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Periodontal Disease and the Risk for Adverse Pregnancy Outcomes (3 CEUs) Engaging Hygienists, Nurses and Social Service Professionals in Prevention and Early Care of Oral Disease in Women of Childbearing Age An Obstetrician and Periodontist Translate Periodontal-Systemic Research to Preserve the Health of Pregnant Women A Peer-Reviewed Journal November 2006, Vol. 1, No. 4

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Page 1: Periodontal Disease and the An Obstetrician andPeriodontal Disease and the Risk for Adverse Pregnancy Outcomes (3 CEUs) Engaging Hygienists, ... from both dentistry and medicine, in

Periodontal Disease and theRisk for Adverse

Pregnancy Outcomes (3 CEUs)

Engaging Hygienists, Nurses and Social Service

Professionals in Prevention and

Early Care ofOral Disease in Women of

Childbearing Age

An Obstetrician and Periodontist Translate Periodontal-SystemicResearch to Preserve

the Health ofPregnant Women

A Peer-Reviewed Journal

November 2006, Vol. 1, No. 4

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Better Oral Health for Better Overall Health

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*#1 recommended by periodontists does not include specialty toothpastes.1. Data on file. Colgate-Palmolive, New York, NY. 2. Panagakos FS, et al. J Clin Dent. 2005;16(suppl):S1-S19.

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TABLE OF CONTENTSA Peer-Reviewed Journal

GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4 1

VOLUME 1, NUMBER 4 — NOVEMBER 2006

Raising the Bar 7 Stephanie BrunnerStudents Step up to Make a Difference in Prenatal Care Elizabeth Rugroden Kimberly Hanson

Letter from the Editors 8 Casey HeinCharles M. Cobb

Guest Editorial 10 Renee SamelsonGrand Rounds with Dr. Renee Samelson

Literature Review 14 David W. PaquettePeriodontal Disease and the Risk for Adverse Pregnancy Outcomes

Continuing Education Test 26

Original Article 28 Steven J. KerpenAn Obstetrician and Periodontist Translate Periodontal- Adiel FleischerSystemic Research to Preserve the Health of PregnantWomen at Risk for Adverse Pregnancy Outcomes

Original Article 40 Jacki S. WittEngaging Hygienists, Nurses and Social Service Karen B. WilliamsProfessionals in an Interdisciplinary Model for Prevention Patricia J. Kellyand Early Care of Oral Disease in Women of Childbearing Age

Raising the Bar 50 Ronald BurakoffNew York State Leading the Way in Establishing Guidelines for Oral Care in Pregnancy

Tools for Implementation 54

Statement of Editorial Purpose: The editorial purpose of Grand Rounds in Oral-Systemic Medicine™ is to raise awareness of the importance of the relationship between oral and systemic health, and advance the understanding of oral-systemic science and its appropriate integration into the clinical practice of mainstream dentistry and medicine by providing editorial that:• Compels members of the dental and medical communities to embrace the growing body of science called oral-systemic medicine and accept the

uncertainty of its ongoing evolution.• Translates/transfers credible and relevant scientifi c fi ndings and scholarly thought related to oral-systemic medicine into authoritative editorial

that is educational and engages all sectors of the health-care professions (i.e., physicians and nurses, dentists and hygienists and allied health-care providers).

• Stimulates collaboration and innovative thinking on how to transcend professional boundaries to integrate clinical protocols that include application of oral-systemic medicine in everyday patient care.

Policy on Submission of Manuscripts: The opportunity to contribute to the editorial mission of Grand Rounds in Oral-Systemic Medicine™ is offered to author candidates by honorary invitation. As such, unsolicited manuscripts are generally not accepted. Manuscripts published in Grand Rounds in Oral-Systemic Medicine™ are written by authors who are invited to contribute to this body of knowledge based upon their academic, research or clinicalexpertise, from both dentistry and medicine, in specifi c subject matters that pertain to oral-systemic medicine.

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Oral health may be influenced by plaque control, nutrition, fluoride

exposure, hormonal changes, medical conditions, medications

and/or medical treatments. Oral bacteria (plaque) produce

acids that may destroy tooth enamel after long

periods of time. Frequency of a highly acidic oral

environment increases the risk for dental disease.

In many cases, dental disease can be prevented.

Prevention starts as early as primary tooth

development. Oral health care should be

promoted throughout pregnancy, infancy,

childhood, teen and adult life. Special attention

to oral care should be enforced when certain

medical conditions may influence the oral

environment. Increased awareness of potentially

unhealthy oral conditions may help prevent oral

infection, or promote early detection, thereby

motivating improvement and management.

Monitoring oral pH will allow patients to evaluate an

acidic environment, and change their oral care routines to

increase oral pH to a healthier level, thereby reducing the risk of

dental disease.

Beutlich® pH Paper15 ft. roll of pH paper, dispenser and color chart to test saliva pH in the range of 4.5-7.5

• Identify an acidic oral environment

• Increase awareness through regular monitoring

• Improve oral care to prevent continuous exposureto acid production

• Reduce risk of dental caries or periodontal disease

• For in-vitro use only

Ask your Beutlich representative for more information or contact us at (800) 238-8542 M-Th: 7:30 a.m. – 5:00 p.m., F: 7:30 a.m. – 4:00 p.m. CT. www.beutlich.com.

PROMOTE HEALTH

Prevent Disease

PHMJ 310 1205

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Casey Hein, BSDH, MBA, Chief Editor,[email protected]

Charles M. Cobb, DDS, PhD, Editor-at-Large,[email protected]

Lyle Hoyt, Senior Vice President,Group Publisher, [email protected]

Craig Dickson, Publisher,[email protected]

Kersten Hammond, BS, Technical Editor,[email protected]

Zach Turner, Medical Illustrator,[email protected]

Duane DaPron, Coordinator of Editors Contributing Editors — Penny Anderson,Ted Anibal, Vicki Cheeseman, Mark Hartley, Kevin Henry, Meg Kaiser, Kristen Wright

Production — Katie Blair, Production Mgr.

Salomon Amar, DDS, PhDBoston University

Caren Barnes, RDH, MSUniversity of Nebraska Medical Center

Don Callan, DDSPrivate Practice, Little Rock, AR

Christina DeBiase, BSDH, MA, EdDWest Virginia University

Tim Donley, DDS, MSDPrivate Practice, Bowling Green, KY

James Ferguson, II, MDUniversity of Kentucky

William Giannobile, DDS, MS, DMedScUniversity of Michigan

Joan Gluch, RDH, PhDUniversity of Pennsylvania

Lorne Golub, DMD, MSc, MD (honorary)State University of NY at Stony Brook

Marilyn Goulding, RDH, BSc, MOSNiagara College of Canada

Martin Greenfi eld, MDPrivate Practice, Great Neck, NY

Robert Greenwald, MDLong Island Jewish Medical Center, NY

Sara Grossi, DDS, MSEast Carolina University

AdministrationFrank T. Lauinger, Chairman;Robert F. Biolchini, President & CEO

Display SalesEast: Chris Page, (518) 373-0622Key Accounts: Craig Dickson, (630) 690-2472Southeast: David Hurlbrink, (717) 244-3148Midwest/West: Amy Frazin, RDH,

(773) 763-7680Pennsylvania, Delaware: Auggie James

(847) 548-0409Midwest/South: Marvin R. Ashworth,

(800) 331-4463, ext. 6266Sales Assistant: Machele Galloway,

(918) 831-9756Circulation — Linda Thomas, Manager; Kelli

Berry, Mailing List Sales, (800) 944-0937

J. Michael Gruenwald, MDUniversity of Arkansas for Medical Sciences

JoAnn Gurenlian, RDH, PhDPrivate Consulting, Haddonfi eld, NJ

Georgia Johnson, DDS, MSUniversity of Iowa

Lauren Kilmeade, RDHPrivate Practice, Great Neck, NY

Barbara Kunselman, RDH, MSUniversity of Cincinnati

Evanthia Lalla, DDS, MSColumbia University

Samuel Low, DDS, MS, MEdUniversity of Florida

Simon MacNeill, BDS, DDSUniversity of Missouri-Kansas City

Diane McClure, RDH, MSSt. John’s Hospital, Springfi eld, MO

Lenora McClean, RN, EdDState University of NY at Stony Brook

Brian Mealey, DDS, MSUniversity of Texas at San Antonio

Sushma Nachnani, PhDClinical Research, Culver City, CA

John Novak, BDS, LDS, MS, PhDUniversity of Kentucky

Grand Rounds in Oral-Systemic Medicine™ (ISSN #1559-6133 [1559-6141, digital version]). Published quarterly by PennWell Corporation, 1421 S. Sheridan, Tulsa, OK 74112. Subscrip-tions for 1 year are $100 for USA, $120 for international; single-copy rates are $25 for USA, $30 for international. POSTMASTER: Please send change of address Form 3579 to Grand Rounds in Oral-Systemic Medicine™, P.O. Box 3557, Northbrook, IL 60065-3557. Return un-deliverable Canadian addresses to P.O. Box 122, Niagara Falls, ON L2E 6S4 ©2005 by PennWell Corporation. All rights reserved. The opinions expressed in articles in this magazine are those of the authors or sources stated and not those of the publisher. All prices quoted in advertisements are in U.S. funds. Portions of the subscriber list are made available to carefully screened compa-nies that offer products and services that may be important for your career. If readers do not wish to receive those offers and/or information, please contact list services at (847) 559-7501.

Staff

2006 Advisory BoardDavid Paquette, DMD, MPH, DMSc

University of North Carolina at Chapel Hill

William Reeves, DDSPrivate Practice, Oklahoma City, OK

Jonathan Richter, DDSPrivate Practice, Great Neck, NY

C. Austin Risbeck, RDHPrivate Practice, San Francisco, CA

Louis Rose, DDS, MDPrivate Practice, Philadelphia, PA

Maria Ryan, DDS, PhDState University of NY at Stony Brook

Frank Scannapieco, DMD, PhDState University of NY at Buffalo

James Sciubba, DMD, PhDJohns Hopkins University

Stanley Shanies, MD, FACPPrivate Practice, New Hyde Park, NY

Jon Suzuki, DDS, PhD, MBATemple University

Cheryl Thomas, RDHPrivate Consulting, Galveston, Texas

Clay Walker, PhDUniversity of Florida

Karen Williams, RDH, MS, PhDUniversity of Missouri-Kansas City

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Raising the Bar

Pregnancy is an exciting time for expectant parents; however, most expectant parents are unaware of the potential impact periodontal infection has on the gesta-

tion period and birth weight of newborns. One of our dental hygiene instructors, Debbie Schumacher, brought this unmet area of healthcare to our attention. After we researched the evidence that supports a relationship between periodontal disease and preterm birth (PTB), we were compelled to fol-low our instructor’s lead. We developed a prenatal education-al program to help pregnant women understand the impor-tance of oral health. Another key component was teaching expectant parents about prevention of childhood caries. Our presentation covers oral hygiene during pregnancy in addi-tion to infancy and childhood. To complement our PowerPoint presentation, we developed a pamphlet, and pre- and post-quizzes that were given to expectant parents at each class. Some of the issues discussed with the parents are pregnancy gingivitis, periodontitis, baby bottle decay, early childhood caries, the importance of retaining the primary dentition, what to do when children have avulsed teeth, and the benefi ts of xylitol.

Currently, we are delivering our presentation to prenatal classes at Luther Midlefort Hospital in Eau Claire, WI. The prenatal class director has been very supportive and introduces us by telling her class, “Listen closely, as this is infor-mation that you will not get from your nurse practitioner, obstetrician, gynecologist, pediatrician, or anyone else”. The expectant parents in the prenatal classes have been receptive and many are surprised by how much their perception of oral health infl uences the oral health of their children. Data from the pre-test indicate that most expectant parents do not know how to detect signs of decay in their children’s mouths, and most are unaware that babies acquire cariogenic bacteria through saliva transmission, such as sharing a spoon and other saliva sharing activities. Overall, expectant parents provide positive feedback and recommend this information be incorporated into all prenatal classes.

In Community Dental Health class we are working toward certifi cation to teach healthcare providers about the oral-sys-temic link and how to administer fl uoride varnishes at well baby visits. This certifi cation will allow us to extend our reach to more healthcare professionals, with greater opportunities to distribute our educational materials. We are also developing a new program aimed at increasing the awareness of the oral-systemic link among local nurses, obstetricians, and gyne-cologists, with the hope they will incorporate this information into their practices. In the near future, we plan to reach out to low income populations by educating nurse practitioners affi liated with Women Infant and Children (WIC) programs. By doing this, the nurse practitioners can inform and instruct women on how to care for themselves and their children.

The experiences we have shared in developing and implementing these educational programs have been fulfi lling and it is rewarding to know we are helping our community. The goals of these programs have focused more on pre-vention than treatment. We believe that if prevention becomes a priority in our community, we will be able to look forward to a decrease in PTBs, a decrease in baby bottle decay, a decrease in early childhood caries, and improved oral and systemic health.

By Stephanie Brunner, Elizabeth Rugroden, and Kimberly Hanson†

Students Step up to Make a Differencein Prenatal Care

Left to right: Dental hygiene students Kimberly Hanson, Elizabeth Rugroden, and Stephanie Brunner.

† Dental hygiene students at Chippewa Valley Technical College, Eau Claire, WI

GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4 7

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Casey Hein Charley Cobb

Evidence to support the link between periodontal disease and the potential for serious consequences to systemic health has provided us with new opportunities for intervention of interrelated infl ammatory diseases and conditions. Yet, the opportunity to make the most signifi cant difference may be in addressing “the legacy link”. By applying what we have

learned about the association of periodontal diseases and the risk for adverse pregnancy outcomes, we may have the op-portunity to touch two lives — the life of the mother and the life of the child. Indeed, the science in support of medical-dental guidelines related to oral healthcare in pregnancy has evolved. These guidelines provide the potential to reverse the risk of adverse pregnancy outcomes for multiple generations, thereby providing a lasting legacy of healthcare.

This holds great promise for the fi eld of obstetrics. With the steady increase of overall preterm birth (PTB) rate in the United States, new models of care are well overdue. Today, about 10% of all births are preterm, with the frequent aftermath of serious functional abnormalities such as asthma, low IQ, cerebral palsy, and poor motor skills which often convey lifelong limitations for premature infants. Approximately one-half of all preterm deliveries present with an unknown etiology. It is hypothesized that maternal infection and infl ammation may play a primary role in many of these unexplained preterm deliveries. The imperative for enlisting dental professionals in the fi ght to extend gestation stems from scientifi c evidence implicating bacterial organisms associated with periodontal diseases in triggering a cascade of immunoinfl ammatory events which may eventuate PTB.

What could be the magnitude of impact on the incidence of adverse pregnancy outcomes and prematurity if medical and dental providers began to share knowledge and collaborate to achieve the best possible outcomes of prenatal care? The authors who contributed to this issue of Grand Rounds in Oral-Systemic Medicine™ are all committed to fi nding that answer. We are particularly honored to have Dr. Renee Samelson, a highly respected obstetrician, weigh in on the importance of oral health during pregnancy in her guest editorial. Samelson was among those who spearheaded New York State Department of Health’s recently released practice guidelines on Oral Health Care during Pregnancy and Early Childhood, the fi rst guidelines to discuss the role of both medical and dental providers in caring for the oral health of pregnant women. Dr. David Paquette’s cut-to-the-chase review of the literature related to periodontal disease and adverse pregnancy outcomes will provide readers with a comprehensive look at the present state of this research. Case studies contributed by a private practice periodontist, Dr. Steven Kerpen, in collaboration with a highly respected neonatologist, Dr. Adiel Fleischer, demonstrate the rationale for proper oral evaluation and appropriate referral of pregnant women at risk from oral infl ammation. And fi nally, academic nursing and dental hygiene professionals, Witt, Kelly, and Williams, team up to propose a collaborative approach to preconceptional care aimed at decreasing the risk for preterm labor and birth. Their work in this area presents a very compelling rationale for transdisciplinary care specifi c to obstetrics.

We believe that these authors’ contributions to this special issue of Grand Rounds will provide our readers with convincing evidence of the risk periodontal diseases pose during pregnancy, and a vision for future models of care that show promise in dramatically decreasing the rate of adverse pregnancy outcomes. For future generations of women who may be at greater risk for complications of pregnancy, and their offspring who may be at risk for PTB, we must embrace these new models of collaborative care, and with this commitment, perhaps provide one of the greatest promises yet in reversing the legacy link.

Letter from the Editors

CAN SHARED RESPONSIBILITY FOR PREGNANCY OUTCOMES REVERSE THE LEGACY LINK?

8 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

Sincerely yours,

Casey Hein, BSDH, MBA Charles Cobb, DDS, MS, PhDChief Editor, [email protected] Editor-at-Large, [email protected]

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In 2001, the New York State Department of Health received a letter from a practicing physician from Guthrie Clinic, near Owego, New York, regarding his concerns about lack of access to dental care. He detailed the case of a pregnant woman who could not find a dentist to treat her abscessed teeth. She self-treated with

large doses of acetaminophen and her liver eventually failed. The fetus died, and the woman was transported to Pittsburgh for a liver transplant.

We know that a woman’s health during pregnancy affects both her and her fetus. Although dentists are trained inde-pendently from physicians and insurance reimbursements are managed separately, oral health remains a vital part of overall health. With periodontal disease detectable in up to 30% of pregnant women, why is it so diffi cult for these women to fi nd dentists willing to treat them, especially when emerging evidence shows an association between peri-odontal disease and adverse pregnancy outcomes, such as premature delivery and low birth weight (LBW)?1

Part of the answer lies in the fact that until this year, there were no evidence-based guidelines for dentists concerning the care of pregnant women.

