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El-Hakim, Paul W. Major and Carlos Flores-MirMichael P. Major, Manisha Witmans, Hamdy Graziela De Luca Canto, Vandana Singh,systematic review and meta-analysissleep-disordered breathing in children: Aclinical examinations to assess Diagnostic capability of questionnaires and

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JADA 145(2) http://jada.ada.org February 2014 165

ORIGINAL CONTRIBUTIONS

Diagnostic capability of questionnaires and clinical examinations to assess sleep-disordered breathing in childrenA systematic review and meta-analysis

Graziela De Luca Canto, DDS, MSc, PhD; Vandana Singh, DDS, MSc; Michael P. Major, DMD, MSc, FRCD; Manisha Witmans, MD, FRCPC; Hamdy El-Hakim, MD, FRCS(Ed), FRCS(ORL-HNS); Paul W. Major, DDS, MSc, FRCD(C); Carlos Flores-Mir, DDS, DSc, FRCD(C)

Pediatric sleep-disordered breathing (SDB) is a diagnosis that reflects a spectrum of symptoms and conditions, ranging from snoring to upper airway resistance syndrome to obstructive sleep

apnea (OSA).! The prevalence of snoring in children has been reported to be at least "# percent,$," and it is the most prevalent symptom of pediatric obstructive sleep apnea (POSA).# In contrast, the prevalence of POSA is reported to be from ! through # percent.%-&

Pediatric SDB symptoms include habitual snoring, excessive daytime sleepiness, disturbed sleep and day-time neurobehavioral problems.',( Although tonsil and adenoid hypertrophy is acknowledged generally as the most common etiology of SDB,!) evidence indicates that a growing number of other risk factors contribute to SDB such as obesity,( craniofacial anomalies,( neuromuscular disorders,( nasal abnormalities,& waist circumference,& metabolic factors,& neck circumference,!) ethnicity,!! asth-ma,!$ local environmental irritants!" and preterm birth.* If SDB is left untreated, it can be a cause of significant morbidity in children and could lead to growth failure, neurocognitive and behavioral abnormalities, and car-diovascular effects, including cor pulmonale, ventricular dysfunction and systemic hypertension.!

SDB is of significant relevance to practicing den-tists as it has been associated with a variety of oral and craniofacial problems, such as a retrusive chin,!# Class II malocclusion,!# vertical growth direction!# and sleep bruxism.!%-$)

Sleep laboratory–based polysomnography (PSG) is considered the reference standard for the diagnosis and

ABSTRACT

Background. +e reference standard for the diagno-sis of pediatric sleep-disorder breathing (SDB) is a full polysomnography (PSG) (an overnight sleep study). +ere are many obstacles to children being able to undergo a full PSG; therefore, the authors evaluated the diagnostic value of alternative diagnostic meth-ods (clinical history and physical examination) for pediatric SDB.Types of Studies Reviewed. +e authors selected articles in which the investigators’ primary objective was to evaluate the diagnostic capability of physi-cal evaluations and questionnaires compared with the current reference standard (that is, a full PSG) to diagnose SDB in children younger than 18 years. +e authors searched several electronic databases without limitations.Results. Using a two-step selection process, the authors identi,ed 24 articles and used them to conduct a qualitative analysis. +ey conducted a meta-analysis on 11 of these articles. Among these articles, only one involved a test that had diagnostic accuracy good enough to warrant its use as a screening method for pediatric SDB, but its diagnostic accuracy was not suf-,cient to be considered a true diagnostic tool (that is, a replacement for full PSG) for pediatric SDB.Practical Implications. +e involvement of dentists in the screening process for pediatric SDB can con-tribute signi,cantly to children’s health. +e identi-,ed questionnaire could be considered an acceptable screening test to determine which children to refer to a sleep medicine specialist.Key Words. Obstructive sleep apnea; sleep apnea syndrome; decision making; evidence-based dentistry.JADA 2014;145(2):165-178.

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assessment of SDB in children.$! However, conducting PSG sleep studies is onerous and labor-intensive, leads to substantial discomfort for children and their families, and is relatively inaccessible to children. Waiting times between referral for evaluation and diagnosis com-monly are five to six months worldwide.$$ The relative complexity and costs associated with PSG for diagnosing most sleep disorders has spurred the quest for alterna-tive diagnostic methods, particularly for children.$$ The alternative diagnostic methods that have been evaluated include medical history and physical examination,!,$" audiotaping,$# videotaping,$% pulse oximetry$* and ab-breviated PSG.$&

Investigators in numerous studies have assessed the accuracy of clinical symptoms and signs in indicating the presence of POSA, but they found that the accuracy var-ied significantly for different symptoms and signs, as well as across studies.$' This scenario supports the execution of systematic reviews and meta-analyses to determine which signs and symptoms can be used in the diagnosis of SDB. Authors of systematic reviews have evaluated the diagnostic value of questionnaires, clinical assessments or both as related to the use of PSG to diagnose SDB in children.$'-") However, these reviews focused on the physician’s use of these methods, ignoring the growing role of dentists."!-"# We have identified potentially perti-nent studies$!,"%-#" that were not included in the previous systematic reviews for different reasons.

Because dentists commonly are not able to make refer-rals for PSG, we conducted a systematic review to evaluate the diagnostic value of alternative tests that are available in dental practice—specifically, clinical history, physical examination or both—to diagnose SDB in children.

METHODSWe conducted this systematic review by following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist.## We did not register the systematic review protocol.

Eligibility criteria. We selected only articles in which the primary objective was to evaluate the diagnostic capability of a clinical evaluation (that is, clinical history, physical examination or both), questionnaire or both to diagnose pediatric SDB. Full PSG had to be used as the reference test. The evaluated population had to be children from ) to !' years of age. We considered studies that were published in any language. We excluded pub-lished reviews, letters and personal opinions.

