Meta-analysis of Parental Protection of Children From Tobacco … · searched Medline (Ovid),...

Meta-analysis of Parental Protection of ChildrenFrom Tobacco Smoke Exposure

abstractBACKGROUND AND OBJECTIVE: Worldwide, roughly 40% of childrenare exposed to the damaging and sometimes deadly effects of tobaccosmoke. Interventions aimed at reducing child tobacco smoke exposure(TSE) have shown mixed results. The objective of this study was to per-form a systematic review and meta-analysis to quantify effects ofinterventions aimed at decreasing child TSE.

METHODS: Data sources included Medline, PubMed, Web of Science,PsycNet, and Embase. Controlled trials that included parents of youngchildren were selected. Two reviewers extracted TSE data, as assessedby parentally-reported exposure or protection (PREP) and biomarkers.Risk ratios and differences were calculated by using the DerSimonianand Laird random-effects model. Exploratory subgroup analyses wereperformed.

RESULTS: Thirty studies were included. Improvements were observedfrom baseline to follow-up for parentally-reported and biomarker datain most intervention and control groups. Interventions demonstratedevidence of small benefit to intervention participants at follow-up(PREP: 17 studies, n = 6820, relative risk 1.12, confidence interval [CI]1.07 to 1.18], P , .0001). Seven percent more children were protected inintervention groups relative to control groups. Intervention parentssmoked fewer cigarettes around children at follow-up than did controlparents (P = .03). Biomarkers (13 studies, n = 2601) at follow-upsuggested lower child exposure among intervention participants(RD 20.05, CI 20.13 to 0.03, P = .20).

CONCLUSIONS: Interventions to prevent child TSE are moderately ben-eficial at the individual level. Widespread child TSE suggests potentialfor significant population impact. More research is needed to improveintervention effectiveness and child TSE measurement. Pediatrics2014;133:698–714

AUTHORS: Laura J. Rosen, PhD,a Vicki Myers, MSc,a,b

Melbourne Hovell, PhD,c David Zucker, PhD,d and MichalBen Noach, MSca,e

aDepartments of Health Promotion, bEpidemiology, School ofPublic Health, Sackler Faculty of Medicine, and eStatistics andOperations Research, Faculty of Exact Sciences, Tel AvivUniversity, Ramat Aviv, Israel; cCenter for BehavioralEpidemiology and Community Health, School of Public Health, SanDiego State University, San Diego, California; and dDepartment ofStatistics, Hebrew University, Jerusalem, Israel

KEY WORDSsecondhand smoke exposure, tobacco smoke exposure, meta-analysis, systematic review, child

ABBREVIATIONSCCR—cotinine/creatinine ratioCI—confidence intervalCT—controlled trialPREP—parentally reported exposure or protectionRCT—randomized controlled trialRD—relative differenceRR—relative riskSHS—secondhand smokeTHS—thirdhand smokeTSE—tobacco smoke exposure

Dr Rosen conceptualized and designed the study, oversaw allaspects of the research, performed the systematic review of theliterature, extracted data from the original studies, contributedto the statistical analysis, wrote sections of the manuscript, andedited the entire manuscript; Ms Myers contributed tosystematically reviewing the literature, extracted data from theoriginal articles, contributed to the data analysis, andcontributed to the writing of the manuscript; Dr Hovellcontributed to the design of the meta-analysis andinterpretation of the data and edited the manuscript forscientific content; Dr Zucker assisted with various statisticalissues in the analysis of the manuscript and edited themanuscript; Ms Ben Noach contributed to the design of thestudy, the systematic review of the literature, data extraction,data analysis, data interpretation, and writing of themanuscript; and all authors approved the final version of themanuscript.

www.pediatrics.org/cgi/doi/10.1542/peds.2013-0958

doi:10.1542/peds.2013-0958

Accepted for publication Jan 10, 2014

Address correspondence to Laura J. Rosen, PhD, School of PublicHealth, Sackler Faculty of Medicine, Tel Aviv University, POB 39040,Ramat Aviv, Israel 69978. E-mail: [email protected]

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mailto:[email protected]

Exposure to tobacco smoke, whichcauses serious disease and shortenslife,1 is a leading public health issueworldwide.2 Children are especiallysusceptible to toxicity from secondhandsmoke (SHS) because of their size anddevelopmental stage,1 with increasedrisk of sudden infant death syndrome,middle ear disease, more severe asthma,pneumonia, and lowered lung function,as well as school absenteeism anddays of restricted activity.1,3 Detrimentalhealth effects of SHS exposure persistinto adulthood,4 with children of smok-ing parents at greater risk for tobaccouse.5 Worldwide, 40% of children areexposed to SHS.6 The importance ofprotecting children from SHS is recog-nized by the World Health Organization,7

the Environmental Ministers of the G8,8

and US Healthy People 2020.9

Thirdhand smoke (THS) is defined as“residual tobacco smoke contaminationthat remains after the cigarette isextinguished.”10 Particulate matterfrom cigarette smoke may settle onhome surfaces, and be released into theair over a period of months. Youngchildren may be exposed to THS fromcontact with their parents’ clothing,from furniture or carpets, or from up-holstery in cars or homes.11 Harm at-tributed in the past to SHS exposuremay have included harm due to THSexposure. The term “tobacco smokeexposure (TSE)” is used in this article todenote a combination of SHS and THSexposure.

Children, particularly young children,spend much of their time in the home.Although there have been sporadicinitiatives regarding regulation ofsmoking in homes, private cars, and theopen air public spaces that childrentend to frequent, regulation of the homeenvironment is generally rare.12 Hence,reliable protection remains an elusivegoal.

In the past few decades, researchershave explored means to convince families

and caretakers to voluntarily protectchildrenfromTSE.Somehave focusedongetting parents to quit smoking to pro-tect their children. However, the impactofsuchprogramshasbeen limited. First,some smokers are unwilling toquit or toparticipate in smoking-cessation pro-grams. Second,most parents do not quiteven within the context of controlledtrials aimed at promoting cessation tobenefit the children.13,14 Even amongthose who do quit, many may return tosmoking.15 Further, smoking cessationof 1 smoker in the home does not fullycontrol exposure when other familymembers, child caretakers, and/orfriends continue to smoke in the homeor when with the child. Thus, cessationinterventions, although important, arenot successful for most families inwhich smoking occurs, and are notsufficient to fully protect children frommultiple sources of exposure.