I was honored to work with Drs. Jayanth Kumar and Elmer Green and the Bureau of Dental Health at the New York State Department of Health to address this problem. This initiative focused on developing a consensus opinion derived from an expert panel charged with the responsibility to develop guidelines for prenatal care providers, oral health professionals, and child health professionals with respect to the oral health of pregnant women. These guidelines, entitled “Oral Health Care during Pregnancy and Early Childhood: Practice Guidelines,” have recently been published. The hope is that these guidelines will give dentists the information and confi dence they need to begin to treat pregnant women in their practices.

The New York State guidelines were developed to incorporate oral health into routine healthcare practices. The guide-lines propose that prenatal care providers assess maternal oral health and oral health professionals provide needed care to pregnant women. These clinical practices can have a profound impact on oral health and thus overall health of women and their families.

Another goal of the guidelines is to change the perceptions of pregnant women regarding the importance of oral health, and to dispel misconceptions about dental care. For example, dental work during pregnancy does not increase the risk of spontaneous abortions or result in other harm to the fetus. The guidelines encourage women to consider dental visits as routine and equally as important as getting an ultrasound during pregnancy. Prenatal care occurs at a unique time in women’s lives, when women are motivated to improve health behaviors. Prenatal care of most pregnant women is covered by commercial insurance or Medicaid (in most states), which provides health care professionals and educators a specifi c window of opportunity to challenge the misperception that oral healthcare in pregnancy is a luxury and intercept women at risk for adverse pregnancy outcomes.

It is also important to educate mothers about the ways in which they can promote their children’s oral health. Tooth de-cay remains the single most common chronic disease of childhood causing untold misery for children and their families.2 Early childhood caries (ECC) is not simply the result of a bad inheritance and too much candy — today we know that ECC is a preventable infectious disease. Research indicates that mothers and other intimate caregivers who harbor cario-

Guest Editorial

Renee Samelson, MD, MPH, FACOG, Associate Medical Director, Division of Family Health, New York State Department of Health, Albany, NY

GRAND ROUNDS WITHDR. RENEE SAMELSON

10 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

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• Do Not Inject

• Needle-free anesthesia for adults for scaling and root planing procedures

• Can be used for a single tooth, quadrant or whole mouth

• 30-second onset

(lidocaine and prilocaine periodontal gel) 2.5% / 2.5%

®

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To order or for more information on Oraqix, contact your authorized DENTSPLY distributor or call DENTSPLY Customer Service at 1.800.225.2787.Visit our website at www.oraqix.com.

Needle-free, Patient Friendly Anesthesia for Scaling & Root Planing

Don't Get Stuck Without It!• Oraqix is a novel formulation of lidocaine and prilocaine that dispenses as a liquid, then sets as a gel at body temperature.• Oraqix should not be used in those patients with congenital or idiopathic methemoglobinemia. • Indicated for adults who require localized anesthesia in periodontal pockets during SRP procedures. • Contraindicated in patients with hypersensitivity to amide type local anesthetics or any other product component.• Oraqix is applied first to the gingival margin, then periodontal pocket with the use of an Oraqix™ Dispenser and a blunt-tip applicator.• Most common adverse reactions in clinical studies were application site reactions, headache and taste perversion.Please see the accompanying brief summary of the prescribing information.

PM-Oraqix-0119 11/06

PHARMACEUTICAL

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11/0611/06

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genic bacteria in their mouths can spread these bacteria to their infants during saliva-sharing activities.3 Mothers need to know that activities like tasting baby’s food with a spoon that is then placed into the baby’s mouth can result in ECC.3 Some communities have partnered with dental hygienists to provide teaching and dental prophylaxis to pregnant women followed up by home visits during the fi rst year of life to reinforce healthy behaviors that mini-mize the transmission of cariogenic bacteria.

The importance of maternal oral health cannot be over-emphasized. With the understanding that LBW is a com-mon endpoint of a multifactorial problem, we must edu-cate consumers and health professionals to understand that oral infection may be the origin of infection of the placental unit. The message that oral infection and in-fl ammation can present a signifi cant challenge to preg-nant women must be reinforced and presented to a wide array of practitioners. I agree with Dr. Maria Ryan when she wrote, “As emerging information is shared with prac-titioners in publications such as this one, both medical and dental professionals will be empowered to make treatment decisions based on the latest fi ndings”.4

Interdisciplinary care is healthcare rendered in an orga-nized framework by a variety of disciplines.5 Ideal pre-

natal care has traditionally been provided by a team that includes the prenatal care provider, clinic nursing staff, nutritionist, medical social worker, and ultrasonographer. This issue of Grand Rounds in Oral-Systemic Medicine™ will provide clinicians with the knowledge they need to incorporate oral healthcare and education into prenatal care. From now on, we must insist that this team also include the oral health professional.

References1. Scannapieco FA, Bush RB, Paju S. Periodontal disease as a

risk factor for adverse pregnancy outcomes. A systematic

review. Ann Periodontol 2003;8:70-78.

2. Beltran-Aguilar ED, Barker LK, Canto MT, et al. Surveillance

for dental caries, dental sealants, tooth retention, edentulism,

and enamel flurosis - United States, 1988-1994 and 1999-

2002. [54/SS-3], 1-44. 8-26-2005. Atlanta, GA, Epidemiology

Program Office, CDC. MMWR.

3. Berkowitz R. Causes, treatment and prevention of early

childhood caries: A microbiologic perspective. J Can Dent Assoc 2003;69:304-307.

4. Ryan M. Grand rounds with Dr. Maria Ryan. Grand Rounds in Oral-Sys Med 2006;1:12-13.

5. Duthie EH. Grand rounds with Dr. Edmund H. Duthie Jr.

Grand Rounds in Oral-Sys Med 2006;3:10-13.

Grand Rounds with Dr. Renee Samelson

GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4 13

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Introduction

Pregnancy and parturition involve a complex series of molecular and biological events for mother and fetus. Preg-nancy complications, which include preterm delivery and LBW, represent major public health problems because of their prevalence, associated mortality, economic burden and long-term disability. Approximately 500,000 in-

fants or 12.3% of all births in the U.S. were delivered preterm (gestational age <37 weeks) in 2003 (a 16% increase since 1990).1 Similarly, 7.8% of infants were classifi ed as having (LBW) (births weighing <2,500 g or 5.5 lb: an 18% increase since 1984). Very low birth weight (VLBW, births weighing <1,500 g or 3.3 lb) affected only 1.4% of infants and has been essentially stable since 1998. Preterm delivery, LBW and VLBW are associated with increased risks for early death and costs for care. Preterm infants are 75 times more likely to experience early death.1 Meanwhile, the risks of early death are 5 times higher and more than 100 times higher for moderately LBW (1,500–2,499 g) and VLBW infants respectively as compared with normal weight infants. While hospital inpatient service costs are consistently and signifi cantly higher for preterm infants, cumulative healthcare costs for each surviving preterm infant over the fi rst 5 years of life were ap-proximately $20,000 higher than the estimated costs for term infants (1998-1999).2 Long term disability for surviving preterm infants include pulmonary abnormalities, cerebral palsy and neurological or developmental disabilities.3,4

Human observational studies have identifi ed a number of risk factors for preterm delivery and LBW infants.5 These include maternal age <18 years or >35 years, underweight or overweight prior to the pregnancy, short stature and smoking. Women who are black, African American or of low socioeconomic status have higher rates for pregnancy com-plications. Physical and psychological stresses have also been associated with higher preterm rates. Overall, a maternal or

David W. Paquette, DMD, MPH, DMSc†

AbstractAdverse pregnancy complications, which include preterm delivery, delivery of low birth weight (LBW) infants and preeclampsia, represent major public health problems in the United States (U.S.) and globally. While infl ammatory events in maternal and fetal membranes occur during normal parturition, they appear elevated for preterm deliver-ies. The objective of this article is to examine whether periodontal disease or infection may contribute to the risk for preterm birth (PTB) and other pregnancy complications from an evidence-based perspective. Observational human studies conducted over the past decade demonstrate a consistent and strong association between maternal exposure to periodontal disease and adverse pregnancy outcomes. Current data from 4 clinical trials indicate that mothers receiving periodontal disease interventions exhibit a lower incidence of preterm delivery and LBW infants. Maternal and fetal exposures to gram-negative periodontal pathogens and their products appear to trigger infl ammatory events in both mother and the fetus, which may stimulate early rupture of membranes and parturition. While the comple-tion and publication of defi nitive intervention studies are forthcoming, clinicians and patients should be aware of this emerging evidence and should appreciate the role of maternal oral health during pregnancy.

Citation: Paquette D. Periodontal disease and the risk for adverse pregnancy outcomes. Grand Rounds in Oral-Sys Med

2006;4:14-24. (Digital version Grand Rounds in Oral-Sys Med 2006;4:14-25a.)

(A complimentary copy of this article may be downloaded at www.thesystemiclink.com.)

Key Words: Periodontal disease, infl ammation, pregnancy, low birth weight, preeclampsia

† Associate Professor and Graduate Program Director, Department of Periodontology, Center for Oral and Systemic Diseases, University of North Carolina School of Dentistry, Chapel Hill, NC

PERIODONTAL DISEASE ANDTHE RISK FOR ADVERSEPREGNANCY OUTCOMES

Literature Review

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Paquette. Periodontal disease and the risk for adverse pregnancy outcomes

Reference Population Periodontal Outcome Adverse Pregnancy Findings and Conclusions or Exposure Outcome

Offenbacher U.S.; ≥60% of sites with Birth weight <2,500 g, Signifi cant association betweenet al. 1996 (16) 93 cases and clinical attachment gestational age <37 periodontal disease and preterm LBW 31 controls levels ≥3 mm weeks, preterm labor (OR=7.5, 95% CI 1.95-28.8) and/or premature rupture of membranes

Davenport United Kingdom; Mean pocket depth Preterm delivery <37 No association detected foret al. 2002 (31) 236 cases and (mm) weeks and birth weight periodontal disease and preterm LBW 507 controls <2,499 g (OR=0.83, 95% CI 0.68-1.00)

Goepfert U.S.; Clinical attachment Spontaneous PTB Signifi cantly higher risk for PTBet al. 2004 (22) 59 cases and levels ≥5 mm <32 weeks for mothers with periodontal 44 controls disease (OR=3.4, 95% CI 1.5-7.7)

Radnai Hungary; 41 ≥1 site with probing Premature labor, Signifi cant association betweenet al. 2004 (26) cases and 44 depth ≥4 mm and spontaneous rupture of periodontal disease and preterm LBW controls bleeding on probing membranes and/or the (OR=5.4, 95% CI 1.7-17.3) ≥50% birth weight of the newborn ≤2,499 g

Jarjoura U.S.; ≥5 sites with Preterm delivery Signifi cant association betweenet al. 2005 (23) 83 cases and clinical attachment <37 weeks periodontal disease and preterm 120 controls levels ≥3mm delivery (OR=2.75, 95% CI 1.01-7.54)

Moliterno Brazil; 76 cases ≥4 sites with pocket Preterm delivery <37 Signifi cantly higher risk for pretermet al. 2005 (29) and 75 controls depth ≥4 mm and weeks and birth weight LBW for mothers with periodontal clinical attachment <2,500 g disease (OR=3.48, 95% CI 1.17-10.36) levels ≥3 mm

Buduneli Turkey; 53 cases Mean pocket depth Preterm delivery <37 No statistically signifi cant differenceset al. 2005 (33) and 128 controls (mm) weeks or birth weight between the cases and controls with re- <2,500 g gard to clinical periodontal parameters

Moore United Kingdom; Number of sites Preterm delivery No association between periodontalet al. 2005 (37) 61 cases and with pocket depth <37 weeks disease and PTB 93 controls ≥5mm

Bosnjak Croatia; 17 cases >60% of sites with Spontaneous PTB Signifi cant association betweenet al. 2006 (24) and 64 controls clinical attachment <37 weeks periodontal disease and PTB levels ≥4 mm (OR=8.13, 95% CI 2.73-45.9)

Skuldbol Denmark; Pocket depth ≥4 Preterm delivery No difference in mean periodontal et al. 2006 (35) 21 cases and mm and bleeding <35 weeks parameters between the 2 groups; 33 controls on probing no association between periodontal disease and PTB

Radnai Hungary; ≥1 site with probing Preterm delivery Signifi cant association betweenet al. 2006 (27) 77 cases and depth ≥4 mm and <37 weeks and periodontal disease and preterm LBW 84 controls bleeding on probing birth weight <2,500 g (OR= 3.32, 95% CI 1.64-6.69) ≥50%

Contreras Colombia; Pocket depth and Preeclampsia: blood Signifi cant association for periodontalet al. 2006 (43) 130 cases and clinical attachment pressure ≥140/90 disease and preeclampsia 243 controls loss ≥4 mm and mmHg and ≥2+ (OR=3.0, 95% CI 1.91-4.87) bleeding on probing proteinuria

Table 1Summary of case control observational studies on periodontal disease and adverse pregnancy outcomes (OR: odds ratio; CI: confi dence interval)

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fetal genetic predisposition for premature birth emerges as one of the stronger risk factors. Women born preterm are more likely to deliver preterm. In addition, approxi-mately 20% of women who deliver a preterm infant sub-sequently have another PTB with the same partner.6 Twin studies of pregnancy complications estimate the herita-bility of PTB ranging between 17 and 36%.7,8 Maternal or fetal genetic polymorphisms in pro-infl ammatory cy-tokines such as tumor necrosis factor-alpha (TNF-α) may increase the risk for preterm delivery at least 2-fold in populations; hence, variations in genes regulating infl am-mation may alter maternal responses to certain exposures during pregnancy and affect the timing of parturition.9,10

One important exposure implicated in PTB is infection of the genitourinary tract, called “bacterial vaginosis”. This infection is generally associated with a decrease in the normal lactobacillus-dominated fl ora of the vagina and an increase in gram-negative anaerobes and facultative species. While bacterial vaginosis is a relatively com-mon condition (approximately 10% of all pregnancies), the bacterial pathogens or their products may ascend to the cervix and cause infl ammation of the maternal-fetal membranes (chorioamnionitis).11 The resulting infl amma-tion of these membranes in turn may initiate preterm la-bor or rupture of membranes.

Infl ammatory events occur in maternal-fetal membranes and the placenta during normal parturition; however, in-fl ammatory cytokine expression is markedly higher for women who deliver preterm.12 These fi ndings support the hypothesis that maternal infections “as exposures” may trigger infl ammatory events involving the fetal-placen-tal unit and stimulate early parturition. The objective of this paper is to examine whether periodontal disease or infection may contribute to the risk for PTB and other pregnancy complications from an evidence-based per-spective.

Observational studies relating to periodontaldisease and preterm low birth weightObservational studies (case control and cohort) relating periodontal disease and preterm LBW are summarized in Tables 1 and 2. At least 3 systematic reviews or meta-analyses have been conducted to examine the available evidence on the relationship between periodontal disease and adverse pregnancy outcomes.13-15 The last of these reviews identifi ed 25 clinical studies, 22 of which were observational (13 case-control and 9 cohort studies).15 The authors highlighted that the majority of the identifi ed studies (18) implicated an association between periodon-tal disease and an increased risk for adverse pregnancy outcomes (odds ratios ranging from 1.10 to 20.0), while only 7 of the studies found no evidence of an association (odds ratios ranging from 0.78 to 2.54 and not statistical-

ly signifi cant). Although the authors noted heterogeneity among the studies for defi nitions of periodontal disease and pregnancy outcomes, they concluded that a positive association between periodontal disease and pregnancy complications likely exists.

Offenbacher and colleagues were the fi rst to hypothe-size that periodontal disease exposes the pregnant host to gram-negative pathogens (e.g., Porphyromonas gin-givalis, Tannerella forsythia and Camplylobacter rec-tus), lipopolysaccharide (LPS, endotoxin) and infl amma-tory mediators (e.g., prostaglandin E2, interleukin-1 and TNF-α) placing the fetal-placental unit at risk for adverse outcomes. Offenbacher and colleagues16 tested their hy-pothesis in a case-control study involving 124 pregnant or postpartum women. Here, cases were defi ned as moth-ers having preterm LBW infants (weighing <2,500 g, gestational age <37 weeks, preterm labor and/or prema-ture rupture of membranes). Controls were all mothers with normal birth weight infants. Assessments included a broad range of known obstetric risk factors such as tobacco usage, drug use, alcohol consumption, level of prenatal care, parity, genitourinary tract infections and weight gain during pregnancy. Each subject received a full-mouth periodontal examination to determine clinical attachment levels. Mothers having preterm LBW infants (for fi rst or any birth) had signifi cantly more advanced periodontal disease or clinical attachment loss than the respective control subjects with normal birth weight in-fants. Multivariate logistic regression models controlling for other known risk factors demonstrated that periodon-tal disease (≥60% of sites with clinical attachment loss ≥ 3mm) was a signifi cant risk factor for preterm LBW with an adjusted odds ratio (OR) of 7.5 (95% CI 1.95-28.8). These initial case control data indicated that women with clinical periodontal disease were 7.5 times more likely to have a preterm LBW infant or adverse pregnancy out-come.