Information sources and search strategies. We de-veloped detailed individual search strategies for each of the following bibliographic electronic databases: MED-LINE, PubMed, Embase, Cochrane Library and LILACS. (More information on the search strategies is provided in Appendix !, which can be found in the supplemental data to the online version of this article [found at http://jada.ada.org/content/!#%/$/!*%/suppl/DC!].) We also

hand searched the reference lists in the selected articles for any additional references that might have been missed in the electronic database searches. We under-took a gray literature search by using Google Scholar. We limited this search to the !)) most recent hits. We con-ducted all searches from beginning dates through Aug. !(, $)!", across all databases. We managed the references by using software (RefWorks-COS, ProQuest, Bethesda, Md.) and removed duplicate hits.

Study selection. We selected articles in two phases. In phase !, two authors (G.L.C., V.S.) independently reviewed the titles and abstracts for all of the references. They excluded any articles that did not appear to meet the inclusion criteria from further evaluation. In phase $, they applied the same selection criteria to the full text of the articles to determine which ones to include, as some abstracts may have presented study details incorrectly or only partially. The same two authors independently reviewed all full-text articles. Any disagreement in the first or second phase was resolved by means of discus-sion and mutual agreement between the two authors. A third author (C.F.-M.) became involved, when required, to make a final decision.

Data collection process. One author (G.L.C.) col-lected the required information (authors, year of publica-tion, country, sample size, ages of participants, methods, index test, reference standard and findings) from the selected articles. A second author (V.S.) cross-checked all the retrieved information. Again, any disagreement was resolved by means of discussion and mutual agreement between the two authors. The third author (C.F.-M.) was involved, when required, to make a final decision.

Data items. For each of the included studies, we recorded the author, year of publication, country, size and demographic features of the sample (age range and mean), type of diagnostic approach (questionnaire, clini-cal, PSG) and the results related to diagnostic capabilities of the tests.

Risk of bias in individual studies. We evaluated the methodology of selected studies by using the !#-item Quality Assessment Tool for Diagnostic Accuracy Stud-ies (QUADAS).#% Two authors (G.L.C., V.S.) scored each data item as “yes,” “no” or “unclear” and assessed inde-pendently the quality of each included study. The third author (C.F.-M.) resolved any disagreement between the authors.

ABBREVIATION KEY. OSA: Obstructive sleep apnea. OSA-18: Obstructive Sleep Apnea-18. OSAS: Obstructive sleep apnea syndrome. PDSS: Pediatric Daytime Sleepiness Scale. POSA: Pediatric obstructive sleep apnea. PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses. PSG: Polysomnography. PSQ: Pediatric Sleep Questionnaire. QUADAS: Quality Assessment Tool for Diagnostic Accuracy Studies. SDB: Sleep-disordered breathing. SDSC: Sleep Dis-turbance Scale for Children. SRBD: Sleep-Related Breathing Disorder.







Summary measures. Sensitivity and specificity of the diagnostic tests were the main outcomes evaluated.

Synthesis of results. We evaluated the diagnostic capability of the clinical criteria or questionnaire against PSG. We combined the individual results by means of a meta-analysis by following the appropriate Cochrane Collaboration guidelines.#* We used software (Review

Manager %.$, The Nordic Cochrane Centre, Copenhagen, Denmark) to construct receiver operating characteristic (ROC) graphs and forest plots as part of the meta-anal-ysis. Some of the required data were not specified in the articles, so we had to calculate the data or obtain it from the articles’ authors.

Risk of bias across studies. To decrease heterogene-

Iden

tifi

cati

onSc

reen

ing

Elig

ibili

tyIn

clud

edRecords identified through database search

(n = 1,811)

Records after duplicates removed(n = 1,127)

Records screened(n = 33)

Records excluded(n = 1,094)

Additional articles identifiedfrom reference lists of thearticles selected during the

initial search(n = 2)

Full-text articles excluded withreason

(n = 11)

Articles excluded becauseof insufficient information

for meta-analysis(n = 8)

Articles excluded becauseanalyzed only signs and

symptoms (n = 4)

Articles excluded becauseunavailable/incorrect data for

meta-analysis (n = 1)

Lack of full polysomnography (n = 2)

Different target condition(n = 7)

Insufficient information(n = 1)

Other methods (n = 1)

Full-text articles assessed for eligibilty(n = 35)

Studies included in qualitative synthesis(n = 24)

Studies included in qualitative synthesis(n = 12)

Studies included (n = 11)

Records identifiedthrough other

sources(n = 100)

PubMed(n = 954)

Embase(n = 407)

MEDLINE(n = 370)

LILACS(n = 24)

CochraneLibrary

( n = 56)

Figure 1. Flowchart of the literature search and selection criteria. Source: Moher and colleagues.44







TABLE 1

Summary of descriptive characteristics of studies in included articles.AUTHOR, YEAR

COUNTRY SAMPLE SIZE, NO. AGE METHODS FINDINGSIndex Test Reference

StandardBrockmann and Colleagues,39 2011

Chile 21 children with neuromuscular diseases

Range, 2-17 years; mean, 10.7 years

Questionnaire (Montgomery-Downs and colleagues53)

PSG* The questionnaire showed a moderate sensitivity and specifi city. Nevertheless, the high negative predictive value of the questionnaire may support its use for screening patients for SDB.† A follow-up of the questionnaire’s scores may identify patients who would benefi t from PSG.

