Parental smoking and respiratory tract infections in children

Transcription

1 PAEDIATRIC RESPIRATORY REVIEWS (2001) 2, doi: /prrv , available online at on MINI-SYMPOSIUM: SMOKING: EFFECTS ON THE PAEDIATRIC LUNG Parental smoking and respiratory tract infections in children J. K. Peat 1, V. Keena 2, Z. Harakeh 3 and G. Marks 4 1 Department of Paediatrics and Child Health, University of Sydney, Australia; 2 Institute of Respiratory Medicine, Royal Prince Alfred Hospital, Camperdown NSW 2050, Australia; 3 Faculty of Health Sciences, Maastricht University, The Netherlands; and 4 Cooperative Research Centre for Asthma, Royal Prince Alfred Hospital, Camperdown NSW 2050, Australia KEYWORDS environmental tobacco smoke, children, respiratory tract infection. Summary The adverse health consequences of exposing children to tobacco smoke have been well documented. Re-calculation of the data available from cohort and crosssectional studies worldwide shows that between excess hospitalisations and between 1000 to 5000 excess diagnoses per young children as result from respiratory infections can be directly attributed to parental smoking. Results of published meta-analyses support these figures, which are probably under-estimated because of the effects of non-differential misclassification bias. These excess infections are a source of preventable morbidity and have a high cost to the community. They also have important long-term consequences because children who have respiratory infections in early life are at an increased risk of developing asthma in later childhood. More effective strategies that prevent smoking in young people before they become parents have the potential to lead to reductions in these high rates of unnecessary morbidity in the next generation of children. C 2001 Harcourt Publishers Ltd INTRODUCTION The health consequences of exposing children to environmental tobacco smoke (ETS) have been a concern for over 30 years and have elicited wide-reaching governmental health reports and systematic reviews. These reports and reviews have been based on a vast number of research studies that have documented the effect of parental smoking in increasing respiratory infections and other respiratory illnesses in children. In this article, we summarise the evidence that parental smoking leads to increased respiratory infections in early life and we explore the consequences of such infections on the future respiratory health of the child. Correspondence to: Associate Professor Jennifer Peat, Clinical Epidemiology Unit, The Children s Hospital at Westmead, Locked Bag 4001, WESTMEAD NSW 2145, Australia. Fax: ; Tel: HISTORY OF RESEARCH INTO EFFECTS OF PARENTAL SMOKING ON CHILDREN The first studies to document the effects of parental smoking in increasing the incidence of respiratory infections in infancy were conducted over 30 years ago. 1 In 1974, a large cohort study of over 2000 children showed that children whose parents smoked had a significantly increased risk of having pneumonia or bronchitis with an odds ratio of 2.3 (95% CI 1.4 to 3.6). 2 Since then, a large number of epidemiological studies have been undertaken to verify these effects. The study methods have varied widely in that there have been crosssectional, longitudinal, case control, cohort and retrospective studies. Exposure has been ascertained using a wide variety of definitions and respiratory outcomes have been measured using not only different definitions but also different methods of data collection, including /01/ $35.00/0 C 2001 Harcourt Publishers Ltd

2 208 J. K. PEAT ET AL. parental questionnaires, primary care contacts or hospital admissions. Nevertheless, the evidence that these studies have provided has been fairly consistent: most show that exposure to parental smoking significantly increases the risk of respiratory infections in children. (A full list of studies and their methods can be accessed at METHODOLOGICAL ISSUES In assessing the evidence from these studies, it is important to consider any possible biases that could lead to underestimation or overestimation of the measures of effect. On the one hand, information from questionnaire responses about outcomes and exposures are often prone to recall bias. In addition, total exposure can be difficult to quantify because parents may change their smoking habits during the child s lifetime and additional exposure may occur in places outside the home. However, nonsystematic misclassification of exposed and non-exposed children will lead to an under-estimation of the actual risks associated with exposure to tobacco smoke. Nonsystematic misclassification of the presence or absence of respiratory infections will also lead to an underestimation of the risk. Thus, any odds ratios from studies or from meta-analysis will tend to be conservative in magnitude and the actual effect in the community is likely to be much larger than actually measured. On the other hand, estimates of associations between parental smoking and respiratory infections could be overestimated if parents who smoke are more aware of symptoms in their child, or if a parent whose child has an infection is more likely to recall smoking. However, this is unlikely since studies show that parents, when questioned in conjunction with an illness in their child, tend to underestimate the child s exposure to tobacco products. 