Offenbacher and colleagues17-19 proceeded to conduct a prospective cohort study, entitled Oral Conditions and Pregnancy (OCAP), which was designed to determine whether maternal periodontal disease was predictive of preterm (<37 weeks) or very preterm (<32 weeks) birth. One thousand and twenty pregnant women were peri-odontally examined antepartum (<26 weeks’ gestation) and postpartum. Again, logistic regression models were developed using maternal exposure to either periodon-tal disease at enrollment or disease progression during pregnancy (clinical attachment loss ≥2mm at ≥1 site) as independent variables and adjusting for known risk fac-tors (e.g., previous preterm delivery, race, smoking, social domain variables and other infections). Overall, the in-cidence of PTB was 11.2% among periodontally healthy women, compared with 28.6% in women with moderate-

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Reference Population Periodontal Outcome Adverse Pregnancy Findings and Conclusions or Exposure Outcome

Offenbacher U.S.; Moderate-severe Preterm delivery <37 Moderate-severe periodontal diseaseet al. 2001, 2006; 1,020 subjects disease: ≥4 sites weeks; very preterm (RR=1.6, 95% CI 1.1-2.3) andLieff et al. with pocket depths <32 weeks progressive disease (RR=2.4, 95% CI 2004 (17-19) ≥5 mm and clinical 1.1-5.2) are signifi cant risk factors attachment levels for preterm delivery ≥2 mm; progressive disease: ≥1 site with clinical attachment loss ≥2mm

Jeffcoat et al. U.S.; Severe or Preterm delivery <37 Severe or generalized periodontal 2001 (21) 1,313 subjects generalized disease: weeks disease is associated with preterm ≥90 sites with delivery (OR=4.45, 95% CI 2.16, 9.18) clinical attachment levels ≥3mm

Lopez et al. Chile; ≥4 teeth showing Preterm delivery <37 Signifi cant association between 2002 (30) 639 subjects ≥1 site with pocket weeks and birth weight periodontal disease and preterm LBW depth ≥4 mm and <2500 g (RR=3.48, 95% CI 1.17-10.36) with clinical attachment level ≥3 Boggess et al. U.S.; Severe disease: ≥15 Preeclampsia: blood Signifi cantly higher risk for2003 (42) 763 subjects sites with pocket pressure >140/90 mm preeclamsia among women with severe depths ≥4 mm; Hg and ≥1+ proteinuria (OR=2.4, 95% CI 1.1-5.3) or progressive disease: progressive (OR=2.1, 95% CI 1.0-4.4) ≥4 sites with periodontal disease increases in pocket depth ≥2 mm and resulting in pockets ≥4 mm in depth

Holbrook et al. Iceland; Pocket depth ≥4 Preterm delivery < 37 No association between periodontal2004 (32) 96 subjects mm weeks or birth weight disease and preterm LBW <2,500 g

Moore et al. United Kingdom; % of sites with Preterm delivery <37 No association between periodontal2004 (38) 3,738 subjects pocket depth >4 weeks or birth weight disease case defi nitions and preterm or 5mm <2,500 g delivery or LBW

Moreu et al. Spain; % sites with pocket Preterm delivery <37 Higher severity of periodontal disease2005 (28) 96 subjects depths ≥3 mm weeks and birth weight among those having LBW infants <2,500 g

Rajapaske et al. Sri Lanka; Pocket depth, Preterm delivery < 37 No association between periodontal2005 (34) 227 subjects bleeding and plaque weeks and birth weight disease and preterm delivery scores > median value <2,500 g (OR=2.3, 95% CI 0.9-6.3) in the total cohort Boggess et al. U.S.; Moderate-severe Small-for-gestational-age Association between periodontal2006 (20) 1,017 subjects disease: ≥15 sites births: birth weight disease and small-for-gestational-age with pocket depths <10% for gestational births (RR=2.3, 95% CI 1.1-4.7) ≥4 mm age

Meurman et al. Finland; Community Preterm delivery <37 No association between poor periodontal2006 (36) 207 subjects Periodontal Index weeks, birth weight health and pregnancy or delivery for Treatment <2,500 g, caesarean complications Needs section, gestational diabetes or hypertension, preeclampsia or infant Apgar score <7

Table 2Summary of cohort observational studies on periodontal disease and adverse pregnancy outcomes (OR: odds ratio; RR: relative risk; CI: confi dence interval)

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severe periodontal disease (adjusted risk ratio or RR=1.6, 95% CI 1.1-2.3). Antepartum moderate-severe periodon-tal disease was associated with an increased incidence of spontaneous PTBs (15.2% versus 24.9%, adjusted RR=2.0, 95% CI 1.2-3.2). Similarly, the unadjusted rate of very preterm delivery was 6.4% among women with periodontal disease progression, signifi cantly higher than the 1.8% rate among women without disease progression (adjusted RR=2.4, 95% CI 1.1-5.2). This second study by the Offenbacher group implicated maternal periodontal disease exposure and progression as independent risk factors for PTB outcomes.

A subsequent analysis of OCAP data further indicates that maternal periodontal disease is associated with small-for-gestational-age births.20 Defi ning “small-for-gesta-tional-age” as birth weight less than the tenth percentile for gestational age, Boggess and colleagues20 reported that the prevalence of small-for-gestational-age births was signifi cantly higher among women with moder-ate or severe periodontal disease compared with those with health or mild disease (13.8% versus 3.2%). Indeed, mothers with moderate or advanced periodontal disease were 2.3 times (RR, 95% CI 1.1-4.7) more likely to have small-for-gestational-age infants as compared with moth-ers with periodontal health even after adjusting for age, smoking, drugs, marital/insurance status and preeclamp-sia (i.e., pregnancy-related hypertension with proteinuria or edema).

Jeffcoat and colleagues21 also found a positive associa-tion between maternal periodontal disease and PTB in a comparable U.S. cohort study involving 1,313 pregnant subjects. Complete periodontal, medical and behavioral assessments were made between 21 and 24 weeks’ gesta-tion for each subject. Gestational ages of the infants were determined following delivery, and logistic regression modeling was performed to assess any relationship be-tween periodontal disease and PTB while making adjust-ments for other known risk factors. Notably, subjects with severe or generalized periodontal disease had an adjusted OR of 4.45 (95% CI 2.16, 9.18) for preterm delivery (<37 weeks) as compared with periodontally healthy subjects. The adjusted OR increased with advancing prematurity to 5.28 (95% CI 2.05, 13.60) before 35 weeks gestational age and to 7.07 (95% CI, 1.70-27.4) before 32 weeks ges-tational age. Hence, mothers with severe periodontal dis-ease were 4 to 7 times more likely to deliver a preterm infant relative to mothers with periodontal health.

Two other observational studies involving U.S. populations report a consistent association for maternal periodontal disease and preterm LBW. One case-control study involved 59 women with early spontaneous PTBs (<32 weeks of ges-tation), 36 women with early indicated PTBs (<32 weeks of

gestation), and 44 controls with uncomplicated births at term (≥37 weeks).22 Severe periodontal disease (clinical at-tachment loss ≥5mm) was more common in the spontane-ous PTB group (49%) as compared with the indicated pre-term and term control groups (25% and 30% respectively). The odds for severe periodontal disease and spontaneous PTB were 3.4 (95% CI 1.5-7.7). For the second observation-al study involving 83 preterm cases (<37 weeks’ gestation) and 120 term delivery controls, PTB was associated with severe periodontitis (i.e., >5 sites with clinical attachment loss ≥3mm, adjusted OR=2.75, 95% CI 1.01-7.54).23

This relationship has been explored in other cross sec-tional and cohort populations around the globe. Bosnjak and colleagues24 reported an adjusted OR of 8.13 (95% CI 2.73-45.9) for maternal periodontal disease and PTB for a Croatian population (17 preterm cases and 64 controls). Similarly, a Finnish study25 involving 130 consecutively enrolled pregnant mothers found that those with peri-odontal disease were 5.5 times (95% CI 1.4-21.2) more likely to have preterm deliveries or adverse pregnancy outcomes. Two case control studies involving Hungarian subjects found positive associations between maternal early localized periodontitis (>1 site with probing depth >4 mm and bleeding on probing ≥50%) and preterm LBW (OR=5.4, 95% CI=1.7-17.3; OR= 3.32, 95% CI: 1.64-6.69).26,27 Another observational study with 96 Spanish pregnant women found a higher severity of periodontal disease (percentage of sites with probing depths >4mm) among those having LBW infants relative to those with normal weight infants.28 Moltitiero and colleagues29 mea-sured periodontal and birth outcomes for 150 Brazilian mothers and reported a signifi cant association between periodontitis and LBW with an OR of 3.48 (95% CI 1.17-10.36). Chilean mothers with periodontal disease appear to be 3.5 times (RR, 95% CI 1.5-7.9) more likely to have a preterm LBW infant versus mothers with periodontal health.30

A smaller number of observational studies involving populations in Europe and Asia have failed to detect any signifi cant association between maternal periodontal dis-ease and adverse pregnancy outcomes.31-37 One promi-nent prospective study fi nding no association was con-ducted at Guy’s and St. Thomas’ Hospital Trust in London and involved a large cohort of 3,738 pregnant subjects.38

Regression analysis indicated no signifi cant relationships between the severity of periodontal disease (periodontal pocketing or clinical attachment loss) and either PTB or LBW. The investigators did note a correlation between poorer periodontal health and mothers who experienced a late miscarriage. A subsequent analysis on nonsmokers within this same population confi rmed no associations be-tween poor periodontal health and either PTB or LBW.39 Again, nonsmoking mothers who experienced late mis-

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carriages exhibited a higher mean probing depth as com-pared with the subjects with term births. This same group of investigators performed genetic testing (restriction fragment length polymerase techniques) on a sub-cohort of 48 preterm cases and 82 control subjects.40 There were no signifi cant associations reported for the tested cytokine polymorphisms (interleukin-1β + 3,953 and TNF-α-308 al-lelic variants), prematurity and the severity of periodon-tal disease. In addition, the combination of genotype and periodontal disease did not increase the risk of preterm delivery in this subcohort. These studies reporting no as-sociation are a small proportion of the total available evi-dence collected to date and suggest that differences in the susceptibility to periodontal disease associated-prematu-rity may occur in certain global populations.

Association of periodontal disease and preeclampsiaPreeclampsia is a common hypertensive disorder of preg-nancy that independently contributes to maternal and infant morbidity and mortality. Accordingly, atherosclerotic-like changes in placental tissues involving oxidative and infl ammatory events are thought to initiate the develop-ment of preeclampsia.41 Boggess and colleagues42 hy-pothesized that maternal exposure to periodontal disease or infection may be associated with the development of preeclampsia. Using data collected as part of the OCAP study, the investigators conducted logistic regression analyses on outcomes collected from 763 women who were enrolled at less than 26 weeks gestation and who delivered live infants. Preeclampsia (defi ned here as blood pressure >140/90 mmHg on 2 separate occasions, and ≥1+ proteinuria on catheterized urine specimen) af-fected 5.1% of subjects. The adjusted OR for severe peri-odontal disease at delivery (≥15 sites with pocket depths ≥4 mm) and preeclampsia was 2.4 (95% CI 1.1-5.3). For women exhibiting periodontal disease progression during pregnancy (≥4 sites with increases in pocket depth >2 mm and resulting in pockets >4 mm in depth), the adjusted OR was 2.1 (95% CI 1.0-4.4). After adjusting for other risk factors such as maternal age, race, smoking, gestational age at delivery, and insurance status, the results from this cohort study indicate that severe and progressive mater-nal periodontal disease during pregnancy is associated with an increased risk for preeclampsia.

This same hypothesis was tested in a case control study conducted in Colombia and including 130 preeclamptic (blood pressure ≥140/90 mmHg and ≥2+ proteinuria) and 243 non-preeclamptic women recruited between 26 to 36 weeks of pregnancy.43 In addition to sociodemographic data, obstetric risk factors and clinical periodontal out-comes, Contreras and colleagues43 examined the mater-nal subgingival microbial fl ora sampling and anaerobic culture techniques. Sixty-four percent of preeclamp-tic women had chronic periodontitis (pocket depth and

clinical attachment loss ≥4 mm and bleeding on probing OR=3.0, 95% CI 1.91-4.87) versus 37% of controls. Notably, a higher proportion of preeclamptic women were infected subgingivally with periodontal pathogens including P. gin-givalis (OR=1.77, 95% CI 1.12-2.8), T. forsythia (OR=1.8, 95% CI 1.06-3.00) and Eikenella corrodens (OR=1.8, 95% CI 1.14-2.84). This case control report demonstrates a consistent relationship between exposure to periodontal disease or subgingival pathogens and preeclampsia in pregnant women.

Evidence from intervention studiesIntervention studies (controlled clinical trials) provide the highest level of evidence in establishing a risk factor and causality in the relationship. Four published intervention studies provide early evidence that preventive and treat-ment interventions aimed at reducing maternal periodon-tal infection and infl ammation may reduce the likelihood of preterm LBW infants (Table 3).

Mitchell-Lewis and colleagues44 conducted a non-ran-domized pilot trial involving 164 U.S. inner-city minority pregnant women. One group received full mouth debride-ment (scaling with hand and/or ultrasonic instruments) plus tooth polishing and oral hygiene instructions. The second group received no periodontal intervention. No differences in clinical periodontal status were observed between preterm LBW cases and women with normal birth outcomes, but preterm LBW mothers had signifi -cantly higher levels of subgingival pathogens like T. for-sythia and C. rectus. Strikingly, while 18.9% of women receiving no periodontal intervention delivered preterm LBW infants, only 13.5% of the treated women had pre-term LBW infants.

A second pilot trail conducted in the U.S. involved 366 women with periodontitis recruited between 21 and 25 weeks gestation.45 Subjects were stratifi ed for risk fac-tors (previous spontaneous PTB at <35 weeks, body mass index <19.8 or bacterial vaginosis as assessed by Gram stain) and randomized to 1 of 3 treatment groups as fol-lows: 1) dental prophylaxis plus placebo capsule; 2) scal-ing and root planing plus placebo capsule; or 3) scaling and root planing plus metronidazole capsule (250 mg t.i.d. for 1 week). An additional group of 723 pregnant women meeting the same criteria for periodontitis but receiving no intervention served as the negative control. Women treated with scaling and root planing plus place-bo capsules exhibited the lowest incidence rate for PTB <35 weeks (0.8%). Those treated with dental prophylaxis plus placebo capsules or scaling and root planing plus metronidazole capsules exhibited intermediate incidence rates for preterm deliveries (4.9% and 3.3% respective-ly). In contrast, the rate of PTB for the untreated refer-ence group was 6.3%. This trial supported the hypothesis

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Paquette. Periodontal disease and the risk for adverse pregnancy outcomes

Reference Population Periodontal Interventions Findings and Conclusions Disease Tested Inclusion Criteria

Mitchell-Lewis U.S.; No defi ned Full mouth Although no signifi cant et al. 2001 (44) 164 subjects criteria debridement plus inter-group differences tooth polishing were detected, 18.9% of and oral hygiene women receiving no periodontal instructions versus intervention delivered preterm no treatment LBW infants versus 13.5% of the treated women Jeffcoat et al. U.S.; ≥3 sites with 1) Dental No signifi cant inter-group 2002 (31) 366 subjects clinical prophylaxis differences in preterm delivery attachment plus placebo rates were detected, but women levels ≥3 mm capsule; treated with scaling and root 2) scaling and planing plus placebo capsules root planing plus exhibited the lowest incidence placebo capsule; rate for PTB or 3) scaling and root planing plus metronidazole capsule

Lopez et al. Chile; Periodontitis: Immediate The incidence for preterm LBW2002 (46) 351 subjects ≥4 teeth with mechanical was signifi cantly lower for ≥1 site periodontal women receiving immediate exhibiting therapy versus (1.84%) versus delayed pocket depth delayed (10.11%) treatment ≥4mm and (postpartum) clinical treatment attachment loss ≥3 mm

Lopez et al. Chile; Gingivitis: ≥25% Immediate Women with gingivitis receiving2005 (47) 870 subjects of sites bleeding (supra- and delayed intervention were on probing but subgingival signifi cantly more likely to deliver no clinical scaling, tooth preterm as compared to women attachment polishing, receiving immediate periodontal loss ≥2 mm and daily treatment (OR=2.76, 95% antimicrobial CI 1.29-5.88) rinsing) versus delayed (postpartum) treatment

Table 3Summary of intervention studies on periodontal disease and adverse pregnancy outcomes (OR: odds ratio; CI: confi dence interval)

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that mechanical periodontal therapy alone may reduce PTB in pregnant women with periodontitis.

Lopez and co-workers46,47 have reported results from 2 intervention studies con-ducted in Chile demonstrating consistent, signifi cant and benefi cial effects of me-chanical periodontal therapy on preterm LBW outcomes. In the fi rst trial, the in-vestigators enrolled 351 pregnant women with clinical evidence of periodontitis (≥4 teeth with ≥1 site exhibiting pocket depth >4mm and clinical attachment loss >3 mm) and randomized them to immediate me-chanical periodontal therapy (scaling and root planing) versus delayed (postpartum) treatment.46 The total incidence of PLBW in this cohort of periodontitis subjects was 6.26%. For women treated for periodontal disease, the incidence of PLBW was only 1.84%, while the incidence was 10.11% in untreated women. When a multivariate logistic regression analysis was performed controlling for other risk factors, delayed periodontal disease treatment was the strongest factor related to PLBW with an OR of 4.70 (95% CI 1.29-17.13). In the second trial, 870 pregnant women with gingivitis (≥25% of sites bleeding on probing but no clinical attach-ment loss ≥2 mm) were randomly assigned to immedi-ate versus postpartum periodontal treatment (supra- and subgingival scaling, tooth polishing and daily rinsing with 0.12% clorhexidine gluconate).47 Those receiving imme-diate periodontal treatment also received maintenance therapy plus oral hygiene instructions every 2 to 3 weeks until delivery. Accordingly, the incidence of preterm LBW in the immediate treatment group was 2.14% versus 6.71% for the control group (OR=3.26, 95% CI 1.56-6.83). After adjusting for other known risk factors, women with gingivitis receiving delayed intervention were almost 3 times more likely to deliver preterm as compared with women who received periodontal treatment (OR=2.76, 95% CI 1.29-5.88). Collectively, these clinical trials indi-cate that mechanical intervention in pregnant mothers with gingivitis or periodontitis can reduce the incidence of preterm LBW.