Some researchers have focused ongetting parents to protect their childrenby moving their smoking and others’smoking behaviors away from thehome, car, or child. In particular, smoke-free homes and smoke-free cars havebeen emphasized. Tools used to effectchange have included cognitive behav-ioral approaches, motivational inter-viewing, self-help materials, individualcounseling, and biofeedback. Previousreviews have, for the most part, usednarrative synthesis.5,16–19 No meta-analyses have been performed toquantify and test the effects of theinterventions on decreasing child ex-posure.

In this article, we presentmeta-analysesof original studies evaluating inter-ventions aimed at protecting childrenfrom TSE. The key outcome variableswere (1) parentally reported child ex-posure or protection (PREP), and (2)biomarkers of child exposure. We per-formed exploratory subgroup analysesin an attempt to identify “active ingre-dients” of effective interventions.

METHODS

Data Sources and Search Strategy

We conducted a number of literaturesearches, and were familiar with theliterature from previous research. Wereport here on our final search, whichwas a targeted search performed withthe aid of a librarian specializing inmedical databases (Ruth Suhami). Wesearched Medline (Ovid), PubMed, Psy-cINFO, Web of Science, and Embase forarticles published through the begin-ning of October 2013. We created thesearch strategy in Medline and thenadapted it to all other databases, ac-cording to each database’s vocabularyand syntax. We used both index termsand keyword searches, as follows:

� Medline: We used the followingMESH terms: Tobacco Smoke Pollu-tion OR (Parents AND “Tobacco UseCessation”).

� Embase: We used the followingEMTREE terms: second hand smokeOR passive smoking OR (smokingcessation AND parents).

� PsycINFO: We used the Index Term“Passive Smoking”.

� All databases: We searched for thefollowing keywords: second-handsmoke OR passive smoking OR envi-ronmental tobacco smoke OR invol-untary smoking OR Tobacco smokeexposure (with all variations of spell-ings and endings).

We limited all searches to the agegroups of newborn/infant/child.

We used a randomized controlled trial(RCT)filter for thesearch, requiringeacharticle to be a randomized controlledtrial or a controlled clinical trial. We ex-cluded the following publication types:case-control study, cross-sectional study,meta-analysis, systematic review, pro-tocol, observational study, and guideline.

In cases in which data on relevantoutcomes were collected but requiredinformationwasmissing,weattempted

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to contact study authors for data. Wereceived additional information fromauthors of 15 studies.20–34

Data Extraction

Data were independently extracted byat least 2 of 3 reviewers (LJR, VM, MBN),and then compared. Differences wereresolved through discussion.

Methodological Quality

We assessed study design, blinding ofobservers, percent follow-up, fidelity totreatment (eg, how many participantsreceived the intervention), andwhetherthe control group received an activeintervention.

Study Eligibility

To be included, the studies had to meetthe following criteria:

� Study design: RCT using a clusteror individual-level randomizationscheme, quasi-randomized RCT, orcontrolled trial (CT).

� Participants: Parents (mother, fa-ther, or both parents) of childrenbetween the ages of 0 and 6 years.Trials that included children olderthan 6 years were acceptable onlyif children 6 years old or youngerwere also included.

� Types of interventions: Any type ofintervention that had as one of itsaims helping parents decrease TSEof their children.

� Length of observation period: Mini-mum 1 month from start of interven-tion. In studies reporting differentfollow-up times, we used the longestavailable period.

Data Analysis

1. We descriptively examined changesin outcome variables for each study,by intervention group.

2. We used meta-analyses to comparebetween intervention groups for eachoutcome. For parentally reported

outcomes, we examined (1) valuesat follow-up, and (2) change fromstudy beginning to end. For bio-markers and parentally reportednumbers of cigarettes smokedaround the children, we did nothave sufficient data on change, andso compared values at follow-up.

Study Outcomes

1. Parentally-reported exposure orprotection (PREP)

PREP included home smoking bans,changes insmoking location toprotectchild, smoking around the child,moving the child away from others’smoking, being in action/maintenancephase of child TSE protection, and ex-posure of the child. We examined (1)values of PREP at the end of the study,and (2) changes in values of PREPfrom beginning to end of the study.

2. Parentally reported number of ciga-rettes smoked around the child. Be-cause measurement differed fromstudy to study (number of cigarettesper day, week, or month), we stan-dardized each value by dividing bya pooled SD.35

3. Biomarkers of tobacco smoke expo-sure: measured levels of cotinine ornicotine in urine, blood, saliva, orhair. Because the measurement dif-fered from study to study (raw val-ues, logged values, geometric means,cotinine/creatinine ratios [CCRs]),we standardized each value by us-ing a pooled SD.35

Explanatory Variables

We extracted and categorized the fol-lowing variables:

Child-related subgroups: Child age atrecruitment, child cohort.

Intervention-related subgroups: Re-cruitment setting, intervention set-ting, provider, intervention intensity,length of observation, interventioncomponents: biochemical feedback,

counseling, phone support, self-helpmaterials, cessation medication use,air cleaner.

Study quality–related subgroups:Study design, blinding of observers,follow-up of participants, fidelity totreatment, provision of active inter-vention to the control group duringthe study period.

Statistical Analysis

Meta-analytic Approach

Statistical analyses and meta-analyseswere performed by using RevMan 5.2.7(Cochrane Collaboration, Copenhagen).We used the DerSimonian and Lairdrandom-effects method with 95% CIs topool results.36 We chose to use therandom-effects method because weassumed that different interventionconditions would be associated withdifferent effects, and we were in-terested in getting an average of thetrue effects from the population of in-tervention studies (as opposed to anestimate of a single population effect,as would be the case were we to usethe fixed-effects method).35

For the biomarker analysis and paren-tally reported number of cigarettes towhich the child was exposed, we stan-dardizedeachvaluebyusingapooledSDfrom the study, and present risk differ-ences (RDs). For PREP, we present rela-tive risks (RRs) and RDs. Estimates arepresented with 2-sided 95% CIs. ThepooledRRsandRDswereestimatedwithweights based on the inverse variancemethod and adjusted for the random-effects assumption.35

We performed meta-analyses on thefollowing outcomes: (1) PREP at studyend, (2) change in PREP from baseline toend, (3) number of cigarettes smokedaround child at study end, and (4) bio-markers at the end of the study.

