the peri-natology teams and experts working in the deliveryroom under shift conditions provide direct service toemergency pregnant women with high risk who admitto the hospital for the first time without any perinatol-ogy record and have their labors under emergency con-ditions. Besides, the lack of performance criteria accord-ing to the rates of cesarean section when providingdelivery service is also important.[30] Carrying out cesare-an section at high rates in pregnant women who areevaluated to be in the high risk pregnancy group in linewith the data and the literature is an expected condition.

ConclusionIt is important to evaluate the services provided by thehospital on different aspects and analyze the dataaccordingly. Therefore, except general obstetric data,the admitting patients and their results should be dis-tinguished in terms of the services of tertiary center,and perinatology results also should be presentedexcept general pregnancy data. The rate of cesareansection was 61.8% in the Perinatology group whichcontain all groups and 35.4% in the Pregnancy group.

In the studies for decreasing the hospital rates ofcesarean section, it is important to do different prepara-tions to decrease the impacts of Group 1 (nulliparouspatients with single pregnancy and head presentation),Group 2 (nulliparous patients with single pregnancy and

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head presentation, term, before labor) and Group 5(multiparous patients with at least one uterine scar andhead presentation, ≥37 weeks of gestation). These arethe practices for not to increase the rates of primarycesarean section such as being insistent for labor induc-tion before deciding cesarean section, not consideringtubal ligation as a facilitator indication for cesarean sec-tion indication and performing external cephalic versionin appropriate patients with breech presentation. Inaddition, providing appropriate conditions for vaginaldelivery after cesarean section is another possible prac-tice to decrease current rate of cesarean section.However, considering labor only as a medical practiceand procedure is not a proper and sufficient approach; itwill be the best to evaluate it within social, legal and sys-temic aspects in order to bring the approach and therates of cesarean section into the optimal limits.[31]

Conflicts of Interest: No conflicts declared.

References1. Cunningham FG, Leveno KJ, Bloom SL, Spong CY, Dashe

JS, Hoffman BL, et al. Cesarean section and postpartum hys-terectomy In: Williams obstetrics. 24th ed. NewYork:McGraw- Hill Education; 2014. p. 587–8.

2. T.C. Sa¤l›k Bakanl›¤› Ana Çocuk Sa¤l›¤› ve Aile Planlamas›Genel Müdürlü¤ü. Do¤um ve sezaryen eylemi yönetimrehberi. Ankara: Damla Matbaac›l›k; 2010.

3. WHO. Appropriate technology for birth. Lancet 1985;2:436–7.

4. Souza JP, Betran AP, Dumont A, De Mucio B, GibbsPickens CM, Deneux-Tharaux C, et al. A global referencefor caesarean section rates (C-Model): a multi country cross-sectional study. BJOG 2016;123:427–36.

5. Hacettepe Üniversitesi Nüfus Etütleri Enstitüsü. 2013Türkiye Nüfus ve Sa¤l›k Araflt›rmas›. Ankara: HacettepeÜniversitesi Nüfus Etütleri Enstitüsü, T.C. Kalk›nmaBakanl›¤› ve TÜB‹TAK; 2014. s. 150.

6. T.C. Sa¤l›k Bakanl›¤›. Sa¤l›k ‹statistikleri Y›ll›¤› 2015.Ankara: T.C. Sa¤l›k Bakanl›¤›; 2015. Retrieved from: www.sagem.gov.tr/dosyalar/SIY_2015.pdf

7. Mathai M, Hofmeyr GJ, Mathai NE. Abdominal surgicalincisions for caesarean section. Cochrane Database Syst Rev2013;(5):CD004453.

8. Begum T, Rahman A, Nababan H, Hoque DME, Khan AF,Ali T, et al. Indications and determinants of caesarean sec-tion delivery: evidence from a population-based study inMatlab, Bangladesh. PLoS One 2017;12:e0188074.

9. Betrán AP, Temmerman M, Kingdon C, Mohiddin A, OpiyoN, Torloni MR, et al. Interventions to reduce unnecessarycaesarean sections in healthy women and babies. Lancet 2018;392:1358–68.

10. T.C. Sa¤l›k Bakanl›¤›. Do¤um ve sezaryen eylemi yönetimrehberi. Ankara: T.C. Sa¤l›k Bakanl›¤›; 2010. Retrieved from:http://sbu.saglik.gov.tr/Ekutuphane/kitaplar/a%C3%A7sap27.pdf

11. Robson MS. Can we reduce the caesarean section rate? BestPract Res Clin Obstet Gynaecol 2001;15:179–94.

12. WHO. Robson classification: implementation manual.Geneva: WHO; 2017. Retrived from: https://www.who.int/reproductivehealth/publications/maternal_perinatal_health/robson-classification/en/

13. FIGO Working Group on Challenges in Care of Mothersand Infants During Labour and Delivery. Best practiceadvice on the 10-Group Classification System for cesareandeliveries. Int J Gynaecol Obstet 2016;135:232–3.

14. Cagan M, Tanacan A, Aydin Hakli D, Beksac MS. Changingrates of the modes of delivery over the decades (1976, 1986,1996, 2006, and 2016) based on the Robson-10 group classifi-cation system in a single tertiary health care center. J MaternFetal Neonatal Med 2019:1–8.

15. Ono T, Matsuda Y, Sasaki K, Satoh S, Tsuji S, Kimura F, etal. Comparative analysis of cesarean section rates usingRobson Ten-Group Classification System and Lorenz curvein the main institutions in Japan. J Obstet Gynaecol Res 2016;42:1279–85.

16. Gerli S, Favilli A, Franchini D, De Giorgi M, Casucci P,Parazzini F. Is the Robson’s classification system burdened byobstetric pathologies, maternal characteristics and assistentiallevels in comparing hospitals cesarean rates? A regional analy-sis of class 1 and 3. J Matern Fetal Neonatal Med 2018;31:173–7.

17. Guida JP, Pacagnella RC, Costa ML, Ferreira EC, Cecatti JG.Evaluating vaginal-delivery rates after previous cesarean deliv-ery using the Robson 10-group classification system at a terti-ary center in Brazil. Int J Gynaecol Obstet 2017;136:354–5.

18. Triunfo S, Ferrazzani S, Lanzone A, Scambia G. Identificationof obstetric targets for reducing cesarean section rate using theRobson Ten Group Classification in a tertiary level hospital.Eur J Obstet Gynecol Reprod Biol 2015;189:91–5.

19. Tan JK, Tan EL, Kanagalingan D, Tan LK. Rational dissec-tion of a high institutional cesarean section rate: an analysisusing the Robson Ten Group Classification System. J ObstetGynaecol Res 2015;41:534–9.

20. Ferreira EC, Pacagnella RC, Costa ML, Cecatti JG. TheRobson ten-group classification system for appraising deliver-ies at a tertiary referral hospital in Brazil. Int J GynaecolObstet 2015;129:236–9.

21. Abdel-Aleem H, Darwish A, Abdelaleem AA, Mansur M.Usefulness of the WHO C-Model to optimize the cesareandelivery rate in a tertiary hospital setting. Int J Gynaecol Obstet2017;137:40–4.

22. Hanson C, Betrán AP, Opondo C, Mkumbo E, Manzi F,Mbaruku G, et al. Trends in caesarean section rates between

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Page 58: ISSN 1305–3124 JOURNAL PERINATAL · Ahmet Yal›nkaya,Diyarbak›r, Turkey Jun Yoshimatsu, Osaka, Japan Emre Zafer, Ayd›n, Turkey Yaron Zalel, Tel Aviv, Israel Ivica Zalud, Honolulu,

2007 and 2013 in obstetric risk groups inspired by the Robsonclassification: results from population-based surveys in a low-resource setting. BJOG 2019;126:690–700.

23. Erkal Aksoy Y, Sert E, Er, M, Öztrük Can H. Robson OnGruplu S›n›fland›rma Sistemine göre sezaryen do¤umlar›nincelenmesi. Uluslararas› Hakemli Hemflirelik Araflt›rmalar›Dergisi (UHD) 2015;(3):17–25

24. Süzer Özkan F, Demirci N. Factors affecting delivery pref-erence of primigravida women: a qualitative study. TurkiyeKlinikleri Journal of Nursing Science 2018;10:103–14.

25. Sar›kaya E (Ed.). Do¤um flekli tercihinin multidisipliner irdelen-mesi çal›fltay kitap盤›. Ankara: TACESE; 2017. Retrieved from:https://www.tuseb.gov.tr/uploads/tacese_calistay_kitapcigi.pdf

26. Robson M, Hartigan L, Murphy M. Methods of achievingand maintaining an appropriate caesarean section rate. BestPract Res Clin Obstet Gynaecol 2013;27:297–308.

27. ACOG Practice Bulletin No. 205: Vaginal birth after cesare-an delivery. Obstet Gynecol 2019;133:e110–e127.

28. Hofmeyr GJ, Hannah M, Lawrie TA. Planned caesareansection for term breech delivery. Cochrane Database SystRev 2015;(7):CD000166.

29. Tsakiridis I, Mamopoulos A, Athanasiadis A, Dagklis T.Management of breech presentation: a comparison of fournational evidence-based guidelines. Am J Perinatol 2019 Jun5. doi:10.1055/s-0039-1692391

30. Singh R, Nath Trivedi A. Is the caesarean section rate a per-formance indicator of an obstetric unit? J Matern FetalNeonatal Med 2011;24:204–7.

31. Türk Perinatoloji Derne¤i. Do¤um eylem plan› 2019–2023.‹stanbul: Türk Perinatoloji Derne¤i; 2019. Retrieved from:http://cdn.perinatal.org.tr/files/TPD/sezeryan_TPD%20gorusu_2019.pdf

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Seasonal change of the prevalence of hypertensivedisorders of pregnancy

Cuma Tafl›n1 , K›v›lc›m Bektafl2

1Department of Gynecology and Obstetrics, Faculty of Medicine, Mersin University, Mersin, Turkey 2Gynecology and Obstetrics Clinic, Mardin K›z›ltepe State Hospital, Mardin, Turkey

İDİD

IntroductionPreeclampsia (PE) is a multisystemic disease of pregnan-cy presenting with proteinuria and hypertensive after 20weeks of gestation. Eclampsia (E) is a serious complica-

tion presenting with seizures in a patient with preeclamp-sia. While PE has different prevalence rates dependingon humidity, temperature and environmental factors, it isseen in 5–7% of all pregnancies. Hypertensive disorders

Özet: Gebeli¤in hipertansif bozukluklar›n›nprevalans›n›n mevsimsel de¤iflimiAmaç: Preeklampsinin patogenezi hala yeterince anlafl›lmam›flt›r.Son araflt›rmalar, insidans›n gebe kalma ve do¤um mevsimine gö-re de¤iflti¤ini göstermifltir. Mersin ilinde do¤um mevsimi ile pre-eklampsi prevalans› aras›nda bir iliflki olup olmad›¤›n› belirlemekiçin kesitsel bir çal›flma yap›lm›flt›r. Yöntem: Son 12 y›lda hastanemizde do¤um yapan 9547 gebenintaburcu kay›tlar› incelendi; 542 hipertansif gebenin hastane tabur-cu kay›tlar›n›n retrospektif analizi yap›ld›. Mevsimler; ilkbahar(mart, nisan, may›s), yaz (haziran, temmuz, a¤ustos), sonbahar (ey-lül, ekim, kas›m) ve k›fl (aral›k, ocak, flubat) olarak ele al›nd›. Has-tal›klar›n da¤›l›m›na göre ayl›k harita ç›kar›ld›. Bulgular: Hipertansif hastal›klar ile do¤um yapan 542 kad›n›n içe-risinde en s›k olarak (%42.1) hafif preeklampsi izlendi. Hipertansifgebelik en s›k k›fl ay›nda (%27.5) gözlendi. Ocak ve temmuz ay›ndaprevalans oran› (%10.2 ve %10) di¤er aylara göre daha yüksek izlen-di ve may›s ay›nda prevalans› herhangi bir aya göre daha düflük(%4.2) izlendi. Sonuç: Mersin’deki kad›nlar aras›nda hipertansif gebelik preva-lans› yaz ve k›fl aylar›nda do¤um yapan hastalarda daha yüksek, ilk-bahar için daha düflük saptand›. Bu sonuçlarla farkl› mevsimlerdes›cakl›k ve nem de¤iflikliklerinin preeklampsiyi etkileyebilece¤i gö-rülmektedir. Bu verileri do¤rulamak için daha genifl kapsaml› ko-hort çal›flmalar›na ihtiyaç vard›r.

Anahtar sözcükler: Gebeli¤in hipertansif bozukluklar›, mevsim-sel da¤›l›m, prevalans.

Correspondence: Cuma Tafl›n, MD. Department of Gynecology and Obstetrics, Faculty of Medicine, Mersin University, Mersin, Turkey.e-mail: [email protected] / Received: August 7, 2019; Accepted: September 24, 2019Please cite this article as: Tafl›n C, Bektafl K. Seasonal change of the prevalence of hypertensive disorders of pregnancy. Perinatal Journal2019;27(2):101–104. doi:10.2399/prn.19.0272008

Original Article

Perinatal Journal 2019;27(2):101–104©2019 Perinatal Medicine Foundation

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Abstract

Objective: The pathogenesis of preeclampsia is still unclear. Recentresearches show that the incidence varies depending on the seasonsof conception and labor. We carried out a cross-sectional study todetermine whether there is a correlation between labor season andpreeclampsia prevalence in Mersin or not. Methods: The discharge records of 9547 women who delivered inour hospital in the last 12 years were reviewed, and the dischargerecords of 542 hypertensive pregnant women were analyzed retro-spectively. The seasons were reviewed as spring (March, April, andMay), summer (June, July and August), autumn (September, Octoberand November), and winter (December, January, February). Monthlymap was established according to the distribution of the diseases. Results: Mild preeclampsia (42.1%) was the most common conditionin 542 women who delivered with the hypertensive diseases.Hypertensive pregnancy was observed most commonly in winter(27.5%). Prevalence was higher in January and July (10.2% and 10%,respectively) than other months, and it was lower in May than anyother month (4.2%). Conclusion: The prevalence of hypertensive pregnancy in womenin Mersin was higher than the patients who delivered in summer andwinter months, and it was lower in spring. With these results, it isseen that temperature and humidity changes in different seasonsmay affect preeclampsia. Cohort studies with wider populations areneeded to confirm these data.

