Journal of Epidemiology and Community Health 1990; 44: 224-230

Acute respiratory illness in Adelaide children:breast feeding modifies the effect of passivesmoking

Alistair Woodward, Robert M Douglas, Neil M H Graham, Helen Miles

Department ofCommunity Medicine,University ofAdelaide, Box 498GPO, Adelaide, SouthAustralia 5001,AustraliaA WoodwardR M DouglasN H M GrahamH Miles

Correspondence to:Dr WoodwardDr Douglas's currentaddress: National Centre forEpidemiology andPopulation Health,Australian NationalUniversity, Canberra,AustraliaDr Graham's currentaddress: Departnent ofEpidemiology, JohnsHopkins University,Baltimore, Maryland, USA

Accepted for publicationDecember 1989

AbstractStudy objective-The aim was to

investigate the relation between passivesmoking and childhood acute respiratoryillness.Design-The study involved an initial

postal survey on a random sample ofchildren followed by a case-control studybased on the survey. A respiratory illnessscore was calculated from maternal reportsof episodes of illness in the previous 12months.Setting-The study was a population

survey based on Adelaide metropolitan areain South Australia.Participants-The reference population

(n= 13 996) was all live born childrenregistered in South Australia in 1983 whoseparents lived in Adelaide metropolitanarea. Of these, 4985 families were contactedby post and from 2125 respondents, 1218(58%) gave consent for home interview."Cases" were children with respiratoryillness scores in the top 20%, controlling forage and time of year (n = 258); "controls"were taken in the bottom 20% (n = 231).Measurements and main results-

Maternal smoking in the first year of lifewas associated with a doubling in relativeodds of respiratory proneness in the child(odds ratio=2-06, 95% CI 1'25-3'39) afteradjustment for confounding by parentalhistory ofrespiratory illness, other smokersin the home, use of group child care,parent's occupation, and levels of maternalstress and social support. There was noevidence that this association wasattributable to differences in the waysmoking and non-smoking parentsperceived or managed childhood acuterespiratory illness. Maternal smoking in thefirst year, without smoking in pregnancy,was also associated with increased risk ofrespiratory proneness (odds ratio 1'75, 95%CI 1-03-3'0), showing an effect of passivesmoking independent of any in utero effect.There was a strong negative effectmodification by breast feeding: relativeodds of respiratory proneness withmaternal smoking were seven times higheramong children who were never breast fedthan among those who were breast fed.Conclusions-The results suggest a

relatively small but real effect of passivesmoking on childhood acute respiratoryillness. Effect modification by breastfeeding may be due to a combination ofbehavioural and biological mechanisms.

Acute respiratory illness is the most commoncause of morbidity in childhood, world wide, andis a major cause of mortality in many countries.'While most acute respiratory episodes are selflimiting, the total cost to parents, children andhealth services is immense. There may also beimportant long term sequelae, such as the effectsof glue ear on speech development and learning,2and increased susceptibility to illness anddiminished respiratory function following lowerrespiratory illness in infancy.3

Investigations of the social and environmentalcauses of acute respiratory illness have tended tofocus on the most severe manifestations of illness,typically episodes of lower respiratory illnessleading to admission to hospital. However,patients admitted to hospital form a tiny fractionof all children suffering from acute respiratoryillness.4The burden of childhood acute respiratory

illness in the community is not spread evenly.Some children are affected rarely, while others arerepeatedly ill.5 The group at the top end of thefrequency distribution tends to be stable overtime: not only do children with early lowerrespiratory illness predominate amongst thosewho suffer from chest illness in later years, butthere is also evidence of "tracking" of rates of lesssevere respiratory illness.6