Heterogeneity and Publication Bias

We used the I2 statistic to investigatestatistical heterogeneity. This describes


the percentage of the variability in effectestimates that is due to heterogeneityrather than sampling error (due tochance).37 Existence of publication biaswas assessed via visual examination offunnel plots.35

Exploratory Subgroup Analyses

We performed exploratory analyses forPREP using the following subgroups:intervention intensity, counseling, bio-chemical feedback, fidelity to protocol,and control group intervention.

RESULTS

Description of Studies

Our targeted, systematic search pro-duced 386 articles. We were aware of 4additional articles that did not appearin the search, bringing the total to 390.Two records were duplicates and wecould not find any information on 2records. We scanned titles of a total of386 articles. Most articles (n = 276)were excluded on the basis of title, andanother 35 were excluded after read-ing the abstract. Seventy-five full-textarticles were read. Forty-five studieswere excluded for the following rea-sons: no relevant outcomes, 18 stud-ies38–55; the trial did not includea control group, 7 studies56–62; theinterventions were not aimed at pa-rents of young children, 3 studies63–65;the reporting period was,1 month, 2studies66,67; data necessary for analysiswere missing, 10 studies68–77; the pa-per was a review article, 1 study78; thearticle was a protocol, 2 studies79,80;the article was a follow-up of a pre-vious study, 1 study81; there was notrue control group (eg, 2 active inter-ventions were compared), 1 study82.

Thirty studiesmet the inclusion criteriafor this review.20–34,83–97

The trialswere published between 1994and 2013. A flowchart describing theidentification process is presented inFig 1. Study characteristics of includedtrials are presented in Tables 1 and 2.

Study Characteristics

Intervention Components

Interventions included the followingcomponents: self-help materials, 20studies,23,25,26,28,29,33,83–95,97; face-to-facecounseling, 26 studies20–26,28–34,84–92,95–97;telephone counseling, 13 stud-ies21–25,31,33,83–85,90,93,96; free nico-tine replacement therapy to helpparents quit smoking, 1 study25; bio-chemical feedback, 4 studies31,32,92,93;and air cleaners, 2 studies20,27.

Intervention Intensity

In 11 studies, up to 1 session (eitherface-to-face or on the phone)was given26,27,30,83,86,87,89,92,94,95,97; in 18of the studies .1 session wasgiven.20–25,28,29,31–33,84,85,88,90,91,93,96 One studydid not report the number of sessions.34

Control Group Intervention

In 9 of the studies, the control groupparticipants received some sort of in-

tervention that was specific to trialparticipants related to smoking, cessa-tion, or risk to children from smok-ing.24,26,28,83,86,91,92,94,95 In 7 studies,control groups received asthma edu-cation that may or may not havereferred to TSE, or reported the pro-vision of very brief advice to controlgroup participants as part of usualcare.20,23,29–32,96 In 14 studies, the controlparticipants received usual care, hadcontact for measurement only, or re-ceived an unrelated control group in-tervention.21,22,25,27,33,34,84,85,87–90,93,97

Biomarkers

Of the 13 studies presenting biomarkerinformation at follow-up, 9 presented uri-nary cotinine or urinary CCR20,23–25,31–33,93,96;2 presented salivary cotinine22,26; 1 pre-sented serum cotinine27; and 1 presentedhair nicotine and cotinine.21

Blinding

Seventeen studies reported blindingof observers20,22–27,30,31,33,34,83,84,88,89,95,97;

FIGURE 1Flowchart for identification of studies.

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TABLE1

Characteristicsof

Included

Studies

Study

Ageat

Recruitm

enta

Child

Cohortb

Recruitm

entS

ettingc

InterventionSettingd

Provider

eInterventionIntensity

fLength

ofObservation

Intervention

Componentsg

Abdullah2005

835y(2)

Well(1)

Health

center

visitor/database

(1)

Phone(1)

Nurse(1)

3phone(1)

1,3,6mo

A,C

Baheiraei20118

4,1y(1)

Well(1)

Health

center

–routine

check-up

(1)

Health

center

+phone(2)

Research

assistant(4)

Mother:1inperson,

2phoneFather:

3phone(2)

3mo

A,B,C

Butz2011

206–12

y(2)

Sick

(asthm

a)(2)

Hospital/pediatric

database

ofasthmatic

children(2)

Home(1)

Health

coach/nurse(1)

4asthmaeducation

sessions

+2air

cleaners

(2)

6mo

B,F

Chan

2006

85,18

y(2)

Sick

(2)

Hospital(2)

Hospital(4)

Nurse(1)

1-In-person,

1-Phone(2)

3,6,12

mo

A,B,C

Chellini20138

6Notspecified

(2)

Mixed

(3)

Publichealth

facilities,

hospitalsandoutside

superm

arkets(3)

NR(3)

Trainedhealth

visitors

(4)

Counseling,self-

help,and

gifts

1(1)

4mo

A,B

Conw

ay2004

211–9y(2)

Well(1)

Community

(3)

Home/phone(1)

Community

health

advisors

(4)

6home/phone(2)

3,12

mo

B,C

Eriksen1996

87,4y(2)

Well(1)

Child

health

centers

(well-childvisits)(1)

Child

health

centersor

home(duringwell

child

visitsby

health

visitors)(3)

Health

visitor

(clinicstaff)(3)

1lengthened

visit

+2brochures(1)

1mo

A,B

Fossum

2004

341–4wk(1)

Well(1)

Child

health

centers(3)

Child

health

center

(2)

Nurse(1)

NR(3)

3mo

BGreenberg1994

88,

1mo(1)

Well(1)

Hospital–

birth(1)

Home(1)

Nurse(1)

4homevisits(2)

7,12

mo

A,B

Groner

2000

89,

12y(2)

Mixed

(3)

Primarycare

center

(3)

Primarycare

center

(3)

Nurse(1)

1meeting+

self-help(1)

1,6mo

A,B

Halterm

an2013

223–10

y(2)

Sick

(asthm

a)(2)

School(3)

Home(1)

Nurse(1)

3(1

face-to-face

and2phone

calls)(2)

7–9mo

B,C

Hovell2000

24,4y(2)

Well(1)

Community

(3)

Home+phone(1)

Research

assistant(4)

7:3Home,4

phone(2)

3,6,12

mo

B,C

Hovell2002

233–17

y(2)

Asthmatic(2)

Community

+media(3)

Home(1)

Research

assistant(4)

8:7in-person

+1phone

booster(2)

4,7,10,13mo

A,B,C

Hovell2009

25,4y(2)

Well(1)

Community

(3)

Home+Phone(1)