Keywords: Hypertensive disorders of pregnancy, seasonal distri-bution, prevalence.

ORCID ID: C. Tafl›n 0000-0002-9315-4791; K. Bektafl 0000-0002-5628-9929

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of pregnancy (HDOP) are the third most common rea-son of maternal mortality in the USA.[1] Early diagnosisand close follow-up are important in the patients withPE. In these patients, abruptio placentae, acute kidneyfailure, cerebrovascular and cardiovascular complicationsand disseminated intravascular coagulation are associatedwith DIC.[2,3]

The previous studies showed that PE/E incidencehas seasonal trends. It is reported that this trend mayresult from the ambient temperature and humidity. Intheir study performed on 11,000 pregnant women inSouth Africa, Immink et al. found that PE prevalencereaches its highest level in winter with a rate of 13.6%.[4]

Mumbai carried a study in the tropical season of India,and found that the incidence of eclampsia was high dur-ing the monsoon period when temperature is lower andhumidity is high.[5] Tam et al. reported in their study per-formed in Hong Kong that PE incidence was higher inpregnant women during June.[6]

Philips et al. investigated the correlation betweendelivery season and PE, and found that PE likelihoodincreased by 70% in women who conceived in summermonths compared to those who conceived in springmonths.[7] In our study, we investigated whether there isa correlation between the seasons and preeclampsia.

MethodsThe discharge records of 9547 pregnant women whodelivered in the Gynecology and Obstetrics Clinic of

Mersin University in the last 12 years were reviewed ret-rospectively. The discharge records of 228 preeclampsiacases, 143 severe preeclampsia cases, 24 superimposedpreeclampsia cases, 60 cases with HELLP syndrome(hemolysis, thrombocytopenia, and elevated liverenzymes), 23 chronic hypertension cases and 147 healthycontrol patients were analyzed. Multiple pregnancieswere excluded from the study. The patient data wereanalyzed by using IBM SPSS (IBM Corp., Armonk, NY,USA) version 24. Chi-squared test was used for the fre-quencies of HDOP patients in multiple groups.Bonferroni test was used to compare the months. Thevalue p<0.05 was considered statistically significant.

ResultsWhen HDOP patients are evaluated according to theirdemographic characteristics in our study, the mean ageof the cases in all groups except the patients withHELLP syndrome and PE are significantly differentthan the control group (Table 1). In our study, eclamp-sia is seen in younger pregnant women while superim-posed PE, chronic hypertension (HT) and gestationalHT (GI HTI) are seen in advanced ages. In terms offetal weight, we found statistically significant resultswhen groups are compared among each other and to thecontrol group. We found that fetal weight decreased asthe clinical severity of the diseases increased (low birthweight <2500 g, very low birth weight <1500 g), and thatthe frequency of intrauterine growth retardation

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Table 1. The demographic characteristics of the patients with gestational hypertension.

PE Severe Superimposed E HELLP Chronic GI HT ControlPE PE HT group

(n=228) (n=143) (n=24) (n=34) (n=60) (n=23) (n=30) (n=147)(33.1%) (20.8%) (3.5%) (4.9%) (8.7%) (3.3%) (4.4%) (21.3%)

Ort±SD Ort±SD Ort±SD Ort±SD Ort±SD Ort±SD Ort±SD Ort±SD p

Maternal age (year) 30.9±5.9 30.3±6.5 33.1±5.6 26.0±6.2 31.2±7.5 37.6±5.4 34.7±5.3 30.1±6.1 0.372

Week of gestation during delivery 35.2±3.2 33.4±3.5 34.5±4.7 33.2±3.4 33.0±3.8 36.5±3.0 36.9±2.1 38.5±0.6 <0.001

n (%) n (%) n (%) n (%) n (%) n (%) n (%) n (%) p

Oligohydramnios 20 (10.6) 23 (19.5) 2 (10) 2 (7.1) 6 (12.5) 3 (15.8) 5 (20) 0 (0) <0.001

Anhydramnios 3 (1.6) 5 (4.2) 0 (0.0) 0 (0.0) 0 (0.0) 1 (5.3) 3 (12.0) 0 (0.0) 0.049

IUGR 83 (43.7) 58 (48.7) 6 (30.0) 15 (53.6) 27 (54.0) 4 (21.1) 13 (52.0) 0 (0.0) <0.001

IUFD 1 (0.5) 3 (2.5) 0 (0.0) 2 (7.1) 4 (8.0) 0 (0.0) 0 (0.0) 0 (0.0) 0.094

Preterm (< 34 weeks) 58 (30.5) 61 (51.3) 6 (30.0) 15 (53.6) 29 (58.0) 4 (21.1) 2 (8.0) 0 (0.0) <0.001

E: eclampsia; GI HT: gestational HT; HT: hypertension; IUFD: Intrauterine fetal demise; IUGR: intrauterine growth restriction; Mean±SD: mean ± standard deviation; PE: preeclampsia.

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increased (p<0.05). However, there was no significantdifference among the disease groups in terms of fetal sex.

In terms of the demographic characteristics of thepatients, patients deliver at earlier weeks as expectedwhen the severity of the disease increases, and the resultsare significantly different compared to the control group(p<0.05). HDOP prevalence varies according to themonths. As seen in Fig. 1, the lowest prevalence is inMay and the highest values are in summer and wintermonths. The prevalence peaks after May andSeptember. This seasonal distribution is similar in mostof the diseases in HDOP.

DiscussionIn our study, we found that HDOP has the highest val-ues in January and July, in which HDOP presents a sea-sonal correlation, and has the lowest values at the end ofMay. There are some differences when our study iscompared to the previous studies. In consistence withthe previous studies, we found that HDOP incidenceincreased in periods when the temperature is lower.[4,5]

However, the prevalence in our study had the lowestvalue in summer months in which humidity and temper-ature were the highest. This result is different than theresults of other studies which found similar correlationwith humidity.[7] In a study performed in Norway, it wasreported the monthly prevalence of PE was the lowest inAugust and the highest in December.[8] We found thatthese results are consistent with our study. In the studyof Ali et al. performed in Sudan, the authors reportedhigher prevalence for PE in periods with high tempera-ture and low humidity.[9] Also, Morikawa et al. found intheir study performed in Japan that HDOP was themost common in winter and early spring and the leastcommon in summer, and concluded that this result maybe associated with environmental factors.[10] Theseresults are consistent with our study. In the city that weconducted our study, the humidity is high in summerwith the highest level in August, and reaches to the low-est levels in winter and spring.

Our other purpose in this study was to group patientsand to determine the prevalence by considering the con-ception periods of these patients as well. In months thatthe patients with HDOP conceived, there was consisten-cy with the date of birth. The increases and decreases inthe sub-groups of HDOP are parallel as shown in thegraphs of the Fig. 1. Ambient temperature, the number

of daylight hours, seasonal food and diet, infections andthe changes of plasma volume in weather changes wereasserted to explain this seasonal change of preeclampsiaand eclampsia patients.[4,7]

Heat shock proteins which endanger the changes ofpreimplantation embryos were detected in animalexperiments.[11] It was claimed that cold air may causevasospasm.[8] In our study, the consistency with theconception date in our patients support preimplanta-tion and/or implantation period. In summary, wefound in our study that the patients who conceive anddeliver in winter months such as December and inspring months HDOP prevalence is higher than theother months, while it is lower in end of summer andearly autumn months. We found that our results areconsistent with the results of other studies reportingthe peak and the lowest prevalence.[8,12]

The seasonal trend in the preeclampsia may dependon various factors such as the maternal serum vitaminD and the duration spend in a sunny weather whichaffects maternal serum vitamin D.[13,14] The potentialrole of vitamin D in preeclampsia is a new study field.As known, the pathogenesis of preeclampsia has anumber of biological processes that may be affected byvitamin D such as immune dysfunction, placentalimplantation, and abnormal angiogenesis.[13]

ConclusionWe found consistent results in our study compared tothe previous studies. In our study, we found that the rateof HDOP was higher in winter and summer months inwhich humidity and temperature are low, and that it

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Fig. 1. Prevalence in patients with HDOP throughout the year.

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reached to the lowest levels in spring months, particular-ly in May. When these patients were ranked accordingto the conception months, the rate graphic of all patientswere consistent with the delivery week although therewas no consistency in the sub-groups of HDOP. Theresults of our study show that HDOP rate depends onthe environmental factors (i.e. humidity, temperature,vitamin D, etc.), and therefore, this is the reason to seediseases more frequently in particular periods.

Conflicts of Interest: No conflicts declared.

References1. Wagner LK. Diagnosis and management of preeclampsia.

Am Fam Physician 2004;70:2317–24.2. ACOG Committee on Practice Bulletins--Obstetrics. ACOG

practice bulletin. Diagnosis and management of preeclampsiaand eclampsia. Number 33, January 2002. Obstet Gynecol2002;99:159–67.

3. Brunelli VB, Prefumo F. Quality of first trimester risk pre-diction models for pre-eclampsia: a systematic review. BJOG2015;122:904–14.

4. Immink A, Scherjon S, Wolterbeek R, Steyn DW. Seasonalinfluence on the admittance of pre-eclampsia patients inTygerberg Hospital. Acta Obstet Gynecol Scand 2008;87:36–42.

5. Subramaniam V. Seasonal variation in the incidence ofpreeclampsia and eclampsia in tropical climatic conditions.BMC Womens Health 2007;7:18.

6. Tam WH, Sahota DS, Lau TK, Li CY, Fung TY. Seasonalvariation in pre-eclamptic rate and its association with the ambi-ent temperature and humidity in early pregnancy. GynecolObstet Invest 2008;66:22–6.

7. Phillips JK, Bernstein IM, Mongeon JA, Badger GJ. Seasonalvariation in preeclampsia based on timing of conception. ObstetGynecol 2004;104:1015–20.

8. Magnus P, Eskild A. Seasonal variation in the occurrence ofpre-eclampsia. BJOG 2001;108:1116–9.

9. Ali AA, Adam GK, Abdallah TM. Seasonal variation andhypertensive disorders of pregnancy in eastern Sudan. J ObstetGynaecol 2015;35:153–4.

10. Morikawa M, Yamada T, Yamada T, Cho K, Sato S, MinakamiH. Seasonal variation in the prevalence of pregnancy-inducedhypertension in Japanese women. J Obstet Gynaecol Res 2014;40:926–31.

11. Krininger CE 3rd, Stephens SH, Hansen PJ. Developmentalchanges in inhibitory effects of arsenic and heat shock ongrowth of pre-implantation bovine embryos. Mol Reprod Dev2002;63:335–40.

12. Bodnar LM, Catov JM, Roberts JM. Racial/ethnic differencesin the monthly variation of pre-eclampsia incidence. Am JObstet Gynecol 2007;196:324.e1–5.

13. Bodnar LM, Catov JM, Simhan HN, Holick MF, PowersRW, Roberts JM. Maternal vitamin D deficiency increasesthe risk of preeclampsia. J Clin Endocrinol Metab 2007;92:3517–22.

14. Baker AM, Haeri S, Camargo CA Jr, Espinola JA, StuebeAM. A nested case-control study of midgestation vitamin Ddeficiency and risk of severe preeclampsia. J Clin EndocrinolMetab 2010;95:5105–9.

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Anthropometric differences in the newborns withbrachial plexus palsy, clavicle fracture in pregnancies

without risk factorHüseyin K›yak1 , Alev At›fl Ayd›n2 , Gökhan Bolluk2 , Emel Canaz3 ,

1Gynecology and Obstetrics Clinic, ‹stanbul Kanuni Sultan Süleyman Training and Research Hospital, ‹stanbul, Turkey2Gynecology and Obstetrics Clinic, Perinatology Department, ‹stanbul Kanuni Sultan Süleyman Training and Research Hospital, ‹stanbul, Turkey

3Department of Obstetrics and Gynecology, Faculty of Medicine, ‹stanbul Bilim University, ‹stanbul, Turkey

İDİDİDİD

Özet: Risk faktörü olmayan gebeliklerde brakiyalpleksus felci ve klavikula k›r›¤› olgular›ndayenido¤anda antropometrik farkl›l›klarAmaç: Omuz distosisi aç›s›ndan düflük risk tafl›yan olgularda braki-yal pleksus felci, klavikula k›r›¤› ve omuz/humerus k›r›¤› komplikas-yonlar›n› yaflayan yenido¤anlar›n antropometrik verilerinden yarar-lanarak antenatal de¤erlendirmeye yönelik öngörü oluflturmak. Yöntem: Distosik do¤uma neden olabilecek fetal makrozomi,maternal diyabet, maternal obezite ve gebelikte afl›r› kilo al›m›,omuz distosisi öyküsü, do¤um indüksiyonu, epidural anestezi gibirisk faktörleri d›flland›ktan sonra hastane veri taban›ndan retros-pektif olarak ç›kar›lan do¤um komplikasyonu olgular›, ayn› obs-tetrik ve demografik özellikleri tafl›yan, ancak do¤um travmas› ya-flamayan, ayn› tart› ve cinsiyette yenido¤an verileri ile birebir efl-lefltirildi. Bulgular: 185 yenido¤an komplikasyonu gözlendi; bunlar›n 149 ta-nesi klavikula k›r›¤›, 8 tanesi omuz ve humerus k›r›¤›, 28 tanesi debrakiyal pleksus felci olarak s›n›fland›r›ld›. Do¤um komplikasyonuyaflanan olgularda do¤umun 2. evresinin anlaml› flekilde daha uzunoldu¤u görüldü (p=0.01; 22.41±6.98 dakikaya karfl›l›k 24.23±6.43dakika). Omuz distosisi, komplikasyonlar›n yafland›¤› çal›flma gru-bunda daha s›k gözlendi (p=0.0001; s›kl›¤› %32.97’ye karfl›l›k %2.7).Antropometrik ölçümler aç›s›ndan gö¤üs çevresi / bafl çevresi oran-lar›n›n ROC çal›flmas› anlaml› saptand›, oran›n 0.97’den büyük ol-mas› durumunda (AUC=0.903; sensitivite %77.84, spesifisite%89.73, PPD %88.3, NPD %80.2, LR 7.58) omuz distosisi vekomplikasyonlar› öngörebilece¤i görüldü. Komplikasyonlar›n 4000gram›n üstündeki olgularda anlaml› olarak artmaya bafllad›¤› saptan-d› (p=0.029). Sonuç: Do¤um kanal› içinde omuzlar ve uzant›lar› travmaya aç›k-t›r. ‹leri sürdü¤ümüz hipotezde neonatal antropometrik verilerkomplikasyonlar ile anlaml› flekilde korele bulunmufltur. Bir öngö-rüde bulunmak için, antenatal dönem ve özellikle de eylem s›ras›n-da fetal bafl ölçümlerinin yan› s›ra ayr›ca bisakromiyal çap ve gö¤üsçevresi ölçümleri yard›mc› olabilir.