Passive smoking is a major risk factor forchildhood acute respiratory illness. A simple tallyofpublished reports (disregarding variation in thequality of the studies) shows that out of 32 studiespublished up to June 1988, 22 found that lowerrespiratory illness was significantly (p < 0 05)more common amongst children whose parentssmoked.7Ofthe 10 studies which reported no statistically

significant association of parental smoking andchildhood acute respiratory illness, only three"'0included children in the 0-2 years age group. Thefirst two studies cited gave no details of thenumber of participants in this age range; theother'0 had low statistical power.The most plausible non-causal explanations for

the association of passive smoking and childhoodacute respiratory illness include reporting bias(studies have relied largely on parents' reports ofexposure and outcome), differential use of healthservices, confounding by some aspect ofpsychosocial stress, and confounding by fetalexposure to smoke products.The aim of this study was to investigate the

relation between passive smoking and childhoodacute respiratory infection in children inmetropolitan Adelaide, after controlling for theseand a wide range of other possible confoundingfactors.

225Breast feeding, passive smoking, and acute respiratory illness in children

MethodsThe study took place in two stages: a postal surveyconducted in 1985 of a random sample of childrenwhose births were registered in South Australia in1983; followed by a case-control study based onthe survey.The reference population (n = 13 996) was all

live bom children whose births were registered inSouth Australia in 1983, and whose parents' placeof residence as shown on the birth registrationform was within the Adelaide metropolitan area(total population 900 000). The EpidemiologyBranch of the South Australian HealthCommission took a 1-in-2 random sample of thesebirth registrations. Addresses were deleted if theywere inadequate for postal purposes, or if theywere within the metropolitan area but relativelyinaccessible for interview (being more than 30minutes drive from the University of Adelaide).Of the remaining 5830 addresses, a randomlyselected sample of 5000 was chosen for posting.After further exclusions due to incompleteaddresses, a total of 4985 questionnaires wereposted.

Initially, names of mothers were included onquestionnaires sent out. Following an incidentwhich raised concern over possible breaches inconfidentiality it was decided not to use thisinformation with the remainder of the postings.Eighty per cent of the questionnaires were postedto addresses only.

THE SURVEY QUESTIONNAIREThe postal questionnaire was based on one whichhad been used successfully in a previous study inAdelaide," and was pretested in two pilot studiesinvolving 250 children drawn from the lists ofbirth registrations in 1980 and 1984. It consistedof 24 questions in the form of a half A5 sizebooklet.'2 The accompanying letter wasaddressed to the mother by name in the firstposting only; otherwise it was headed "To theHouseholder". The letter included a briefdescription of the study and an invitation to fillout the questionnaire if the household included a

The listaimed to provide as comprehensive a listas possible of the manifestations of acuterespiratory illness, in terms which had been foundpreviously11 to be understood by most parents.

Questionnaires were sent out between July1985 and December 1985 in five postings of about1000 questionnaires each, at intervals ofapproximately one month. Each posting includedaddresses of children bom in a common 2-3month period. Reminder postcards were sent toall addresses one week after the first posting, and afurther letter and copy of the questionnaire weresent to all addresses from which a response hadnot been received by three weeks after the initialposting. Ofthe 4985 questionnaires sent out, 2854(57-3%) were returned completed. Two hundredand thirty six questionnaires were excludedbecause the children described were born beforeNovember1st 1982 or after December 31 1983,and so were unlikely to have had their birthsregistered in 1983. (In South Australia there is alegal penalty if births are not registered within 60days.) The survey participants numbered 2618children, with a mean age of 26 months (range 18months to 3 years) at the time the questionnaireswere completed.A respiratory illness score was calculated for

each participant, based on the responses to thefirst question in the questionnaire (tableI). Foreach illness listed, a value of 0 was assigned foranswers in the first column (indicating the childhad "NEVER" suffered this illness in the last 12months). A value of 1 was assigned for answers of"RARELY", 2 for "SOMETIMES", 3 for"FREQUENTLY", and 4 for answers in the extremeright hand column ("CONSTANTLY"). Values forthe 13 illnesses were then summed. Extra pointswere added if the child suffered at all frompneumonia or asthma (+2 if either conditionrecorded, + 4 if both conditions recorded). Therespiratory score could range from 0 (no illnessesreported) to a theoretical maximum of 56(representing a child who was reported to beconstantly ill with all the listed conditions).