Carroll and Colleagues,56 1995

United States

83 children with snoring, SDB or both who were referred for PSG

Range, 5.4 months-14.8 years; mean (SD‡), 5.6 years (3.4)

Questionnaire§ PSG Primary snoring cannot be distinguished reliably from OSAS¶ diagnosed on the basis of clinical history.

Chan and Colleagues,40 2012

China 102 Chinese children with suspected POSA#

Range, 2-18 years; mean (SD), 10.7 (3.5) years

Questionnaire (PSQ** from Chervin and colleagues,21)

PSG Chinese SRBD†† Scale was not accurate in identifying POSA in snoring children in Hong Kong

Chau and Colleagues,55 2003

China 62 children referred to sleep clinic for suspected POSA


Questionnaire (modifi ed from a validated questionnaire by Brouillette and colleagues4)

PSG Snoring every night is an important risk factor in identifying POSA. Priority for PSG should be given to children with this symptom.

Chervin and Colleagues,21 2000

United States

81 children who had SRBD confi rmed by means of PSG or during an appointment at one of general pediatric clinics

Range, 2-18 years

Questionnaire (PSQ)

PSG The SRBD Scale is a valid and reliable instrument that can be used to identify SDB or associated symptom constructs in clinical research when PSG is not feasible.

Chervin and Colleagues,51 2007

United States

105 children (patients and control schedule for adenotonsillectomy and unrelated surgical care, respectively)

Range, 5.0-12.9 years; mean (SD), 8.4 (1.9) years

Questionnaire (PSQ) and behavioral and cognitive testing

PSG The SRBD Scale predicts PSG results to an extent that it is useful for research but not reliable enough for most individual patients. The authors could not conclude that the SRBD scale is an adequate substitute for PSG in clinical practice.

Esteller More and Colleagues,41 2012

Spain 170 children with SDB

Range, 2-10 years

Questionnaire§ and physical examination

PSG Despite limitations in the correlation between clinical data and PSG, especially in preoperative results, PSG remains the reference standard diagnostic tool.

Ferreira and Colleagues,37 2009

Brazil 40 children from sleep laboratory

Range, 3-18 years

Questionnaire (SDSC‡‡ from Bruni and colleagues58)

PSG The SDSC had internal consistency and convergent and discriminatory validity. It can be used in population-based studies to screen for pediatric SDB.

Gasparini and Colleagues,42 2012

Italy 34 pediatric patients with congenital or acquired craniomaxillofacial malformations


Questionnaire (obstructive airway child test)

PSG Obstructive airway child test was shown to be a highly effi cient method to evaluate and diagnose POSA. The examination focused on clinical signs and symptoms because clinical history reported by parents can be more accurate than any instrumental examination.

* PSG: Polysomnography. † SDB: Sleep-disordered breathing. ‡ SD: Standard deviation. § The author did not identify the questionnaire. ¶ OSAS: Obstructive sleep apnea syndrome. # POSA: Pediatric obstructive sleep apnea. ** PSQ: Pediatric Sleep Questionnaire. †† SRBD: Sleep-Related Breathing Disorder. ‡‡ SDSC: Sleep Disturbance Scale for Children. §§ OSA-18: Obstructive Sleep Apnea-18. ¶¶ OSA: Obstructive sleep apnea. ## PDSS: Pediatric Daytime Sleepiness Scale.







TABLE 1 (CONTINUED) AUTHOR, YEAR

COUNTRY SAMPLE SIZE, NO. AGE METHODS FINDINGS

Index Test Reference Standard

Goldstein and Colleagues,1 2012

United States

94 children suspected of having SDB referred for PSG

Range, 2-12 years

Questionnaire (OSA-18§§), clinical assessment

PSG The Clinical Assessment Score-15 tool proved useful in an offi ce setting and correctly diagnosed 72 percent of otherwise healthy referred children when compared with PSG. It correlated well with external measures and demonstrated a good response to clinical change. It can be used to evaluate most children, and PSG can be used for patients with more severe obstructive symptoms, children with discrepancies between the history and physical examination fi ndings and children who remain symptomatic after adenotonsillectomy.


United States

30 children with obstructive symptoms

Range, 1-14 years

History,§ physical examination, tape recording of breathing during sleep

PSG Clinical prediction of a positive result from a PSG in a group of children with history of nighttime breathing diffi culties is sensitive but poorly predictive if PSG is used as a reference standard.

Lamm and Colleagues,24 1999

United States

23 children referred by pediatricians and otolaryngologists for possible OSA¶¶

Range, 1.5-18 years; mean, 5.7 years

Questionnaire§ and audiotape

PSG Clinical history could not separate patients with primary snoring from those with OSA. Because the patient’s history can be inconclusive, the reference standard for the diagnosis of OSA remains the PSG.

Li and Colleagues,54 2001

China 50 children suspected to have POSA

Mean (SD), 6.45 (2.7) years

Questionnaire,§ physical examination, electrocardiogram, chest radiograph

PSG Signs and symptoms suggestive of OSA can lead to a high detection rate and confi rmation of OSA by means of PSG.

Li and Colleagues,48 2006

China 229 children with suspected POSA

Range, 5-15 years

Questionnaire (Hong Kong Children Sleep Questionnaire) and physical examination

PSG The Hong Kong Children Sleep Questionnaire is a useful, valid and reliable screening instrument for OSA in children.

Montgomery-Downs and Colleagues,53 2004

United States

122 children Preschoolers: mean (SD), 4.5 (0.62) yearsolder children: mean (SD), 6.5 (0.52) years

Questionnaire§ PSG Scores derived from parent-report questionnaires of children’s snoring and other sleep and wake behaviors can be used as surrogate predictors of snoring or SDB in children. However, design and interpretation should consider age, risk status and the purpose of the screening assessment.