Anahtar sözcükler: Yenido¤an antropometrik ölçümleri, omuzdistosisi, do¤um travmas›.

Correspondence: Ali Gedikbafl›, MD. Gynecology and Obstetrics Clinic, Perinatology Department, ‹stanbul Kanuni Sultan Süleyman Training and ResearchHospital, ‹stanbul, Turkey. e-mail: [email protected] / Received: September 2, 2019; Accepted: September 30, 2019Please cite this article as: K›yak H, At›fl Ayd›n A, Bolluk G, Canaz E, Ulaflk›n Z, Gedikbafl› A. Anthropometric differences in the newborns withbrachial plexus palsy, clavicle fracture in pregnancies without risk factor. Perinatal Journal 2019;27(2):105–112. doi:10.2399/prn.19.0272009

Original Article

Perinatal Journal 2019;27(2):105–112©2019 Perinatal Medicine Foundation

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Abstract

Objective: To make predictions for antenatal evaluation by usinganthropometric data of the newborns which undergo the complica-tions of brachial plexus palsy, clavicle fracture and shoulder/humerusfracture in cases with low risk in terms of shoulder dystocia. Methods: After the risk factors that may cause deliveries with dysto-cia such as fetal macrosomia, maternal diabetes, maternal obesity andexcessive weight gain during pregnancy, history of shoulder dystocia,labor induction and epidural anesthesia were ruled out, birth compli-cation cases found in the hospital database retrospectively werematched one by one with data of the newborns which had sameobstetric and demographic characteristics, same weights and gendersbut did not undergo labor trauma. Results: A total of 185 newborn complications were observed, and ofthese complications, 149 were classified as clavicle fracture, 8 as shoul-der and humerus fracture, and 28 as brachial plexus palsy. It was seenthat the 2nd stage of labor was significantly longer in the cases whichunderwent birth complication (p=0.01; 22.41±6.98 minutes vs.24.23±6.43 minutes). Shoulder dystocia was more frequent in thestudy group which had complications (p=0.0001; 32.97% vs. 2.7%).In terms of anthropometric measurements, the ROC analysis of tho-rax circumference / head circumference ratio was significant, and itwas seen that shoulder dystocia and the complications could be pre-dicted in case that the ratio is higher than 0.97 (AUC=0.903; sensitiv-ity 77.84%, specificity 89.73%, PPV 88.3%, NPV 80.2%, LR 7.58).It was found that the rate of complications increased significantly incases which were above 4000 g (p=0.029). Conclusion: Shoulders and its extensions are vulnerable to traumawithin birth canal. In our hypothesis, neonatal anthropometric datawere significantly correlated with the complications. In order tomake a prediction, bisacromial diameter and thorax circumferencemeasurements as well as fetal head measurements may be helpfulduring antenatal period and labor in particular.

Keywords: Newborn anthropometric measurements, shoulderdystocia, labor trauma.

ORCID ID: H. K›yak 0000-0001-7580-9179; A. At›fl Ayd›n 0000-0001-9999-3273; G. Bolluk 0000-0002-3506-6806;E. Canaz 0000-0002-2047-548X; Z. Ulaflk›n 0000-0001-6808-179X; A. Gedikbafl› 0000-0002-4727-0310

Zemzem Ulaflk›n1 , Ali Gedikbafl›2 İDİD

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IntroductionDespite many developments in obstetric diagnosis andprediction recently, shoulder dystocia has still been oneof the most important issues that an obstetrician mayface during labor. While it may occur by the obstructionof the anterior should of fetus by the symphis pubis dur-ing the move of fetus within pelvis, it also can be seen asthe obstruction of posterior shoulder by sacral promon-tory.[1] In cephalic vaginal deliveries, the incidence ofshoulder dystocia may vary between 0.2% and 3%.[2]

Also, brachial plexus palsy (BPP) develops in about 4%to 40% of these cases.[3,4] It was also seen that the risk ofclavicle fracture increases in some newborns duringshoulder obstruction.[5,6] However, clavicle fracture mayoccur spontaneously in many cases.[7,8]

The mechanism of BPP during shoulder dystocia hasbeen considered as the case where the fetal head ismoved away from the fetal body on axial plane throughlateral traction by applying excessive force. However, apotential clavicle fracture that may occur in the mean-time may be protective by increasing the cavity necessaryfor brachial plexus as well as the thoracic structure dur-ing a dystocic labor. A clavicle fracture may decrease thecompression during the move of brachial plexus togeth-er with thorax by increasing the cavity between clavicleand 1st rib actively. On the other hand, clavicle fractureitself is a sign of labor trauma and it indicates anincreased risk for BPP.[9] There is no consensus in the lit-erature about the argument that the clavicle fracture inthe presence of shoulder dystocia increases the severityof BPP. A retrospective study showed that a concomitantclavicle fracture supported the neurological recovery.[10]

On the other hand, another study reported that claviclefracture was neither protective for the brachial plexusinjury nor helped for the prediction of the severity of theinjury.[11] However, by any means, the development ofBPP is an unpredictable issue for obstetricians in termsof medicolegal problems and the debates have beenmaintained within the scope of the interaction of intrin-sic and iatrogenic forces on nerve damage.[12]

Many risk factors such as fetal macrosomia, maternaldiabetes, advanced maternal age, maternal obesity andexcessive weight gain during pregnancy, presence ofpolyhydramnios, history of shoulder dystocia, abnormalprogress and dysfunction in labor, labor augmentation,and the need for operative vaginal labor.[13–15] However,some anthropometric studies on the newborns show that

there may be some differences in the newborns undergo-ing shoulder dystocia.[16–20]

Our aim in this study is to present newborn charac-teristics in complications such as BPP and clavicle,shoulder and humerus fractures with or without shoul-der dystocia in our clinic and to make high suspicion andprediction for a potential shoulder dystocia and its com-plications. In order to achieve this purpose, we aimed tostudy with a group which was cleared of shoulder dysto-cia and its potential complications during pregnancyperiod as much as possible.

MethodsThe shoulder dystocia is defined subjectively in manysettings. In our clinic, the case when it takes more than60 seconds after head is delivered and seen in the per-ineum and/or that it is necessary to perform an addi-tional maneuver (such as McRoberts, suprapubic pres-sure, rotation maneuvers or knee-elbow position) if theshoulders have not been delivered yet is defined asshoulder dystocia.[21] On the other hand, any complica-tion may not be seen which can be detected definitelyaccording to the examination findings of newborns inthe cases with labor dystocia. In fact, the opposite alsoapplies where complications may develop withoutshoulder dystocia or without noticing the presence ofshoulder dystocia.[20–22] Brachial plexus injury is thedecreased movement in the upper extremity on rele-vant side compared to the other active upper extremitydepending on the trauma and paresis of relevant nervestructure.[1] The diagnosis of open or closed claviclefracture or arm/humerus fracture is established by thex-ray imaging together with the newborn examination.

The cases with dystocia or hypoxic ischemicencephalopathy associated with difficult labor were notincluded in our study. The exclusion criteria of ourstudy were the establishment of the diagnosis of gesta-tional diabetes mellitus (GDM) during antepartum peri-od on the basis of OGTT during pregnancy, maternalbody mass index (BMI) being over 30 kg/m2 at labor,presence of the history of shoulder dystocia in multi-parous women, deliveries before 37 weeks of gestationwithin intrapartum period, pregnant women whounderwent induction or epidural anesthesia for thelabor, and instrumental vaginal delivery which increasethe risk of shoulder dystocia. Measuring estimated birthweight above 4500 g together with duplicated measure-

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ments in our hospital is an indication of cesarean sec-tion. Therefore, the fetuses whose estimated birthweights were calculated above 4500 g before birth andborn with the birth weight above 4500 g were excludedfrom the study; however, the newborns with estimatedbirth weights below 4500 g and born with the birthweight above 4500 g were included in the study.

The newborns which had the complications of clavi-cle fracture, brachial plexus palsy/injury and shoulder/humerus fracture and born according to the hospitaldatabase were determined between January 2013 andJune 2019 and the study group was established by exclud-ing non-matching cases according to their relevant ante-and intrapartum characteristics. As the control group, thepregnant women in the study group were matched oneby one with data of the newborns which had same obstet-ric and demographic characteristics, same weights andgenders but did not undergo labor trauma. After exclud-ing the prenatal factors associated with pregnancy whichmay lead to dystocic labor (fetal macrosomia, maternaldiabetes, maternal obesity and excessive weight gain dur-ing pregnancy, history of shoulder dystocia, labor induc-tion, epidural anesthesia), second stage of labor, new-born’s sex, newborn weight, Apgar scores and anthropo-metric measurements of newborns for head and thoraxcircumferences were compared together with the mater-nal demographic data.

In this study, the statistical analyses were performedby NCSS (Number Cruncher Statistical System) 2007Statistical Software (Kaysville, UT, USA). The descrip-tive statistical methods (mean, standard deviation, medi-an, interquartile range, frequency and percentage distri-butions), Shapiro-Wilk normality test for the distribu-tion of variables, one-way variance analysis for the com-parisons of variables showing normal distribution, inde-pendent t test for the comparison of two samples,Kruskal-Wallis test for the comparisons among groupsnot showing normal distribution, Mann-Whitney U testfor the comparison of two samples, and chi square testfor the comparisons of the qualitative data were used forthe analyses of the data. In the differential diagnosis ofbrachial plexus injury, prediction point was calculatedfor the variables of head circumference, thorax circum-ference and the ratio of thorax circumference/head cir-cumference by using the values of ROC AUC, sensitiv-ity, specificity, positive predictive value, negative predic-tive value and LR (+). The significance level of theresults was considered p<0.05.

ResultsA total of 185 newborn complications with the neces-sary characteristics were observed between January2013 and June 2019. Of them, 149 were classified asclavicle fracture, 8 as shoulder and humerus fracture,and 28 as brachial plexus palsy. Relevant maternal data,the duration of the 2nd stage of labor, presence ofshoulder dystocia, Apgar scores and the associationbetween newborn heights and weights for the studygroup and the control group are shown in Table 1.Accordingly, it was seen that the 2nd stage of labor wassignificantly longer in the cases which underwent thebirth complication (p=0.01; 22.41±6.98 minutes vs.24.23±6.43 minutes). Similarly, shoulder dystocia wasmore frequent in the study group which had complica-tions (p=0.0001; 32.97% vs. 2.7%). In the studygroups, 1-minute and 5-minute Apgar scores were sig-nificantly lower (p=0.0001 for 1-minute Apgar scoreand p=0.005 for 5-minute Apgar score).

No difference was observed between two groups interms of birth weights due to the matching performed(Table 2). However, when newborn measurementswere evaluated, it was seen that head and thorax cir-cumferences were significantly higher in the compli-cated study group. In the mechanism of BPP builtabove, thorax and head circumferences were propor-tioned since the fetal head was moved away from thefetal body on axial plane through lateral traction byapplying excessive force (Fig. 1).[9,23] The ROC analysisof thorax circumference / head circumference ratio wassignificant, and it was seen that shoulder dystocia andthe complications could be predicted in case that theratio is higher than 0.97 (AUC=0.903; sensitivity77.84%, specificity 89.73%, PPV 88.3%, NPV 80.2%,LR 7.58).

When the cases with clavicle fracture, shoulder/humerus fracture and brachial plexus palsy/injury inwhich the complications were observed in the studygroup were evaluated separately in terms of demograph-ic and anthropometric data, it was seen that the associa-tion of shoulder dystocia was higher in brachial plexuscases (Table 3) (p=0.025; association with brachialplexus: 53.57%). It was found that the complicationsincreased significantly in cases above 4000 g but below4500 g (p=0.029). No difference was observed in terms ofthe other parameters.