Biological plausibility and evidence from animal modelsMothers with periodontal disease and preterm deliver-ies do not appear to harbor any unique subgingival mi-crobial biofi m.48,49 Indeed, preterm mothers harbor the same “red” and “orange” complex of periodontal bacteria as non-pregnant subjects with periodontal disease.50 The levels of these subgingival bacteria are signifi cantly higher among preterm mothers as compared with moth-ers with term deliveries.48 Additionally, these heightened

exposures appear to result in systemic infl ammatory events. For example, Pitiphat and colleagues51 exam-ined the relationship between periodontal disease and the acute phase infl ammatory marker, C-reactive protein (CRP), in pregnancy. The investigators measured plasma CRP in 35 pregnant subjects with periodontitis (≥1 site with alveolar bone loss ≥3 mm) and a random sample of 66 periodontally healthy pregnant subjects matched on age, race and ethnicity. Mean CRP levels were 65% higher among pregnant women with periodontitis as compared with controls (2.46 mg/l and 1.49 mg/l respec-tively). These elevations in CRP implicate maternal ex-posure to periodontal disease in upregulating maternal systemic infl ammatory pathways.

A series of investigations published by the Offenbacher group49 indicate that maternal as well as fetal immuno-infl ammatory responses to periodontal pathogens may explain the biological plausibility of the risk association.In an initial report on 812 deliveries, the investigators measured maternal postpartum IgG and fetal IgM anti-body levels to specifi c oral pathogens via whole bacterial immunoblots.49 For preterm infants, there was a 2.9-fold higher prevalence of IgM seropositivity for one or more of the red or orange complex periodontal bacteria as com-pared with term babies (19.9% versus 6.9% respectively). A lack of maternal IgG antibody to organisms of the red complex was associated with an increased rate of prema-turity with an OR of 2.2 (CI 1.48-3.79). The highest rate of prematurity (66.7%) was observed among those mothers without a protective red complex IgG response coupled with a fetal IgM response to orange complex microbes (combined OR 10.3). In a second report, the investigators analyzed 640 umbilical cord blood specimens for levels of

Paquette. Periodontal disease and the risk for adverse pregnancy outcomes

22 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

Fig. 1: Proposed model for relationship between periodontal disease orinfection and adverse pregnancy outcomes

Fetal exposure toperiodontalpathogens

Maternal responses:CRP, poor IgGpoor IgG response

Fetal responses:IgM, CRP, TNF-α,prostaglandin E2,8-Isoprostane Bacterial vaginosis

Maternal age, weight,stature, smoking, ethnicity,

stress, geneticsBacteremias,endotoxemias

Maternal exposure to periodontalpathogens and

products

Prematurerupture of

membranes,preterm birth,

low birth weight,preeclampsia,

intrauterine fetal growth restriction

Periodontal diseaseor infection

Inflammationtrigger (TNF-α, IL-1)

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CRP, IL-1β, IL-6, TNF-α, prostaglandin E2, 8-isoprostane and IgM specifi c for periodontal bacteria.52 The incidence of PTB rates was signifi cantly higher for infants with elevated fetal cord blood levels of 8-isoprostane, TNF-α and IgM for periodontal pathogens. The combined effects of fetal IgM seropositivity plus detectable CRP, or high 8-isoprostane, PGE2 or TNF-α resulted in signifi cantly in-creased risk for PTB with adjusted OR ranging between 4.1 and 7.6. The fi ndings from these two reports demon-strate that: 1) Fetal exposure to periodontal pathogens and specifi c IgM responses occur; 2) maternal antibody protects the fetus from exposure and potential prema-turity; and 3) the risk for PTB is greatest among fetuses that also demonstrate an infl ammatory response.

Fetal exposures to periodontal pathogens also appear to increase the risk for maternal vaginal bleeding during pregnancy. Examining pregnancy outcome data on 661 pregnant women and the corresponding fetal cord blood samples, Boggess and colleagues53 recently found that fi rst- or second-trimester vaginal bleeding were associ-ated signifi cantly with fetal exposure (IgM seropositivity) to periodontal pathogens (adjusted RR=1.8, 95% CI 1.3-2.5). Meanwhile, the adjusted hazard ratio for PTB among women with fi rst- or second-trimester bleeding and fetal exposure to oral pathogens was 6.4 (95% CI: 2.6-16.0). While maternal vaginal bleeding may be associated with fetal exposure to oral pathogens and increased risk for PTB, it could not be determined whether fetal exposure to oral pathogens caused or simply accompanied the bleed-ing.

Lastly, experimental evidence from animal models com-bining periodontal infection and pregnancy consistently support the risk relationship observed in humans. Collins and colleagues54 fi rst demonstrated that pregnant ham-sters implanted with subcutaneous chambers and chal-lenged with P. gingivalis exhibited smaller mean fetal weights. Similar studies in mice further demonstrate that subcutaneous infection with P. gingivalis or C. rec-tus during pregnancy increases maternal serum TNF-α levels, enhancing fetal growth restriction, resorptions and lethality.55-58 Maternal infection with C. rectus may also alter mouse fetal brain development. Furthermore, DNA sequences specifi c for P. gingivalis can be detected in fe-tal mouse and rabbit liver and placental tissues following maternal infection with the organisms.56,59 These experi-mental data from animals demonstrate that maternal in-fections with specifi c periodontal pathogens result in fetal exposures and dissemination of pathogens in fetal tissues, which in turn may affect fetal growth and development.

Summary and conclusionsFigure 1 summarizes proposed mechanisms relating periodontal disease and pregnancy outcomes. In gener-

al, maternal and fetal exposures to gram-negative peri-odontal pathogens and their products trigger infl amma-tory events in both mother and the fetus that may hasten rupture of membranes and parturition. The cumulative evidence demonstrates that mothers with clinical signs of periodontal disease pose a signifi cantly higher risk for preterm delivery, LBW, preeclampsia and other ad-verse pregnancy outcomes. In reviewing the evidence as of 2003, a consensus panel convened by the American Academy of Periodontology concluded, “In light of the strength and consistency of the association between peri-odontal disease and adverse pregnancy outcomes and the overall benefi ts of oral health, ... patients and healthcare providers should be informed that periodontal interven-tion may prevent adverse pregnancy outcomes”.13

Although studies reported since 2003 have continued to build the body of evidence in support of an association between periodontal disease and adverse pregnancy out-comes, there remains some potential bias, e.g., inconsis-tent defi nition of periodontal disease and the relatively limited number of randomized controlled trial studies. Ultimately, as with many new clinical issues, further clini-cal and laboratory research is needed to examine the po-tential associations between periodontal disease and the increased risk of PTB, LBW, preeclampsia, early loss of pregnancy, and intrauterine fetal growth restriction.

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between preterm birth and early periodontitis. A pilot study.

J Clin Periodontol 2004;31:736-741.

27. Radnai M, Gorzo I, Urban E, et al. Possible association

between mother’s periodontal status and preterm delivery. J Clin Periodontol 2006;33:791-796.

28. Moreu G, Tellez L, Gonzalez-Jaranay M. Relationship between

maternal periodontal disease and low-birth-weight pre-term

infants. J Clin Periodontol 2005;32:622-627.

29. Moliterno LF, Monteiro B, Figueredo CM, et al. Association

between periodontitis and low birth weight: a case-control

study. J Clin Periodontol 2005;32:886-890.

30. Lopez NJ, Smith PC, Gutierrez J. Higher risk of preterm birth

and low birth weight in women with periodontal disease. J Dent Res 2002;81:58-63.

31. Davenport ES, Williams CE, Sterne JA, et al. Maternal perio-

dontal disease and preterm low birthweight: case-control

study. J Dent Res 2002;81:313-318.

32. Holbrook WP, Oskarsdottir A, Fridjonsson T, et al. No link

between low-grade periodontal disease and preterm birth: a

pilot study in a healthy Caucasian population. Acta Odontol Scand 2004;62:177-179.

33. Buduneli N, Baylas H, Buduneli E, et al. Periodontal infections

and pre-term low birth weight: a case-control study. J Clin Periodontol 2005;32:174-181.

34. Rajapakse PS, Nagarathne M, Chandrasekra KB, et al.

Periodontal disease and prematurity among non-smoking Sri

Lankan women. J Dent Res 2005;84:274-277.

35. Skuldbol T, Johansen KH, Dahlen G, et al. Is pre-term labour

associated with periodontitis in a Danish maternity ward? J Clin Periodontol 2006;33:177-183.

36. Meurman JH, Furuholm J, Kaaja R, et al. Oral health in

women with pregnancy and delivery complications. Clin Oral Investig 2006;10:96-101.

37. Moore S, Randhawa M, Ide M. A case-control study to investi-

gate an association between adverse pregnancy outcome and

periodontal disease. J Clin Periodontol 2005;32:1-5.

38. Moore S, Ide M, Coward PY, et al. A prospective study to in-

vestigate the relationship between periodontal disease and

adverse pregnancy outcome. Br Dent J 2004;197:251-258.

39. Farrell S, Ide M, Wilson RF. The relationship between maternal

periodontitis, adverse pregnancy outcome and miscarriage in

never smokers. J Clin Periodontol 2006;33:115-120.

40. Moore S, Ide M, Randhawa M, et al. An investigation into the

association among preterm birth, cytokine gene polymor-

phisms and periodontal disease. BJOG 2004;111:125-132.

41. Ramos JG, Martins-Costa S, Edelweiss MI, et al. Placental bed

lesions and infant birth weight in hypertensive pregnant

women. Braz J Med Biol Res 1995;28:447-455.

42. Boggess KA, Lieff S, Murtha AP, et al. Maternal periodontal

disease is associated with an increased risk for preeclamp-

sia. Obstet Gynecol 2003;101:227-231.

43. Contreras A, Herrera JA, Soto JE, et al. Periodontitis is asso-

ciated with preeclampsia in pregnant women. J Periodontol 2006;77:182-188.

44. Mitchell-Lewis D, Engebretson SP, Chen J, et al. Periodontal

infections and pre-term birth: early findings from a cohort

of young minority women in New York. Eur J Oral Sci 2001;109:34-39.

Paquette. Periodontal disease and the risk for adverse pregnancy outcomes

24 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

For additional references to this article, please consult the digital version of Grand Rounds in Oral-Systemic Medicine™ at www.thesystemiclink.com.

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45. Jeffcoat MK, Hauth JC, Geurs NC, et al. Periodontal disease

and preterm birth: results of a pilot intervention study. J Periodontol 2003;74:1214-1218.

46. Lopez NJ, Smith PC, Gutierrez J. Periodontal therapy may

reduce the risk of preterm low birth weight in women

with periodontal disease: a randomized controlled trial. J Periodontol 2002;73:911-924.

47. Lopez NJ, Da Silva I, Ipinza J, et al. Periodontal therapy re-

duces the rate of preterm low birth weight in women with

pregnancy-associated gingivitis. J Periodontol 2005;76:2144-

2153.

48. Urban E, Radnai M, Novak T, et al. Distribution of anaerobic

bacteria among pregnant periodontitis patients who experience

preterm delivery. Anaerobe 2006;12:52-57.

49. Madianos PN, Lieff S, Murtha AP, et al. Maternal periodontitis

and prematurity. Part II: Maternal infection and fetal exposure.

Ann Periodontol 2001;6:175-182.

50. Socransky SS, Haffajee AD, Cugini MA, et al. Microbial com-

plexes in subgingival plaque. J Clin Periodontol 1998;25:134-

144.

51. Pitiphat W, Joshipura KJ, Rich-Edwards JW, et al. Periodontitis

and plasma C-reactive protein during pregnancy. J Periodontol 2006;77:821-825.

52. Boggess KA, Moss K, Madianos P, et al. Fetal immune re-

sponse to oral pathogens and risk of preterm birth. Am J Obstet Gynecol 2005;193:1121-1126.

53. Boggess KA, Moss K, Murtha A, et al. Antepartum vaginal

bleeding, fetal exposure to oral pathogens, and risk for pre-

term birth at <35 weeks of gestation. Am J Obstet Gynecol 2006;194:954-960.

54. Collins JG, Windley HW 3rd, Arnold RR, et al. Effects of a

Porphyromonas gingivalis infection on inflammatory me-

diator response and pregnancy outcome in hamsters. Infect Immun 1994;62:4356-4361.

55. Lin D, Smith MA, Champagne C, et al. Porphyromonas gingi-

valis infection during pregnancy increases maternal tumor

necrosis factor alpha, suppresses maternal interleukin-10,

and enhances fetal growth restriction and resorption in mice.

Infect Immun 2003;71:5156-5162.

56. Lin D, Smith MA, Elter J, et al. Porphyromonas gingivalis in-

fection in pregnant mice is associated with placental dissemi-

nation, an increase in the placental Th1/Th2 cytokine ratio,

and fetal growth restriction. Infect Immun 2003;71:5163-

5168.

57. Yeo A, Smith MA, Lin D, et al. Campylobacter rectus me-

diates growth restriction in pregnant mice. J Periodontol 2005;76:551-557.

58. Offenbacher S, Riche EL, Barros SP, et al. Effects of mater-

nal Campylobacter rectus infection on murine placenta, fetal

and neonatal survival, and brain development. J Periodontol 2005;76:2133-2143.

59. Boggess KA, Madianos PN, Preisser JS, et al. Chronic maternal

and fetal Porphyromonas gingivalis exposure during pregnan-

cy in rabbits. Am J Obstet Gynecol 2005;192:554-557.

Paquette. Periodontal disease and the risk for adverse pregnancy outcomes

25A GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

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Continuing Education Test Questions for

This CE course is intended for dentists and dental hygienists. The cost of this course is $45 for 3 CEUs. The test and personal information may be accessed and downloaded at www.thesystemiclink.com. Check the box that corre-sponds to your answer. After completing the test, fi ll in the personal information on the next page and return the form and test answers via either of two options:

1) Submit via U.S. Mail to:

Grand Rounds in Oral-Systemic Medicine™

1421 S. Sheridan RoadTulsa, OK 74112

2) Submit via fax to (918) 831-9804

For inquiries about the results of this Continuing Education Test, contact Carroll Hull at (800) 633-1681.

HEADLINEHEADLINE 2

Continuing Education Test Questions for

1. Approximately 500,000 infants in the U.S. were deliv-ered preterm (gestational age <37 weeks) in 2003. This represents ____% of all births.

❏a 6.3❏b 9.3❏c 12.3❏d 15.3

2. Preterm infants are ____ times more likely to experi-ence early death.

❏a 15❏b 35❏c 55❏d 75

3. All of the following long-term disabilities have been as-sociated with surviving preterm infants EXCEPT:

❏a Cerebral palsy ❏b Kidney dystopia ❏c Pulmonary abnormalities❏d Neurologic or development disabilities

4. All of the following risk factors for preterm delivery have been identifi ed in human observational studies EXCEPT:

❏a Smoking❏b Low serum folic acid levels❏c Maternal age less than 18 years❏d Maternal genetic predisposition for preterm delivery

5. Periodontal disease exposes the pregnant female to a variety of factors that place the fetal-placental unit at risk for adverse outcomes. All of the following factors may be involved EXCEPT:

❏a TNF-alpha❏b Bradykinin❏c Prostaglandin E2

❏d Lipopolysaccharide (endotoxin)❏e Gram-negative pathogenic bacteria

PERIODONTAL DISEASE AND THE RISK FOR ADVERSE PREGNANCY OUTCOMES3 CEUs

26 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

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6. Offenbacher and colleagues reported that antepar-tum moderate to severe periodontal disease was associ-ated with an increased incidence of spontaneous preterm births. The reported risk ratio (RR) was _____ with a 95% confi dence interval (CI) ranging from 1.2 to 3.2.❏a 1.5❏b 2.0❏c 2.5❏d 3.0

7. Offenbacher and colleagues reported that antepartum moderate to severe periodontal disease was associated with an increased rate of very preterm delivery. The re-ported adjusted risk ratio (RR) was _____ with a 95% con-fi dence interval (CI) ranging from 1.1 to 5.2.❏a 1.6❏b 2.0❏c 2.4❏d 3.0

8. A study by Boggess and colleagues reported that mothers with moderate or advanced periodontal disease were _____ times more likely to have small-for-gestational-age infants as compared to mothers with periodontal health.❏a 1.3❏b 1.8❏c 2.3❏d 2.8

9. A study conducted in Finland involving 130 consecu-tively enrolled pregnant women found that those with periodontal disease were ______ times more likely to have preterm deliveries or adverse pregnancy out-comes.

❏a 2.5❏b 3.5❏c 4.5❏d 5.5

10. Although the Guy’s and St. Thomas Hospital (London, England) study found no signifi cant relationship between the severity of periodontal disease and either preterm birth or low birth weight, they did note a correlation between poor periodontal health and _________.

❏a Late miscarriage❏b Fetal growth restriction❏c Development of the fetal CNS❏d Maternal postpartum complications

Questions are based on a manuscript by David W. Paquette, DMD, MPH, DMSc, entitled “Periodontal Disease and the Risk for Adverse Pregnancy Outcomes”.

Paquette. Periodontal disease and the risk for adverse pregnancy outcomes: ce test questions

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Introduction

It is widely accepted that periodontal disease extends beyond the oral cavity. The traditional role of the general dentist and periodontist in maintaining health and structure of the masticatory system, while suffi cient in itself, is expanding to include systemic disease. Periodontal disease, which represents a chronic, low-grade infection, has

been proposed as an independent risk factor in cardiovascular disease (CVD),1-3 ischemic stroke,4,5 specifi c pulmonary disorders,6 and other multi-factorial chronic diseases/conditions. In addition, suffi cient research indicates a bidirec-tional relationship between infl ammatory periodontal disease and diabetes.7,8 Clearly, the traditional role of the dentist is changing from a reparative model to a medical model with the inherent implications of diagnosis, treatment and appre-ciation of systemic interactions.

Nowhere is this new obligation more poignant than in diag-nosing and treating infl ammatory periodontal disease in the context of pregnancy and individuals at risk of having preterm or low birth weight (LBW) babies. In addition to the enormous

AbstractNo aspect of periodontology is more challenging than translating research relating to the potential relationship of peri-odontal disease to adverse pregnancy outcomes into clinical practice. While awaiting results of multi-site intervention studies and emergence of a professional consensus on this subject, dental and obstetrical health providers must ac-cept a degree of uncertainty and proceed deliberately yet cautiously in extrapolating research to clinical practice. Most recent research on the treatment of pregnant women in a dental offi ce represents a new paradigm, and in many ways reverses decades of established doctrine. Accumulating evidence suggests that rather than acting as bystanders dental and obstetrical health providers must play active roles in a patient’s pregnancy. The relationship between periodontal infection and adverse pregnancy outcomes is a serious topic of investigation. Clearly, clinicians must be confi dent that interventional therapies are safe and present no threat to the normal development of the fetus.