child between the ages of 1 and 3 years. THE CASE-CONTROL STIDYParents were asked to provide information on The final posting was excluded from interview

the amount of acute respiratory illness suffered by because it clashed with the Christmas period andtheir child in the previous 12 months, by filling summer holidays. Of the 2125 completedout the question shown in table I. The illnesses questionnaires received from the first fourlisted include a mixture of medical diagnoses and postings, 1218 (57.30o) gave consent for homesigns and symptoms of acute respiratory illness. interviews. "Cases" were children whose

respiratory score fell within the top 2000 of scoresin the same posting, and "controls" were those

Table I Respiratory illness question, postal survey children whose respiratory scores were within the

Q.1. In the last 12 months, how much did your child suffer from the illnesses listed below? bottom 20%o of scores in their posting. Home(Please circle your answer). interviews were carried out with parents of 258

0 bouts 1-2 bouts 3-8 bouts More than Most of cases and 231 controls by three research nurses.8 bouts the time The interview schedule was pretested with 80

Cough NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY parents of children from the and birth

Hayfever NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY registration lists.Wheeze or NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY To investigate the management of childrenasthma

Bronchitis NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY with acute respiratory illness, seven hypotheticalBronchiolitis NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY case histories were described, and in each case

Croup NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY mothers were asked to respond to statements

Sore throat NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY about the best course of action, with eitherThick nasal NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY "strongly agree", "agree", "disagree", "strongly

dischargeEarache NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY disagree" or "don't know". In addition toDischarging NEVER RARELY SOMETIMES FREQUENTLY CONSTANTLY examining the statements singly, responses were

ear pooled to give an "illness management score",

Alistair Woodward, Robert M Douglas, Neil M H Graham, Helen Miles

which quantified respondents' ability to discern psychological distress, also from the precedingminor from possibly serious acute respiratory one month, were collected via the 12 item versionillness. This score was devised by selecting for of the General Health Questionnaire.'5 Womeneach case history the statement which the who scored above the medians for all three stressinvestigators judged a priori to provide the measures were defined as the "high" stress group,clearest test of "appropriate" use of medical while those scoring below themedians for all threeservices. "Don't know" responses were measures were defined as the "low" stress group.discarded, other responses were given numerical The remainder were defined as experiencingvalues of 1-4, and the total summed to give a score moderate stress. The median scores were Lifewhich ranged from 7 ("non-discriminating" use Events Inventory 23 (range 0-216), Dailyof medical services) to 28 ("discriminating" use), Hassles Scale 9 (range 0-64), and General Healthwith a median value of 16. Deletion of "don't Questionnaire 1 (range 0-12). Questionnaire dataknow" responses was effectively the same as were collected also on maternal social supports,assigning a score of 0 for that statement (no-one using a modified form of the Maternal Socialreplied "don't know" to all statements). Support Index.'6 Seven aspects of social supportAt the end ofthe interview, mothers were asked were scored, then summed to give a global index

to complete a self administered questionnaire (range 0-19, median 13). "Poor" support waswhich included three components of perceived defined as scoring below the median, "good"stress-major life events, minor life events ("daily support as a score above the median.hassles"), and psychological distress. Major lifeevents in the previous 12 months were assessed DATA ANALYSISusing the Life Events Inventory,'3 with the Statistical analysis was by conventional bivariateexclusion of 10 items not relevant to mothers of techniques included on SPSS-X, and the logisticyoung children. Minor, irritating, day to day regression package in SYSTAT. Confidencestressful events over the last month were assessed limits on odds ratios were calculated using the testusing the Daily Hassles Scale.'4 Data on maternal based method described by Breslow and Day.'7

Table II Maternal smoking and other factors associated with respiratt

CrudeRisk factor Prone Not prone OR

Maternal smoking after birthYesNo

Sex of childMaleFemale

Other children in familyYesNo

Father's history ofrespiratory illness

YesNo

Mother's history ofrespiratory illness

YesNo

Use of group child careYesNo

Occupation(Congalton grade)