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DiscussionOur study, which analyzes relevant data after the estab-lishment of the clinic, retrospectively evaluates anthropo-metric measurements of the newborns with clavicle frac-ture, shoulder/humerus fracture and brachial plexuspals/injury which can be seen together with shoulder dys-tocia in terms of obstetrics. In 1982, Modanlou et al.[23]

published some anthropometric data of the newbornswith and without shoulder dystocia and reported thatshoulder circumference was higher in the cases withshoulder dystocia and the ratios of shoulder circumfer-ence/head circumference were also high in these cases. Inthe same study, the authors reported that anthropometricmeasurements were more explicit in the newborns of dia-

betic women. Even macrosomia and the presence of dia-betic mothers-newborns predicts only 55% of the shoul-der dystocia cases, the data that may contribute to theprediction of birth complications which may be identifiedin this way have importance.[24] Except these two risk fac-tors, the studies showed that different additional antepar-tum and intrapartum factors such as maternal obesity andexcessive weight gain during pregnancy, history of shoul-der dystocia, abnormal progress of labor and dysfunction,and the need of operative vaginal labor may also con-tribute.[13] By excluding all these factors, we conductedour study through newborns’ anthropometric data andshoulder dystocia physiopathology, and from this point ofview, we tried to present prediction hypothesis.

Table 1. Maternal data, labor stage and newborn data.

Control group Study group n=185 n=185 p

Gravida Mean±SD 2.46±1.49 2.44±1.430.936*

Median (IQR) 2 (1–3) 2 (1–3)

Parity Mean±SD 1.03±1.1 1.01±1.080.948*

Medyan (IQR) 1 (0–2) 1 (0–2)

Maternal age (year) Mean±SD 26.85±5.81 26.66±5.66 0.751†

BMI (kg/m2) Mean±SD 27.32±3.67 27.26±3.29 0.869†

2nd stage of labor (min) Mean±SD 22.41±6.98 24.23±6.43 0.01†

Shoulder dystocia Not available 180 (97.30%) 124 (67.03%)0.0001‡

Available 5 (2.70%) 61 (32.97%)

Sex Male 107 (57.84%) 95 (51.35%)0.210‡

Female 78 (42.16%) 90 (48.65%)

1-minute Apgar score Mean±SD 8.2±0.9 7.69±1.4 0.0001†

5-minute Apgar score Mean±SD 9.4±0.78 9.15±0.94 0.005†

Newborn height (cm) Mean±SD 50.96±1.53 50.94±2.25 0.949†

Newborn’s birth weight (g) Mean±SD 3768.11±415.36 3772.33±408.78 0.922†

*Mann-Whitney U test; †Independent t test; ‡Chi square test.

Table 2. Correlation between anthropometric measurements and weights.

Control group Study group n=185 n=185 p

Birth weight (g) <4000 135 (72.97%) 131 (70.81%)0.644*

>4000 50 (27.03%) 54 (29.19%)

Birth weight (g) <4500 174 (94.05%) 176 (95.14%)0.646*

>4500 11 (5.95%) 9 (4.86%)

Head circumference (cm) Ort±SS 35.53±1.19 35.92±1.51 0.006†

Thorax circumference (cm) Ort±SS 33.22±1.35 34.72±1.48 0.0001†

The ratio of thorax circumference / head circumference Ort±SS 0.93±0.03 0.98±0.03 0.0001†

*Chi square test; †Independent t test.

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Consistence with the literature, we saw in our studythat the 2nd stage of labor prolonged in the complicat-ed cases.[1,24,25] Hypothetically and in accordance with thedefinition of the shoulder dystocia, this prolongationmay be associated with the prolonged delivery of fetalshoulders. However, as seen in our study, the prolonga-tion of the 2nd stage of labor may occur since head andthorax circumferences are higher and due to the passageof a larger object through the vagina and thus the fric-tional resistance although the weights of complicatedpatient group and control group are similar. Althoughshoulder dystocia is not present in all complicated cases,there was a significant association in the complicatedpatients and particularly in the BPP sub-group in ourstudy. The functional recovery within 6 months afterBPP is related to the level of current injury; while therecovery rate after the injuries of higher levels such asC5–C6 and C5–C7 is 64%, the recovery rate for paresisin lower levels such as C5–T11 decreases to 14%.[1,2]

While the same resources point out the association ofbrachial plexus and shoulder dystocia, fracture compli-cations such as clavicle fracture increases with the pres-ence of shoulder dystocia, but they may occur withouthaving any labor issue.[5–8]

While there are different publications on biometricmeasurements in the literature for the prenatal predic-tion of shoulder dystocia,[16–18,26–33] most of them focus onthe prediction associated with the difference betweenhead and abdominal circumferences with shoulder dys-tocia in antenatal follow-ups and their relevant calcula-tions. Unfortunately, these studies concluded that thedystocia cannot be predicted by antenatal measure-ments. On the other hand, only one study evaluated thecorrelation between the measurement of antenatalshoulder (bisacromial) diameter and macrosomia.[20] Inthis study, Youssef et al. developed the formula oftransthoracic diameter + (2 × forearm length) and meas-ured the bisacromial diameter indirectly, and theyreported macrosomia prediction as 88.4% and sensitivi-ty as 96.4% for a threshold value of 15.4 cm. However,this study does not have any data for shoulder dystocia.Similarly, in our literature review, we found only a lim-ited number of data in the literature for shoulder dysto-cia and newborns’ shoulder diameter.[19,23] These datashowed that shoulder circumference measurement innewborns after birth were explicit in dystocic labors.The difficulties in the intrauterine process are the twoends of the shoulders showing variation which do not

locate on an anatomic position in the same plane, andbeing unable to evaluate them in the same plane withinthe birth canal in association with fetal and shouldermovements which are a part of labor.

Similar to our study, we found a limited number ofdata in the literature evaluating shoulder dystocia and themeasurement of thorax circumference.[19,23,34–36] Thesestudies, similar to our study, compared the measurementsand differences of head circumference and thorax circum-ference of the newborns having postnatal complications,and highlighted that the measurement of the thorax cir-cumference was statistically significant. In one of thesestudies, Li et al.[36] retrospectively evaluated the antenatal

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Fig. 1. The anthropometric measurement and the ROC curve ana-lysis of the rates.

AUC SE 95% CI

Head circumference (cm) 0.590 0.030 0.538 – 0.641

Thorax circumference (cm) 0.766 0.025 0.719 – 0.808

The ratio of thorax circumference / 0.903 0.016 0.868 – 0.931head circumference

Cut-off Sensitivity Specificity PPV NPV LR (+)

Head circumference (cm) >35 58.38 58.38 58.4 58.6 1.40

Thorax circumference (cm) >33 78.38 59.46 65.9 73.3 1.93

The ratio of thorax >0.97 77.84 89.73 88.3 80.2 7.58circumference / head circumference

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data of the newborns undergoing shoulder dystocia andbirth complications similar to our study, and reportedthat the measurement of postnatal thorax circumferenceand the ratio of newborn thorax circumference/head cir-cumference were statistically significant. In our study, wefound that both head circumference and thorax circum-ference were significantly higher in the study groupundergoing complication, and wanted to highlight thatthese postnatal data may be statistically significant in theprediction indirectly. While trying to highlight the diffi-culty of measuring the bisacromial diameter in womenduring labor, we hypothesized that it may be possible tomeasure the thorax diameter on the plane of four-cham-ber cavity in rather more stable conditions and ultrasoundcross-section. After we observed that the ratios of thoraxcircumference/head circumference of newborns in par-ticular were statistically significant, and that the compli-cations associated with birth trauma were present partic-ularly in the newborns with a weight above 4000 g, weinitiated a prospective study in our clinic for that purpose

in order to reflect these measurements into antenatalassessments and to evaluate the hypothesis.

ConclusionThe antenatal studies for the prediction of birth compli-cations that may develop during labor with or withoutshoulder dystocia are insufficient. The studies per-formed so far have mainly focused on the determinationof the risk groups, and they are not completely helpfulfor the prediction of conditions that may develop duringlabor. Additional data are required to evaluate both birthchannel and the fetus inside completely during labor.The newborns with the same weight may have differentphysical characteristics, and therefore these differencesshould be taken into consideration. While fetal cranialstructures within the birth canal are relatively more pro-tected in the calvarium, the shoulders and the relevantextensions are vulnerable to the trauma as more labileand moving organ parts. Therefore, we have seen in ourhypothesis that neonatal anthropometric data and the

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Table 3. Newborn data together with the correlation of the complications with shoulder dystocia.

Clavicle fracture Shoulder and arm fracture Brachial plexus palsyn=149 n=8 n=28 p

Shoulder dystocia Not available 104 (69.80%) 7 (87.50%) 13 (46.43%) 0.025*Available 45 (30.20%) 1 (12.50%) 15 (53.57%)

Gravida Mean±SD 2.46±1.39 2.5±1.69 2.32±1.61 0.886†

Median (IQR) 2 (1–3) 2 (1–4.5) 2 (1–3)

Parity Mean±SD 1.03±1.04 1.13±1.46 0.86±1.21 0.698†

Median (IQR) 1 (0–2) 0.5 (0–2) 0 (0–1.75)

BMI (kg/m2) 27.23±3.32 27.79±3.13 27.26±3.31 0.899‡

2nd stage of labor (min) 24.18±6.62 24.25±5.6 24.46±5.79 0.978‡

Maternal age (year) 27.02±5.71 24.13±4.88 25.5±5.39 0.184

Sex Male 81 (54.36%) 5 (62.50%) 9 (32.14%) 0.079*Female 68 (45.64%) 3 (37.50%) 19 (67.86%)

Height (cm) 50.99±2.38 50.88±0.99 50.71±1.8 0.836‡

Weight (g) 3750.98±394.25 3741.25±417.9 3894.82±472.36 0.228‡

Weight (g) ≤4000 112 (75.17%) 4 (50.00%) 15 (53.57%) 0.029*>4000 37 (24.83%) 4 (50.00%) 13 (46.43%)

Weight (g) ≤4500 143 (95.97%) 8 (100.00%) 25 (89.29%) 0.259*>4500 6 (4.03%) 0 (0.00%) 3 (10.71%)

Head circumference (cm) 35.5±1.18 35.88±1.55 35.57±1.17 0.680‡

Thorax circumference (cm) 34.67±1.43 34.88±1.64 34.96±1.71 0.604‡

The ratio of thorax circumference / head circumference

0.98±0.03 0.97±0.04 0.98±0.03 0.486‡

1-minute Apgar score 7.74±1.28 7.88±1.13 7.36±1.97 0.378‡

5-minute Apgar score 9.19±0.83 9±0.76 8.93±1.41 0.350‡

*Chi square test; †Kruskal-Wallis test; ‡One-way variance analysis.

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measurements of head circumference together with thethorax circumference in particular were significant in thecomplicated cases. In order to make a prediction,bisacromial diameter and thorax circumference meas-urements as well as fetal head measurements may behelpful during antenatal period and labor in particular.

Conflicts of Interest: No conflicts declared.

References1. Committee on Practice Bulletins--Obstetrics. Practice

Bulletin Number No 178: Shoulder dystocia. Obstet Gynecol2017;129:e123–e133.

2. Gherman RB, Chauhan S, Ouzounian JG, Lerner H, Gonik B,Goodwin TM. Shoulder dystocia: the unpreventable obstetricemergency with empiric management guidelines. Am J ObstetGynecol 2006;195:657–72.

3. Kees S, Margalit V, Schiff E, Mashiach S, Carp HJ. Featuresof shoulder dystocia in a busy obstetric unit. J Reprod Med2001;46:583–8.

4. Bofill JA, Rust OA, Devidas M, Roberts WE, Morrison JC,Martin JN Jr. Shoulder dystocia and operative vaginal deliv-ery. J Matern Fetal Med 1997;6:220–4.

5. Lopez E, de Courtivron B, Saliba E. Neonatal complicationsrelated to shoulder dystocia. [Article in French] J GynecolObstet Biol Reprod (Paris) 2015;44:1294–1302.

6. Karahanoglu E, Kasapoglu T, Ozdemirci S, Fad›loglu E,Akyol A, Demirdag E, et al. Risk factors for clavicle fractureconcurrent with brachial plexus injury. Arch Gynecol Obstet2016;293:783–7.

7. Beall MH, Ross MG. Clavicle fracture in labor: risk factorsand associated morbidities. J Perinatol 2001;21:513–5.

8. Ozdener T, Engin-Ustun Y, Aktulay A, Turkcapar F, OguzS, Yapar Eyi EG, et al. Clavicular fracture: its incidence andpredisposing factors in term uncomplicated pregnancy. EurRev Med Pharmacol Sci 2013;17:1269–72.

9. Doumouchtsis SK, Arulkumaran S. Are all brachial plexusinjuries caused by shoulder dystocia? Obstet Gynecol Surv2009;64:615–23.

10. Wall LB, Mills JK, Leveno K, Jackson G, Wheeler LC,Oishi SN, et al. Incidence and prognosis of neonatal brachialplexus palsy with and without clavicle fractures. ObstetGynecol 2014;123:1288–93.

11. Leshikar HB, Bauer AS, Lightdale-Miric N, Molitor F,Waters PM; TOBI Study Group. Clavicle fracture is notpredictive of the need for microsurgery in brachial plexusbirth palsy. J Pediatr Orthop 2018;38:128–32.

12. Gonik B, Zhang N, Grimm MJ. Prediction of brachialplexus stretching during shoulder dystocia using a computersimulation model. Am J Obstet Gynecol 2003;189:1168–72.

13. Mehta SH, Sokol RJ. Shoulder dystocia: risk factors, pre-dictability, and preventability. Semin Perinatol 2014;38:189–93.

14. Erdo¤an K, Yapar Eyi EG. Comparison of high and lowdoses of oxytocin protocols in multiparous pregnant womenin terms of labor durations and fetal-maternal complications.Perinatal Journal 2017;25:11–8.