Both dentists and obstetricians have an obligation to collaborate and coordinate efforts to disseminate new clinical information. Here, to stimulate discussion of medical-dental collaboration in treating pregnant patients with periodon-tal disease, a periodontist and perinatologist offer their perspectives on the plausibility of a link between periodontal disease and adverse pregnancy outcomes. In addition, clinical protocols and accompanying case studies illustrating efforts to reduce the infl ammatory burden and decrease risk of adverse pregnancy are presented.

Citation: Kerpen S, Fleischer A. An obstetrician and periodontist translate periodontal-systemic research to preserve the health

of pregnant women at risk for adverse pregnancy outcomes. Grand Rounds in Oral-Sys Med 2006;4:28-38. (Digital version

Grand Rounds in Oral-Sys Med 2006;4:28-39a.)

(A complimentary copy of this article may be downloaded at www.thesystemiclink.com.)

Key Words: Periodontal disease, pregnancy, adverse outcomes, preconceptional care, preterm birth

Steven J. Kerpen, DMD, MPH† Adiel Fleischer, MD‡

† Private Practice Limited to Periodontics, Great Neck, NY; Attending Dentist, Long Island Jewish Medical Center, New Hyde Park, NY

‡ Associate Chairman of Obstetric and Gynecology and Chief Maternal Fetal Medicine, Long Island Jewish Medical Center, New Hyde Park, NY; Assistant Professor, Department of Obstetrics and Gynecology, Albert Einstein College of Medicine, Bronx, NY

AN OBSTETRICIAN ANDPERIODONTIST TRANSLATE PERIODONTAL-SYSTEMICRESEARCH TO PRESERVE THE HEALTH OF PREGNANT WOMEN AT RISK FOR ADVERSE PREGNANCY OUTCOMES

Original Article

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fi nancial burden these outcomes pass on to society and the possibility of long-term disabilities,9-11 the psychologi-cal stress suffered by families of preterm and LBW ba-bies is signifi cant. The contrast between the joys of giving birth to a healthy versus a dangerously premature child is heart-wrenching. Anyone who has witnessed a new-born, sometimes small enough to be held in the palm of a hand, whisked from its mother to a neonatal intensive care unit understands the gravity of the situation. A few more weeks in the mother’s womb could have enabled a happier outcome.12

An obstetrician’s perspective on the potentialof periodontal infection to trigger adversepregnancy outcomesSuccessful pregnancy, and obstetric practice in general, has a major impact on a nation’s health. Beyond the nega-tive impact on the immediate family, adverse pregnancy outcomes have an effect on society. There is a high in-cidence of neurological sequelae associated with pre-maturity and an increase in commensurate healthcare costs, in addition to the potential loss of earning ability in this population. In recognition of these issues, the U.S. Public Health Service included obstetrical indicators in programs reported in Healthy People 2000, and Healthy People 2010.13,14 The major goals of both programs are to increase the span of healthy life, reduce health dispari-ties between individuals and improve access to preventive services.13,14 Preventive medicine for obstetrics fi gures prominently within this plan, and 3 out of 18 indicators selected to assess community health address obstetrical care.13,14 These obstetric indicators are as follows: infant mortality, LBW deliveries, and starting prenatal care in the fi rst trimester of pregnancy.13,14 A specifi c goal of the program is to increase signifi cantly the number of pri-mary care providers offering preconceptional counseling and prenatal care.13,14

Prenatal care: the cornerstone of contemporary obstetricsCurrently over 90% of white women and only 78% of African-American or Hispanic women start prenatal care during the fi rst trimester of pregnancy, shortly after moni-toring 1 or 2 missed menstrual periods.15 It is the practice of this physician co-author to conduct a complete physical exam, obtain a complete blood count (CBC), blood type, Rh-immune globin (RH) type, rubella, venereal disease research laboratory (VDRL), hepatitis and human immu-nodefi ciency virus (HIV) status and review the patient’s personal and family history during the fi rst prenatal visit. If the patient is unsure of her last menstrual period or has an irregular menstrual period, or if uterine size is not consistent with the patient’s menstrual age, an ultrasound exam is performed to establish the age of pregnancy.

Timing of subsequent prenatal examinations should be

based on the patient’s risk status. For low risk patients, visits at 4-6 week intervals until 34 weeks and weekly visits after 36 weeks gestation are appropriate. Patients at risk for adverse pregnancy outcomes are seen at closer intervals for observation and fetal testing. At each return visit maternal and fetal well-being is assessed. These parameters can include maternal blood pressure measurements, monitoring weight gain, uterine analy-sis, measuring uterine size and checking for potential edema.16-18

Specifi c symptoms, e.g., headaches and/or blurred vi-sion, abdominal pain, contractions, pelvic pressure, leak-age of fl uid from vagina or vaginal bleeding, should be investigated and call for thorough evaluation, including ultrasound exams, cervical length measurements and biochemical testing. The latter can include specifi c cervi-cal cultures or monitoring levels of cervical fi bronectin or systemic infl ammatory cytokines.

As new risk factors for adverse pregnancy outcomes are defi ned, the format and content of prenatal care will change accordingly. At this time, considering the potential association between infl ammatory periodontal disease and preterm birth (PTB) rates, it is imperative that oral health is considered during the fi rst prenatal visit. For obstetric patients who have not had a dental evaluation in the preceding 6 months, steps should be undertaken to complete that evaluation as soon as possible.19

The importance of preconceptional care/counseling in the prenatal periodAn important component of prenatal care is preventive care prior to conception, commonly referred to as pre-conceptional care and counseling. In a 1989 report, the U.S. Public Health Service expert panel on the content of prenatal care stated, “The preconceptional visit may be the single most important healthcare visit when viewed in the context of its effect on pregnancy outcome”.14 Preconceptional sessions address both maternal and fe-tal risks, such as the incidence of congenital anomalies, intrauterine growth restriction (IUGR) and premature birth. For patients with known pre-existing complica-tions like diabetes mellitus, high blood pressure, cardiac disease, pulmonary disease, prenatal disease, lupus, clot-ting disorders, or epilepsy, potential interactions between physiologic changes associated with pregnancy and their disease status must be thoroughly evaluated. Some in-dividuals will require adjustment or discontinuation of medications prior to conception. For example, improving glycemic control for diabetic subjects, changing anti-sei-zure medication, changing anti-hypertension medication or changing from oral anticoagulants to heparin therapy could signifi cantly decrease the incidence of fetal con-genital anomalies. Other individuals may require more

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intensive medical or surgical therapy prior to conception. Such changes must be implemented as early as possible, since by the time of the fi rst prenatal visit, which normally occurs at 6-10 weeks gestation, fetal development could already be compromised.20-29

In addition to targeting individuals with pre-existing conditions, expanding preconceptional counseling to all women of childbearing age who are considering a future pregnancy, including those without known medical con-ditions, would be valuable. A personal history and a full medical evaluation during that visit could identify medi-cal conditions (e.g., hypertension) or lifestyles that should be addressed prior to conception.

Signifi cant fetal risks are associated with alcohol, smoking and/or recreational drug use. Alcohol abuse, particularly in early gestation, leads to mental retardation and a series of dysmorphic facial features known as fetal alcohol syn-drome.30-32 Smoking and use of street drugs are associated with poor fetal growth (intrauterine growth retardation), premature placenta separation (abruptio placenta), PTB, and behavioral and learning disabilities.33-35 Clearly, modi-fying patient behaviors and lifestyle prior to conception would drastically decrease the impact these risk factors had on pregnancy outcome.

Preconceptional counseling should also address environ-mental exposure for individuals working in specifi c high-risk professions. Infectious exposure is important for healthcare providers with a high risk of contracting viral induced infections, e.g., cytomegalovirus,36,37 varicella,38,39 or parvovirus.40,41 Individuals working in such environ-ments should have their immune status (antibody titers to specifi c infectious agents) tested to assess the risk of exposure during a future pregnancy.

PTB One of the most important obstetrical complications lead-ing to long-term sequelae is PTB. Prematurity accounts for almost 75% of perinatal mortality and over 50% of neurological morbidity42 and is by far the largest contrib-utor to cerebral palsy. More importantly, despite advances in diagnosing and managing preterm labor, the rate of PTBs is rising. Based on the March of Dimes report in 2003, prematurity rates in the U.S. are over 11%43 with signifi cant differences between races.44 Most neonatal deaths and long-term morbidity come from the 2% of in-fants born before 32 weeks gestation and weighing less than 1500 grams.12

The primary complications leading to PTB are: 1) indi-cated preterm delivery; 2) premature labor; 3) preterm rupture of membranes; and 4) cervical incompetence.45 Several medical and obstetrical complications can place

the well-being of the mother or fetus in jeopardy and jus-tify a decision to deliver a fetus prematurely to improve maternal or fetal outcome. Some of these are: severe hypertension, cardiac disease, lupus, anti-phospholipids syndrome and long-standing diabetes. Obstetrical com-plications include preclampsia, fetal IUGR or placental abnormalities such as placenta previa and abruptio pla-centa.46 All of these complications place the unborn fetus and sometimes the mother at considerable risk, making even premature delivery the only option for a reasonable perinatal outcome.

Most PTBs (over 70%), however, result from premature labor, premature rupture of membranes (PROM), cervi-cal incompetence or a combination of these risk factors.45 There is apparently considerable overlap from a clinical standpoint between patients with cervical incompetence presenting initially with PROM, patients with PROM go-ing into preterm labor, and patients with preterm labor having spontaneous rupture of membranes shortly after the onset of contractions.47,48 While the specifi c etiology of these conditions has not been fully elucidated, it is likely that a common trigger leading to PTB is responsible for many of these processes. One extensively investigated po-tential trigger is the association between local or distant infection and premature labor/preterm rupture of mem-branes.49-52 Bacterial invasion of amniotic fl uid (AF) has been documented by positive AF cultures in 10-25% of all patients with premature labor and intact membranes.53 Among individuals with PROM, the incidence of a posi-tive AF culture can be as high as 40%.54 Many patients, however, show pathological evidence of infl ammatory changes, but their bacterial cultures remain negative.55 This observation supports the hypothesis that the onset of preterm contractions, PROM or cervical changes can re-sult from an infl ammatory response to a distant infectious stimulus. Infection upregulates production of cytokines, which in turn stimulate the immune response leading to physiological and biochemical changes.56,57

Proinfl ammatory cytokines in turn increase the production of prostaglandins, which are potent stimulators of uterine contractions.58-60 Furthermore, specifi c pro-infl ammatory cytokines, such as interleukin-1 (IL-1), IL-6, IL-8 and tu-mor necrosis factor-alpha (TNF-α) stimulate synthesis of matrix metalloproteinases (MMPs),61,62 enzymes that can remodel collagen leading to softening and weakening of the uterine cervix and fetal membranes. The net result of these changes is a signifi cant increase in the risk of premature cervical effacement, cervical dilation, PROM, preterm contraction and eventually PTB.63

A recent National Institute of Health sponsored Preterm Prediction Study64 compared 194 women who had experi-enced a single spontaneous birth to an equal number of

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subjects who delivered at term. Plasma was collected at 24 weeks gestation to measure levels of the pro-infl am-matory cytokine granulocyte colony-stimulation factor (GCSF). GCSF levels were highly correlated with the risk of spontaneous delivery at <32 weeks gestation. GCSF values over the 75th percentile were seen among 50% of preterm deliveries compared with 14% of controls. It is important to note that none of these patients had symptoms indicative of preterm labor at the time that blood samples were ob-tained. In a second study65 of patients with preterm labor, AF analysis showed elevated IL-6 levels in 88% of subjects that went on to deliver prematurely compared with 12% of those who stopped contracting and went to term. In this study, levels of cytokines Il-6, IL-1 and TNF-α in AF were all positively correlated with histologic evidence of cho-rioamnionitis. Finally, it has been reported that cervical IL-6 concentrations at 24 weeks gestation are signifi cantly higher in women who subsequently had a PTB secondary to premature labor compared with those who delivered at term.66 Collectively, all of these studies suggest that early spontaneous PTB is associated with an infl ammatory pro-cess manifested by the presence of specifi c cytokines in maternal plasma several weeks before the PTB event.

Until recently, the cervical/vaginal area was considered the only infectious source capable of triggering an infl am-matory reaction leading to PTB. Data now supports the hypothesis that an infl ammatory response to a distant in-fectious source, like periodontal disease, also constitutes a risk factor for PTB.67,68 Periodontitis is a chronic bacterial condition that serves as a reservoir for gram-negative mi-crobes and a source of pro-infl ammatory mediators, par-ticularly during periods of disease exacerbation. Indeed, serum levels of 1L-1, TNF-α, 1L-6, and C-reactive protein (CRP) have all been shown to be elevated in individuals with periodontitis.69 These cytokines stimulate the infl am-matory process, indirectly facilitate prostaglandin pro-duction and increase MMP production, which collectively promotes preterm labor, PROM and eventually PTB.70

These fi ndings, as well as the long-term benefi ts of oral health, indicate that it is in a patient’s best interest to in-clude periodontal evaluation in obstetrical and prenatal care. Individuals with signifi cant pathology could then be offered treatment likely to reduce the incidence of preg-nancy complications.71,72 This initiative requires a broad educational effort by both the obstetrical and dental com-munities. Furthermore, oral health evaluation should also be included in preconceptional counseling so that women can begin pregnancy with minimal risk of PTB.

A periodontist’s perspective on the potentialof periodontal infection to triggeradverse pregnancy outcomesIt is not surprising that periodontal infection can promote

systemic sequelae. It has been estimated that the surface area of the periodontal pocket epithelium exposed to bac-terial insult is 20 cm2 (assuming 6 mm probing depths and 28 teeth), comprising a signifi cant potential infectious load.73 In contrast to other transcutaneous appendages, i.e., nail beds where thick keratinized tissue forms a virtu-ally impenetrable barrier, the body is protected from a very harsh oral environment by a precariously fragile epithelial layer. The epithelial barrier protecting the subjacent con-nective tissues and alveolar bone (pocket and junctional epithelium) can be as thin as a few cell layers, is void of a stratum granulosum and stratum corneum and lacks im-mune surveillance cells (Langerhans cells).74 The occur-rence of micro-ulcerations in this epithelial barrier is one of the early events in pathogenesis of periodontal disease.75 The presence of such ulcerations explains how local in-fection can have distant ramifi cations.76-79 The periodontal pocket is host to very large quantities of gram-negative bacteria.80 Each gram (wet weight) of plaque, composed of 1.0 x 1011 organisms, presents a continuous challenge or infectious burden.80 Transient bacteremias occur dur-ing mastication, tooth brushing, and various dental pro-cedures.81-83 One study determined that bacteremia has a 1,000-fold greater chance of occurring for physiologic rea-sons (i.e., tooth brushing and mastication) than from dental extraction.84 A direct relationship between periodontal in-fl ammation and incidence of bacteremia has also been re-ported.81 Periodontal disease is extraordinarily prevalent. The results of epidemiologic studies vary with how clinical parameters are measured. Such studies, however, indicate prevalence in the U.S. ranging from approximately 27 to 78 million adults.85 Collectively, the 5 most recent epidemiolog-ic studies indicate that an average of 58 million U.S. adults has moderate to severe periodontal disease.85

While it is crucial that oral care providers be aware of accumulating evidence relating oral bacteria and infl am-mation to adverse pregnancy outcomes, it is obvious that obstetrical colleagues are the pivotal point for implemen-tation of this science in clinical practice. As evidence for this link increases, it is imperative that dental providers raise awareness of this relationship within the medical community.

The challenge in light of emerging evidenceClinicians face a challenge in order to change the care of women of childbearing age and those who are pregnant. A Centers for Disease Control and Prevention (CDC) study found that only one-half of women with oral problems made an appointment during pregnancy.86 The reason most often cited is fear of harming the fetus, and many dentists share this anxiety. It is the experience of these authors that pregnant women may not receive proper oral care. Too often patients are referred from generalist to special-ist or placed on antibiotics or pain relievers for too long be-

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cause of a reluctance to treat. Obstetrical colleagues need to consider a collaborative approach to educating mutual patients and integrating and coordinating care.

Research in support of guidelines for careof pregnant patientsThe following discussion supports guidelines for co-man-agement of pregnant patients at risk for adverse preg-nancy as a result of oral infl ammation. It is based on re-ported intervention studies, an understanding of the sig-nifi cance of infl ammation and the incidence of pregnancy gingivitis.

Three notable intervention studies — one by Jeffcoat and colleagues87 and two by Lopez and colleagues88,89

— collectively indicate that treatment of infl ammatory periodontal disease during early stages of pregnancy has benefi cial effects. Jeffcoat and colleagues87 followed 366 patients with periodontitis. In that study the reference group had a preterm delivery of slightly over 6%, and all treatment groups did better. The group that received scaling and root planing had a preterm delivery rate of less than 1%.87 Lopez88 and colleagues conducted a ran-domized, controlled clinical trial involving 400 pregnant women.88 All women in the treatment group received periodontal care between the 9th and 21st week of ges-tation. Periodontal treatment consisted of plaque control instruction, scaling and root planing and rinsing with 0.12% chlorhexadine once a day.88 After active treat-ment, patients were seen for maintenance every 2 to 3 weeks until delivery.88 Preterm LBW deliveries in the un-treated control group were >10%, while those in the test group (those receiving periodontal therapy) were <2%.88 Interestingly, in a follow-up study, Lopez and colleagues89 showed that not only chronic periodontitis but also gingi-vitis were associated with preterm delivery. Signifi cantly, treating gingivitis during pregnancy reduced preterm de-livery from 6.71% to 2.14%.89 These fi ndings are highly signifi cant given the prevalence of pregnancy gingivitis.