Studycounselor(4)

14:10in-person,

4phone(2)

3,6,12,18mo

A,B,C,D

Huang2013

90,3y(2)

Unknow

n(3)

Hospitalpediatric

department(2)

NR(3)

Research

nurse(1)

3(1

video/

counseling

+2phone

calls)(2)

1mo

A,B,C

Irvine

1999

262–12

y(2)

Asthmatic(2)

Asthmaticdrug

registries

(2)

Home(1)

Nurse(1)

1inperson

+3leaflets(1)

12mo

A,B

Krieger2005

914–12

y(2)

Asthmatic(2)

Community

health

clinic+hospital/

emergency(3)

Home(1)

Community

health

workers

(4)

5to9visits(2)

12mo

A,B

Lanphear

2011

276–12

y(2)

Asthmatic(2)

Hospitalvisit(2)

Home(1)

Research

assistant(4)

2aircleaners

(1)

12mo

F


TABLE1

Continued

Study

Ageat

Recruitm

enta

Child

Cohortb

Recruitm

entS

ettingc

InterventionSettingd

Provider

eInterventionIntensity

fLength

ofObservation

Intervention

Componentsg

McIntosh1994

926mo–17

y(2)

Asthmatic(2)

Seekingasthma

care

(2)

PediatricPulmonary

clinic(2)

Physician(2)

1counseling+

mailed

biofeedback(1)

4–6mo

A,B,E

Prokhorov2013

94,18

y(2)

Well(1)

Studydatabase

–

cohortofMexican

households

(1)

Home(1)

Interviewers/

Projectstaff(4)

1comicbook

+2

illustrated

storybooks(1)

6,12

mo

A

Severson

1997

282wk(1)

Well(1)

Wellinfantvisit(1)

Clinic(2)

Nurse,projectstaff(5)

5advice

during

well-carevisits(2)

12mo

A,B

Stotts2013

29Infants(1)

Prem

ature

babies

–high

respiratory

risk

(2)

Hospital-NICU

(2)

Hospital(2)

MIcounselor

(4)

2MIsessions(2)

6mo

A,B

Streja2012

952–14

y(2)

Asthmatic(2)

Outpatient

clinics,mobile

asthmavans,schools,

community

agencies

andhospitalERs

(3)

NR(3)

Projectstaff(4)

1minimalcounseling

+video,workbook(1)

6,12

mo

A,B

Teach2006

301–17

y(2)

Asthmatic(2)

Hospitalvisit(2)

Clinic(2)

Doctor

and

educator

(5)

1visit(1)

6mo

B

Tyc2013

96,18

y(2)

Patientswith

cancer

(2)

Medicalrecords(2)

NR(3)

Trained

counselors

(4)

6:3face-to-face

+3phonecalls

(2)

3,6,9,12

mo

B,C

Wakefield2002

931–11

y(2)

Asthmatic(2)

Pediatricoutpatient

clinicsofhospitals(2)

Phone(1)

NR3:2phonecalls

+1letter

(2)

6mo

A,C,E

Wilson

2001

323–12

y(2)

Asthmatic(2)

Hospitalemergency,

inpatient,or

outpatient

dept.(2)

Outpatientcaresetting

(2)

Nurse-educator

(1)

3in-person(2)

6,12

mo

B,E

Wilson

2011

313–12

y(2)

Asthmatic(2)

HMOdatabase,flagged

asusersofasthma

medsor

with

asthma

diagnosis(2)

Outpatientcaresetting

(2)

Registered

respiratory

care

practitioner

andaregistered

respiratory

therapist(5)

6:3visits+3

phonecalls

(2)

6,12

mo

B,C,E

Yilmaz

2006

97,16

y(2)

Well(1)

Wellinfantclinicinhospital(1)

Wellinfantclinic(2)

Nurse(1)

1face-to-face

+documents(1)

6mo

A,B

Zakarian

2004

33,4y(2)

Well(1)

Community

health

clinics(1)

Clinic,phone

(2)

Clinicstaffw

orking

asstudycounselors

(health

educators,

nurses,m

edical

assistants)(3)

7:3in-person

+4phone(2)

12mo

A,B,C

ER,emergencyroom

;MI,motivationalinterview

;NR,notreported;NICU,Neonatalintensivecare

unit.

a(1)=OnlyInfants,(2)=NotOnlyInfants.

b(1)=Well,(2)=Sick,and

(3)=Mixed,Unknown.

c(1)=WellH

ealth

Center

orDatabase

ofWellChildrenor

HealthyBirths,(2)

=Sick

Visitor

SeekingAsthmaCare

orDatabase

ofSick

Children,(3)=Mixed/Other/Unknow

n.d(1)=Homeor

Phoneor

Home+Phone,(2)=Clinic/HospitalorClinic/HospitalplusPhone,(3)=Mixed/Other/Unclear.

e(1)=Nurse,(2)=Doctor,(3)

=ClinicStaff,(4)=ProjectStaff/Research

Assistant,(5)=Mixed/Unknown.

f(1)=Up

to1Face-to-FaceMeetingWith

orWithoutS

elf-H

elp,(2)=More,(3)=NotReported.

gA=self-helpmaterials,B

=counseling,C=phonesupport,D=medication,E=biochemicalfeedback,F

=aircleaners.

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TABLE2

MethodologicalCharacteristicsof

Included

Studies

No.Randomized

Design

Blinding

ofObservers

PercentFollow-up

PercentParticipants

Received

Full

Intervention

Fidelitya

WhatC

ontrolGroupReceived

b

Abdullah2005

83952

RCT

Yes

88NR

NRPrintedself-helpmaterials(1)

Baheiraei20118

4130

RCT

Yes

9394%

High

Usualcare(4)

Butz2011

20126

RCT

Yes

91NR

NRAsthmaeducation(2)

Chan

2006

851483

RCT

NR86

NRNR

Usualcare(4)

Chellini20138

6218

RCT

NR95

NRNR

Self-helpmaterials(1)

Conw

ay2004

21143

RCT

NR89

NRNR

Measurementonly(4)

Eriksen1996

87443

RCT

NR82

NRNR

Nothing(noinform

ationgivenunless

requested)

(4)

Fossum

2004

3441

CTYes

73NR

NRUsualcare(4)

Greenberg1994

88933

RCT

Yes

7196%

High

Measurementonly(4)

Groner

2000

89479

RCT

Yes

48NR

NRSafetyinform

ation(4)