PensionersLow (6,7)Medium (4,5)High (1,3)

Mother's educationLowHigh

StressHighMediumLow

Social supportLowHigh

Breast feedingYesNo

Other smokers at homeYesNo

Use of health servicesNon-discriminatingDiscriminating

102156

49 2 43182 1-0

157 107 1-80101 124 1-0

21642

172 1-7659 1-0

93 48 231150 179 1-0

131123

116142

53 3-54176 10

61 2-26169 1-0

16 9 2-8064 34 2-97144 136 1-6733 52 1-0

85173

46 1 98185 1-0

88 33 3-96126 116 1 9142 72 1-0

121131

97 1 19125 1-0

209 208 04749 23 1.0

104 81 1-25154 150 1-0

145 90 2-01113 141 1-0

OR = odds ratio; CI = confidence interval

Confounding and effect modification wereexplored using the approach recommended by

ory proneness Rothman"8: firstly, calculation of stratified riskestimates and comparison of crude and adjusted

95°' CI] odds ratios (calculated by the Mantel-Haenszel[S% CI]t method)'9 and secondly, multivariate analysis by[1 63-3-61] logistic regression. Adjusted risk estimates were

calculated from coefficients in the logistic model,in the conventional fashion.

[126-2 58]

Results[114--2741 The proportion of questionnaires returned and

eligible for this study was 2618/4989 (52 50o). Onthe basis ofthe first posting, which was addressed

[1-54-3-47] to named individuals, we estimate thatapproximately 29% of families never received thequestionnaire, as they had moved since the birth

[2.41-5 20] of their child.The distribution of the respiratory scores

calculated from survey questionnaires is shown in[1-55-3 31] the figure. The reliability of the score was tested

by asking again at interview about children'srespiratory illnesses in the previous 12 months,

(113-6397] and calculating a second respiratory score in the[1063-5239][1-02-2-73]

[1-31-2-98]300-

[2-31-6-78][1-21-3-02]

[0-83-1-71] v

LL

[0-28-080]

[0-87-1-81]

200-

100'

n.-

U :U

a muU

U%U

0 0 -2 3

0 10 20 30 40 50

[1 40-2 88] Respiratory illness score

Frequency distribution of respiratory illness score

M.. so I

226

u

Breast feeding, passive smoking, and acute respiratory illness in children

same manner as the score calculated from themailed questionnaires. There was virtually nooverlap of study groups on retest: fewer than 1%(4/489) of children in the "not prone" group hadscores on retesting which were in the "prone"range, or vice versa.The proportions of women who reported

smoking during pregnancy and in the first 12months after birth were 23-6% and 27-7%.Women included in the interview study wereasked the same questions a second time, atinterview. Only 11/487 (2-3%) of mothers gaveinconsistent information concerning smoking inthe first 12 months after birth, as did 9/487 (1 8%)concerning smoking in pregnancy.Table II shows the relation of maternal

smoking to respiratory proneness. In this table"breast fed" includes all children ever breast fed.A history of respiratory illness for the mother orfather was recorded if the parent reported thatthey had ever been treated by a doctor for asthma,bronchitis or emphysema. Group child care wasdefined as current use of a child care centre orcreche, excluding family day care, occasionalhome care or play groups. Occupation was thereported usual occupation of the chief incomeeamer in the household, coded using theCongalton seven point scale.20 (Those retired or

Table III Passive smoking and respiratory proneness, by breast feeding

Prone Not prone Odds ratio [950o CI]

BREAST FEDMaternal smoking after birthYes 71 46 1-81 [1-18-279]No 138 162

NOT BREAST FEDMaternal smoking after birthYes 31 3 11-5 [3-4-38 5]No 18 20Homogeneity x2 = 7-27 (DF = 1), p < 0-01