Pagel and Colleagues,36 2004

United States

74 children who reported daytime sleepiness on questionnaire

Range, 3-16 years

Questionnaire§ and physical examination

PSG In a clinical grouping of pediatric psychiatry patients reporting daytime sleepiness by questionnaire, polysomnographically defi ned OSA diagnosed by means of PSG is common.

Preutthipan and Colleagues,47 2000

Thailand 65 children with POSA

Younger than 15 years

Questionnaire (modifi ed from Carroll and colleagues,56)

PSG Although some parent observations are more frequently reported in children with severe OSAS, neither any single nor combinations of observations accurately predict the severity of OSAS. PSG still is needed to determine the severity of obstruction.

Sanchez-Armengol and Colleagues,49 1996

Spain 12 children with symptoms indicative of upper airway obstruction and who had received a diagnosis of adenotonsillar hypertrophy

Mean (SD), 4.5 (1.5) years

Questionnaire§ PSG No relationship observed between clinical and PSG fi ndings.







ity, we separated the studies into four groups to conduct the meta-analysis according to the index test (question-naire, questionnaire and physical examinations, ques-tionnaire or physical examinations and other tests, and physical examinations and another test).

Additional analyses. We conducted additional analy-sis by using positive predictive values (PPV), negative predictive values (NPV), positive likelihood ratios (LR+), negative likelihood ratios (LR-), diagnostic odds ratios (DOR) and Youden index.

Diagnostic terminology. Definitions of the diagnos-

tic terms we used and what they imply can be found in Appendix $ in the supplemental data to the online ver-sion of this article (found at http://jada.ada.org/ content/!#%/$/!*%/suppl/DC!).

RESULTSStudy selection. In phase !, we found !,'!! references across the five electronic databases. After we removed the duplicate articles, we had !,!$& different references. After we conducted a comprehensive evaluation of the abstracts, we excluded !,)(# articles, resulting in a final

TABLE 1 (CONTINUED) AUTHOR, YEAR

COUNTRY SAMPLE SIZE, NO. AGE METHODS FINDINGS

Index Test Reference Standard

Sproson and Colleagues,52 2009

United Kingdom

61 children with snoring history


Questionnaire (PSQ from Chervin and colleagues21) and clinical evaluation

PSG The clinical diagnostic process for OSA is reasonably insensitive and has low specifi city. The studied algorithm discriminated poorly between children with and without severe OSA. Realistic diagnostic screening guidelines for POSA are overdue in the United Kingdom, where access to PSG is limited.

Supriyatno and Colleagues,10 2010

Indonesia 110 children with obesity and snoring symptoms


Physical examination, lung function test, paranasal sinus radiograph

PSG Tonsillar hypertrophy, adenoid hypertrophy and neck circumference are the main risk factors of OSAS in obese adolescents.

Weatherly and Colleagues,35 2004

United States

34 children from otolaryngology practices that had scheduled them to undergo adenotonsillectomy

Range, 5-12.9 years; mean, 8.2 years

Questionnaire (PSQ from Chervin and colleagues21)

PSG Children with clinical diagnoses of SDB may not consistently meet PSG criteria for this disorder. Negative answers to questions about daytime mouth breathing and habitual snoring might help clinicians recognize children who would not have a diagnosis of SDB by means of PSG. Clinical identifi cation of SDB confi rmable by means of PSG could be improved.

Xu and Colleagues,57 2006

China 50 children consecutively referred to a sleep clinic for suspect OSA

Range, 4-18 years

Questionnaire,§ physical examination, radiograph of postnasal space for upper airway assessment

PSG Combining clinical and radiologic fi ndings might be helpful to screen for children with clinically signifi cant OSA who need earlier investigation and intervention.

Yang and Colleagues,38 2010

Taiwan 28 teenagers with OSA and 34 normal controls to evaluate its clinical utility

28 teenagers with OSA: mean (SD), 13.07 (1.98) years34 normal control participants: mean (SD), 13.97 (1.71) years

Questionnaire (PDSS## from Drake and colleagues59)

PSG The PDSS is a reliable and valid tool for the measurement of sleepiness in clinical youth populations. When used as a screening tool, it is useful for diagnosing sleep disorders involving more severe pathological sleepiness such as narcolepsy.

Yang and Colleagues,43 2012

China 527 children with snoring history

Range, 7 months-15 years; mean, 4.42 years

Questionnaire (OSA-18), physical examination and electronic nasopharyngoscopy

PSG This study’s screening method and diagnosis of OSA in children is feasible and practical. Not only is this screening method simple and economic, but it also takes into account three important aspects worthy of consideration in the diagnosis of OSAS: the child’s history, physical examination and any auxiliary investigations.







number of "" articles in phase !. We identified two addi-tional studies from the reference lists of these "" studies. Therefore, we retrieved "% articles to conduct a full-text review and excluded !! of the articles. We included these remaining $# articles in the qualitative synthesis. A flowchart of the process of identification, inclusion and exclusion of studies is shown in Figure !.

Study characteristics. The $# articles were published in different journals: five articles were in pediatric journals,$#,#),#&-#( seven were in otolaryngology jour-nals,!,"%,#!,#",%)-%$ five were in sleep medicine journals,$!,"*,"&,"(,%" three were in general medicine journals,!),%#,%% two were in pulmonology journals,%*,%& one was in a psychiatry journal"' and one was in a dentistry journal.#$ Sample sizes ranged from !$#( to %$&.#" Most of the studies’ inves-tigators included children with SDB symptoms in their samples. Investigators in one article specifically studied children with congenital neuromuscular diseases,"( and those in another article specifically studied children with acquired craniomaxillofacial malformations.#$ The studies were conducted in !) countries: Brazil,"& Chile,"( China,#),#",#',%#,%%,%& Indonesia,!) Italy,#$ Spain,#!,#( Taiwan,"' Thailand,#& the United Kingdom%$ and the United States.!,$!,$#,"%,"*,%),%!,%",%* Most of the articles were written in English; one was written in Chinese,#" and two were writ-ten in Spanish."(,#!