Halterm

an2013

22530

RCT

Yes

96NR

NRNothing(noETScounseling)

(4)

Hovell2000

24108

RCT

Yes

12mo.Questionnaire:89

12mourine:87

92%

High

Briefadvicetoquitsm

okingandnotexpose

childrentoETS(1)

Hovell2002

23193

RCT

Yes

9798%

High

Asthmamanagem

ent(2)

Hovell2009

25150

RCT

Yes

8754%

Moderate

Usualcare(4)

Huang2013

90355

QuasiRCT

NR83

NRNR

Measurementonly(4)

Irvine

1999

26501

RCT

Yes

87NR

NRLeafleton

smoking(1)

Krieger2005

91274

RCT

No78

NRNR

Lowintensity

intervention–1visitincluding

home

assessment+

actionplan

(1)

Lanphear

2011

27225

RCT

Yes

96100%

High

Inactiveaircleaner(4)

McIntosh1994

9292

RCT

NR78

(self-report)

NRNR

Counselingon

passivesm

oking,advice

toquit

smokinginside

home(1)

Prokhorov2013

9491

RCT

NR81

NRNR

Self-helpforquitting(1)

Severson

1997

282901

ClusterRCT

NR69

NRNR

Minimalintervention–self-helpmaterialson

passive

smokingandquittingor

stayingquit(1)

Stotts2013

29144

RCT

NR69

71%

Moderate

Usualhospitalcare,includinginform

ationon

dangersof

smoking,notsm

okingaround

infant,orquitting(3)

Streja2012

95242

RCT

Yes

73NR

NRBrochure

onimportance

ofSHSas

asthmatrigger(1)

Teach2006

30488

RCT

Yes

9071%

Moderate

Asthmaeducationbooklet(2)

Tyc2013

96135

RCT

NR93

84%

High

Standard

care

controlgroup:Briefadvice

aboutd

angers

ofandchild

protectionfrom

TSE(3)

Wakefield2002

93292

QuasiRCT

NR90

85%

High

Usualcare(4)

Wilson

2001

3287

RCT

NR69

73%

Moderate

Asthmaeducation(2)

Wilson

2011

31352

RCT

Yes

9677%

Moderate

Asthmaeducation(2)

Yilmaz

2006

97375

RCT

Yes

97NR

NRUsualcare(4)

Zakarian

2004

33150

RCT

Yes

8572%

Moderate

Measurementonly(4)

NR,Not

Reported;SHSe,Secondhand

smokeexposure.

aHigh,.

80%;m

oderate,50%–79%;low

,,50%.

b(1)=SHSe

orsm

okingcounseling,(2)=asthmaeducation,(3)=briefm

entionas

partofusualcare,(4)=usualcare/measurement/unrelatedintervention.


1 study reported nonblinding of observ-ers91; and the remaining 12 studies did notreport on blinding.21,28,29,32,85–87,90,92–94,96

Fidelity

Seven studies reported high fidelity,with at least 80% of participants re-ceiving the full intervention23,24,27,84,88,93,96;6 studies had moderate fidelity, with50% to 79% of participants receivingthe intervention25,29–33; and the re-maining 17 studies did not reportfidelity.20–22,26,28,34,83,85–87,89–92,94,95,97

Intervention Effects

Parentally Reported Outcomes

PREP at baseline, follow-up, and/orchange in PREP are presented for 23studies in Table 3. PREP improved in86.4% (19/22) of intervention groups and90.9% (20/22) of control groups. We wereunable to describe change in 1 study thatpresented only data at follow-up.83

1. PREP at follow-up.

Seventeen studies (n =6820),20,23,28–32,83–86,88,90–94 were includedin the analysis of PREP at follow-up(Fig 2A). Benefit was apparent in88.2% (15/17) of studies,with 29.4% (5/17) showing a statistically significantadvantage to the intervention group.Risk ratios from individual studiesranged from 0.97 to 2.05, with anoverall RR of 1.12 (CI 1.07 to 1.18], P,.0001), showing a small but statisticallysignificant benefit to the interventiongroup. The RD was 0.07 (CI 0.05 to 0.09,P, .0001), indicating a benefit to 7%of the intervention families.

2. Seven studies (n = 1639) were in-cluded in the analysis of change inPREP from baseline to follow-up(Fig 2B).21,26,86,87,89,95,97 Benefit was sug-gested in 71.4% (5/7) of studies, with42.9% (3/7) reaching statistical signif-icance. The overall risk ratio showedmoderate, but not statistically signifi-cant, benefit of the interventions (RR1.44, CI 0.90 to 2.29], P = .13).

3. Eight studies (n = 908) were in-cluded in the analysis of numberof cigarettes to which the childrenwere exposed (Table 4, Fig 2C). Forall 7 studies that had available dataat baseline and follow-up, the num-bers of cigarettes smoked aroundchildren decreased from baselineto follow-up in both the interven-tion and control groups. At studyend, positive effect of the interven-tion was indicated in 75% (6/8) ofstudies,20,21,24,25,27,96 with 2 studiesshowing statistically significant im-provement in the interventiongroup.24,25 RDs ranged from 20.81to 0.20. The overall RD was 20.24(CI 20.46 to 20.03, P = .03), show-ing a statistically significant differ-ence between intervention and controlgroups at study end.

Biomarker Outcomes

Table 5 presents changes in bio-markers from baseline to follow-up.Levels of biomarkers decreased, onaverage, in 11 of the 13 interventiongroups20–26,31–33,93 and in 10 of the 13control groups.20,22,23,25–27,31–33,93

Thirteen studies (n = 2601) (Fig 2D)were included in the analysis of bio-marker assessment of child exposureat follow-up.20–27,31–33,93,96 A positive ef-fect of the intervention was found in61.5% (8/13) of the studies,20–22,24,25,26,31,32

with 1 study24 showing a statisticallysignificant advantage to the in-tervention group. RDs for the individualstudies ranged from 20.52 to 0.20.Overall, the RD was20.05 (CI20.13 to0.03, P = .20), demonstrating a trendtoward benefit without statistical sig-nificance.

Publication Bias

Funnel plots for the 4meta-analysesarefound in Fig 3. The funnel plots for thePREP and biomarker analyses showindication of publication bias.