Pregnancy gingivitis should be very familiar to this read-ership. Occurring in 30-70% of pregnancies,90,91 it is an acute form of gingivitis characterized by erythema, ede-ma, hyperplasia, increased gingival bleeding, and in many cases, formation of pyogenic granulomas.92 It begins around the second month of pregnancy and generally ex-hibits resolution following parturition.93 For decades, gin-givitis during pregnancy was considered little more than a nuisance and treated symptomatically, while assuring the patient that it would improve after delivery.

Given the brief period of time that a woman is pregnant, it is possible that simply having a history of periodontal disease is not enough to guarantee an exposure to the fetus. Gingival infl ammatory activity, with or without at-

tachment loss, may be of equal or even greater impor-tance when evaluating the impact of periodontal disease on systemic health.94

A 2006 study by Offenbacher95 and colleagues in the Journal of Obstetrics and Gynecology is illuminating. In this prospective study, 1,020 women received both an-tepartum and postpartum periodontal examination. The authors found that women with clinically active and pro-gressive periodontal disease were at signifi cant risk for delivery at a gestational age of <32 weeks.95 The adjust-ed risk ratio was 2.4. Disease progression in this study was defi ned as ≥4 sites with ≥2 mm of increased probing depths at each site, with the postpartum probing depth being 4 mm or more.95 In a typical patient with 28 teeth, 128 sites were measured, that is, 6 sites per tooth.95 The authors concluded that if a mere 2.3% of recorded pock-ets progress (e.g., 4 sites), there is a potential danger to the fetus.95 This data is startling since the mortality rate for neonates born before 35 weeks is 11.4-fold greater than that for babies born after 35 weeks.95 The rate of morbidity in this group of neonates is higher as well.96

Finally, Moss97 and colleagues described clinical risk fac-tors associated with disease occurrence and progression by following 891 pregnant women prior to 26 weeks of gestation and within 48 hours of delivery.97 Using the defi -nitions of Offenbacher and colleagues, they showed that having >10% sites with bleeding upon probing and ≥4 sites with a probing depth of ≥4 mm was signifi cantly predictive of disease progression during pregnancy.97 The study also showed that the number of sites that showed gingivitis/periodontitis incidence/progression (GPIP) was relatively small (1.7%), but the number of patients with progression was signifi cant (46.7%).97 Most sites that changed were not previously diseased, in that probing depths were 3 mm.97 This data is plausible given that periodontal dis-ease is relatively uncommon in this age group of women, while the incidence of pregnancy gingivitis is high. The authors noted that GPIP occurred more frequently in pre-molar and molars than on anterior teeth and was more likely to occur on inter-proximal sites. One-quarter of the patients in this study experienced deteriorated periodon-tal status.97 The study identifi ed several non-dental risk factors, including: young age, weight increase above de-sired limit, African-American racial group, tobacco use, food stamp eligibility and lack of medical insurance.97

Both the Offenbacher and Moss studies strongly suggest that clinicians begin developing a scientifi cally-based program to treat pregnant patients. Risk factors can be identifi ed and a rational treatment plan designed based on those factors and clinical periodontal status. A strong case can be made for treating maternal periodontal disease, and the incidence of gingival infl ammation could be a predictor of danger to

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the fetus.97 It is therefore logical to develop programs to eliminate or prevent maternal gingival infl ammation. The goal should be a “zero tolerance” policy towards infl amma-tion during this very brief period in a woman’s life.

Cross-referrals gaining traction Obstetricians and obstetric nurses are the obvious start-ing points to implement an interdisciplinary protocol to prevent preterm delivery. Among obstetricians, the prac-tice of screening for infl ammatory periodontal disease and referring at-risk women to dental care providers has not been widely accepted. The Task Force in Oral Care and Pregnancy for the State of New York19 and The American Academy of Periodontology98 recommend that every wom-an be referred for an oral examination early in pregnancy. This examination would typically occur between 9 and 12 weeks of pregnancy. The obstetrician should question every pregnant woman concerning signs and symptoms of periodontal disease, such as bleeding, red, swollen or tender gums (Table 1). The obstetrician should also know

whether the patient is at risk for periodontal disease be-cause of smoking, family history or a condition such as di-abetes (Table 2). Finally, it is the opinion of the co-authors that any patient with a history of preterm delivery or who is at risk for such a condition (Table 3) should be referred for an evaluation of a potential role of oral infl ammation in their pregnancy. It is reasonable to ask that general den-tists and dental specialists (periodontists) work together to provide optimum care. It is the opinion of the co-authors that patients at minimal risk either for periodontal disease or preterm delivery should be referred to a general dentist. Following evaluation they should be educated concerning the potential role of gingival infl ammation on pregnancy and placed on an intensive preventive program as early as possible. It is also the co-authors’ opinion that at-risk patients should have periodic preventive treatments, in-cluding prophylaxis, and evaluation of oral hygiene effec-

• Bleeding gums during brushing• Red, swollen or tender gums• Gums that have pulled away from teeth• Persistent bad breath• Pus between gums and teeth (leaving bad taste)• Loose or separating teeth

Table 1Signs and symptomsof periodontal disease99

• Smoking — up to 7 times more likely• Genetic/family history — 3 to 5 times more likely• Smokers with a family history of a parent or sibling

who lost a tooth at an early age are 10 times more likely to develop periodontal disease

• Diabetes — up to 5 times more likely• Race — African-Americans show 3 times greater

risk• Socioeconomic issues — low income and education

increases risk• Stress• Obesity• Decreased immune response — HIV, immunosup-

pressant use• Medications — calcium channel blockers, dilantin,

cyclosporin• Alcohol use

Table 2Risk factors for periodontal disease

• Previous PTB• Previous pregnancy losses• Hypertension• Other medical complications• Smoking• Drug/alcohol abuse• Low socioeconomic status• Poor nutrition• Low initial body mass index• Race (African-Americans have higher incidence of

PTBs)

Table 3Risk factors for preterm delivery

• Orthodontic bands and appliances• Overhanging restorations• Decay as trap for plaque• RPD clasps• Malpositioned teeth• Partially impacted third molars• Open contacts• Tongue rings• Root concavities• Food retention areas• Mobility• Subgingival margins or margins at gingiva• Medications — calcium channel blockers, phenytoin,

cyclosporin A (hyperplasia)• Allergies

Table 4Local and systemic risk factors101

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tiveness. Patients who during pregnancy exhibit increased gingival infl ammation, evidence of pyogenic granuloma formation, periodontal abscess formation or evidence of bone loss should be considered for referral to a specialist (periodontist).

The severity of infl ammatory periodontal disease and the obstetrician’s appraisal of preterm delivery risk should determine whether a case is triaged to a generalist or a specialist. Patients at signifi cant risk of periodontal dis-ease (e.g., diabetes patients, smokers, users of anti-seizure medications), those diagnosed with or exhibiting symp-toms of periodontal disease or individuals with a history of pregnancy gingivitis should be considered for referral to a periodontist. Detailed examination of hard and soft tis-sues should be performed, including measuring periodon-tal pocket depth and evaluation of bleeding on probing, plaque index and clinical attachment loss. The ability of the patient to perform adequate home care should also be assessed, and acute infection should be diagnosed and treated immediately. Local (Table 4) and systemic risk fac-tors for periodontal disease and infl ammation should be noted. These could be numerous and require referral back to a general dentist or physician. The following case stud-ies illustrate what the co-authors believe is optimal care of women during childbearing years. These cases repre-sent examples of transdisciplinary interactions. They are not meant to imply that these dental interventions affected pregnancy outcomes or prove a causal relationship.

Case 1 (Figure 1) involves a 32-year-old woman seen for a routine perinatal visit to her obstetrician at the ninth week of pregnancy. The patient had been under the care of a general dentist for several years, and her last visit was one month prior to conception. She believed that her

mouth was in an excellent state of health. Her obstetri-cian suggested that she have an oral examination per-formed by her general dentist.

During the second trimester the patient reported gingival pain and bleeding to her obstetrician. The obstetrician then referred the patient to a periodontist. Several interproxi-mal areas exhibited marginal infl ammation, tenderness and bleeding on probing. The patient was diagnosed with pregnancy gingivitis. Full mouth x-rays taken prior to con-ception were provided. Radiographs, an additional intra-oral image, and periodontal charts of this case may be ac-cessed for viewing in the Collateral Case Study Information section available at www.thesystemiclink.com.

Periodontal infl ammation was controlled with scaling and root planing and oral hygiene instruction. Periodontal maintenance was performed on a monthly basis until de-livery. After parturition the patient was advised to return to her general dentist for routine dental care.

Case 2 (Figure 2) describes a 35-year-old woman with a history of pregnancy loss as a result of preterm delivery. Her previous pregnancy resulted in PROM, which led to premature labor. Delivery was at 24 weeks, and the baby died. The patient was seen for preconceptional counseling before attempting another pregnancy. The obstetrician noted that the patient had several complaints suggestive of periodontal disease, i.e., persistent bad breath and bad taste. She was referred to a periodontist for an oral health examination.

The patient was diagnosed with chronic periodontitis. Gingival tissues exhibited the cardinal signs of infl amma-tion including friable and rolled marginal tissue, edema,

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Fig. 1

Case 1. Physician identifi cation and referral to periodontist of a case of pregnancy gingivitis

Case 1

Fig. 2

Case 2. Physician identifi cation and referral of at-risk woman dur-ing preconceptional counseling

Case 2

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medical history revealed a recent pregnancy loss at 22 weeks. Radiographs, an additional intraoral image, and periodontal charts of this case may be accessed for viewing in the Collateral Case Study Information section available at www.thesystemiclink.com.

The patient was referred back to her obstetrician who reviewed the possible association between periodontal disease and adverse pregnancy outcomes. The patient and the obstetrician agreed that the periodontal condi-tion should be treated and controlled prior to conception. During an ensuing pregnancy the patient was placed on a strict periodontal maintenance schedule.

ConclusionDuring the past decade studies have appeared both in the obstetric and periodontal literature supporting the link between periodontal disease and adverse pregnancy outcome. Dentists and obstetricians now have a unique opportunity to make an impact on this important public health issue. Collaborative, transdisciplinary care, while presenting unique challenges, must be implemented and disseminated. It is imperative that treatment be facilitat-ed by seamless communication between physicians and dentists.99 Medical and dental providers must work coop-eratively to overcome widely held beliefs that dental care during pregnancy harms a fetus. It has been the experi-ence of the co-authors that this collaboration can be ef-fective and benefi cial in clinical practice.

Local and state organizations have begun to recognize the importance of oral healthcare during pregnancy. It must be remembered that multi-site, large-scale interven-tion studies have yet to be reported. The New York State Department of Health19 has offered guidelines that state,

Kerpen, Fleischer. An obstetrician and periodontist translate ...

erythema and bleeding upon gentle probing. A gingival exudate was noted as well as accumulation of bacterial plaque. Radiographs, an additional intraoral image, and periodontal charts of this case may be accessed for view-ing in the Collateral Case Study Information section avail-able at www.thesystemiclink.com.

The periodontist initiated a comprehensive treatment plan. Periodontal infl ammation was controlled with stan-dard therapies. Meticulous attention to hygiene was en-couraged as well as frequent recalls during her ensuing pregnancy, which was successful.

Case 3 (Figure 3) describes a 27-year-old white female who is pregnant for the fi rst time. The patient sees a den-tist only when she has a “problem”. When the obstetrician interviewed the patient, she reported no signs or symp-toms of periodontal disease, but discussed her mother’s recent periodontal surgery. Periodontal records and an additional intraoral image of this case may be accessed for viewing in the Collateral Case Study Information sec-tion available at www.thesystemiclink.com.

At her fi rst prenatal visit at 8 weeks, the obstetrician re-ferred her to a general dentist for an oral examination. The dentist made a diagnosis of gingivitis. The patient was educated about the importance of oral hygiene dur-ing pregnancy. The patient responded well to mechanical treatment and oral hygiene instruction. She was placed on a two-month maintenance schedule until 36 weeks.

Case 4 (Figure 4) involves a 27-year-old African-American woman with a history of chronic periodontal disease. Her dentist referred her to a periodontist for periodontal therapy. The periodontist’s review of her

Fig. 3

Case 3. Progressive intervention of periodontal infl ammation dur-ing pregnancy through obstetrician-dentist collaboration

Case 3

Fig. 4

Case 4. Periodontal disease and pregnancy loss as incidental fi nd-ings: cross-referral to an obstetrician

Case 4

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“Without waiting for the outcome of these clinical trials, healthcare professionals can take actions now to address oral health problems in pregnant women”. The Long Island (NY) Regional Perinatal Forum has identi-fi ed Oral Health in Pregnancy as a topic worth implement-ing in a countywide action plan. In addition, at least 1 ma-jor health insurance company has begun to recognize peri-odontal care during pregnancy as a medical necessity.100

As governmental and private organizations begin to rec-ognize the importance of oral health in pregnancy, it is the joint responsibility of dental and obstetrical health pro-viders to integrate this new information into the practice of dentistry and obstetrics.

Editor’s Note: The intraoral photographs and accompa-nying radiographs, and periodontal records of the case studies were contributed by Frank Formica, DDS.

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For additional references to this article, please consult the digital version of Grand Rounds in Oral-Systemic Medicine™ at www.thesystemiclink.com.

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Introduction

Preterm birth (PTB), which is responsible for most neonatal deaths in newborns, is a serious health concern in the United States. In 2004, 12.5% of all births were preterm (before 37 weeks of gestation). Unfortunately, over the last decade, the overall PTB in the U.S. has risen steadily and increased by about 30% since 1981.1

The articles in this issue of Grand Rounds provide strong evidence supporting a physiologic and epidemiologic re-lationship between periodontal disease and adverse pregnancy outcomes, including PTB. These fi ndings challenge healthcare professionals to ensure that women of childbearing age receive high quality preventive dental care in addition to other preconceptional measures recommended by healthcare professionals and consumer organiza-tions.

Organizations such as the Centers for Disease Control and Prevention (CDC) and the March of Dimes have identifi ed strategies to decrease PTBs. The March of Dimes’ National Prematurity Campaign increases public awareness about

Jacki S. Witt, JD, MSN, RNC, WHNP, CNM†Karen B. Williams, RDH, PhD‡Patricia J. Kelly, RN, PhD, MPH, FNP§

† Clinical Associate Professor, School of Nursing, University of Missouri-Kansas City, Kansas City, MO

‡ Professor, School of Dentistry, University of Missouri-Kansas City, Kansas City, MO

§ Associate Professor, School of Nursing, University of Missouri-Kansas City, Kansas City, MO

ENGAGING HYGIENISTS, NURSES AND SOCIAL SERVICE PROFESSIONALS IN AN INTERDISCIPLINARY MODEL FOR PREVENTION AND EARLY CARE OF ORAL DISEASES IN WOMEN OF CHILDBEARING AGE

AbstractCompelling physiologic and epidemiologic evidence is establishing a strong link between periodontal disease and preterm labor and birth. Because many women do not seek care during the first critical few weeks after conception, it is imperative that health professionals intervene proactively at various levels of prevention (e.g., primordial, primary, secondary) during periodic contact with women before pregnancy or soon after conception. Preconceptional counseling and care have traditionally been provided primarily by medicine and nursing. The authors recommend a broad-based, patient-focused, interdisciplinary preconceptional care model to ensure provision of preventive dental education and care. Using, as a foundation, the 5 “A”s approach promoted by the U.S. Public Health Service in its “Treating Tobacco Use and Dependence Clinical Practice Guideline”, the authors present a community-based, interdisciplinary strategy for improving risk factor assessment, increasing knowledge about the importance of risk factors on pregnancy outcomes, and developing new skills related to oral health and periodontal disease. All health professionals share roles in providing preventive care. An ideal strategy for successful preventive care is a collaboration of medical, nursing, dental, and social service professionals to provide preconceptional care aimed at reducing and controlling gingival/periodontal inflammation, with the goal of decreasing the rate of preterm labor and birth.

Citation: Witt J, Williams K, Kelly P. Engaging hygienists, nurses and social service professionals in an interdisciplinary model for

prevention and early care of oral disease in women of childbearing age. Grand Rounds in Oral-Sys Med 2006;4:40-48. (Digital

version Grand Rounds in Oral-Sys Med 2006;4:40-48.)

(A complimentary copy of this article may be downloaded at www.thesystemiclink.com.)

Key Words: Oral health, pregnancy, preconceptional counseling, nursing, dental hygienist, interdisciplinary care

40 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

Original Article

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The Academy of Dental Therapeutics and Stomatology is an ADA CERP Recognized Provider.

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Witt, Williams, Kelly. Engaging hygienists, nurses and social service professionals in an interdisciplinary model for prevention ...

risks of premature birth and provides educational pro-grams to professionals and consumers to identify and reduce the risks of PTB.2 The CDC has identifi ed 10 mea-sures to improve women’s health before pregnancy.3 They are: 1) Individual responsibility throughout the lifespan; 2) consumer knowledge and awareness; 3) preventive visits; 4) interventions for identifi ed risks; 5) intercon-ceptional care; 6) pre-pregnancy checkups; 7) health in-surance coverage for women with low incomes; 8) pub-lic health programs and strategies; 9) research; and 10) monitoring improvements. The recommendations were developed to guide consumers and health professionals and to increase the number of women who enter preg-nancy in optimal health.

In addition to the March of Dimes and CDC recommenda-tions, the review of Healthy People 2010 objectives, pub-lished in March of 2004, identifi es additional steps needed to achieve Oral Health Objectives by 2010.4 Two of the 7 suggestions relate to preconceptional care: 1) Enhancing oral health literacy for parents and prospective parents; and 2) seeking ways to ensure that “high risk women of childbearing age” receive preconceptional counseling.