The following index tests were evaluated: !$ articles used only questionnaires,$!,"%,"&-#),#$,#&,#(,%",%%,%* five articles used questionnaires and physical examinations,!,"*,#!,#',%$ six articles used questionnaires or physical examinations and other tests,$#,#",%),%!,%#,%& and one article used only physi-cal examinations and other tests.!)A summary of the descriptive characteristics of included articles is provided in Table !.!,#,!),$!,$#,"%-#",#&-%(

Risk of bias within studies. The overall percentage of the QUADAS#% criteria for each article is provided in Table $.!,!),$!,$#,"%-#",#&-%& The percentage of QUADAS#% criteria met ranged from %&.! to &'.* percent.

Results of individual studies. The results of !#!,!),$!,"*-"(,#$,#",#',%"-%%,%& of the $# articles concluded that ques-tionnaire, physical examination or both or some selected signs or symptoms can diagnose pediatric SDB reliably. The results of !)$#,"%,#),#!,#&,#(-%$,%* articles showed opposite findings.

Synthesis of results. We constructed a diagnos-tic table by using the data extracted from each article (Table "!,!),$!,$#,"%-#",#&-%&). In Table ", we present all accuracy measurements (we evaluated accuracy by means of the sensitivity and the specificity of the test). We divided the studies into four groups according to the index test (questionnaire, questionnaire or physical examinations, questionnaire or physical examinations and other tests, and only physical examinations and other tests). The investigators in some studies provided more than one accuracy measurement for different parts of the same index test (for example, results for several items of one

questionnaire). These data are shown in Table #"*,#&,%%,%& (page !&#). Only !! articles!,!),$!,$#,"',#),#",#',%)-%$ had enough data to be included in our quantitative synthesis (meta-analysis). We contacted one of the authors of an addi-tional article"( and asked him to provide some missing data. Although we received some extra data, it still was not possible for us to include those data in the meta-analysis owing to missing information. In the !! included articles, investigators analyzed !,#$# people.

The diagnostic accuracy (that is, sensitivity, specificity and (% percent confidence interval) of the studies includ-ed in a meta-analysis is shown in Figure $!,!),$!,$#,"',#),#",#',%)-%$ (page !&#). Sensitivity and specificity for different selected

TABLE 2

Criteria met, according to the Quality Assessment Tool for Diagnostic Accuracy Studies.AUTHOR, YEAR QUALITY ASSESSMENT TOOL

FOR DIAGNOSTIC ACCURACY STUDIES CRITERIA MET (%)

Brockmann and Colleagues,39 2011

64.3

Carroll and Colleagues,56 1995 78.6

Chan and Colleagues,40 2012 78.6

Chau and Colleagues,55 2003 71.2

Chervin and Colleagues,21 2000 71.2

Chervin and Colleagues,51 2007 78.6

Esteller More and Colleagues,41 2012

71.2

Ferreira and Colleagues,37 2009

71.2

Gasparini and Colleagues,42 2012

64.3


64.3


64.3

Lamm and Colleagues,24 1999 57.1

Li and Colleagues,54 2001 57.1

Li and Colleagues,48 2006 64.3

Montgomery-Downs and Colleagues,53 2004

64.3

Pagel and Colleagues,36 2004 64.3

Preutthipan and Colleagues,47 2000

71.2

Sanchez-Armengol and Colleagues,49 1996

64.3

Sproson and Colleagues,52 2009

71.2


71.2

Weatherly and Colleagues,35 2004

64.3

Xu and Colleagues,57 2006 57.1

Yang and Colleagues,38 2010 64.3

Yang and Colleagues,43 2012 64.3







studies varied substantially. The authors of only two studies reported excellent sensitivity: Chervin and col-leagues$! ().'! percent) and Goldstein and colleagues%) ().($ percent). The investigators in three studies!,#',%!

reported good sensitivity ().&& percent, ).&* percent, ).&' percent, respectively). Investigators in none of these five studies!,$!,#',%),%! reported excellent specificity; only Chervin and colleagues$! and Li and colleagues#' had

TABLE 3

Diagnostic accuracy of index tests.INDEX TEST STUDY, AUTHOR (YEAR) SAMPLE

SIZE, NO.