15. Akyol A, Talay H, Gedikbafl› A, Ark C, Ülker V, Özdemir Ç. The factors effective on the macrosomic deliveries ofnon-diabetic pregnant women. Perinatal Journal 2014;22:83–7.

16. Secher AL, Bytoft B, Tabor A, Damm P, Mathiesen ER.Fetal sonographic characteristics associated with shoulderdystocia in pregnancies of women with type 1 diabetes. ActaObstet Gynecol Scand 2015;94:1105–11.

17. Larson A, Mandelbaum DE. Association of head circumfer-ence and shoulder dystocia in macrosomic neonates. MaternChild Health J 2013;17:501–4.

18. Burkhardt T, Schmidt M, Kurmanavicius J, Zimmermann R,Schäffer L. Evaluation of fetal anthropometric measures topredict the risk for shoulder dystocia. Ultrasound ObstetGynecol 2014;43:77–82.

19. Winn HN, Holcomb W, Shumway JB, al-Malt A, Amon E,Hobbins JC. The neonatal bisacromial diameter: a prenatalsonographic evaluation. J Perinat Med 1997;25:484–7.

20. Youssef AEA, Amin AF, Khalaf M, Khalaf MS, Ali MK,Abbas AM. Fetal biacromial diameter as a new ultrasoundmeasure for prediction of macrosomia in term pregnancy: aprospective observational study. J Matern Fetal NeonatalMed 2019;32: 2674–9.

21. Spong CY, Beall M, Rodriques D, Ross MG. An objectivedefinition of shoulder dystocia: prolonged head-to-bodydelivery intervals and/or the use of ancillary obstetricmaneuvers. Obstet Gynecol 1995;86:433–6.

22. Miller LA. Shoulder dystocia: planning for the unpre-dictable. J Perinat Neonatal Nurs 2014;28:256–8.

23. Modanlou HD, Komatsu G, Dorchester W, Freeman RK,Bosu SK. Large-for-gestational-age neonates: anthropomet-ric reasons for shoulder dystocia. Obstet Gynecol 1982;60:417–23.

24. Acker DB, Sachs BP, Friedman EA. Risk factors for shoulderdystocia. Obstet Gynecol 1985;66:762–8.

25. Anderson JE. Complications of labor and delivery: shoulderdystocia. Prim Care 2012;39:135–44.

26. Cohen B, Penning S, Major C, Ansley D, Porto M, GariteT. Sonographic prediction of shoulder dystocia in infants ofdiabetic mothers. Obstet Gynecol 1996;88:10–3.

27. Cohen BF, Penning S, Ansley D, Porto M, Garite T. Theincidence and severity of shoulder dystocia correlates with asonographic measurement of asymmetry in patients withdiabetes. Am J Perinatol 1999;16:197–201.

28. Rajan PV, Chung JH, Porto M, Wing DA. Correlation ofincreased fetal asymmetry with shoulder dystocia in the non-diabetic woman with suspected macrosomia. J Reprod Med2009;54:478–82.

29. Miller RS, Devine PC, Johnson EB. Sonographic fetal asym-metry predicts shoulder dystocia. J Ultrasound Med 2007;26:1523–8.

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30. Abramowicz JS, Robischon K, Cox C. Incorporating sono-graphic cheek-to-cheek diameter, biparietal diameter andabdominal circumference improves weight estimation in themacrosomic fetus. Ultrasound Obstet Gynecol 1997;9:409–13.

31. Parantainen J, Palomäki O, Talola N, Uotila J. Clinical andsonographic risk factors and complications of shoulder dysto-cia – a case-control study with parity and gestational agematched controls. Eur J Obstet Gynecol Reprod Biol 2014;177:110–4.

32. Athukorala C, Crowther CA, Willson K; AustrailianCarbohydrate Intolerance Study in Pregnant Women(ACHOIS) Trial Group. Women with gestational diabetesmellitus in the ACHOIS trial: risk factors for shoulder dys-tocia. Aust N Z J Obstet Gynaecol 2007;47:37–41.

33. Chauhan SP, Lynn NN, Sanderson M, Humphries J, ColeJH, Scardo JA. A scoring system for detection of macrosomiaand prediction of shoulder dystocia: a disappointment. JMatern Fetal Neonatal Med 2006;19:699–705.

34. Hitschold T, Grewe J. Shoulder dystocia – risk factors andindicators. A retrospective analysis within an obstetric collec-tive of 14,913 deliveries. [Article in German] Z GeburtshilfeNeonatol 2008;212:211–6.

35. Kozovski I, Popova A, Protopopov F, Petkova U, ChernevaS. Fetal shoulder girdle dystocia during labor. [Article inBulgarian] Akush Ginekol (Sofiia) 1990;29:18–22.

36. Li N, Li Q, Chang L, Liu C. Risk factors and clinical predic-tion of shoulder dystocia in non-macrosomia. [Article inChinese] Zhonghua Fu Chan Ke Za Zhi 2015;50:17–21.

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Özet: Fetal konotrunkal kalp anomalileri: Prenataltaramada dört oda görünümü yeterli mi?Amaç: Bu çal›flmada hastanemiz perinatoloji ünitesinde konotrun-kal kalp anomalisi tan›s› alan olgular›n kay›tlar› incelenerek prena-tal dönemde konotrunkal kalp anomalisi tan›s›na yönlendiren fak-törlerin de¤erlendirilmesi ve prenatal konotrunkal kalp anomalisitan›s› ile ilgili fark›ndal›¤›n art›r›lmas› amaçland›.

Yöntem: Ocak 2015 – Aral›k 2016 tarihleri aras›nda Kanuni Sul-tan Süleyman E¤itim ve Araflt›rma Hastanesi Perinatoloji Ünite-sinde konotrunkal kalp anomalisi tan›s› alan olgular›n yönlendiril-me nedenleri, efllik eden kalp d›fl› anomali ve kromozom anomali-si varl›¤›, olgular›n perinatal sonuçlar› ve postnatal dönemde tan›-n›n do¤rulanma baflar›s› de¤erlendirildi.

Bulgular: Tüm konjenital kalp anomalilerinin içinde konotrunkalkalp anomalisi s›kl›¤› %20.4 idi. Çal›flmaya dahil edilen 101 olgu-nun 37’sinde (%36.6) gebelik terminasyonu gerçeklefltirildi. ‹ntra-uterin fetal ölüm 5 (%5) olguda gözlendi. Olgular›n %26.7’sindekromozom anomalisi ve %34.7’sinde kalp d›fl› ek yap›sal anomalisaptand›. Canl› do¤an 59 (%58.4) olgunun 52’sinde (%88.1) pre-natal tan› do¤ruland›. Olgular›n yaln›zca %27.7’sinde dört oda gö-rünümünün anormal oldu¤u saptand›.

Sonuç: Dört oda görünümünün konotrunkal kalp anomalilerindes›kl›kla normal olmas› nedeni ile bu anomalilerin prenatal tan› s›k-l›¤›n›n art›r›labilmesi için temel fetal kardiyak tarama programla-r›nda üç damar ve üç damar trakea kesitleri rutin olarak görüntü-lenmelidir.

Anahtar sözcükler: Konjenital kalp anomalileri, konotrunkal kalpanomalileri, fetal ekokardiyografi.

Abstract

Objective: In this study, we aimed to assess the factors leading tothe diagnosis of conotruncal heart anomaly in the prenatal period byreviewing the records of the cases which were diagnosed with theconotruncal heart anomaly in our perinatology unit, and to raise theawareness of the diagnosis of prenatal conotruncal heart anomaly.

Methods: The referral reasons, the presence of concomitant non-car-diac anomaly and chromosomal anomaly, perinatal outcomes of thecases and the confirmation success of the diagnosis at postnatal periodof the cases which were diagnosed with the conotruncal hearth anom-aly at the Perinatology Unit of Kanuni Sultan Süleyman Training andResearch Hospital between January 2015 and December 2016 wereevaluated.

Results: Among all congenital cardiac anomalies, the incidence ofconotruncal heart anomaly was 20.4%. The termination of pregnan-cy was performed in 37 (36.6%) of 101 cases included in the study.Intrauterine fetal death was observed in 5 (5%) cases. Chromosomalanomaly and non-cardiac additional structural anomaly were foundin 26.7% and 34.7% of the cases, respectively. Prenatal diagnosis wasconfirmed in 52 (88.1%) of 59 (58.4%) cases which born alive. It wasfound that four-chamber view was abnormal in only 27.7% of the cases.

Conclusion: Three vessels (3V) and three vessels trachea (3VT)views should be displayed routinely in basic fetal cardiac screening inorder to increase the prenatal diagnosis frequency of these anomaliesas four-chamber view is mostly normal in conotruncal heart anomaly.

Keywords: Congenital cardiac anomalies, conotruncal heartanomalies, fetal echocardiography.

Fetal conotruncal heart anomalies: is four-chamberview sufficient in the prenatal screening?

Baflak Kaya1 , Deniz Kanber Açar2 , Ahmet Tayyar1 , Helen Bornaun3 ,

1Perinatology Unit, Department of Obstetrics and Gynecology, ‹stanbul Medipol University, ‹stanbul, Turkey 2Perinatology Clinic, Dr. Sadi Konuk Training and Research Hospital, University of Health Sciences, ‹stanbul, Turkey

3Pediatric Cardiology Clinic, Kanuni Sultan Süleyman Training and Research Hospital, University of Health Sciences, ‹stanbul, Turkey4Pediatric Cardiology Clinic, Mehmet Akif Ersoy Thoracic and Cardiovascular Surgery Training and Research Hospital, University of Health Sciences, ‹stanbul, Turkey

5Perinatology Unit, Gynecology and Obstetrics Clinic, Kanuni Sultan Süleyman Training and Research Hospital, Health Sciences University, ‹stanbul, Turkey

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Correspondence: Baflak Kaya, MD. Perinatology Unit, Department of Obstetrics and Gynecology, ‹stanbul Medipol University, ‹stanbul, Turkey.e-mail: [email protected] / Received: September 4, 2019; Accepted: September 30, 2019Bu yaz›n›n at›f künyesi: Kaya B, Açar DK, Tayyar A, Bornaun H, Ayy›ld›z P, Polat ‹. Fetal conotruncal heart anomalies: is four-chamber view sufficientin the prenatal screening? Perinatal Journal 2019;27(2):113–118. doi:10.2399/prn.19.0272010

Original Article

Perinatal Journal 2019;27(2):113–118©2019 Perinatal Medicine Foundation

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ORCID ID: B. Kaya 0000-0002-2257-2355; D. K. Açar 0000-0001-8072-2262; A. Tayyar 0000-0003-1257-8742; H. Bornaun 0000-0001-9431-2256; P. Ayy›ld›z 0000-0002-1811-3658; ‹. Polat 0000-0001-9434-3976

Pelin Ayy›ld›z4 , ‹brahim Polat5 İDİD

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IntroductionThe migration anomaly of cardiac neural crest cells caus-es conotruncal heart anomalies characterized by defect inthe conotruncal septum.[1] It has been reported that10–12% of all cardiac anomalies are conotruncal heartanomalies in the postnatal series[2,3] and 16–30% in theprenatal series.[4–8]

Due to the necessity of evaluation and treatment inthe early postpartum period in the presence of fetalconotruncal heart anomaly, identifying these anomaliesduring intrauterine period is of vital importance.[9,10] Theprenatal diagnosis also enables to investigate concomitantstructural and chromosomal anomalies, provide consul-tancy to the family through multidisciplinary approachand plan the labor in appropriate tertiary centers.However, four-chamber view being normal in the major-ity of conotruncal anomalies makes it difficult to establishdiagnosis during prenatal period.[6] Therefore, the rates ofdetecting conotruncal heart anomalies are low in thescreening programs where ventricle outlets are not exam-ined and only four-chamber view is evaluated.[5,11]

In this study, we reviewed the records of the caseswhich were diagnosed with the conotruncal heart anom-aly in the perinatology unit of our hospital. We evaluat-ed the reasons for referral to our hospital, the presenceof concomitant non-cardiac anomaly and chromosomalanomaly, perinatal outcomes of the cases, and the confir-mation success of the diagnosis at postnatal period. Ourmain purpose in this study is to assess the factors leadingto the diagnosis of conotruncal heart anomaly in the pre-natal period, and to raise the awareness of the diagnosisof prenatal conotruncal heart anomaly.

MethodsThe records of 537 cases diagnosed with fetal cardiacanomaly in the Perinatology Unit of Kanuni SultanSüleyman Training and Research Hospital betweenJanuary 2015 and December 2016 were reviewed. Of110 cases which were diagnosed with double outlet rightventricle, transposition of the great arteries (TGA),tetralogy of Fallot (TOF) and truncus arteriosus (TA),the records of 101 were reviewed after 9 cases which didnot come for follow-ups and whose postnatal outcomescould not accessed were excluded from the study. Theapproval of ethics committee for this study was obtainedfrom the Ethics Committee of ‹stanbul MedipolUniversity with the decision no. E.45864.

All fetal ultrasonographic examinations were carriedout by maternal-fetal medicine specialists via Voluson 730and Voluson E6 (GE Medical Systems, Milwaukee, WI,USA) ultrasonography devices. Multiple planes were usedin the fetal echocardiographic examinations includingfour-chamber view, right and left ventricle outlets, threevessels (3V) and three vessels trachea (3VT) views, andlong and short axial views (Figs. 1 & 2). The relationshipand the localization of great vessels, outlet narrowness andthe presence of ventricular septal defect (VSD) werereported. Detailed anatomic examination was performedin all fetuses by fetal echocardiography. After the diagno-sis, the family was informed by maternal-fetal medicinespecialist, pediatric cardiologist and medical genetic spe-cialist. They were informed about the anomaly type, itspotential relationship with chromosomal anomalies,potential fetal and postnatal prognosis, and the optionsthat may be exercised in the management of pregnancy.The presence of chromosomal anomaly was evaluated bychorionic villus sampling, amniocentesis or cordocentesisin the prenatal period and by peripheral blood culture inthe postnatal period in case of the clinical suspicion. Thecases whose echocardiography, cardiac catheterization orsurgical records could be accessed in the postnatal periodwere included in the study.