To increase research-based knowledge about risk identi-fi cation, prevention and treatment of preterm labor and birth and improved epidemiological surveillance systems, the Institute of Medicine (IOM) recently released a report endorsed by the March of Dimes and the American College of Obstetricians and Gynecologists calling for aggressive research aimed at improving prediction and prevention of preterm labor and birth.1 Subsequently, the U.S. Senate Health, Education, Labor and Pension Committee unani-mously approved the Prematurity Research Expansion and Education for Mothers who Deliver Infants Early (PREEMIE) Act (S. 707) in June of 2006.5 In addition to funding grants and surveillance systems, the PREEMIE Act, which allocates $18 million per year, will fund the Interagency Coordinating Council on Prematurity and Low Birthweight, which will oversee activities authorized by the act, a measure also supported by the IOM.1

Two studies suggest that active periodontal interven-tions in pregnant women, such as scaling and root plan-ing (with or without antibiotics), can reduce preterm la-bor and birth.6,7 It is not clear whether the presence of periodontal disease has a causative effect on PTB (i.e., whether periodontal pathogens, either directly or indi-rectly through production of infl ammatory cytokines, in-duce early labor). It is also possible that women who give birth prematurely have periodontal disease or intrinsic infl ammatory conditions or an innate immunity trait pre-disposing them to both conditions. Evidence supporting a link between periodontal disease and PTB should, how-

ever, alert healthcare providers to the need for prevention efforts.1 Since PTB can result in signifi cant morbidity and mortality for infants, emotional stress for the family and fi nancial cost to society, addressing periodontal health is-sues prior to conception or very early in pregnancy should contribute to reduction of preterm labor and birth associ-ated with poor dental health.

Despite extensive evidence supporting periodontal dis-ease as a risk factor for preterm labor and birth, diffu-sion of this concept into health prevention programs and clinical practice has been slow. More critically, consumer awareness among pregnant women is extremely low. A recent report from the CDC’s Pregnancy Risk Assessment Monitoring System (PRAMS) showed that women have negative perceptions about seeking oral healthcare dur-ing pregnancy. The CDC encourages health education pro-gram planners to give increased attention to this area.8 Other data from PRAMS suggest that 12 to 25% of women report dental problems during pregnancy and that only approximately half sought care.9 Ensuring effective health promotion and preventive dental care for women of child-bearing age, especially those with limited access to tra-ditional dental care delivery models, requires collabora-tion between medical/nursing, dental/dental hygiene, and social service professionals. An interdisciplinary model of prevention and care must be developed to bring underuti-lized resources and healthcare professions to the forefront of preconceptional care. In this paper a preliminary inter-disciplinary model for preconceptional screening, assess-ment, and interventions are proposed that can be adapted for use in community health environments.

What is preconceptional care? Preconceptional care has been defi ned as interventions which focus on the identifi cation and modifi cation of risks for preventable or modifi able adverse pregnancy outcomes (such as preterm labor and birth).3 Over a decade ago, the Department of Health and Human Services published Healthy People 2000, which proposed to “increase avail-ability of appropriate preconceptional care and counsel-ing”.10 Medical and nursing providers who treat women aged 15 to 44 are providing preconceptional care includ-ing counseling women about daily folic acid supplementa-tion, rubella immunity, smoking cessation, and alcohol and illicit drug use.11,12 Barriers to providing effective precon-ceptional counseling include the fact that approximately one-half of all pregnancies in the U.S. are unplanned (to-taling 3 million per year) and few women specifi cally seek preconceptional care or counseling.12-15 In addition, many women are not aware they are pregnant during the fi rst 4-10 weeks of pregnancy when the embryo/fetus is most susceptible to effects of maternal health and exposures. Even among women who know they are pregnant, about

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20% of them do not seek prenatal care during the critical fi rst trimester.14,16

Because of the complexity of the current healthcare sys-tem, preconceptional care may be fragmented. The authors engaged a more diverse web of providers, including social workers and dental care providers who are knowledge-able of preconceptional counseling, in order to further fa-cilitate reduction of adverse pregnancy outcomes as new scientifi c evidence becomes available.

Current preconceptional guidelines for medical providers can be grouped into the following 4 categories:3,16

• Assessment of maternal health• Ensuring appropriate immunity levels for diseases

harmful to the embryo/fetus• Screening for conditions harmful to the embryo/fetus • Counseling

Preconceptional care now includes: Discontinuing or ad-justing dosages of prescribed drugs such as isotretinoins, warfarin, anti-seizure, and anti-hypertensive drugs that are known teratogens; minimizing occupational expo-sures to environmental toxins; screening for sexually transmitted diseases and human immunodefi ciency virus; and screening for intimate partner violence. In addition, guidelines suggest educating women who may become pregnant about folic acid supplementation, healthy diet, and adequate exercise; discontinuing alcohol, tobacco and illicit drug use; and rubella, varicella and hepatitis B im-munizations.10 A primary goal of preconceptional care is to provide education to delay pregnancy until risks of ad-verse pregnancy outcomes can be minimized.17

Chronic infections, including gingivitis and periodonti-tis, should also be addressed in preconceptional care. Estimates of the prevalence of gingival or periodontal dis-eases in women of childbearing age vary, depending on how the study defi nes severity of disease. Data obtained from a large national sample in NHANES III suggest that approxi-mately one-fourth of women aged 20 to 39 show evidence of gingivitis or periodontitis.17 Other estimates from a large prospective study, the Oral Conditions and Pregnancy study (OCAP), suggest that approximately 57% of pregnant wom-en exhibit signs of mild disease, and another 13-14% show moderate to severe periodontitis.18-20

Of particular interest to dental clinicians is the CDC’s April 2006 report, Recommendations to Improve Preconception Health and Health Care: United States. While this docu-ment acknowledges a link between a mother and child’s oral health with respect to transmission of cariogenic bac-teria, it inappropriately references 3 pivotal studies show-ing a link between periodontal disease and preterm labor,

not transmission of cariogenic bacteria. No further dis-cussion of oral health appears in the document, nor are oral health experts listed as members of the work groups or advisory panel.3 Recently, within the extensive, 600-page IOM report on PTB, only 2 paragraphs are devoted to maternal periodontal disease. Of concern is the fact that no dental health professionals are represented on the committee.1 In spite of a growing body of evidence on periodontal disease as a risk factor for preterm labor and birth, diffusion into the mainstream of medical and dental practice has been slow.

A model for practiceSince many women present for an initial prenatal ap-pointment only after the fi rst trimester of pregnancy, preventive strategies must target a larger population of women of childbearing age at earlier stages of preg-nancy. Health professionals other than physicians and nurses, such as dentists, dental hygienists or social ser-vice professionals, often have regular communication with women through periodic preventive care visits. This contact provides a unique opportunity to provide early counseling regarding health risks potentially impacting pregnancy (e.g., preterm labor and birth) and to refer high-risk individuals to preconceptional or early pre-natal care. In 1997, 43% of adults and 48% of adoles-cents sought dental care within the previous 12 months; Healthy People 2010 objective 21-10 aims to increase this number to 56% by 2010.21 Unfortunately, only 20% of individuals in the <200% of poverty level sought oral healthcare, requiring community-based systems or so-cial service professionals to be the primary component of any preventive model. Irrespective of where women of childbearing age enter the healthcare system, dental hygiene/dental, nursing/medical, and social service pro-viders must be knowledgeable about preconceptional care and skilled in providing appropriate counseling and timely referrals of women at risk. Figure 1 illustrates the ongoing cycle of preventive education and care, begin-ning with primordial prevention in pubertal girls and continuing through secondary prevention activities.

Additionally, use of a standardized method for risk as-sessment could be useful for busy professionals in con-tact with women of childbearing age. A proposed model for prevention can be conceptualized as one of shared responsibility in which medical, nursing, dental, and so-cial service professionals identify potential risk factors for adverse pregnancy outcomes (either before pregnan-cy or immediately after conception) and provide coun-seling, education or referral to the appropriate health professional for interventions (Figure 2).

A well known approach that can be adapted to imple-

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ment this model is known as the 5As. This method is promoted by the U.S. Public Health Service in its Treating Tobacco Use and Dependence Clinical Practice Guideline and endorsed by the American College of Obstetricians and Gynecologists for reducing smoking during pregnancy.22 The strategy utilizes a brief counseling intervention that includes the following components:

• Ask about smoking. • Advise about behavior change. • Assess willingness to quit. • Assist by providing materials and

support.• Arrange for follow-up.

The approach could be expanded and adapted to preconceptional counseling by health and social service professionals. That assessment could include the following:

• Ask about the risk factor.• Advise about reducing risk for an

adverse pregnancy outcome.• Assess willingness to engage in risk-

reduction behavior. • Assist by providing specifi c materials,

referrals and/or interventions, as needed.

• Arrange for referral or follow-up as appropriate.

This approach represents a novel para-digm in which women and children are the focus of assessment and interven-tion. Implementation requires synergy between dental, nursing, medical, and social service environments to improve screening for risk factors, increase prac-titioners’ knowledge of the importance of risk factors on pregnancy outcomes, and increase practitioners’ development of new skills. Clearly, this approach ne-cessitates greater cooperation among interdisciplinary team members than the current standard of care. Table 1 outlines application of the 5As for each professional group. Implementation will require cross-training to ensure that specifi c skills in preconceptional care are available to all members of the health-care team.

Fig. 2: Model for interdisciplinary collaborative preconceptional care

Medical/Nursing Dental

Social Service

Provide:• Oral Health• Periodontal Intervention

Provide Assistance:• Identification of immunization, medical, prenatal & dental practices & resources

• Obtaining services & funding for preconceptional, prenatal or dental care

Provide:SmokingCessation

Counseling

Provide:SmokingCessation

Counseling

Provide:SmokingCessation

Counseling

Query, ProvideMaterials &

Oral Health Education

Query, ProvideMaterials &

Oral Health Education

Query, ProvideMaterials &

Oral Health Education

Query, ProvideMaterials & ReferFolic Acid (0.4 mg)

ImmunizationsSTD and HIV testing

Alcohol & other drug use

Query, ProvideMaterials & ReferFolic Acid (0.4 mg)

ImmunizationsSTD and HIV testing

Alcohol & other drug use

Query, ProvideMaterials & ReferFolic Acid (0.4 mg)

ImmunizationsSTD and HIV testing

Alcohol & other drug use

Provide: • Immunizations • Screening & Treatment for STD’s & HIV

• Control of Medical Conditions

Screen, Provide Materials and Refer: • Periodontal inflammation or symptoms of gingival inflammation

DentalMedical/Nursing

Social Service

Fig. 1: Cycle of interdisciplinary preventive care

PRIMARY

Target females of childbearing age

Educate, screen &refer for medical, dentalor social service needsbased on risk factors

PRIMORDIAL

Target girls at puberty

Educate about dentalhygiene & oral health

Ensure access topreventive dental care

SECONDARY

Target females ofchildbearing age

Educate, screen & referfor complete medical,

dental or social serviceevaluation & care

Witt, Williams, Kelly. Engaging hygienists, nurses and social service professionals in an interdisciplinary model for prevention ...

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Education to implement the modelPrevious examples of links between systemic health and adverse pregnancy outcomes (e.g., maternal phenylketon-uria and maternal diabetes mellitus) provide guidance for how interdisciplinary teams can effectively provide appro-priate care. Such approaches require a signifi cant shift in

the paradigm of “patient responsibility”. Dental profes-sionals need to enhance their knowledge of general risk factors in pregnancy and improve counseling skills, as well as make available pregnancy-specifi c health pro-motion materials for patients. Nursing and medical pro-fessionals need to learn to screen patients for common

Key risk factors

Current access to care

Financial resources

Past health-seeking behaviors:

• Immunizations

• OB care

• Dental

Potential for safety risk

Available resources and person’s emotional, physical and fi nancial ability to seek care and change behaviors

Assist individual in:

• Navigating healthcare systems

• Identifying barriers

• Problem solving

• Identifying community and funding resources

• Encouraging use of personal resources

Refer to appropriate health clinic

Arrange for social services and support

Follow-up on use of personal resources

5As Dental Providers Medical Providers Social Service Providers

ASK ADVISE

ASSESS

ASSIST

ARRANGE

Table 1A paradigm of shared responsibility

Tobacco use

Rubella vaccine

Varacella vaccine

Hepatitis B vaccine

Folic acid intake (>0.4mg)

Previous pregnancy outcomes

Family history

Past periodontal history

Willingness to stop smoking

Willingness to seek prenatal care

Need for social services

Provide materials:

• Smoking cessation

• General good prenatal care

• Role of oral health in pregnancy

• Impact of pregnancy on oral health

Refer to public health clinic, dentist or dental hygienist

Arrange for immunizations, support of systemic conditions, reduction in medications, as needed

Arrange for ongoing prenatal care

Tobacco use

Rubella vaccine

Varacella vaccine

Hepatitis B vaccine

Folic acid intake (>0.4mg)

Previous pregnancy outcomes

Family history

Past periodontal history

Willingness to stop smoking

Willingness to seek prenatal care

Need for social services

Provide materials:

• Smoking cessation

• Folic acid

• General good prenatal care

Refer to public health clinic, nurse practitioner or physician

Arrange for periodontal care, as needed

Arrange for periodonal maintenance during and following pregnancy

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Areas of Potential Risk Clinical Plan

Medical History • Have you been diagnosed with any chronic diseases (e.g., asthma, epilepsy,

diabetes, etc.)?

• Are you currently seeing a healthcare provider for your chronic disease(s)?

Nutrition History • Have you lost or gained more than 10 pounds in the past year without

trying to?

• Are you on a special diet? (vegetarian, high protein, etc.)

• Have you ever been diagnosed with an eating disorder?

• Are you concerned that you are not eating a healthy diet?

• Did you eat breakfast this morning?

Tobacco UseDo you smoke cigarettes or use tobacco products?

Gingival or Periodontal Disease • Have you ever been told you have gum disease? • Have you ever been treated for gum disease? • Do your gums bleed when you brush or fl oss your teeth? • Are your gums red, swollen or tender? • Are any of your teeth loose? • Have any of your teeth moved or changed position lately? • Have you ever had a gum abscess?

Medication History • Are you currently taking any prescribed medications? • Are you currently taking any non-prescibed medications, drugs, herbs or

supplements? • Do you take vitamins on a regular basis?

If yes, which of the following are you currently taking? • Multiple Vitamin or Prenatal Vitamin • Vitamin A • Folic Acid • Dietary Supplements _______________________________

Women’s Health • How many times have you been pregnant?

What was the outcome(s)?

• When was your last gynecological exam?

Table 2Proposed brief preconceptional screening instrument

If yes, document specifi c disease(s).

If yes, support continuation; if no, encourage follow-up, especially if planning pregnancy.

If yes, refer to primary healthcare provider for assessment

If yes, ask her if she has talked with a healthcare professional or registered dietician about the nutritional “balance” of the diet and, if she has not, encourage her to do so.

If yes, refer to primary healthcare provider for assessment

If yes, refer to dietician for assessment

If yes, reinforce importance; if no, recommend nutritional counseling with a dietician

If yes, document smoking status and proceed to “advise, assess, assist and arrange”.

If no, perform visual screening.

If yes to 2 or more questions, refer for periodontal assessment.

If yes to either question, discuss importance of talking with prescriber or pharmacist about effects during pregnancy.If yes, clarify.

Support daily useCaution on overuseSupport 0.4 mg dailyDiscuss ingredients and possible risks.

If previous pregnancy(s) with complications, encourage obstetric/gynecologic assessment before pregnancy.If more than 1 year ago, refer for exam.

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signs of gingival/periodontal disease and also have oral health promotion materials available. Social service pro-fessionals must be oriented to the need for timely referral and identifi cation of women of childbearing age who are at high risk. Finally, all participants must collaborate to develop streamlined referral mechanisms that encourage cross-referral when indicated.

Specifi c strategies for fostering an oral-systemic paradigm shift in patient care are as follows:

• Develop direct referral systems between nurses and dental hygienists.

• Modify questionnaires used in dental environments to obtain information about risk factors (e.g., folic acid supplementation, alcohol consumption, tobacco use).

• Improve screening competencies for gingivitis or early periodontitis in healthcare facilities serving women of childbearing age.

• Expand guidelines for health promotion and primary prevention in preconceptional care that include all key elements.

• Develop assessment instruments for use by all health

professionals to assess signs of periodontal infl amma-tion.

• Implement evidence-based intervention strategies.• Increase extramural clinical experiences to ensure

cross-training for medical/nursing students in peri-odontal care environments and for dental/dental hy-gienist students in obstetrical environments.

• Expand knowledge and skills through scholarly ven-ues such as continuing education and creative inter-disciplinary educational opportunities, such as extra-mural rotations and educational curricula available on professional Websites; materials could include:

» PowerPoint presentations » Case examples for learners to analyze and develop

clinical maps » Role-playing of patient interview questions to

explore periodontal disease risk factors and ap-propriate counseling and referral

One potential resource to guide healthcare professionals would be a screening checklist that is easy to use in mul-tiple environments. Table 2 shows such an instrument that can facilitate the “Ask” and “Assist” phase of the

Resources Description Location

DHHS Offi ce of Women’s Health

National Healthy Mothers, Healthy Babies Coalition

CDC Recommendations to Improve Preconception Health and Healthcare – U.S.

Washington State Department of Health: Maternal and Child Health Program Publications

Bright Futures in Practice: Oral Health – National Maternal and Child Oral Health Resource Center

Table 3On-line resources for preconceptional care

Central point for consumers and professionals to obtain preconceptional information from the CDC; most consumer resources available in Spanish.

Covers FAQs with evidence-based responses on diet and nutrition, stress, oral health, smoking, and drugs and alcohol use.

Overviews specifi c goals and recommendations to achieve goals to reduce risks associated with preterm, low birthweight pregnancy outcomes.