PREVALENCE, %

SENSITIVITY, %

SPECIFICITY, %

POSITIVE PREDICTIVE VALUE, %

NEGATIVE PREDICTIVE VALUE, %

Questionnaire Brockmann and colleagues,39 2011 21 61.9* 75 60 33 90

Carroll and colleagues,56 1995 83 42.8* † † † †

Chan and colleagues,40 2012 102 27.5 50 55 30* 75*

Chau and colleagues,55 2003 62 35.5* ‡ ‡ ‡ ‡

Chervin and colleagues,21 2000 81 85.0 81 83* 97* 45*

Ferreira and colleagues,37 2009 40 † † † † †

Gasparini and colleagues,42 2012 34 70.6* † † † †

Montgomery-Downs and colleagues,53 2004

122 † † † † †

Preutthipan and colleagues,47 2000 65 100 ‡ ‡ ‡ ‡

Sanchez-Armengol and colleagues,49 1996

12 † † † † †

Weatherly and colleagues,35 2004 34 88.0 † † † †

Yang and colleagues,38 2010 62 44.4* 68 54 54* 68*

Questionnaire and Physical Examination

Esteller More and colleagues,41 2012 170 † † † † †

Goldstein and colleagues,1 2012 94 70.0* 77 61 82 53

Li and colleagues,48 2006 229 28.8 76 80 61 89

Pagel and colleagues,36 2004 74 39.2 ‡ ‡ ‡ ‡

Sproson and colleagues,52 2009 61 62.0 68 61 74* 54*

Questionnaire or Physical Examination and Other Test

Chervin and colleagues,51 2007 105 39.0* 78 72 64* 84*

Goldstein and colleagues,50 1994 30 43.3* 92 29 50 83

Lamm and colleagues,24 1999 23 48.0* 45 83 71* 62*

Li and colleagues,54 2001 50 90.0 † † † †

Xu and colleagues,57 2006 50 62.0* ‡ ‡ ‡ ‡

Yang and colleagues,43 2012 527 69.0* 63 79 87‡ 49‡

Physical Examination and Other Test

Supriyatno and colleagues,10 2010 110 38.2 62 100 100 81

* Data not available in the original article. Calculated from information available in the article.† Data not available in the article.‡ Calculated the accuracy for each symptom.







good specificity values. In the other articles, no single questionnaire or clinical model satisfied the criteria to be an acceptable (that is, close to ideal) diagnostic test. The investigators who analyzed the questionnaire and physical examinations,!,#!,#',%$ on average, found that when both tools are used there probably will be a better performance and a better chance of making a correct

diagnosis. Figure "!,!),$!,$#,"',#),#",#',%)-%$ (page !&*) shows the ROC graphs from four index tests.

Risk of bias across studies. The main methodological limitations of the studies were related to poor reporting of QUADAS items four (“Is the time period between reference standard and index test short enough to be reasonably sure that the target condition did not change between the two tests?”), !) and !! (“Were the index test results interpreted without knowledge of the results of the reference standard?” and “Were the reference stand-ard results interpreted without knowledge of the results of the index test?”) and !" (“Were uninterpretable/inter-mediate test results reported?”).#% Investigators did not assess interobserver agreement in all of the studies.

Additional analysis. Chervin and colleagues$! had the highest LR+ value, and Chan and colleagues#) reported the highest LR- value. Regarding PPV and NPV, Chervin and colleagues,$! Supriyatno and colleagues!) and Yang and colleagues#" had the highest PPV, whereas Goldstein and colleagues,%) Li and colleagues#' and Chervin and colleagues%! had the highest NPV. This finding means that investigators in the first three studies!),$!,#" were relatively good at identifying who really had SDB (true positive), and the investigators in other three studies#',%),%! were better at identifying who did not have the SDB (true negative).

According to the classification presented in Appendix $ in the supplemental data to the online version of this article (found at http://jada.ada.org/content/!#%/$/!*%/suppl/DC!), Chervin and colleagues,$! Li and colleagues#' and Supriyatno and colleagues!) reported fair Youden index ().*#, ).%* and ).*$, respectively) values. The investigators in other articles found significantly lower Youden index values. Investigators in none of the articles reported Youden index values close to !, which would indicate high accuracy.#*

We found three studies$!,#',%! with DORs higher than those in the other studies, which means that the pa-tients who had SDB could be identified more often than patients without SDB ($!.!& times more in Chervin and colleagues,$! !$.'" times more in Li and colleagues#' and '.(& times more in Chervin and colleagues%!) (Table ").

When we considered the signs and symptoms of SDB individually, some of them had better results than the others (Table #). The item that had the highest sensitiv-ity ((! percent) was “snoring every night.”%% However, the specificity for this item was only fair (&% percent). This item also had the highest DOR (")."").%% “Watches child sleeping, afraid about breathing” had excellent sensitiv-ity ('% percent) but poor specificity (#! percent).#& “Long adenoid faces,” “midface hypoplasia,” “micrognathia/ret-rognathia,” “observable apnea” and “observed cyanosis” had excellent specificity but poor sensitivity.#&,%&

DISCUSSIONSummary of evidence. In this systematic review, we investigated the available evidence about the diagnostic

TABLE 3 (CONTINUED)

POSITIVE LIKELIHOOD

RATIO

NEGATIVE LIKELIHOOD

RATIO

DIAGNOSTIC ODDS RATIO

YOUDEN INDEX VALUE

1.9 0.40 4.43* 0.35*

† † † †

1.12 0.90 1.24‡ 0.05‡

‡ ‡ ‡ †

4.87‡ 0.23‡ 21.17‡ 0.64‡

† † † †

† † † †

† † † †

‡ ‡ ‡ †

† † † †

† † † †

1.48* 0.59* 2.50* 0.22*

† † † †

1.97* 0.37* 5.32* 0.38*

3.85* 0.30* 12.83* 0.56*

† † ‡ †

1.70* 0.53* 3.21* 0.29*

2.78* 0.31* 8.97* 0.50*

1.30* 0.26* 5.00* 0.21*

2.71* 0.65* 4.17* 0.29*

† † † †

‡ ‡ ‡ †

3.00‡ 0.47‡ 6.38‡ 0.42‡

Undefi ned 0.38 0‡ 0.62*







TABLE 4

Diagnostic characteristics of various components of the questionnaireand clinical evaluation.COMPONENT SENSITIVITY,