3 Although markers such as urinary or salivary cotinine are potentially attractive for more accurately measuring exposure, they only indicate recent exposure and are not suitable for use in large epidemiological studies of young children. The most reliable evidence of the effect of tobacco smoke exposure on respiratory infections is likely to come from studies in which hospitalisation for infection is used as a primary outcome measurement. In such studies, misclassification bias will be reduced because parents are likely to remember events associated with a serious consequence, such as hospitalisation, more accurately so that the number of false positive and false negative responses will be minimised. In the studies that have been conducted, the definitions of illnesses for which young children have been hospitalised have varied from chest problems and lower respiratory tract illness to classification by International Classification of Disease (ICD) categories. However, in studies in which subjects were below the age of 5 years, the primary cause of hospitalisation is likely to have been a respiratory infection. At this age, infections with the respiratory syncytial virus and other viruses are common. Also, it is extremely difficult to distinguish respiratory tract infections from non-infectious respiratory tract illness such as rhinitis or asthma, which may be difficult to diagnose before the age of 5 years. RESULTS FROM EPIDEMIOLOGICAL STUDIES Figure 1 shows the number of excess cases of hospitalisations for respiratory infection as a result of tobacco smoke exposure in the studies from which this can be calculated. Details of the design of the studies in Figure 1 are listed in Table 1. The results suggest that very large numbers of young children are hospitalised simply because they have been exposed to tobacco smoke. The estimates from the studies in China are much higher than the estimates from the USA and UK and are likely to reflect different local policies for hospitalising children. Although the effects of pre-natal vs post-natal and active vs passive smoking by the mother have been difficult to delineate, the studies in China where few women smoked suggest that passive smoke exposure during pregnancy and after birth is detrimental to child health. Figure 2 shows the number of excess cases of diagnosed respiratory infections that can similarly be attributed to parental smoking from the studies from which these numbers can be calculated. Details of the design of the studies shown in Figure 2 are listed in Table 2. There is a wide variation in estimates between countries from 1000 to over 5000 excess diagnoses/ children that could, again, reflect variations in local diagnostic practices. There have been many other studies that have measured the effect of parental smoking on other outcomes related to less serious lower respiratory tract infections Figure 1 Excess cases of respiratory infection requiring hospitalisation in young children as a result of exposure to parental smoking (see Table 1 for definitions of age range, exposures and outcomes).

3 PARENTAL SMOKING AND RESPIRATORY TRACT INFECTIONS IN CHILDREN 209 Table 1 Details of studies shown in Figure 1. Author and Year of Definition of Definition of Sample citation publication Country respiratory outcome exposure size Age Type of study Ekwo et al USA Hospitalisation for Smoking >5 cigarettes/ 830 <2 years Cross-sectional chest illnesses day by father or mother Chen et al China Hospitalisation for Smoking by family months Cross-sectional first episodes of members respiratory illness Taylor et al UK Hospitalisation for a Smoking by father or years Cross-sectional lower respiratory mother tract illness Chen et al China Hospitalisation for a Family smoking in the months Cross-sectional respiratory illness home Chen et al China Hospitalisation for Tobacco smoke months Cross-sectional respiratory disease exposure in the in children 2500 g household birth weight Figure 2 Excess cases of diagnosed respiratory infections in young children as a result of exposure to parental smoking (see Table 2 for definitions of age range, exposures and outcomes). such as phlegm, cough or cold. The results from these studies have been similar to those of the studies shown in Figure 2, although recall bias is likely to be a much more important issue in such studies. For the outcomes shown in Figure 2, the estimates will be less prone to bias because the labelling of a serious infection is by a doctor and is therefore more likely to improve recall. RESULTS FROM META-ANALYSES The results of the studies conducted up to 1998 to investigate the association between parental smoking and childhood infections have been summarised as systematic reviews and meta-analyses. 