Best practice guidelines using 5As format for multiple preconceptional counseling topics:

• Smoking Cessation During Pregnancy: Guidelines for Intervention

• Domestic Violence and Pregnancy: Guidelines for Screening and Referral

• Substance Abuse During Pregnancy: Guidelines for Screening

Pocket Guide is designed to help health professionals implement specifi c oral health guidelines during pregnancy and postpartum, and in infancy, early childhood, middle childhood and adolescence.

http://www.4women.gov/Pregnancy/tryingtogetpregnant/beforeresources.cfm#preconception

http://www.hmhb.org/pregnant.html#oh

http://www.cdc.gov/mmwr/preview/mmwrhtml/rr5506a1.htm

http://www.doh.wa.gov/CFH/mch/mch_publications.htm

http://www.mchoralhealth.org/pocket.html

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intervention. Questions can be administered in a few min-utes of any medical, dental or social service encounter, enabling quick assessment of potential risk factors. On-line resources for health and social service professionals are listed in Table 3.

ConclusionAll health professionals have a potential role in provid-ing preconceptional care. Because of the established link between periodontal disease and adverse pregnancy out-comes, medical, nursing, dental, and social service profes-sionals should ideally provide preconceptional care aimed at reducing gingival/periodontal infl ammation. In the ab-sence of preconceptional care, early pregnancy counsel-ing should be positive and aimed at teaching a pregnant woman to employ good plaque control through an under-standing of the role of hormones in exacerbating existing disease. Although evidence for a link between periodontal disease and preterm labor and birth continues to grow, directly attributing preterm labor and birth to periodontal disease may be premature and statements to this effect should be avoided until more scientifi c support accumu-lates. It is the ethical and moral obligation of all health professions in contact with women who are or may be-come pregnant to conduct screening and appropriately refer for treatment of any disease, including oral disease, to ensure “best practice” outcomes.

References1. Behrman RE, Butler AS, Editors, et al. Preterm Birth:

Causes, Consequences, and Prevention. Institute of Medicine.

Washington: National Academies Press; 2006: 1, 160.

2. March of Dimes. March of Dimes Urges Federal Legislation

for IOM Prematurity Report. 2006. Available at: http://www.

marchofdimes.com/printableArticles/15796_20548.asp.

Accessed on: 08/26/06.

3. Centers for Disease Control and Prevention. Recommendations

to improve preconception health and health care—United

States. MMWR 2006;55:1-23.

4. U.S. Department of Health and Human Services – Public Health

Service. Progress Review – Oral Health. 2004. Available at:

http://www.healthypeople.gov/data/2010prog/focus21/. Accessed

on: 8/29/06.

5. U.S. Senate Health, Education, Labor and Pension Committee.

Prematurity Research Expansion and Education for Mothers

who Deliver Infants Early Act (S. 707). 2006. Available at:

http://thomas.loc.gov/cgi-bin/cpquery/T?&report=sr298&dbn

ame=109&. Accessed on: 8/31/06.

6. Lopez NJ, Smith PC, Gutierrez J. Higher risk of preterm birth

and low birth weight in women with periodontal disease. J

Dent Res 2002;81:58-63.

7. Jeffcoat MK, Gerur NC, Reddy MS, et al. Current evidence

regarding periodontal disease as a risk factor in preterm

birth. Ann Periodontol 2001;6:183-188.

8. Ressler-Maerlender J, Krishna R, Robison V. Report from

the CDC. Oral health during pregnancy: current research. J Women’s Health 2005;14:880-882.

9. Gaffield ML, Gilbert BJ, Malvitz DM, et al. Oral health during

pregnancy: an analysis of information collected by the

pregnancy risk assessment monitoring system. J Am Dent Assoc 2001;132:1009-1016.

10. Healthy People 2000 Resource List. Available at: http://

odphp.osophs.dhhs.gov/pubs/hp2000/5family2.htm. Accessed

on: 9/22/06.

11. Frey KA. Preconception care by the nonobstetrical provider.

Mayo Clin Proc 2002;77:469-473.

12. Trussell, J, Ellertson, C, Stewart, F. The effectiveness of the

Yuzpe regimen of emergency contraception. Fam Plann Perspect 1996;28:58-64.

13. Besculides M, Laraque F. Unintended pregnancy among the

urban poor. J Urban Health 2004;81:340-348.

14. Henshaw SK. Unintended pregnancy in the United States.

Fam Plann Perspect 1998;30:24-29,46.

15. Darney PD. Hormonal implants: contraception for a new

century. Am J Obstet Gynecol 1994;170:1536-1543.

16. American College of Obstetricians and Gynecologists. ACOG

technical bulletin. Preconceptional Care. Number 205-May,

1995. Int J Gynecol Obstet 1995;50: 201-207.

17. Cullum, AS. Changing provider practices to enhance

preconceptional wellness. J Obstet Gynecol Neonatal Nurs

2003;32:543-549.

18. Dye BA, Selwitz RH. The relationship between selected

measures of periodontal status and demographic and

behavioural risk factors. J Clin Periodontol 2005;32:798-808.

19. Offenbacher S, Boggess KA, Murtha AP, et al. Progressive

periodontal disease and risk of very preterm delivery. Obstet Gynecol 2006;107:29-36.

20. Leiff S, Boggess KA, Murtha AP, et al. The oral conditions and

pregnancy study: Periodontal status of a cohort of pregnant

women. J Periodontol 2004;75:116-126.

21. U.S. Department of Health and Human Services. Healthy

people 2010: Objectives for Improving Health. Available

at: http://www.healthypeople.gov/Document. Accessed on:

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22. U.S. Department of Health and Human Services, Public

Health Service (June, 2000). Treating Tobacco Use and

Dependence Clinical Practice Guideline No. 18 (revised).

June 2005. Available at: http://www.surgeongeneral.gov/

tobacco/treating_tobacco_use.pdf. Accessed on: 9/1/06.

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In 2001, a case of a pregnant woman from upstate New York who had diffi culty accessing dental care underscored the importance of oral health care. This case spawned increased awareness of issues related to access to care and the need for healthcare delivery systems that promote oral health care during pregnancy. Also brought to the fore-

front was the tremendous knowledge gap that exists among dentists and obstetricians regarding the safety of dental treatment during pregnancy.

The growing body of knowledge that suggests that there is an association between periodontal infection and adverse pregnancy outcomes highlights the need for guidelines for the oral health care of women of childbearing years. New York State appears to be the fi rst in the country to take such action. In the fi rst initiative of this kind, the New York State Department of Health, Bureau of Dental Health convened a task force of dental and medical experts to develop guide-lines on oral health care in pregnancy and early childhood. The expert panel pointed out that “since it is highly unlikely that a suffi cient number of studies will be available in the near future to make evidence-based recommendations for all clinical situations, the group relied on expert consensus when controlled studies were not available to address specifi c issues and concerns”. Despite these limitations, the panel was able to agree on specifi c advisory statements to assist prenatal care providers and oral health professionals in the care of pregnant women. The panel also included recom-mendations aimed at improving the oral health of children. The New York State guidelines, entitled “Oral Health Care during Pregnancy and Early Childhood”, have recently been published.

It is appropriate to make oral health an integral part of prenatal care, and it is widely recognized that providing dental care during pregnancy is benefi cial for both mother and child. Accordingly, prenatal care providers are encouraged to screen for oral problems and make appropriate referrals to oral health professionals. The task force concluded the fol-lowing recommendations:

➣ Pregnancy by itself is not a reason to defer routine dental care and necessary treatment for oral health problems. ➣ Dental care is safe and effective during pregnancy. ➣ First trimester diagnosis and treatment, including needed dental x-rays, can be undertaken safely to diagnose disease

processes that need immediate treatment.➣ Needed treatment can be provided throughout the remainder of the pregnancy; however, the time period between

the 14th and 20th week is ideal.➣ Oral health care should be coordinated among prenatal and oral healthcare providers.➣ Elective treatment can be deferred until after delivery.➣ Delay in necessary treatment could result in signifi cant risk to the mother and indirectly to the fetus.

The report also provided specifi c guidance to the dental community by providing answers to what actions are in the best interest of the pregnant woman. Dentists are urged to:

➣ Plan defi nitive treatment based on customary oral health considerations including: ✓ Chief complaint and medical history ✓ History of tobacco, alcohol and other substance use ✓ Clinical evaluation ✓ Radiographs when needed

By Ronald Burakoff, DMD, MPH†

New York State Leading the Way in Establishing Guidelines for Oral Care in Pregnancy

† Clinical Professor, New York University College of Dentistry; Chair, Department of Dental Medicine, Long Island Jewish Medical Center, New Hyde Park, NY

50 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

Raising the Bar

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➣ Develop and discuss a comprehensive treatment plan that includes preventive, restorative and maintenance care.

➣ Provide emergency care at any time during pregnancy as indicated by oral condition.

➣ Provide dental prophylaxis and treatment during preg-nancy, preferably during early second trimester but defi nitely prior to delivery.

The Food & Drug Administration (FDA) created a drug classifi cation system to help clinicians determine wheth-er a therapeutic agent should be used during pregnancy (Table 1). Most medications prescribed for common dis-eases can be used with relative safety. It is also important to note that untreated diseases or conditions may pose a greater risk to the mother and fetus than the medications. Most drugs are in category C (66%) or B (19%) while only 0.7% are category A. Table 2 lists drugs that may be used during pregnancy and some that should be avoided.

Perhaps the most useful guidelines addressed by the task force include advice on specifi c treatment modalities and medications. There has been some confusion on the use of local anesthetics during pregnancy. The task force en-dorsed the use of xylocaine with epinephrine (2%) which is a category B drug. One should note that mepivicaine

3% is a category C drug. While there is speculation that epinephrine may have an effect on uterine muscle, there have been no scientifi c studies to confi rm this effect on a pregnant woman. The task force also addressed the use of 30% nitrous oxide. The panel endorsed its use when topical and local anesthetics are inadequate. When us-ing nitrous oxide the dentist may wish to consult with the prenatal provider. Precautions should be taken to prevent hypoxia, hypotension and aspiration. Because anatomical and physical changes related to pregnancy have anes-thetic implications, most anesthesiologists prefer to use local and regional anesthesia whenever possible.

The task force also addressed the use of radiographs dur-ing pregnancy by concluding that diagnostic radiographs are safe during pregnancy and recommended the use of shielding for pregnant women’s abdomen and neck. The number of radiographs which should be ordered should depend on the clinical condition, and dentists are urged to follow guidelines issued by the FDA. It is important to note that the guidelines do not need to be altered because of

Burakoff. New York state leading the way...

These drugs may be used during pregnancyAntibiotics FDA CategoryPenicillin .................................................................BAmoxicillin ..............................................................BCephalosporins ........................................................BClindamycin ............................................................BErythromycin (except for estolate form) .................B

Analgesics FDA CategoryAcetaminophen .......................................................BAcetaminophen with Codeine .................................CCodeine ...................................................................CHydrocodone ...........................................................CMeperidine ..............................................................BMorphine .................................................................B

After 1st Trimester for 24-72 hours onlyIbuprofen ................................................................BNaprosyn .................................................................B

These drugs should not be used during pregnancyAntibiotics FDA CategoryTetracyclines ...........................................................DErythromycin in the estolate form ..........................BQuinolones ..............................................................CClarithromycin ........................................................C

Analgesics FDA CategoryAspirin ....................................................................C

Table 2Prescription drug use and pregnancy

GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4 51

Category A — Controlled studies show no risk – Ade-quate, well-controlled studies in pregnant women have failed to demonstrate risk to the fetus.

Category B — No evidence of risk in humans – either animal studies show risk (but human fi ndings do not) or, if no adequate human studies have been done, animal fi ndings are negative.

Category C — Human studies are lacking and animal studies are either positive for fetal risk or lacking as well. However, potential benefi ts may justify the poten-tial risk.

Category D — Positive evidence of risk – investigational or post marketing data show risk to the fetus. Neverthe-less, potential benefi ts may outweigh the risk, such as some anticonvulsive medications.

Category X — Contraindicated in pregnancy – studies in animals or humans, or investigational or post marketing reports have shown fetal risk, which clearly outweighs any possible benefi t to the patient, such as isotretinoin and thalidomide.

Table 1FDA use-in-pregnancy ratings for drugs

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pregnancy. Nevertheless, since it is prudent to minimize radiation at all times and especially during pregnancy, routine dental x-rays, panoramic and cephalometric fi lms may be deferred.

Finally, the guidelines’ take away message for the oral healthcare and the prenatal care provider team is that pregnancy in itself is not a contraindication for dental care. There may be other medical conditions concurrent

with pregnancy that may alter treatment choices and the timing of dental procedures may best be performed dur-ing certain times, but necessary dental care should not be delayed because of pregnancy. In fact, dental intervention during pregnancy may have a very benefi cial effect on the health of the mother and fetus. It is incumbent on the oral health and prenatal providers to work as a team to maxi-mize the probability of a good outcome by addressing the oral health needs of the mother.

52 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

Burakoff. New York state leading the way...

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PennWell Corporation, publisher of Dental Economics and RDH, announces the launch of Grand

Rounds in Oral – Systemic Medicine, an authoritative and

compelling new publication focusing on the understanding

of oral – systemic medicine and its appropriate integration into clinical practice of mainstream

dentistryand medicine.

Grand Rounds in Oral-Systemic Medicine translates credible

and relevant scientifi c fi ndings related to oral-systemic medicine

into informative and timely editorial content.

Upcoming issues will cover:

- Pre-term Birth - Oral Cancer

- The Impact of Osteoporosis on Oral Health

- The Impact of Oral Conditions/Diseases on the

Immunocompromised Patient - The Relationship between Periodontal Disease and

Pulmonary Diseases

View our latest issue and subscribe to Grand Roundsin Oral-Systemic Medicine today by visiting

www.thesystemiclink.com.

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TOOLS FOR

54 GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4

As a courtesy to the professions, Grand Rounds in Oral-Systemic Medicine™ has provided patient education materials and templates of letters to assist dentists in developing collaborative relationships with the medical community. Readers are invited to reproduce these copyrighted materials by accessing and downloading (for free) this information from www.thesystemiclink.com. Collateral case study information may also be accessed and viewed/downloaded from www.thesystemiclink.com.

Listing of the additional materials available throughwww.thesystemiclink.com:Collateral Case Study Information (Kerpen & Fleischer)• Case Study 1: Intraoral image, full mouth series of radiographs,

periodontal chart• Case Study 2: Intraoral image, full mouth series of radiographs,

periodontal chart• Case Study 3: Intraoral image, periodontal chart• Case Study 4: Intraoral image, full mouth series of radiographs,

periodontal chart

A New Opportunity for Students ...

Grand Rounds in Oral-Systemic MedicineTM is proud to announce this new student section where our best and brightest dental and dental hygiene students have an opportunity to actively participate in the design and development of valuable patient education materials. This not only enhances students’ educational experiences, but it also provides them with useful publication skills so that they can become the next generation of journal contributors and effective advocates for the clinically applied mission of Grand Rounds. The honor of being selected as the student author of patient education materials will be distributed to all dental and dental hygiene schools. We encourage faculties who work with promising students to submit their names for consideration for this honorary invitation to contribute to the editorial mission of Grand Rounds.

In this inaugural student section, we are happy to recognize Ms. Jane Crawford (with oversight from Dr. Anthony Iacopino) from the Marquette University School of Dentistry in Milwaukee, Wisconsin, for her excellent work in preparing the patient education tool for implementation titled “Helping Patients Understand the Importance of Oral Health Before and During Pregnancy”.

To download a fi le of this patienteducation information, go to:www.thesystemiclink.com

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IMPLEMENTATION

GRAND ROUNDS IN ORAL-SYSTEMIC MEDICINE • NOVEMBER 2006 • VOL. 1, NO. 4 55

To assist dentists in developing collaborative relationships with the medical community, Grand Rounds in Oral-Systemic Medicine™ has provided templates for dentists working in collaboration with physicians of at-risk patients.

These letters may be customized for individual patients by editing the fi elds (which appear in red typeface) as they relate to the unique risk profi le and periodontal treatment plan of a specifi c patient.

A Microsoft Word document of these templates may be downloaded at:www.thesystemiclink.com

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INDICATION

DESCRIPTION:

CLINICAL PHARMACOLOGY:

PHARMACOKINETICS:

CONTRAINDICATIONS:

PRECAUTIONS:GENERAL:

PREGNANCY: TERATOGENIC EFFECTS

NURSING MOTHERS:

PEDIATRIC USE:

CARCINOGENESIS, MUTAGENESIS, AND IMPAIRMENT OF FERTILITY

ADVERSE REACTIONS:

OVERDOSAGE:

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HOW SUPPLIED:

DIRECTIONS FOR USE:

WHAT TO EXPECT WHEN USING PERIDEX ORAL RINSE:

REFERENCES:

NH

H H H H H H

N C C (CH2)6 C C C C C CCl Cl • 2 HOOC CH2OHN N N N N

NH NH NH

HOH OH OH

H OH H H

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Fear Of Flossing?

If patients are afraid to floss because their gums bleed, first let them know that it’s notthe floss that is causing the problem and that daily flossing actually helps improve gumhealth. Then start the patient on PERIDEX® chlorhexidine gluconate 0.12% therapy,the oral rinse indicated for the treatment of gingivitis as characterized by redness andswelling of the gingivae, including gingival bleeding on probing. That’s a claim youwill not hear from the makers of OTC mouthwashes.

For more information, contact your OMNII Preventive Care Consultant or visit our website www.omniipharma.com

PERIDEX is indicated for use between dental visits as part of a professional programfor the treatment of gingivitis. Patients with a known sensitivity to ChlorhexidineGluconate should not use PERIDEX. The effect of PERIDEX on periodontitis hasnot been determined. Common side effects associated with the use of PERIDEX includean increase in the staining of oral surfaces, an increase in calculus formation, and analteration in taste perception. Please see adjacent page for full prescribing information.

Call to order: 800-445-3386©OMNII 2006. PERIDEX is a registered trademark of Zila Pharmaceuticals, Inc.

Gingival bleeding? Make sure patients know it’s not the floss.

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