Heterogeneity of Results

The test for heterogeneity was notsignificant for the PREP at end of studyanalysis (I2 = 23%, P = .18) or for thebiomarker end point (I2 = 0%, P = .57),indicating that the results were ho-mogeneous in those analyses. Hetero-geneity was present in the PREP –

change analysis (I2 = 87%, P , .0001)and the analysis of number of ciga-rettes (I2 = 62%, P = .01)

Exploratory Subgroup Analyses onPREP

The exploratory analyses (see Table 6)included 3 to 14 studies each, with RRsranging from 1.07 to 1.27. Most sub-groups showed significant, albeitsmall, benefit to the interventions.

DISCUSSION

Interventions aimed at aiding parents toprotect their children from TSE showedsmall benefits when assessed by pa-rental report at study follow-up (RR 1.12,CI 1.07 to 1.18, P, .0001; RD 0.07, CI 0.05to 0.09, P , .0001). Although the di-rection of the effect was beneficial,biomarkers at study follow-up did notshow evidence of an intervention effect(RD20.05, CI 20.13 to 0.03, P = .20)

Our results add to previous knowledge,which was primarily obtained fromnarrative reviews. Emmons et al16

found significant reductions in paren-tally reported exposure in 40% (2/5) ofstudies, but did not find significantdifferences in objective biochemicalmeasures. Wewers and Uno,19 in their2002 narrative review of 4 clinicalinterventions, found small improve-ments in exposure associated withclinical interventions, without statisti-cal confirmation. Gehrman et al’s 2003review17 with 19 studies found a smalleffect size (0.34, range20.14 to 1.04)98

due to interventions, again withoutstatistical confirmation. Klerman’s 2004review18 reported benefit in 2 of 3

REVIEW ARTICLE


trials using biochemical measures, and3 of 3 trials using parental reports of thenumber of cigarettes smoked in thehome. Cochrane reviewers in 2008,5(p3)

by using a narrative approach to sum-marize 36 studies, concluded that “ef-fectiveness has not been clearlydemonstrated.” We attribute our moredefinitive findings to the use of formalmeta-analysis: benefits include theability to detect and quantify smallbenefits of interventions.35

The Cochrane review noted “limitedsupport for more intensive counsellinginterventions for parents in such con-texts [eg, child health settings].”5 Ourexploratory analyses, by contrast,found small benefit to both intensive

(RR 1.12, CI 1.07 to 1.18, P, .0001) andless-intensive (RR 1.18, CI 1.02 to 1.35,P = .02) interventions. The lower-intensity interventions included in thisreview used a range of self-help mate-rials, including innovative approaches,such as comic books, story books,videos, and air cleaners.

Observed Benefits Among ControlGroup Participants

One of the most interesting findings ofthis review was the consistent sug-gestion of benefit to control groupparticipants. Many authors of includedstudies21,25,26,86,95,96 remarked on this intheir articles; 90.9% (20/22) of controlgroups in the PREP analysis, and 76.9%

(10/13) of control groups in the bio-marker analysis, showed trends to-ward improvements from baseline tothe end of the study.

There are a number of plausibleexplanations, the most obvious of whichis the effect of monitoring. Hovell et al25

estimated that monitoring alone wasresponsible for about two-thirds of thedecline in exposure among trial partic-ipants. Trial enrollment may be a factor:Wahlgren et al81 found improvements inchild TSE protection after recruitmentbut before the intervention took place.Secular trends may also be of impor-tance: cigarette smoking is decliningin the United States99 and WesternEurope,100 smoke-free regulation is

TABLE 3 PREP, by Intervention Group and Time

Study Variable Intervention Group Control Group

Baseline% (n/N) Follow-up% (n/N) ReportedChange% (n/N)

Baseline% (n/N) Follow-up% (n/N) ReportedChange% (n/N)

Abdullah 200583 Complete home ban NR 36.7% (146/398) NR NR 27.8% (119/428) NRBaheiraei 200184 Home ban 15% (9/60) 33.3% (20/60) NR 11.5% (7/61) 19.7% (12/61) NRButz 2011a,20 Successfully keep child

away from smoke76% (31/41) 97% (37/38) NR 70% (31/44) 79% (33/42) NR

Chan 200685 Mothers move childaway from smoke

32.7% (79/242) 58.3% (49/84) NR 33.3% (80/240) 51% (52/102) NR

Chellini 201386 Smoke-free homes 38.2% (42/110) 50.9% (56/110) NR 34.3% (37/108) 45.4% (49/108) NRStopped smoking indoors NR NR 2.8% (1/36) NR NR 13.3% (6/45)

Conway 2004a,21 Confirmed reducers NR NR 61% (36/59) NR NR 55.6% (35/63)Eriksen 199687 Any positive change NR NR 15.4% (34/221) NR NR 14.4% (32/222)Greenberg 199488 No infant tobacco

smoke exposure67% (195/292) 51% (149/292) 66% (192/291) 46% (134/291)

Groner 200089 Location change NR NR 33% (24/72) NR NR 16% (13/79)Hovell 2002a,23 No exposure (based on

number of cigarettes);3% (3/97) 55% (52/95) 7% (7/96) 46% (43/93)

Huang 201390 Percent in action/maintenancephase (motherswith children)

73.2% (52/71) 87.3% (62/71) 68.6% (59/88) 70.9% (61/88)

Irvine 1999a,26 Parent smokes less in home NR NR 49% (104/213) NR NR 38% (84/222)Krieger 200591 No smoking allowed in home 80% (88/110) 77.3% (85/110) 76% (79/104) 79.8% (83/104)McIntosh 199492 No smoking allowed in home 19% (7/37) 35% (13/37) 14% (5/35) 17% (6/35)Prokhorov 201394 Home smoking ban 0% (0/47) 73% (29/40) 0% (0/44) 56% (20/36)Severson 1997a,28 Smoking never

allowed in home59.5%, 1001/1682 43.6%, 733/1682 57.6% (702/1219) 38.6% (471/1219)

Stotts 2013a,29 Home smoking ban 68.12% (47/69) 86.27% (44/51) 67.65% (23/34) 86.36% (19/22)Streja 201295 Home smoking ban NR NR 25% (22/88) NR NR 30% (26/87)Teach 2006a,30 Percent not smoking

daily in home88% (215/244) 95.6% (218/228) 88.5% (216/244) 90% (209/232)

Wakefield 200293 Home smoking ban 41.4% (53/128) 49.2% (63/128) 39.7% (54/136) 41.9% (57/136)Wilson 2001a,32 Smoking not allowed in home 73.3% (22/30) 90% (27/30) 60% (18/30) 70% (21/30)Wilson 2011a,31 Smoking not allowed in home 65.7% (117/178) 84.0% (142/169) 66.7% (116/174) 77.1% (131/170)Yilmaz 200697 Postintervention

location changeNR NR 73% (81/111) NR NR 11.6% (14/121)

NR, not reported.a Based on published data and/or data provided by author.


increasing across the globe,2 and theprevalence of smoke-free homes amongsmokers has been shown to increasewith regulation against smoking inpublic places.101 Another possible ex-planation is that trials that provide ac-tive, usually weakened, interventions tocontrol group participants, a commontechnique,102 are less likely to show truebenefits of interventions. However, our

subgroup analyses did not support thishypothesis.