4,5 Unlike the studies shown in Figures 1 and 2, the results of case control studies and cross-sectional studies in which no prevalence data are reported can be incorporated. Despite the wide range of study designs, inclusion criteria and outcomes used, the results have been surprisingly consistent with the majority of studies demonstrating a positive association between parental smoking and medical treatment for childhood respiratory infections. Since these meta-analyses were conducted, further studies have only served to confirm rather than refute the results. In general, the vast majority of studies have found a statistically significant association between parental smoking and early childhood respiratory infections with odds ratios that have ranged from In the meta-analyses conducted, random effects models suggest an odds ratio of about 2.0 as the typical effect of parental smoking on early childhood hospitalisation for respiratory illness, with the risk most pronounced in children younger than 2 years. 4 In addition, an odds ratio of 1.7 was calculated as the typical effect on the incidence of a diagnosed lower respiratory infection 4 and an odds ratio of 1.6 as the typical effect of parental smoking on the incidence of early respiratory illness. 5 If children were only exposed to smoking by other family members and not the mother, the odds ratio was approximately 1.3. These odds ratios suggest that, in a population in which the rate of exposure to parental smoking is 40% and the overall rate of diagnosis of childhood respiratory infections such as pneumonia, bronchitis and bronchiolitis is 18%, there will be approximately 2000 excess diagnoses attributable to parental smoking per children. If the rate of hospitalisation is 5%, there will be approximately 1000 excess hospitalisations per children. It is of concern that these high rates of morbidity and use of medical services are potentially preventable. Although odds ratios below 2.0 are sometimes disregarded as clinically unimportant, odds ratios of this magnitude represent a significant public health problem in the case of tobacco smoke exposure simply because of continuing high rates of parental smoking. 6 In some studies, a dose response relationship has been demonstrated with

4 210 J. K. PEAT ET AL. Table 2 Details of studies shown in Figure 2. Author and Year of Definition of Definition of Sample citation publication Country respiratory outcome exposure size Age Type of study Colley et al UK Incidence of bronchitis Smoking by father year Cohort and pneumonia or mother Fergusson et al New Medical consultation for Smoking by father years Cohort Zealand bronchitis and or mother pneumonia Pedreira et al USA Incidence of bronchitis, Smoking by father year Cohort pneumonia or or mother bronchiolitis Taylor et al UK Incidence of at least Smoking by father years Cross-sectional one episode of or mother bronchitis Chen et al China Cumulative incidence Family smoking in Cross-sectional of bronchitis or the home months pneumonia Forastiére et al Italy Prevalence of early Smoking by father years Cross-sectional respiratory infection or mother (bronchitis, pneumonia or bronchiolitis) Peat et al Australia Prevalence of bronchitis Maternal smoking years Cross-sectional diagnosed by a doctor or at a hospital Bravo et al Chile Prevalence of two or Daily exposure to Cohort more episodes of tobacco smoke months acute lower respiratory illness Gergen et al USA Cumulative prevalence Current household months- Cross-sectional of a physician s exposure 2 years diagnosis of chronic bronchitis the risk of children having respiratory infections increasing as the number of cigarettes smoked by the mother increased. The risk of respiratory infections in older children has also been estimated in many studies, with similar consistency of evidence. However, the outcomes have often been described as chronic or wheezy bronchitis, or cough, phlegm, frequent cough and chesty cold. Although the public health importance of these outcomes should not be underestimated, there is no convincing evidence that these symptoms have an important impact on future illness as do severe infections encountered in early life. CONFOUNDING FACTORS We might expect that many factors would confound the effects of parental smoking including an increased exposure to infections through daycare, gender, ethnicity, housing conditions, place of residence, family size, exposure to pets, maternal age, parental education etc. However, in the studies in which these have been measured, the effect of parental smoking has not been consistently influenced by these factors, suggesting that exposure has an independent effect. 5 On the other hand, long-term breastfeeding has been found to protect against the risk of lower respiratory tract infection during the first year of life 7 and there is some evidence that children who are predisposed to developing atopy 8,9 or who have a lower birthweight 10 are at greater risk. MECHANISMS The evidence for the adverse effects of parental smoking on respiratory infections in children is consistent, but the mechanisms by which this occurs are not well documented. Since it is normally impossible to obtain airway tissue from infants and children, we have no direct information of how parental smoking affects the structure of the infant airway wall. However, examination of airway tissue from infants who have died from sudden infant death syndrome shows that inner airway wall thickness is greater in the larger airways of infants whose mothers