SPSS version 24 (Statistical Package for the SocialSciences; SPSS Inc., Chicago, IL, USA) was used for

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Fig. 1. The view of left ventricle outlet in the case with the tetra-logy of Fallot. The distortion in the continuity between aortand ventricular septum is seen. Ao: Aort.

Ao

Right ventricle

Left ventricle

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the statistical analyses. The descriptive statistics weregiven as mean ± standard deviation, median (mini-mum–maximum) and number (percentage).

ResultsDuring 24-month study period, 110 (20.4%) of 537cases, which were diagnosed with congenital cardiacanomaly, had conotruncal heart anomaly. Nine cases,which did not come for follow-ups and whose postnataloutcomes could not accessed, were excluded from thestudy. Mean maternal age of 101 cases included in thestudy was 30.1 years. The weeks of gestation of the casesat the diagnosis varied between 16 and 39. The demo-graphic characteristics of the cases are shown in theTable 1. The number of fetal echo test per case duringdiagnosis and follow-up varied between 1 and 4. It wasfound that the suspicion of fetal cardiac anomaly, thesuspicion of non-cardiac structural anomaly, history ofbaby with congenital cardiac disease, family history andthe presence of concomitant maternal disease were themajor reasons for referral to our hospital.

The termination of pregnancy was performed in 37(36.6%) of 101 cases included in the study. Of 37 caseswhich were terminated, 27 (73%) had non-cardiac addi-tional structural anomaly and 20 (54.1%) had chromoso-mal anomaly. Intrauterine fetal death was observed in 5(5%) cases. Gestational outcomes by diagnosis groupsare shown in Table 2. Prenatal diagnosis was confirmedin 52 (88.1%) of 59 (58.4%) cases which born alive. Ofthe cases born alive, the mean birth was 38.1 weeks, themean birth weight was 2943 g, and the median values of1-minute and 5-minute Apgar scores were 7 and 9,respectively. Eighteen (30.5%) of 59 cases born alivedied at newborn period. The survival rate after the new-born period was 40.5% in all cases. The characteristics ofthe cases born alive are shown in Table 3.

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Fig. 2. Three vessels trachea view in the case with the tetralogy ofFallot. Aortic arc is seen on the left of the trachea but notthe ductal arc. Ao: Aort; PLSVC: Persistent left superiorvena cava; SVC: Superior vena cava.

Table 2. Gestational outcomes by diagnosis groups.

Double outlet right TGA TOF TA Total ventricle (n=45) (n=22) (n=29) (n=5) (n=101)

Termination of pregnancy 18 (40%) 2 (9.1%) 16 (55.2%) 1 (20%) 37 (36.6%)

Intrauterine fetal death 3 (6.7%) 1 (4.5%) 1 (3.4%) 0 5 (5%)

Live birth 24 (53.3%) 19 (86.4%) 12 (41.4%) 4 (80%) 59 (58.4%)

Non-cardiac additional structural anomaly 17 (37.8%) 4 (18.2%) 13 (44.8%) 1 (20%) 35 (34.7%)

Presence of chromosomal anomaly 13 (28.9%) 1 (4.5%) 12 (41.4%) 1 (20%) 27 (26.7%)

TA: Truncus arteriosus; TGA: Transposition of great arteries; TOF: Tetralogy of Fallot. The data were given as number (percentage).

Table 1. The demographic characteristics of the cases and their dis-tribution by the diagnosis groups.

The number of fetuses diagnosed with prenatal conotruncal heart anomaly 101

Maternal age (year) 30.1±6.2Gravida 2 (1–10)Parity 1 (0–5)Alive 1 (0–4)Week of gestation at diagnosis (week) 25.4±5.8Number of fetal echocardiography 1 (1–4)Double outlet right ventricle 45 (44.6%)Transposition of great arteries 22 (21.8%)Tetralogy of Fallot 29 (28.7%)Truncus arteriosus 5 (5%)

The data were given as mean ± SD, median (min–max) or number (percentage).

Ao

SVC

Right

Trachea

PLSVC

Left

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While 19 (70.4%) of 27 cases, who were found tohave chromosomal anomaly, had concomitant non-car-diac structural anomaly, the cardiac anomaly was in iso-lated form in the remaining 8 (29.6%) cases. 34.7% ofthe cases had non-cardiac additional structural anomaly.Additional structural anomalies were found in 37.8% ofthe cases with double outlet right ventricle and in 44.8%of the cases with the tetralogy of Fallot. The prognosesof the cases with non-cardiac additional structural anom-aly and/or chromosomal anomaly are shown in Table 4.

DiscussionConotruncal heart anomalies comprise the majority ofcyanotic congenital heart diseases observed in the firstyear of life.[12] It was reported that the prenatal diagno-sis of these anomalies may decrease postnatal hypoxiaand perioperative mortality.[13,14] Depending on themethod used in the screening of congenital heart dis-eases, the prenatal diagnosis rates reported forconotruncal heart anomalies vary between 39% and80%.[5,11,13,15] In this study where we evaluated the char-acteristics and perinatal outcomes of the cases diag-nosed with conotruncal heart anomaly in the prenatalperiod, we found that conotruncal heart anomalies canbe identified with a high accuracy in the prenatal peri-

od by using multiple planes in addition to the four-chamber view in fetal cardiac screening. Consistentwith the up-to-date literature, we found in our studythat the diagnosis of prenatal conotruncal heart anom-aly indicates poor prognosis together with the presenceof concomitant non-cardiac additional structuralanomaly and chromosomal anomaly.

The recent studies assessing the fetuses with thediagnosis of prenatal conotruncal heart anomalyreported that conotruncal heart anomalies comprise16–30% of all congenital cardiac anomalies.[4–8]

Consistent with the literature, the rate of conotruncalheart anomaly among congenital cardiac anomalies was20.4% in our series.

Some studies reported that the rate of non-cardiacadditional structural anomaly is 22–37% in prenatalseries in the presence of conotruncal heart anomaly.[4,6,7]

Similarly, we found in our study that the 34.7% of thecases had non-cardiac additional structural anomaly,and 77.1% of the cases with additional anomaly under-went the termination of pregnancy. High rates of ter-mination of pregnancy seen in the fetuses with addi-tional anomaly explain the presence of low rate of addi-tional structural anomaly observed in postnatalseries.[16] In the cases we assessed, 48.5% of the non-cardiac additional structural anomalies were centralnervous system anomalies. In a similar study, Paladiniet al. found that 46% of the conotruncal heart anom-alies accompanied by structural anomalies were centralnervous system anomalies.[6]

We found that the incidence of chromosomalanomaly in our cases was 26.7% in conformance withthe up-to-date literature (17–25%).[4,6,7] When weassessed the incidence of chromosomal anomaly by thediagnosis groups in our study which is consistent withthe literature, we found that the presence of concomi-tant chromosomal anomaly was the highest in the caseswith the tetralogy of Fallot (41.4%) and the lowest inthe cases with the transposition of the great arteries(4.5%). It should be kept in mind during prenatal con-sultancy that the incidence of chromosomal anomalyvaries depending on the type of conotruncal anomaly.Depending on the presence of concomitant structuralanomaly and chromosomal anomaly, the pregnancywas terminated in 36.6% of the cases and fetal loss wasobserved in 5% of the cases in the intrauterine period.When we assessed all cases, we observed that the sur-vival rate after newborn period was 40.5%. After

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Table 3. The characteristics of the cases born alive.

Delivery week (weeks) 38.1±1.91

Birth weight (g) 2943±602

1-minute Apgar score 7 (5–9)

5-minute Apgar score 9 (7–10)

Sex (male) 37 (62.7%)

Death in the newborn period 18 (30.5%)

The data were given as mean ± SD, median (min–max) or number (percentage).

Table 4. The prognoses of isolated and non-isolated cases.

Cases with additional structural anomaly

Isolated cases and/or chromosomal (n=58) anomaly (n=43)

Termination of pregnancy 5 (8.6%) 32 (74.4%)

Intrauterine fetal death 1 (1.7%) 4 (9.3%)

Live birth 52 (89.7%) 7 (16.3%)

The data were given as number (percentage).

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excluding the terminations and intrauterine fetal loss-es, the survival rates reported in the literature varybetween 40% and 71% for the fetuses diagnosed withconotruncal heart anomaly.[4,6,7,17–19] It can be suggestedthat the incidence of concomitant structural anomalyand chromosomal anomaly and the quality of medicalcare in the newborn care is responsible for these differ-ences in the survival rates. When we evaluated theprognoses of the cases according to the diagnosisgroups in our study, we found that the rates of livebirths were lower in the cases with the double outletright ventricle (53.3%) and the tetralogy of Fallot(41.4%) depending on the presence of higher rate ofchromosomal anomaly and concomitant non-cardiacstructural anomaly. This finding supports the correla-tion between the poor perinatal prognosis and thepresence of concomitant structural anomaly and chro-mosomal anomaly.

Four-chamber view frequently being normal inconotruncal heart anomalies decreases the rates ofdetecting these anomalies in the basic fetal cardiacscreenings. Four-chamber view is expected to beabnormal only in the cases with wide VSD or ventric-ular hypoplasia.[6] In our study, the four-chamber viewwas abnormal only in 27.7% of the cases while threevessels and three vessels trachea views were abnormalin all cases. Adding three vessels and three vessels tra-chea views, which are obtained technically more easilycompared to the ventricle outlet views, into basic fetalcardiac screening will contribute to the increase ofdiagnosis rates in the prenatal period.

Determining the localizations and relationships ofgreat arteries properly in the prenatal diagnosis ofconotruncal heart anomalies is the major challenge ofthe diagnosis. The greatest errors in the diagnosis par-ticularly in the presence of double outlet right ventri-cle are made while determining the orientation of thegreat arteries. Fetal position, maternal characteristics,week of gestation and the presence of additional anom-alies particularly affecting fetal thorax complicate thediagnosis.[18,20] We found in our study that 7 caseswhose prenatal diagnoses could not be confirmed werediagnosed with another conotruncal anomaly in thepostnatal period. The most important reason is thefailure of proper identification of the localizations ofgreat arteries and their relationship among themselves.The relationships of great arteries with each other andventricles are the other factors affecting the postnatal

prognosis of VSD localization and outlet narrow-ness.[20] Therefore, defining these parameters in detailin the presence of conotruncal heart anomaly diagnosisis very important for the prenatal consultancy given tothe family.

The retrospective design of the study, the presenceof the cases excluded from the study, failure of con-firming the diagnosis by autopsy in the cases whichwere terminated and lost in the intrauterine period arethe major limitations of our study.

ConclusionIn consideration of the results of our study and report-ed in the literature, it is understood that the fetalechocardiography conducted by using multiple planesin the referral centers is successful in the prenatal diag-nosis of conotruncal heart anomalies. The prenataldiagnosis of fetal cardiac anomalies will help the iden-tification of chromosomal anomalies and additionalstructural anomalies which may be associated as well asto provide proper consultancy to the family, plan thelabor under appropriate conditions, take precautionsfor the cardiorespiratory problems that may be facedwhen switching from fetal life to postnatal life, andtherefore to decrease social and legal problems thatmay arise.

The development of sonography technology, rais-ing the awareness of the significance of prenatal diag-nosis of cardiac anomalies, referring risk groups to tar-geted fetal echocardiography, and particularly addingthree vessels and three vessels trachea views into thebasic fetal cardiac screening will contribute to increasethe frequency of prenatal diagnosis of these cases.

Conflicts of Interest: No conflicts declared.

References1. Hutson MR, Kirby ML. Neural crest and cardiovascular

development: a 20-year perspective. Birth Defects Res CEmbryo Today 2003;69:2–13.

2. Hoffman JI, Kaplan S. The incidence of congenital heart dis-ease. J Am Coll Cardiol 2002;39:1890–900.

3. Samanek M, Voriskova M. Congenital heart disease among815,569 children born between 1980 and 1990 and their 15-year survival: a prospective Bohemia survival study. PediatrCardiol 1999;20:411–7.

4. Galindo A, Mendoza A, Arbues J, Graneras A, Escribano D,Nieto O. Conotruncal anomalies in fetal life: accuracy of diag-

Volume 27 | Issue 2 | August 2019

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117

Page 76: ISSN 1305–3124 JOURNAL PERINATAL · Ahmet Yal›nkaya,Diyarbak›r, Turkey Jun Yoshimatsu, Osaka, Japan Emre Zafer, Ayd›n, Turkey Yaron Zalel, Tel Aviv, Israel Ivica Zalud, Honolulu,

nosis, associated defects and outcome. Eur J Obstet GynecolReprod Biol 2009;146:55–60.

5. Rustico MA, Benettoni A, D’Ottavio G, Maieron A, Fischer-Tamaro I, Conoscenti G, et al. Fetal heart screening in low-risk pregnancies. Ultrasound Obstet Gynecol 1995;6:313–9.

6. Paladini D, Rustico M, Todros T, Palmieri S, Gaglioti P,Benettoni A, et al. Conotruncal anomalies in prenatal life.Ultrasound Obstet Gynecol 1996;8:241–6.

7. Sivanandam S, Glickstein JS, Printz BF, Allan LD, AltmannK, Solowiejczyk DE, et al. Prenatal diagnosis of conotruncalmalformations: diagnostic accuracy, outcome, chromosomalabnormalities, and extracardiac anomalies. Am J Perinatol2006;23:241–5.