Comparisons of ParentallyReported and Biomarker EndPoints

Whereas statistically significant in-tervention effects on parentally reportedendpoints (both inPREPat studyend, andnumber of cigarettes smoked around

child) were found in this study, statisti-cally significant intervention effectswerenot demonstrated for biomarkers, al-though a trendwas found toward benefit(RD20.05, CI20.13 to 0.03], P= .20). Thismay be due to several factors. First, itmay be related to the number of trialsand participants included in the re-spective meta-analyses. The analysis in-volving parental report had more power

FIGURE 2Forest plots. Effects of interventions on the following: A, PREPat study end. B, Change in PREP during study. C, Parentally reported number of cigarettes towhichchild was exposed, at study end. D, Biochemically assessed child exposure, at study end.

REVIEW ARTICLE


to detect true differences because it in-cludedmore trials and a greater numberof participants. Second, it may be thatparental reports are unreliable: parentsmay tend to incorrectly estimate expo-sure because they deny exposure or areunaware of it. This leads to 2 problems:first, it is more difficult to detect truedifferences if measurement is inexact,103

and, second, if intervention group

participants underreported exposureto a greater degree than did controlgroup participants, it would lead tooverestimation of intervention benefit. Anadditional possibility is that biomarkers,although considered the gold standardfor evaluation of child exposure,1 may notbe sufficiently sensitive to detect smallchanges in exposure levels. Matt et al104

found that precisely estimating exposure

over a period of 4 to 13 months couldrequire up to 12 urine samples. Wilsonet al32 found that “single, intermittenturine samples provide a relatively crudeindex of both typical and maximal expo-sure.”p.1718 Inexact measurement lowersthe probability of detecting true in-tervention effects.103 Finally, it is possiblethat biomarkers and parental reportsmeasure different quantities, particularly

FIGURE 2Continued.


as urinary cotinine reflects short-termexposure. This is supported by themixed correlations reported in studiesof parentally reported and biochemi-cally measured child TSE: Hovell et al105

found correlations of between 0.22 and0.75, and a more recent study106 foundcorrelations ranging from 0.02 to 0.80.Any of these reasons, or a combination,may have contributed to the different

findings in biochemically measuredversus parentally reported child TSE.

Implications

� Benefits of interventions to help par-ents protect children from TSE arereal, but small on an individual level.

� At a population level, such benefitscould have significant public healthimpact.

� Benefit was observed both formore-intensive and less-intensiveinterventions.

� Trends toward improvements duringthe trial period were observed inmost control groups, for both bio-chemical and parentally reportedend points, indicating either an ef-fect of trial participation or of mon-itoring.

TABLE 4 Parental Report of Number of Cigarettes to Which Child was Exposed, by Intervention Group and Time

Study Variable Intervention Group Control Group Pooled

Baseline Follow-up Baseline Follow-up Follow-up

Mean SD n Mean SD n Mean SD n Mean SD n SD

Butz 2011a,20 Ncigs smoked in home 11.25 10.18 36 5.61 8.02 31 16.9 12.86 39 9.08 10.15 36 9.23Conway 2004a,21 Ncigs per mo (log transformed) 1.75 0.52 72 1.06 0.7 60 1.85 0.51 71 1.27 0.77 67 0.74Fossum 2004a,34 Ncigs/maternal and other indoor exposure NA 18.5 25.3 26 NA 13.9 17.4 15 22.78Hovell 2000a,24 Ncigs per wk/total maternal

exposure (log transformed)3.96 0.84 47 2.26 1.78 41 3.95 0.99 53 3.01 1.61 51 1.68

Hovell 2009a,25 Ncigs per wk/ total maternal exposureinside and outside (log transformed)

3.54 1.06 71 1.75 1.96 61 3.72 1.03 64 3.18 1.54 61 1.76

Lanphear 2010a,27 Ncigs in home 12.9 1.85 110 9.4 2.41 104 13.3 2.2 115 9.8 2.41 103 2.41Tyc 2013b,96 Ncigs per wk child exposed to

(log-transformed geometric means)2.56 1.82 69c 1.39 1.97 62 2.25 2.06 66c 1.5 2.28 63 2.13

Zakarian 2004a,33 Ncigs per wk/ total exposure insideand outside) (log transformed)

4.5 0.55 76 3.14 1.59 59 4.53 0.61 74 2.96 1.57 68 1.58

NA, not available; Ncigs, number of cigarettes.a Based on published data and/or data provided by author.b Data were log-transformed to calculate SDs on the basis of reported asymmetric CIs, which occurred because of use of geometric means. Original data: Intervention baseline: mean: 13, CI 8.4to 19.8; Intervention follow-up: mean: 4, CI 2.4 to 6.4; Control baseline: mean: 9.5, CI 5.7 to 15.4; Control follow-up: mean: 4.5, CI 2.5 to 7.7.c Numbers of participants measured at baseline were not reported. We estimated this value with numbers of participants randomized.