5 PARENTAL SMOKING AND RESPIRATORY TRACT INFECTIONS IN CHILDREN 211 smoked more than 20 cigarettes/day. 11 The direct consequences of these abnormal increases in airway thickness are not known, but it seems biologically plausible that airways that are thickened in early life may be more prone to airway narrowing and to respiratory infections. In addition, exposure to tobacco smoke in utero leads to lower birthweight and thus to smaller lungs and reduced airway size. As narrow airways are much more readily obstructed by inflammation, oedema and mucus, they may be more prone to invasion by respiratory pathogens such as respiratory syncytial virus. This hypothesis is supported by the finding of higher rates of hospitalisation for infections in low-birthweight babies. 10 Studies of nicotine metabolites such as cotinine show that tobacco products are absorbed by children, particularly small children, in a direct relation to levels of exposure. If exposure to tobacco smoke only led to certain well-defined outcomes then we would suspect that it only influenced specific mechanisms. However, the finding that there is a consistent effect of parental smoking on many signs and symptoms of respiratory infections suggests that exposure influences a wide variety of mechanisms in the airways. Exposure may damage the epithelium and allow allergens and pathogens to cross into the airways or may impair defence mechanisms such a mucociliary clearance and thus increase susceptibility to pathogens. It is also possible that inhalation of tobacco smoke in early life can cause direct damage to the naso-pharyngeal mucosa and can alter cell-mediated immunity and epithelial function. 12,13 The lungs undergo rapid and extensive changes in growth and development in early childhood and may be particularly vulnerable to harmful environment exposures, especially since the immune system is immature. SEQUELAE OF EARLY INFECTIONS The effect of lower respiratory tract infections in early life on the aetiology of later respiratory illnesses is complex, with some studies showing that children who have experienced infections in early life are prone to developing asthma and other studies showing that they are protected. It is thought that some types of infection in early life skew immune responses away from a T helper type 2 (Th2) response that promotes the development of allergic responses towards a Th1 type response that protects against allergic responses. Thus, it has been postulated that the increased prevalence of asthma in developed countries in the last two decades may be a result of fewer childhood infections leading to protection from microbial exposures. This hypothesis is supported by ecological evidence which shows that the prevalence of asthma has increased in the presence of improved standards of hygiene, increased rates of immunisation and reduced rates of cross-infections as a result of fewer siblings and more spacious housing. 14 Direct evidence comes from studies in which immunisation is associated with an increased incidence of atopy and of asthma. 15 However, a recent study shows that only repeated viral infections other than lower respiratory tract infections early in life are associated with a reduced risk of children developing asthma. 16 There is good epidemiological evidence that early respiratory infection is an important risk factor for the development of asthma and airway hyper-responsiveness (AHR) in later childhood 17,18 and many asthmatic children have a history of recurrent lower respiratory tract illnesses in early life. 19 Other studies which support this hypothesis that infection predisposes to asthma are those in which treatment with antibiotics in early life, which are a reliable marker of the presence of infection, is associated with asthma in later childhood with an odds ratio of approximately ,21 It is possible that respiratory infections in the early life of some children are a marker of airways that are prone to developing inflammatory responses. Many children with respiratory infections may have been exposed to respiratory syncytial virus which is a common respiratory pathogen in young children which often results in acute viral bronchiolitis. 22 Animal studies suggest that exposure to this virus in early life often leads to increased sensitisation to allergens and to AHR, although the mechanisms are not clear. BENEFITS OF PREVENTING EXPOSURE As a result of the many studies that have documented the adverse effects of parental smoking, there is now an undisputed consensus amongst health professionals that children should not be exposed to tobacco smoke. Prevention of exposure would be a critical primary step in working towards prevention of lower respiratory tract respiratory infections in young children especially since respiratory tract infections are the most common, and potentially most severe, of infections treated by health care practitioners. 23 Thus, it is important to work towards preventing such illnesses not only because they are a major cause of morbidity but also because they have adverse consequences for future respiratory health and are a significant financial cost to families and to communities. In a recent study in the USA, maternal smoking was associated with an increased health care expenditure of $120/year for children under age 5 years of age and $175/year for children under 2 years of age. Exposure to tobacco smoke was responsible for 19% of all expenditures for childhood respiratory conditions. 24 The public health implications of exposing children to tobacco smoke have been succinctly summarised. 25 Evidence suggests that there is a dose response