8. Boudjemline Y, Fermont L, Le Bidois J, Fraisse A, KachanerJ, Villain E, et al. Prenatal diagnosis of conotruncal heart dis-eases. Results in 337 cases. [Article in French] Arch Mal CoeurVaiss 2000;93:583–6.

9. Yoo SJ, Golding F, Jaeggi E. Ventricular outflow tract anom-alies: so-called conotruncal anomalies. In: Yagel S, SilvermanNH, Gembruch U, editors. Fetal cardiology. 2nd ed. NewYork, NY: Informa Healthcare; 2009. p. 305–27.

10. Aydemir NA, Güven MA, Bak›r ‹, Enç Y, Bilal MS. Importanceof prenatal diagnosis in transposition of the great arteries: casereport. Perinatal Journal 2007;15:68–72.

11. Vergani P, Mariani S, Ghidini A, Schiavina R, Cavallone M,Locatelli A, et al. Screening for congenital heart disease withthe four-chamber view of the fetal heart. Am J Obstet Gynecol1992;167:1000–3.

12. Gedikbasi A, Oztarhan K, Gul A, Sargin A, Ceylan Y.Diagnosis and prognosis in double-outlet right ventricle. AmJ Perinatol 2008;25:427–34.

13. Bonnet D, Coltri A, Butera G, Fermont L, Le Bidois J,Kachaner J, et al. Detection of transposition of the great arter-ies in fetuses reduces neonatal morbidity and mortality.Circulation 1999;99:916–8.

14. Tzifa A, Barker C, Tibby SM, Simpson JM. Prenatal diagno-sis of pulmonary atresia: impact on clinical presentation andearly outcome. Arch Dis Child Fetal Neonatal Ed2007;92:F199–203.

15. Wyllie J, Wren C, Hunter S. Screening for fetal cardiac mal-formations. Br Heart J 1994;71(4 Suppl):20–7.

16. Lurie IW, Kappetein AP, Loffredo CA, Ferencz C. Non-car-diac malformations in individuals with outflow tract defects ofthe heart: the Baltimore-Washington Infant Study (1981–1989).Am J Med Genet 1995;59:76–84.

17. Allan LD, Sharland GK, Milburn A, Lockhart SM, GrovesAM, Anderson RH, et al. Prospective diagnosis of 1006 con-secutive cases of congenital heart disease in the fetus. J AmColl Cardiol 1994;23:1452–8.

18. Tometzki AJ, Suda K, Kohl T, Kovalchin JP, Silverman NH.Accuracy of prenatal echocardiographic diagnosis and prog-nosis of fetuses with conotruncal anomalies. J Am Coll Cardiol1999;33:1696–701.

19. Kaguelidou F, Fermont L, Boudjemline Y, Le Bidois J, BatisseA, Bonnet D. Foetal echocardiographic assessment of tetralo-gy of Fallot and postnatal outcome. Eur Heart J 2008;29:1432–8.

20. Gelehrter S, Owens ST, Russell MW, van der Velde ME,Gomez-Fifer C. Accuracy of the fetal echocardiogram indouble-outlet right ventricle. Congenit Heart Dis 2007;2:32–7.

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A case achieved at 28 weeks of gestation by cervical cerclage with retained placenta after

expulsion of nonviable fetus underwent selective termination in multifetal pregnancy

P›nar Özcan , Mehmet Serdar Kütük , Taha Takmaz , Havva Sevde ‹fllekDepartment of Gynecology & Obstetrics, Faculty of Medicine, Bezmialem Vak›f University, Istanbul, Turkey

İDİDİDİD

Özet: Ço¤ul gebelikte selektif terminasyon uygulanan nonviyabl fetüsün tahliyesinden sonraplasenta retansiyonlu servikal serklaj ile 28. gebelikhaftas›na ulaflan olgu Amaç: Çal›flmam›zda, stimüle edilmifl intrauterin inseminasyonsonras›nda dikoryonik ve diamniyotik gebelikte çoklu yap›sal ano-mali ve trizomi 13 nedeniyle selektif terminasyon uygulanan özelbir olguyu sunmay› amaçlad›k. Olgu, 20. gebelik haftas›nda selek-tif terminasyon uygulanan nonviyabl fetüsün 21. gebelik haftas›n-da tahliyesi sonras›nda plasenta retansiyonlu servikal serklaj ile 28.gebelik haftas›na ulaflt›.

Olgu: Yirmi iki yafl›ndaki hastaya (G1P0), aç›klanamayan inferti-lite nedeniyle intrauterin inseminasyon (IUI) uyguland›. Gebeli-¤in 12. haftas›nda, ultrason muayenesiyle dikoryonik diamniyotikikiz gebelik do¤ruland›. ‹kiz A için 20. gebelik haftas›nda trizomi13 nedeniyle selektif terminasyon uyguland› ve 21. gebelik hafta-s›nda ventrikülomegali, vermis agenezisi, mikrognati, mikroftalmi,hipertelorizm, her iki elde polidaktili, kalpte atriyoventriküler ka-nal defekti saptanan ve her iki böbrekte hiperekojenik ve polikistikgörüntülemeye sahip ölü ikiz A, normal do¤umla al›nd›. Enfeksi-yon parametrelerinin olmamas› üzerine, antibiyoterapi ve tokolizalt›nda ölü ikiz A’n›n al›nmas›ndan sonra McDonald-Shirodkarserklaj› uyguland›.

Sonuç: Vajinal do¤um gerçeklefltirildi ve 28. gebelik haftas›nda1150 g a¤›rl›¤›nda, 8/9 Apgar skoruna sahip erkek bebek do¤du.Selektif redüksiyon sonras› nonviyabl fetüsün tahliyesini izleyennonviyabl fetal plasenta retansiyonu maternal ve fetal riski art›rsada, gebeli¤i sürdürmek için servikal serklaj alternatif bir uygulamaolarak düflünülebilir.

Anahtar sözcükler: Dikoryonik diamniyotik ikiz gebelik, fetal re-düksiyon, trizomi 13, servikal serklaj, IUI, yap›sal anomali.

Correspondence: P›nar Özcan, MD. Department of Gynecology & Obstetrics, Faculty of Medicine, Bezmialem Vak›f University, Istanbul, Turkey.e-mail: [email protected] / Received: June 3, 2019 2019; Accepted: September 3, 2019Please cite this article as: Özcan P, Kütük MS, Takmaz T, ‹fllek HS. A case achieved at 28 weeks of gestation by cervical cerclage with retained placenta after expulsion of nonviable fetus underwent selective termination in multifetal pregnancy. Perinatal Journal 2019;27(2):119–124.doi:10.2399/prn.19.0272005

Case Report

Perinatal Journal 2019;27(2):119–124©2019 Perinatal Medicine Foundation

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Abstract

Objective: We aimed to present a special case underwent the selec-tive termination because of multiple structural anomaly and trisomy13 in dichorionic and diamniotic pregnancy after stimulatedintrauterine insemination. It achieved at 28 weeks of gestation bycervical cerclage with retained placenta after expulsion of nonviablefetus at 21 weeks of gestation which underwent selective terminationat 20 weeks of gestation.

Case: Twenty-two-year-old patient (G1P0) underwent intrauterineinsemination (IUI) for unexplained infertility. A dichorionic diamni-otic twin pregnancy has been confirmed by the ultrasonographicexamination at 12 weeks of gestation. The selective termination fortwin A was performed at 20 weeks of gestation because of trisomy 13and at 21 weeks of gestation dead twin A with ventriculomegaly, ver-mian agenesis, micrognathia, microphthalmia, hypertelorism, poly-dactyly on both hands, atrioventricular channel defect in the heart,hyperechogenic and polycystic imaging on both kidneys was deliv-ered normally. On the absence of infection parameters, McDonald-Shirodkar cerclage were carried out after the delivery of the deadtwin A under antibiotherapy and tocolysis.

Conclusion: Vaginal delivery was performed and 1150 g male babywith 8/9 Apgar score was born at 28 weeks of gestation. Cervical cer-clage may take into consideration an alternative to prolong the preg-nancy, although the retention of nonviable fetal placenta followingexpulsion of nonviable fetus after the selective reduction may increasematernal and fetal risk.

Keywords: Dichorionic diamniotic twin pregnancy, fetal reduc-tion, trisomy 13, cervical cerclage, IUI, structural anomaly.

ORCID ID: P. Özcan 0000-0002-0306-6422; M. S. Kütük 0000-0001-7895-9180; T. Takmaz 0000-0003-0793-2348; H. S. ‹fllek 0000-0002-9998-4948

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IntroductionMulti-fetal pregnancy is a well-known, adverse out-come of stimulated IUI treatment. Multi-fetal preg-nancies compared to singletons are associated with ahigher risk of maternal and obstetrical complicationssuch as miscarriage, preterm birth, low-birth weight,preeclampsia, gestational diabetes and perinatal mor-tality.[1] The multiple pregnancy rate can be reducedwith single embryo transfer in IVF treatment; howev-er, in OS-IUI treatments, control of the multiple preg-nancy rate is very limited.

The impact of assisted reproduction techniques(ART) on the risk of major congenital malformations(MCM) remains controversial. According to the resultof studies focused on the risk of MCM associated withART and IUI treatment, the use of ART and IUI wasrelated to an increased risk of major birth defects(adjusted OR, 3.11; 95% CI, 1.33–7.27 for the risk ofmajor urogenital malformations in ART; adjusted OR,2.02; 95% CI, 1.10–3.71 for risk of major muscu-loskeletal malformations in IUI; adjusted OR, 1.66;95% CI, 1.00–2.79 for an increased risk of any MCMin ART, and adjusted OR, 7.18; 95% CI, 1.59–32.53for urogenital malformations in ART).[2,3] Even as anadjustment, a contribution of the underlying subfertil-ity problems cannot be completely ruled out given thedifferences in the severity of subfertility. There are afew studies which evaluated the risk of MCM associat-ed with the use of stimulated IUI. Furthermore, thesestudies had some limitations including suboptimalsample size, lack of appropriate comparison groups andlack of the establishment of the risk of different typesof congenital malformations. The incidence of fetalabnormalities has been reported to be higher in multi-ple pregnancies than in singletons.[4–6]

Women with multifetal pregnancies in which onefetus is abnormal and the other is normal have threeoptions: expectant management (do nothing), termi-nate the pregnancy (both normal and abnormal fetus-es), or selective termination (ST) of the abnormal fetusor fetuses. A specific fetus is terminated because of astructural anomaly or a chromosomal abnormality byusing ST.[7] There are several approaches which havebeen described for embryo reduction.[8,9] The mostcommonly applied method is ultrasound-guided trans-abdominal injection of potassium chloride into the

fetal heart.[10,11] The technique of ST because of a struc-tural anomaly or a chromosomal abnormality is notdifferent from those in singleton pregnancies. Butthere are several additional considerations resultingfrom a multiple pregnancy including the procedure-related risk of pregnancy loss, the possibility of mater-nal coagulopathy secondary to the prolonged retentionof a nonviable fetus and the appropriate technique.The complete pregnancy loss rate of ST is at 2.5–7%and it is proportional to the starting and ending num-ber of fetuses.[12–14]

We aimed to present a special case underwent STbecause of multiple structural anomaly and trisomy 13in dichorionic and diamniotic pregnancy after stimu-lated IUI. It achieved at 28 weeks of gestation by cer-vical cerclage with retained placenta after expulsion ofnonviable fetus at 21 weeks of gestation which under-went ST at 20 weeks of gestation.

Case ReportTwenty-two-year-old patient with gravida 1, parity 0which is not able to conceive despite a year of unprotect-ed sexual intercourse has applied to IVF unit of Facultyof Medicine of Bezmialem University. During investiga-tion of infertility, her hormone profile was normal, ahysterosalpingography revealed that uterine cavity wasnormal and the fallopian tubes were bilaterally patent.Her partner’s spermiogram was consistent with normalvalues. The patient underwent ovulation induction andintrauterine insemination for unexplained infertility. Shehas got pregnant with her second ovulation inductionand IUI. A dichorionic diamniotic twin pregnancy hasbeen confirmed by the ultrasonographic examination at12 weeks of gestation and twins had a normal nuchaltranslucency measurement of 1.4 mm and 1.6 mm at 12weeks of gestation. She was referred to our perinatologyclinic for the routine second trimester detailed obstetricultrasonography at 20 weeks of gestation. An anomalyscan was performed at 20 weeks of gestation. In theultrasonographic examination, Twin A had multiple fetalabnormalities, which strongly suggest trisomy 13,including ventriculomegaly, vermian agenesis, microg-nathia, microphthalmia, hypertelorism, polydactyly onboth hands, atrioventricular channel defect in the heart,hyperechogenic and polycystic imaging on both kidneys(Fig. 1). Twin B showed normal fetal anatomy without

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Fig. 1. (a) Vermian agenesis, (b) micrognathia, (c) microphthalmiaand hypertelorism, (d) postaxial polydactyly, (e) hyperecho-genic kidney.

a b

c

e

d

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detected major and/or minor abnormality. The familywas informed about the risk of pregnancy and geneticconsultancy was provided about genetic abnormalityand MCM. Counseling contained detailed discussionof the risk of mid-term ST procedure which includes3–7.5% risk of total pregnancy loss.[15] The family wasalso informed that Trisomy 13 is universally lethalcondition and continuation of pregnancy as twin mightbe an alternative approach although it has its attendantrisks specific for multiple pregnancies and the potentialneed for prolonged intensive care for live-born withmultiple anomalies. The parents opted for selectivereduction of twin A due to their concern for prolongedsuffering for the affected fetus A. ST for twin A withthe presumptive diagnosis of trisomy 13 was performedby transabdominal guided intrathoracic injection ofpotassium chloride at 20 weeks. Amniocentesis per-formed during the termination procedure confirmedtrisomy 13.