Table IV Risk factors for respiratory proneness. Results of logistic regression

Variable Coefficient Adjusted [9500 CI](+ SE) odds ratio

Maternal smoking in first year 0-721 (+0 255) 2 06 [1-25-3 39]

Sex (male) 0-656 (+0-215) 1-93 [1 27-2-93]

No siblings 0 218 (+0 112) 1.24* [1-00-1 55]

Father's history of respiratoryillness 0 519 (+0 239) 1-68 [1-05-2 69]

Mother's history of respiratoryillness 0-787 (+0 229) 2 20 [1 40-3-44]

Child care (use of) 0-798 (+0 227) 2-22 [1-42-3 47]

OccupationHigh (Congalton 1-3) 1-0Medium (Cong. 4,5) 0-446 (+0 290) 1-56 [0-88-2-75]Low (Cong. 6,7) 0 707 (+0364) 2-03 [0-99-414]Pensioner 0-394 (+0 594) 1 48 [046-4.75]StressLow 1-0Moderate 0 711 (+0.276) 2 03 [1-19-3-49]High 0-962 (+0 328) 2 61 [1-37-4-98]Socal support (low) 0169 (+ 0 229) 085 [053-132]

Breast fed (never) 0 493 (+0-316) 1-64 [0-88-3 04]

Other smokers at home (> 1) 0 302 (+0 239) 0-73 [0-46-1-18]Illness management score 0 107 (+ 0028) 0 90t [0-85-0-95]*Refers to multiplicative change in odds for unit increase in number of sibst Refers to multiplicative change in odds for A + 1 in illness management score

presently unemployed were asked to report theirprevious occupation, and were coded by thisoccupation.) The level of mother's education wasdescribed as "low" if the mother reported fewerthan four years post-primary schooling, and"high" with four or more years. Mothers weredescribed as "discriminating" in use of healthservices for childhood acute respiratory illness ifthey scored above the median for the illnessmanagement score, and "non-discriminating" ifthey scored below the median for this score.There was no evidence in the stratified analyses

of effect modification, with the exception ofbreastfeeding (table III). To determine whether theapparent protective effect of breast feeding in thepresence of maternal smoking was related toduration of breast feeding, children in the "everbreast fed" category were divided into thosebreast fed for < 6 months, and those breast fed for> 6 months. Amongst children breast fed for < 6months (n= 194), the relative odds of pronenessdue to maternal smoking were 3-0 (950o CI1 65-4). Amongst children breast fed for >6months (n= 223), the relative odds of pronenessassociated with maternal smoking were 0-8 (950oCI 04-1 7).

Independent variables included in a multiplelogistic regression model were the major predictorvariables from the bivariate analyses, and stress,social support, breast feeding, other smokers athome and the illness management score. With theexception of the illness management score andnumber of siblings, all variables were treated inthe analysis as categorical variables. Nointeraction terms were included in the first model(results shown in table IV).To test whether effect modification by breast

feeding was due to unequal distribution ofconfounding variables between breast feedingcategories, the logistic regression model was runseparately for breast fed and never breast fedinfants. All potential confounders shown in tableIV were included. In the never breast fed group,the adjusted odds ratio for maternal smoking inthe first year was 28-7 (95%o CI 3.67-224 5). Inthe breast fed group, the adjusted odds ratio was1-51 (95% CI 0-87-260).The logistic regression analysis was repeated,

including a first order interaction term: maternalsmoking*breast feeding. As expected, this newmodel provided a better fit to the data (X2 ondifference in log likelihood estimates= 18-4,DF=1, p«0-01). The odds ratio for maternalsmoking versus no smoking was again found to bestrongly influenced by breast feeding status(never breast fed, odds ratio= 13 15 (950o CI2-05-78-35]; breast fed, odds ratio 1-51 [95O0 CI0 88-2 58]). Conversely, the odds ratio ofrespiratory proneness for never breast fedcompared with breast fed was 7-02 where themother smoked, and 0 81 were the mother did notsmoke (this last odds ratio did not differsignificantly from 1).