6 212 J. K. PEAT ET AL. relationship between both the number of smokers within the home and the amount smoked and adverse outcomes for children. 5 However, many children continue to be exposed with rates of maternal smoking during pregnancy often above 30% in developed countries, with much higher rates of post-natal exposure in some communities. For many children, in-utero exposure and smoking in their home remains the major source of exposure. It has been suggested that measurement of urinary cotinine might constitute an efficient method of convincing parents of the reality of exposing their children to tobacco smoke. 26 To reduce early respiratory illness, infants must be protected from maternal smoking and also from smoke from other family and non-family members. Thus, strategies to reduce smoking in the entire community rather than strategies to reduce smoking in parents will be most effective. Significant reductions in the prevalence of smoking in this generation are essential for improving the health of the next generation. PUBLIC HEALTH IMPORTANCE Any successes in reducing parental smoking will also have many other important health outcomes because such exposure is also associated with a higher incidence of other serious childhood conditions such as invasive meningococcal disease, sudden infant death syndrome and a wide range of airways and middle ear diseases which have long term outcomes. There are also other secondary health issues. For example, smokers are less likely to breastfeed their babies. Children who are exposed to parents and family members who smoke are more likely to take up smoking themselves and are therefore at direct risk of having many severe health outcomes from an early age. Compared with the very large number of studies that have been conducted to demonstrate the harm caused by parental smoking, there have been far fewer studies that have reported the effects of interventions to reduce parental smoking and those that have been conducted have been only moderately successful at best. Many women try to quit but fail 27 and interventions often fail to take account of socio-economic disadvantage and other social factors, such as the influence of partners and family members. A study in North America found a decline in recent years in the number of homes where people felt free to smoke in front of children but that only 7% of homes where two or more people smoked were smoke-free. 28 It is essential that new interventions are devised that target young people before they plan to become parents. Legislation may be needed to control tobacco advertising that is specifically directed at young people. FUTURE DIRECTIONS Over the last 3 decades, there has been a steady accumulation of evidence that parents who smoke increase the risk that their child will have a serious respiratory infection in early life. It seems unnecessary to continue to conduct studies that investigate the risks of exposing children to tobacco smoke especially since, for many children, tobacco smoke continues to be an exposure that cannot be avoided. Since most mothers who smoke during pregnancy have taken up the habit in early life and continue to smoke after the baby is born, 29 preventive strategies need to target smokers well before they become parents. To this end, community norms may need to shift further in favour of protecting children from tobacco smoke exposure before interventions can be successful. 30 A huge number of studies have stressed the public health importance of anti-smoking programmes for young people and for prospective parents and, as a result, most mothers are aware of the risks of smoking during pregnancy. 31 However, tobacco companies continue to develop advertising that is attractive to young people 32 and more sophisticated advertising continues to dilute the effects of public health campaigns. Thus, interventions to date have not halted the growth in the proportion of young women who smoke regularly. Until advertising ploys are curtailed and greater resources are invested in health promotion, preventable respiratory infections that often result in hospitalisation or the need for medical management will continue to be prevalent in the next generation of children. PRACTICE POINTS The consequences of exposure to parental smoking can be severe for young children. Parental smoking is an important source of preventable lower respiratory tract infections. Other adverse exposures such as failure to breastfeed are associated with tobacco smoke exposure. Measurement of infant s cotinine levels may help to convince parents of the risk. Parents who smoke are more likely to have children who smoke. Prevention is complex. Successful intervention will have benefits for the entire family. RESEARCH DIRECTIONS What is the most effective method to prevent young people taking up smoking? Are smoking interventions in adolescence or young adulthood most effective in preventing pregnancy exposure?

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