%SPECIFICITY,

%POSITIVE

PREDICTIVE VALUE, %

NEGATIVE PREDICTIVE VALUE, %

POSITIVE LIKELIHOOD

RATIO*

NEGATIVE LIKELIHOOD

RATIO*

Attention Defi cit/Hyperactivity Disorder 52 67 50 68* 1.55 0.72

Diffi cult Breathing 16 84 63 38 1.00 1.00

Frequent Sore Throat/Dry Mouth 29 90 82 44 2.90 0.79

Long Adenoid Faces 10 100 100 40 Undefi ned 0.90

Micrognathia/Retrognathia 0 95 0 36 Undefi ned 1.05

Midface Hypoplasia 16 100 100 41 Undefi ned 0.84

Mouth Breathing During Daytime 26 79 67 40 1.24 0.94

Mouth Breathing During Sleep 68 42 66 44 1.17 0.76

Observable Apnea 36 95 91 47 7.20 0.67

Observed Cyanosis 35 92 75 67 4.38 0.71

Observed Obstructive Apnea 61 65 57 69 1.74 0.60

Shakes Child to Make Him or Her Breathe 64 65 58 71 1.83 0.55

Snoring Disturbs Others 68 58 72 52 1.62 0.55

Snoring Every Night 91 75 67 94 3.64 0.12

Snoring Extremely Loudly 52 78 64 69 2.36 0.62

Tonsillar Hypertrophy 69 53 49 73* 1.48 0.58

Tonsil Size = Grade 3† 81 58 76 65 1.93 0.33

Watches Child Sleeping, Afraid About Breathing 85 41 51 79 1.44 0.37

* Data not available in the original articles. The authors calculated data from information available in the article.† Xu and colleagues57 graded tonsil size by direct visualization: 0, not visible; 1, extending to the pillars; 2, enlarged beyond the pillars but not meet-

ing uvula; 3, meeting the uvula; and 4, “kissing” at the midline. Moderate to severe tonsillar hypertrophy was defined as grade 3 or above.

A. Questionnaire

B. Questionnaire and Physical Examination

C. Questionnaire and Physical Examination and Other Tests

D. Physical Examination and Other Tests

Study TP FP FN TN Sensitivity (95% CI) Specificity (95% CI)




0 0.2 0.4 0.6 0.8 1

Sensitivity (95% CI)

0 0.2 0.4 0.6 0.8 1

Specificity (95% CI)

0 0.2 0.4 0.6 0.8 1


0 0.2 0.4 0.6 0.8 1


0 0.4 0.6 0.8 1


0 0.2 0.4 0.6 0.8 1

0 0.2 0.4 0.6 0.8 1


Sensitivity (95% CI) Specificity (95% CI)

0 0.4 0.6 0.8 1

Yang and Colleagues,38 2010Chan and Colleagues,40 2012Chervin and Colleagues,21 2000

Goldstein and Colleagues,1 2012Li and Colleagues,48 2006Sproson and Colleagues,52 2009

Chervin and Colleagues,51 2007Goldstein and Colleagues,50 1994Lamm and Colleagues,24 1999Yang and Colleagues,43 2012


191456

515026

32125

229

26 0 16 68

18122

34

916

135

465

10129

113226

151612

1713114

16332

91413

194110

0.68 (0.48-0.84)0.50 (0.31-0.69)0.81 (0.70-0.90)

0.77 (0.65-0.87)0.76 (0.64-0.85)0.68 (0.51-0.82)

0.78 (0.62-0.89)0.92 (0.64-1.00)0.45 (0.17-0.77)0.63 (0.58-0.68)

0.62 (0.46-0.76) 1.00 (0.95-1.00)

0.72 (0.59-0.82)0.29 (0.10-0.56)0.83 (0.52-0.98)0.79 (0.72-0.85)

0.61 (0.41-0.78)0.80 (0.73-0.86)0.61 (0.39-0.80)

0.54 (0.37-0.71)0.55 (0.43-0.67)0.83 (0.52-0.98)

Figure 2. Forest plot with the diagnostic accuracy (sensitivity, specificity and 95 percent confidence interval) of each study. TP: True positive. FP: False positive. FN: False negative. TN: True negative. CI: Confidence interval.







capability of the questionnaire, physical examinations or both for diagnosing SDB in children. This subject is particularly important, because SDB is recognized as a potential cause of significant morbidity in children.! Among the health care professionals treating children, dentists are positioned uniquely to identify pediatric SDB by either carefully considering the SDB-related answers during the medical history intake or identifying the ap-parent craniofacial consequences of SDB. The frequency of dental visits also plays a role. A key question is whether dentists have easy access to reliable alternative diagnostic tools. We found a diversity of alternative tests that were compared with the current reference standard (PSG).

In our study, we found that investigators in only two studies reported excellent sensitivity.$!,%) However, al-though Chervin and colleagues$! reported good specific-ity, Goldstein and colleagues%) reported poor specificity. In other words, Chervin and colleagues$! reported a good ability to identify patients both with and without SDB, and Goldstein and colleagues%) reported the ability to identify SDB patients, but they were not able to identify those who did not have SDB.

Although no individual sign or symptom had excel-lent sensitivity and excellent specificity, some items (that is, “long adenoid faces,” ”midface hypoplasia,” “micro-gnathia/retrognathia,” “observable apnea” and “observed cyanosis”) had excellent specificity, which means that in the absence of these signs or symptoms, a person is less likely to have SDB.

In summary, only the Pediatric Sleep Question-

naire (PSQ)$! had a diagnostic accuracy good enough to be used as a screening method for SDB. However, the results of the PSQ$! showed diagnostic values (NPV, LR+, LR- and Youden index values) that were not sufficient for it to be considered a true diagnostic tool for pediatric SDB.