DiscussionIn this study information on both children'srespiratory illnesses and parental smoking wasobtained by questionnaire. It is difficult to testformally the validity of the responses to the

227

Alistair Woodward, Robert M Douglas, Neil M H Graham, Helen Miles

respiratory illness questionnaire, as parents'reporting provides practically the only means ofleaming about episodes of acute respiratoryillness which are never referred to health services.The information obtained in this study may beimprecise at the level of individuals, as motherswere required to interpret illnesses and symptomsin their own way, and to recall events over a 12month period. However, the focus of the studywas differences between groups, rather thanindividuals, and the groups were chosen torepresent the extremes of the range of respiratoryillness. The distance between the groups in termsof reported symptoms and health service use wasconsiderable. (For example, 21-8% of the pronegroup had been admitted to hospital with lowerrespiratory illness in the first 18 months of life,compared with only 1 3% ofthe not prone group.)The interview results showed that thequestionnaire was highly reliable as a means ofdistinguishing the study groups.There are two sources of uncertainty affecting

the estimates of childhood passive smoking usedin this study. These are factors other than parentalsmoking which influence a child's exposure toenvironmental tobacco smoke, and theinaccuracies of self reported parental smoking.The first set of factors was not investigated here.A comparison of self reported maternal smokingwith cotinine levels in stored serum taken inmidpregnancy (unpublished data) indicated thatunderreporting ofsmoking during pregnancy wasnot common-amongst those tested only 9% ofself reported non-smokers had serum cotininelevels indicating likely active smoking (that is, >57 nmol/litre).2' The self reported smoking datawere reliable-when questions about presence orabsence of smoking were asked a second time atthe interview, 98% of mothers gave consistentresponses.

It has been suggested22 that parents'respiratory illnesses may act as intermediatefactors (since parents who smoke suffer morerespiratory tract infections, which may be passedon to children). However there was no sign of thisin our study. In stratified analyses the strength ofthe association between maternal smoking andrespiratory proneness did not vary substantiallyor consistently with mother's or father's history ofrespiratory illness. Consequently, in themultivariate analysis mother's and father's historyof respiratory illness were included as potentialconfounders.With the measures used in this study, there was

no evidence that the association of maternalsmoking and childhood acute respiratory illnesscan be attributed to differences in the way parentsuse health services to care for children withrespiratory illnesses. It must be noted that thereare shortcomings in the measures used. First,without prospective information it is not possibleto determine whether mothers' knowledge andattitudes concerning acute respiratory illness area result or a cause of children's respiratoryproneness. Second, it is not always certain whatconstitutes "appropriate" use of health services.Doctors themselves often disagree on clinicalcriteria and assessment of particular cases (thiswas clearly evident when a sample of generalpractitioners were tested on the cases used in this

study [unpublished data]). Moreover, the"appropriate" course of action in dealing with anill child depends not only on the clinical setting,but also on family circumstances (such asavailability of alternative sources of advice andsupport).The measures of psychosocial stress used in the

study were strongly associated with respiratoryproneness, but did not confound the association ofmaternal smoking and proneness. The relation ofstress and social supports to childhood acuterespiratory illness in this study will be examinedin detail in another paper.There was no means of directly obtaining

information on households which did not respondto the study questionnaire. Aggregated dataobtained from the South Australian HealthCommission for all births in 1983 with parentsresident in the study area showed that childrenwith working class parents were slightlyunderrepresented in the survey but the maternalage and birthweight profiles were similar. Whiledifferential response to the questionnaire maybias survey descriptors such as social class, it isunlikely in our opinion to bias the associationobserved between passive smoking and childhoodacute respiratory illness.