TABLE 5 Biomarkers of Child Exposure to Tobacco Smoke, by Intervention Group and Time

Study Variable Intervention Group Control Group Pooled

Baseline Follow-up Baseline Follow-up Follow-up

Mean SD n Mean SD n Mean SD n Mean SD n SD

Butz 2011a,20 Urine cotinine ng/mL 22.1 20.2 41 22 28.9 38 26 30.4 44 24.3 27.4 42 28.12Conway 2004a,21 Hair nicotine ng/mg (log values) 0.25 0.21 70 0.23 0.18 60 0.23 0.22 69 0.23 0.24 65 1.60Halterman 2011a,22 Salivary cotinine ng/mL 1.25 1.61 264 1.05 1.49 252 1.57 2.83 265 1.16 1.94 255 1.73Hovell 2000a,24 Urine cotinine ng/mL (log values) 2.48 0.76 47 2.44 1.06 40 2.34 0.99 51 2.92 1.19 50 1.13Hovell 2002a,23 Urine cotinine ng/mL (log values) 0.89 0.64 96 0.68 0.67 92 0.78 0.65 96 0.62 0.50 91 0.59Hovell 2009a,25 Urine cotinine ng/mL (log values) 2.38 0.88 75 2.12 1.24 63 2.76 0.78 74 2.43 0.98 61 1.12Irvine 1999a,26 Salivary cotinine ng/mL (log values) 1.04 0.92 213 0.80 1.03 213 1.07 1.09 222 0.84 1.12 222 1.08Lanphear 2010a,27 Serum cotinine ng/mL 1.18 3.9 108 1.19 5.73 105 1.23 3.26 114 1.00 3.71 110 4.80Tyc 2013b,96 Urine cotinine ng/mL (log-transformed

geometric mean)1.36 1.28 69c 1.39 1.31 61c 1.31 1.72 66 1.36 1.71 64 1.53

Wakefield 200293 Urine cotinine CCR nmol/nmol(geometric mean)

22.8 2.8 99 21 3 99 25.7 3.9 110 21 3.3 110 3.16

Wilson 2001a,32 CCR - urinary CCR ng/mL 1.82 1.05 25 1.27 1.31 25 2.34 1.11 26 1.93 1.24 26 1.27Wilson 2011a,31 CCR - urinary CCR 2.68 1.07 178 0.98 1.83 169 2.53 1.07 174 1.11 1.84 172 1.84Zakarian 2004a,33 Urine cotinine ng/mL 2.52 0.93 74 2.30 1.09 52 2.28 0.99 72 2.09 1.04 64 1.07

NA, not available; Ncigs, number of cigarettes.a Based on published data and/or data provided by author.b Data were log-transformed to calculate SDs on the basis of reported asymmetric CIs, which occurred because of use of geometric means. Original data: Intervention baseline: mean: 3.9, CI 2.9to 5.3; Intervention follow-up: mean: 4, CI 2.9 to 5.6; Control baseline: mean: 3.7, CI 2.4 to 5.5; Control follow-up: mean: 3.9, CI 2.6 to 6.0.c Numbers of participants measured at baseline were not reported. We estimated this value with numbers of participants randomized.

REVIEW ARTICLE


� Monitoring of TSE, either by parentalreport or biochemical means, holdspromise as a simple but powerfulmeasure to reduce exposure. Feed-back of an individual child’s levelsmay be essential particularly incomparison with children of non-smoking families. Such monitoringcould, in principle, be conducted atregular health visits. This needs fur-ther investigation.

� At best, the interventions showedonly small benefits at the individuallevel. It is essential to identify power-ful intervention strategies that areacceptable to the families with youngchildren where smoking occurs, andcould be implemented with highfidelity to protocol. It is possible thatimmediate, sensitive feedback frombiomarkers for child TSE, or imme-diate feedback on home or car airnicotine, or THS, could be helpful.This requires advances in immedi-ate biomarker measurement, withpricing that would enable wide-spread implementation.

Strengths and Limitations

To the best of our knowledge, this is thefirst review to quantify and rigorouslytest theeffectsof interventionsaimedatprotecting young children from TSE.Strengths of this review include thetargeted search, the strong methodol-ogy of included studies, testing of in-tervention effects, effect size estimates,and subgroup analyses.

Our research has several limitations.First, we were unable to incorporatebaseline values of biomarkers intothe meta-analyses of biomarkers andnumber of cigarettes smoked aroundthe child because of missing informa-tion about individual-level changes. Wewere able to incorporate baseline in-formation into the analysis of PREP, butonly for a minority of the studies. Al-though all but 1 of the included trialswere randomized, and randomization

FIGURE 3Plots to assess presence of publication bias. A, PREP at study end. B, Change in PREP during study. C,Parentally reported number of cigarettes to which child was exposed, at study end. D, Biochemicallyassessed child exposure, at study end.


tends to produce groups that are equalin measured and unmeasured charac-teristics, this may not hold true for anyspecific trial, and is less likely to hold insmall studies.103

The subgroup analyses of PREP did notprovide information on advantages ofspecific intervention components, per-haps because of the homogeneity of

included studies, and small observedeffect sizes.

CONCLUSIONS

Interventions aimed at parents toreduce TSE in children provide smallbenefits when assessed by parentalreports, although significant dif-ferences between intervention and

control groups at study follow-uptimes were not found for bio-markers. Trends toward improve-ments during the study period wereseen in most of both control and in-tervention groups. Because of thewidespread scale of TSE among youngchildren and the difficulties inherent inconvincing all family members to quitsmoking, substantial gains are possi-ble by reducing exposure. Originalresearch is needed to develop moreeffective programs for reducing childTSE, to accurately measure child ex-posure, and to understand how toefficiently disseminate effective inter-ventions.

ACKNOWLEDGMENTSWe thankMs. RuthSuhami for herassis-tance with the systematic review of theliterature. We also thank the individualswho provided unpublished data and/orprovided additional information onpublishedstudies foruse in this system-atic review.

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TABLE 6 Effects of Intervention Programs on PREP, by Subgroup

RR (CI) P Value No. Studies No. Participants

Biochemical feedbackYes 1.14 (1.03–1.28) .02 4 735No 1.12 (1.06–1.18) ,.0001 13 6085

IntensityUp to 1 personal contact 1.18 (1.02–1.35) .02 5 1652More than 1 personal contact 1.12 (1.07–1.18) ,.0001 12 5168

Face-to-face counselingYes 1.11 (1.06–1.16) ,.0001 14 5654No 1.27 (1.10–1.47) .001 3 1166

Control group interventionYes, specific to project 1.14 (1.03–1.26) .01 6 4307Very brief (part of usual care)

or asthma-related1.09 (1.03–1.15) .002 6 1200

Monitoring alone/unrelated intervention 1.14 (1.02–1.28) .02 5 1333Fidelity to protocolNot reported 1.16 (1.08–1.26) ,.0001 9 4732Moderate (50%–79%) 1.07 (1.02–1.12) .003 4 932High (.80%) 1.16 (1.02–1.31) .02 4 1156

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(Continued from first page)

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2014 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

FUNDING: Supported by the Flight Attendants’ Medical Research Institute Award 072086_YCSA.

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.


DOI: 10.1542/peds.2013-0958 originally published online March 24, 2014; 2014;133;698Pediatrics

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