Overall assessment. Although investigators in most of the $# articles concluded that some questionnaires, physical examinations or both or some selected signs or symptoms could be useful for reliably diagnosing pediatric SDB, the results of the meta-analysis indicated a contrasting situation. We found that only the PSQ$! was a valid instrument that could be used to screen for pediatric SDB. The remaining alternative diagnostic tests did not satisfy the criteria to be an acceptable diagnos-tic or screening tool. The authors of three systematic reviews$'-") reported that almost every sign or symp-tom or combination of signs and symptoms had poor accuracy in diagnosing SDB. Investigators in only one of the reviews identified a few tests with acceptable or excellent diagnostic test accuracy in predicting OSA by means of PSG.") These tests included sleep laboratory–based polygraphy, anterior rhinomanometry and urinary biomarkers. However, the authors stated that there was insufficient evidence to recommend any of these tests as alternatives to PSG for the diagnosis of POSA. In addi-tion, the investigators in three systematic reviews$'-") did not include the article that we found that included the tool with the best accuracy.$! We found this article when we hand searched the selected articles’ reference lists.

Another finding was that when a questionnaire was associated with a physical examination, the performance of the test improved. This finding emphasizes the impor-tance of clinical examinations in the diagnosis of SDB.

SDB is of significant relevance to practicing den-tists, as it has been associated with a variety of oral and craniofacial problems, such as retrusive chin,!# Class II malocclusion,!# vertical growth direction!# and sleep bruxism.!%-$) Considering this association, we found it unusual that only one#$ of the articles we included in our systematic review was published in a dental journal. It is important to increase dentists’ understanding regarding available appropriate screening methods for SDB. Once a pediatric dental patient is identified as being highly likely to have SDB, the dentist should make a proper refer-ral to a pediatric sleep medicine specialist for definitive diagnosis and treatment.

Limitations. Our review had some methodological limitations. Most of the identified studies used a sample from sleep centers or children with complaints about snoring or other breathing symptoms. This can affect the prevalence, which can bias the accuracy of diagnostic tests. In other words, the identified tests that provided acceptable diagnostic values would not respond similarly among the overall population of a pediatric practice. The test results likely will present a wrong result under the

TABLE 4 (CONTINUED)

DIAGNOSTIC ODDS RATIO

YOUDEN INDEX VALUE*

AUTHOR, YEAR

2.10 0.19 Pagel and colleagues,36 2004

1.00* 0 Xu and colleagues,57 2006

3.67* 0.19 Xu and colleagues,57 2006

0* 0.10 Xu and colleagues,57 2006

0* !0.05 Xu and colleagues,57 2006

0* 0.16 Xu and colleagues,57 2006




6.17* 0.27 Preutthipan and colleagues,47 2000




30.33* 0.65* Chau and colleagues,55 2003


2.55 0.22 Pagel and colleagues,36 2004









typical conditions of a pediatric dental practice. Investi-gators in only three studies"(,#$,%" used a sample of children without previously known breathing problems. None reported acceptable accuracy.

The main methodological limitations of the selected studies were the same as those identified in the previous reviews: time between the diagnosis with the reference standard and the alternative tests,$(,") lack of a masked

interpretation of the reference and alternative tests,$(,") and reporting of confusing test results.$(

Although we know that the period between the index test and PSG might have an impact on the results, this time frame generally was not mentioned in the articles. Investigators in only one article"& stated clearly that the tests were masked, but we did not include this study in the meta-analysis because it had incomplete data. In all

SEN

SITI

VITY

SEN

SITI

VITY

SEN

SITI

VITY

SEN

SITI

VITY

SPECIFICITY SPECIFICITY

SPECIFICITY SPECIFICITY

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0

1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0

1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0

A B

C D

21

38

40

10

50

51

43

24

52

148

Figure 3. Receiver operating characteristic curves for each group. A. Questionnaire. B. Questionnaire and physical examination. C. Questionnaire and physical examination and other test. D. Physical examination and other test. The numbers in the graphs refer to the articles’ reference numbers.







of the studies, interobserver agreement was not assessed, and it was not clear how many investigators analyzed the test results or if their techniques were calibrated.

Recommendations for future research. In the future, we need to improve the evaluation of the alternative di-agnostic tests for pediatric SDB by increasing the sample size and improving the methodological quality of valida-tion studies. The quality can be improved by conducting well-controlled and masked studies. We also need to have a better understanding of the pathophysiology of SDB to devise logical algorithms aimed at screening and diagnosing SDB.

CONCLUSIONSThe PSQ$! had the best diagnostic accuracy of the evalu-ated tests. Because it did not attain diagnostic values high enough to replace the current reference standard, PSG, dentists should use it as a screening tool to identify pediatric SDB. This should improve the referral process to pediatric sleep specialists. Q

Dr. Canto is an adjunct professor, Department of Dentistry, Federal Univer-sity of Santa Catarina, Florianopolis, Santa Catarina, Brazil, and a postdoc-toral fellow, School of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada. Address correspondence to Dr. Canto at Department of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, %-'" Edmonton Clinic Health Academy, Edmonton, Alberta, Canada T*G !C(, e-mail [email protected] or [email protected].

Dr. Singh is a clinical instructor, Orofacial Pain Graduate Program, Depart-ment of Dentistry, School of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton Clinic Health Academy, Edmonton, Alberta, Canada.

Dr. Michael P. Major is a clinical assistant professor and the director of the Inter-disciplinary Airway Research Clinic, Division of Orthodontics, School of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.

Dr. Witmans is an associate clinical professor, Department of Pediatrics, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.

Dr. El-Hakim is an associate professor, Pediatric Otolaryngology, Depart-ment of Surgery, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.

Dr. Paul W. Major is a professor and the chair, School of Dentistry, and the senior associate dean, Dental Affairs, Department of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.

Dr. Flores-Mir is an associate professor and the division head, Orthodontics, School of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.

Disclosure. None of the authors reported any disclosures.

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