Reporting bias would influence the results ofthe study if mothers who smoked systematicallyoverreported respiratory illnesses amongst theirchildren, when compared with non-smokers.There are no obvious reasons why this should beso. Within proneness categories, mothers whosmoked had lower illness management scores thannon-smokers. This is consistent with theproposition that smokers tend on balance to"overdiagnose" and "overuse" medical servicesfor children with acute respiratory illness. Theobservation that the rates of admission to hospitalfor conditions other than acute respiratory illnesswere higher among smokers (unadjusted oddsratio=1-27, 950% CI 110-1-62) might alsoindicate a greater propensity for smokers to reportchildren's illnesses in general. However, if such abias did exist, it would be expected to have a muchgreater effect on reported symptoms and illnessesthan on reported hospital admissions, yet theassociations ofmaternal smoking with respiratoryproneness and with admission to hospital withlower respiratory illness in the first 18 months oflife were similar.The strength of the association was moderate

only (representing an approximate twofoldincrease in risk), but consistent with the findingsof other studies which used symptom basedoutcomes.23 24 The association was not specificfor any particular respiratory complaint. In thepostal survey data set, children whose motherssmoked in the first year after birth suffered moreupper respiratory illness, more lower respiratoryillness, and more ear illness. The only respiratorycomplaints which were not significantlyassociated (at p = 005) with maternal smokingwere hayfever (odds ratio=0-80, 950o- CI 0-62-1-03), pneumonia (odds ratio= 1 23, 95%, CI0 67-2 28), and croup (odds ratio= 0-92, 950, CI0-74-1-13). The lack of an association of maternalsmoking with particular respiratory complaintsdoes not weigh heavily against a causalexplanation. It seems quite plausible, in view of

228

Breast feeding, passive smoking, and acute respiratory illness in children

what is known about the toxicology andtransmission of tobacco smoke, that passivesmoking could play a part in initiating oraggravating conditions throughout therespiratory tract.Of the 2607 respondents to the postal survey

who gave full information on smoking, 580(22 20) reported they had smoked during bothpregnancy and the first year after birth, 143(5.4%) reported smoking in the first year but notin pregnancy, and 36 (1 4%) reported smoking inpregnancy but not in the first year after birth. Inthis data set, the odds ratio for proneness withmaternal smoking was substantially reducedwhen adjusted for smoking in pregnancy(adjusted odds ratio= 1 25, 950o CI 0.95-1-64).However, this analysis may represent"overcontrolling", as maternal smoking inpregnancy is very strongly correlated withmaternal smoking in the postnatal period. If theeffect of postnatal smoking on respiratoryproneness was entirely attributable to smoking inpregnancy (as suggested by Taylor andWadsworth25), one would expect no increase inrisk of proneness amongst children of motherswho did not smoke in pregnancy, but did smokepostnatally. In fact there was an increase 1-n risk inthis group, when compared with children whosemothers had never smoked (odds ratio =1 75,950o CI 1-03-3-00).On the basis ofthese findings, the association of

respiratory proneness and maternal smoking inthe first 12 months after birth cannot be entirelyattributed to the effects of maternal smoking inpregnancy. Smoking in pregnancy may have anindependent effect on susceptibility to acuterespiratory illness in childhood. Such an effect isplausible considering the toxic effects of nicotineand tobacco smoke observed in animal studies,26but it will remain difficult to quantify preciselysuch an effect in humans while mothers' smokingin pregnancy is strongly correlated with smokinghabit after the birth.

In this study population children who werebreast fed suffered less respiratory illness thanthose children who were only ever bottle fed, butthe difference was reduced, and no longerstatistically significant (p > 005), when theanalysis was adjusted for confounding factors.Breast feeding modified the effect of maternalsmoking, to decrease the risk of acute respiratoryillness. When children who had never been breastfed were compared with children who had beenbreast fed, the relative odds of pronenessassociated with maternal smoking (adjusted forconfounders) were reduced from 13-2 to 1-5. Thenumber of children in the never breast fed groupwas small, leading to wide confidence intervalsaround the relative odds estimates. However,evidence of effect modification was still presentwhen larger numbers were included in analysis,and children were grouped by duration of breastfeeding. The risk of respiratory pronenessassociated with maternal smoking diminishedwith increasing duration of breast feeding.Amongst children breast fed for more than 6months, there was no increase in risk ofrespiratory proneness associated with maternalsmoking.One possible explanation for this effect