After ST, the patient readmitted to the hospitalwith vaginal bleeding at 21 weeks of gestation. She hadpowerful uterine contraction and the ultrasonographicexamination revealed that cervical length was 20 mm(Fig. 2). Antibiotherapy (ampiciline+sulbactam IV 2g/4id per day for 48 h followed by PO 375 mg/2id for5 days plus azithromycin PO 500 mg per day for 7days)and tocolysis (indomethacin rectal 100 mg once, fol-lowed by PO 25 mg/4id for 2 days) were started.Despite antibiotherapy and tocolysis, after fourth dayof therapy, amniotic leakage occurred and the deadtwin A was delivered normally with full dilated cervixbut the placenta of dead twin A was not delivered. Onthe absence of infection parameters, McDonald-Shirodkar cerclage were carried out after the deliveryof the dead twin A under antibiotherapy and tocolysis.The patient was daily followed up with blood and clin-ic infection parameters. The patient was dischargedand weekly followed up at the outpatient clinic. 15 daysafter cerclage, the patient readmitted with abdominalpain and vaginal bleeding. She had powerful uterinecontraction and cervical length was 23 mm at 25 weeksof gestation. Antibiotherapy and tocolysis were startedagain as described above. Antenatal corticosteroids(betamethasone IM 12 mg/d for 48h) were adminis-tered to enhance fetal lung maturity. Magnesium sul-fate for neuroprotection with a loading dose of 4 g IV

in 20 min followed by a maintenance dose of 2 g/h for24 h was also administered. There was no response ofuterine contraction to antibiotherapy and tocolysis andthe presence of infection, vaginal cephalic delivery wasperformed and 1150 g male baby with 8/9 Apgar scorewas born at 28 weeks of gestation. During admission toNICU, the baby was not underwent intubation and itwas treated with only CPAP for one week and it wasstayed in neonatal unit for two months and it was dis-charged as 3000 g two months later. There was nocomplication related to prematurity in neonatal unit.

DiscussionWe reported a special case which achieved at 28 weeksof gestation by cervical cerclage with retained placentaafter expulsion of nonviable fetus with a structuralanomaly and trisomy 13 underwent ST in dichorionic-diamniotic pregnancy after stimulated IUI.

Selective termination of a specific fetus in multiplepregnancy because of a structural anomaly or a chro-mosomal abnormality is a widely accepted procedure.However, ST of a fetus in multiple pregnancy is notsimilar to a singleton pregnancy, this procedure hasadditional factors that need to be considered in thecontext of a multiple pregnancy. The most unintendedcomplication related to ST is the loss of total pregnan-cy before 24 weeks of gestation. The rate of unintend-

Fig. 2. 20 mm cervical length.

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ed pregnancy loss is generally associated with the ges-tational age at ST, the number of fetuses and havingmore than one fetus selectively terminated. Thepatients who had severe anomalies visible by ultra-sound and invasive diagnostic procedures before ST ismost likely have higher risk of pregnancy loss. Theother important risk related to ST is the possibility ofpre-term birth of a normal fetus and long-term seque-lae resulted from prematurity. Preterm labor is one ofthe factors contributing perinatal morbidity/mortalitymost. The other important risk related to ST is thepossibility of maternal risks arising from retention ofnonviable fetal tissue following the selective reduction.After the expulsion of fetus, the retention of placentais associated with chorioamnionitis, hemorrhage andpreterm delivery. The optimal timing for performingST has been reported in the literature to be as early asparticularly before 18–20 weeks of gestation.[16–18]

Likewise, there are several technical problems relatedto ST of a specific fetus in multiple pregnancy whencompare to fetal reduction for elective indications inmultiple pregnancy. Basically, fetal reduction for elec-tive indications could be accompanied with fewer com-plications when compare to ST of a specific fetus inmultiple pregnancy.[19] Because, during fetal reductionfor elective indications, the technically most easilyaccessible fetus can be selected to reduce as well as thefetus furthest away from the internal cervical os can bereduced to minimize the risk of premature rupture ofmembranes followed by premature delivery.[20] On theother hand, selective fetal reduction is associated withexcellent perinatal outcomes in dichorionic twinswhile selective reduction in monochorionic twins hasan increased procedure-related complications andpreterm delivery rate. A large single-centre series ofselective fetal reduction in monochorionic anddichorionic twins for structural, chromosomal andgenetic abnormalities demonstrated that ST in bothmonochorionic and dichorionic pregnancies is safe andeffective with relatively low loss and prematurityrates.[21] Cervical cerclage has been used widely in themanagement of pregnancies considered at high risk ofpreterm birth. Cerclage in twin pregnancies with dilat-ed cervix ≥1 cm before 24 weeks of gestation signifi-cantly increase latency period from diagnosis to deliv-ery (6.7 weeks). Because of longer latency period from

diagnosis to delivery, it decreases incidence of sponta-neous preterm birth at any given gestational age andimproves perinatal outcome when compared to expec-tant management.[22]

The first challenge related to our case is that wehad to undergo reduction of the twin closest to thecervical os for ST because the structurally or chromo-somally abnormal fetus was the closest to the internalcervical os. It may be increase the risk of prematurerupture of membranes after reduction. The secondchallenge is that the risk results from the prolongedretention of placenta of nonviable fetus after expulsionof the structurally or chromosomally abnormal fetus.We would not like to remove the placenta of abnormalfetus after expulsion of abnormal fetus because its pla-centa located between uterine wall and the non-affect-ed co-twin. If we tried to remove this placenta beforecervical cerclage, it would result in premature ruptureof membranes of the non-affected co-twin and thustotal pregnancy loss. Therefore, we performed cervicalcerclage after expulsion of abnormal fetus to prolongthe pregnancy and to achieve viability of the non-affected co-twin. On the other hand, it may be consid-ered as good prognostic factor for dichorionic twins.

ConclusionSelective termination is a safe procedure with a lowrate of pregnancy loss when performed by experiencedoperators. However, many of the risks related to mul-tifetal pregnancies including preterm labor and deliv-ery may reduce with ST so that ST would be a benefitto the remaining fetus(es) by terminating a fetus with alethal anomaly. But unintended pregnancy loss before24 weeks of gestation is the most important complica-tion of ST. Cervical cerclage may take into considera-tion an alternative to prolong the pregnancy in thosecases, although the retention of nonviable fetal placen-ta following expulsion of nonviable fetus after ST mayincrease maternal and fetal risk. Prophylactic antibio-therapy and close follow-up after cervical cerclageseems to be a reasonable choice to prevent the loss ofnon-affected co-twin and achieve viability of non-affected co-twin.

Conflicts of Interest: No conflicts declared.

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References1. Berkovitz A, Biron-Shental T, Pasternak Y, Sharony R,

Hershko-Klement A, Wiser A. Predictors of twin pregnancyafter ovarian stimulation and intrauterine insemination inwomen with unexplained infertility. Hum Fertil (Camb) 2017;20:200–3.

2. Chaabane S, Sheehy O, Monnier P, Bissonnette F, TraslerJM, Fraser W, et al. Ovarian stimulators, intrauterine ›nsem-ination, and assisted reproductive technologies use and therisk of major congenital malformations – The AtRISKStudy. Birth Defects Res B Dev Reprod Toxicol 2016;107:136–47.

3. Sagot P, Bechoua S, Ferdynus C, Facy A, Flamm X, GouyonJB, et al. Similarly increased congenital anomaly rates afterintrauterine insemination and IVF technologies: a retrospec-tive cohort study. Hum Reprod 2012;27:902–9.

4. Bahtiyar MO, Dulay AT, Weeks BP, Friedman AH, CopelJA. Prevalence of congenital heart defects in monochorion-ic/diamniotic twin gestations: a systematic literature review.J Ultrasound Med 2007;26:1491–8.

5. Luke B, Keith LG. Monozygotic twinning as a congenitaldefect and congenital defects in monozygotic twins. FetalDiagn Ther 1990;5:61–9.

6. Hardin J, Carmichael SL, Selvin S, Lammer EJ, Shaw GM.Increased prevalence of cardiovascular defects among 56,709California twin pairs. Am J Med Genet A 2009;149A:877–86.

7. Berkowitz RL, Lynch L. Selective reduction: an unfortunatemisnomer. Obstet Gynecol 1990;75:873–4.

8. Coffler MS, Kol S, Drugan A, Itskovitz-Eldor J. Early trans-vaginal embryo aspiration: a safer method for selectivereduction in high order multiple gestations. Hum Reprod1999;14:1875–8.

9. Mansour RT, Aboulghar MA, Serour GI, Sattar MA, KamalA, Amin YM. Multifetal pregnancy reduction: modificationof the technique and analysis of the outcome. Fertil Steril1999;71:380–4.

10. Lipitz S, Shulman A, Achiron R, Zalel Y, Seidman DS. Acomparative study of multifetal pregnancy reduction fromtriplets to twins in the first versus early second trimesters afterdetailed fetal screening. Ultrasound Obstet Gynecol 2001;18:35–8.

11. van de Mheen L, Everwijn SM, Knapen MF, Oepkes D,Engels M, Manten GT, et al. The effectiveness of multifetalpregnancy reduction in trichorionic triplet gestation. Am JObstet Gynecol 2014;211:536.e1–6.

12. Eddleman KA, Stone JL, Lynch L, Berkowitz RL. Selectivetermination of anomalous fetuses in multifetal pregnancies:two hundred cases at a single center. Am J Obstet Gynecol2002;187:1168–72.

13. Berkowitz RL, Stone JL, Eddleman KA. One hundred con-secutive cases of selective termination of an abnormal fetusin a multifetal gestation. Obstet Gynecol 1997;90:606–10.

14. Evans MI, Goldberg JD, Horenstein J, Wapner RJ, AyoubMA, Stone J, et al. Selective termination for structural, chro-mosomal, and Mendelian anomalies: international experience.Am J Obstet Gynecol 1999;181:893–7.

15. Eddleman KA, Stone JL, Lynch L, Berkowitz RL. ST ofanomalous fetuses in multifetal pregnancies: two hundredcases at a single center. Am J Obstet Gynecol 2002;187:1168–72.

16. Evans MI, Ciorica D, Britt DW, Fletcher JC. Update onselective reduction. Prenat Diagn 2005;25:807–13.

17. Evans MI, Goldberg JD, Dommergues M, Wapner RJ,Lynch L, Dock BS, et al. Efficacy of secondtrimester selec-tive termination for fetal abnormalities: international collab-orative experience among the world’s largest centers. Am JObstet Gynecol 1994;171:90–4.

18. Lynch L, Berkowitz RL, Stone J, Alvarez M, Lapinski R.Preterm delivery after selective termination in twin pregnan-cies. Obstet Gynecol 1996;87:366–9.

19. Y›lanl›oglu NC, Semiza A, Arisoya R, Kahraman S, GürkancA. The outcome of the multifetal pregnancy reduction pro-cedures in a single centre: a report of 202 completed cases.Eur J Obstet Gynecol Reprod Biol 2018;230:22–7.

20. van de Mheen L, Everwijn SM, Knapen MF, Haak MC,Engels MA, Manten GT, et al. Pregnancy outcome afterfetal reduction in women with a dichorionic twin pregnancy.Hum Reprod 2015;30:1807–12.

20. Nobili E, Paramasivam G, Kumar S. Outcome followingselective fetal reduction in monochorionic and dichorionictwin pregnancies discordant for structural, chromosomal andgenetic disorders. Aust N Z J Obstet Gynaecol 2013;53:114–8.

22. Roman A, Rochelson B, Martinelli P, Saccone G, Harris K,Zork N, et al. Cerclage in twin pregnancy with dilated cervixbetween 16 to 24 weeks of gestation: retrospective cohortstudy. Am J Obstet Gynecol 2016;215:98.e1–98.e11.

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Volume 27 | Issue 2 | August 2019

PERINATALJOURNAL

Contents

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68

77

101

The impact of distress experienced during pregnancy on prenatal attachment

Anayit Margirit Coflkun, Gülflen Okcu, Sedef Arslan

The management of persistent adnexal masses in cesarean section

Aflk›n Evren Güler, Zeliha Çi¤dem Demirel Güler, Özge fiehirli Kinci

The role of systemic inflammatory indexes in predicting preeclampsia and its severity

Onur Bektafl, K›v›lc›m Bektafl, Cuma Tafl›n

Determination of median values of triple screening test hormones for Kayseriregion and their cross-regional comparisons

Nahide Ekici Günay

The knowledge, attitude and behavior levels of midwifery students for thenon-pharmacological methods used in the management of labor pain

Ayfer Arslan, Gamze Temiz

The evaluation of cesarean section rates in accordance with Robson Ten-GroupClassification System and the data of perinatology (tertiary center)

Hüseyin K›yak, Gökhan Bolluk, Emel Canaz, Semra Yüksel, Ali Gedikbafl›

Seasonal change of the prevalence of hypertensive disorders of pregnancy

Cuma Tafl›n, K›v›lc›m Bektafl

Anthropometric differences in the newborns with brachial plexus palsy,clavicle fracture in pregnancies without risk factor

Hüseyin K›yak, Alev At›fl Ayd›n, Gökhan Bolluk, Emel Canaz,Zemzem Ulaflk›n, Ali Gedikbafl›

Fetal conotruncal heart anomalies: is four-chamber view sufficient in theprenatal screening?

Baflak Kaya, Deniz Kanber Açar, Ahmet Tayyar, Helen Bornaun,Pelin Ayy›ld›z, ‹brahim Polat

A case achieved at 28 weeks of gestation by cervical cerclage withretained placenta after expulsion of nonviable fetus underwent selectivetermination in multifetal pregnancy

P›nar Özcan, Mehmet Serdar Kütük, Taha Takmaz, Havva Sevde ‹fllek

Original Article

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Case Report

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