modification is that breast feeding is associatedwith reduced exposure of the infant to smoke,when compared with infants who are bottle fed.This could result from a reduction in the totalamount smoked by the mother, or in the amountsmoked around the infant. There is evidence thatwomen who smoke are less likely to breast feed,27and if they do begin, tend to cease breast feedingearlier than women who do not smoke.28 Nicotinehas been shown in laboratory studies to inhibitprolactin release.29 Therefore, amongst motherswho smoke, those who are breast feeding maytend to smoke less than those who are not breastfeeding. Such a difference was present in thisstudy population, but when the population ofmothers who smoked was stratified by amountsmoked, respiratory proneness remained lesscommon amongst breast fed than bottle fedinfants. This indicates a modifying effect of breastfeeding on risk of proneness due to maternalsmoking, independent of an association of breastfeeding with lower smoking rates.Do mothers who breast feed smoke less around

their child? We obtained no information in thisstudy on the smoking "hygiene" of parents. Inanother study30 we noted a tendency of breastfeeding mothers to smoke less around theirchildren than did mothers who were bottlefeeding. However, the numbers in the subgroupswere small, so were the differences between thetwo groups, and adjustment for socioeconomicstatus reduced the differences further.What biological mechanisms might explain the

modified effect of passive smoking due to breastfeeding? The anti-infective constituents of breastmilk are well known. While these constituentscould not directly counteract the effects oftobacco smoke on the respiratory tract, it may bethat breast feeding tends to tip the balance infavour of the host, by strengthening specific andnon-specific immune defences.3' This protectiveeffect may not be evident when the risk of acuterespiratory illness is low, but becomes apparentwhen the risk of illness increases, due to adverseenvironmental influences such as crowding, poorhygiene, or tobacco smoke. Similar effectmodification has been reported with otherinfectious diseases: for example, a study32 of childmortality in Malaysia found protection againstdiarrhoeal diseases by breast feeding wasstrongest where piped water and/or toiletsanitation were not available.The anti-infective constituents of breast milk

boost passive immunity only, and do not directlyprovide protection much beyond the time thatbreast feeding ceases. However, it may be that themost important effect of breast feeding is topostpone the age at which infection and illnessfirst occur. There is an association between lowerrespiratory illness in the first year of life and longlasting increased risk of severe respiratoryillness.33 If respiratory proneness is indeeddetermined by the age of 6 or 12 months, then thebalance of adverse and favourable factors duringthat critical early period will have effectsthroughout childhood, and maybe beyond.We have found one other published paper34

which reports on the modified effect of passivesmoking, in relation to childhood acuterespiratory illness, with breast feeding. In this

229

Alistair Woodward, Robert M Douglas, Neil M H Graham, Helen Miles

cross section study of 18 month old children inShanghai, the relative risk of hospital admissionfor respiratory illness in heavy smokinghouseholds (20+ cigarettes per day) comparedwith non-smoking households was 1-55 (breastfed children), and 2-96 (artificially fed children).In the Shanghai population the effectmodification cannot be explained by a relationbetween maternal smoking and breast feeding,since none of the mothers smoked. Children'sexposure to smoke was due entirely to smoking byother household members than the mother. Inthese circumstances, the explanation is likely to bea biological protective effect ofbreast milk againstthe irritation of smoke in the respiratory tract.Further research is needed to elucidate themechanisms of such an action.

We wish to thank Dr Philip Ryan for statistical advice,Ms Lorraine Davies, Ms Bemadette Roberts, and MsKim Boatwright for interviewing, and Professor TonyMcMichael for advice on research design and criticalcomments on drafts of this paper.

1 Leowski J. Mortality from acute respiratory infections inchildren under 5 years of age: global estimates. WorldHealth Stat Q 1986; 39: 138-44.

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