Indoor Risk Factors for Asthma in a Prospective Study of Adolescents
McConnell, Rob1; Berhane, Kiros1; Gilliland, Frank1; Islam, Talat1; Gauderman, W. James1; London, Stephanie J.2; Avol, Edward1; Rappaport, Edward B.1; Margolis, Helene G.3; Peters, John M.1
From 1Department of Preventive Medicine, Keck School of Medicine of the University of Southern California, Los Angeles, California;
2National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina; and
3California Air Resources Board, Sacramento, California.
Address correspondence to: Rob McConnell, Department of Preventive Medicine, 1540 Alcazar Street, Suite 236, Los Angeles, CA; firstname.lastname@example.org
This study was supported by the California Air Resources Board (Contract A033-186), the National Institute of Environmental Health Science (Grants #1PO1ESO939581-01 and #5P30ES07048-05), the Environmental Protection Agency (Grant #R826708-01-0 and Contract #CR824034-01-3), the National Heart, Lung and Blood Institute (Grant 1RO1HL61768), and the Hastings Foundation.
Submitted 12 December 2000; final version accepted 29 November 2001.
Background. The risk of asthma associated with pets and other indoor exposures has been examined in both cross-sectional and prospective studies of younger children. However, there has been little investigation of the effect of the indoor environment on incident asthma in adolescents.
Methods. Risk factors for the development of asthma were examined in a cohort of 3535 Southern California school children with no history of asthma at 1993 entry into the study, who were followed for up to 5 years. Newly diagnosed cases of asthma were identified by yearly interview report. A total of 265 children reported a new diagnosis of asthma during the follow-up period; 163 of these had reported no history of wheeze at baseline. The risk associated with indoor exposures assessed by questionnaire at entry into the study was examined using Cox proportional hazards models.
Results. In children with no history of wheezing, an increased risk of developing asthma was associated with a humidifier (relative risk [RR] = 1.7; 95% confidence interval [CI] = 1.2–2.4), any pet (RR = 1.6; 95% CI = 1.0–2.5), or specifically a dog (RR = 1.4; 95% CI = 1.0–2.0) in the home. An estimated 32% of new asthma cases could be attributed to pets.
Conclusions. We conclude that furry pets are a common and potentially remediable risk factor for new onset asthma in adolescents. Our results suggest that a humidifier in the home may contribute to the onset of asthma in this age group.
Asthma is the most common chronic disease of childhood, and there is evidence that the prevalence of asthma has been increasing in the United States during at least the past 20 years. 1 Although this increase is most marked in children under age 5, prevalence is also increasing among adolescents. 1,2 Prospective studies of children have demonstrated associations of asthma with family history of asthma and early life respiratory illnesses. 2–11 Studies have shown that asthma risk factors and prognosis differ by age group. 12
The role of indoor allergen exposure in exacerbating asthma is well known. 13,14 Studies of children have also found associations between asthma prevalence and indoor exposures, including indoor allergens and combustion sources, especially environmental tobacco smoke. 15–18 However, the results of studies examining the role of indoor allergens as a primary cause of asthma lack consistency, and one recent review of prospective and population-based cross-sectional studies of children concluded there is little evidence for a causal relation. 19 Although there are longitudinal studies of indoor exposures and asthma incidence in young children, 20–22 there has been little information reported on the effect of indoor exposures in prospective studies of asthma with onset in adolescence. Such studies would be useful to help elucidate the causes of the asthma epidemic among adolescents and the relation between indoor allergen exposure and asthma in different age groups. Cross-sectional studies are not well suited to identifying how risk factors vary with age of onset of disease, because both the temporal relation with exposure is unclear and the assessment of age of onset is subject to recall bias.
We examined the association of indoor exposures with the subsequent development of asthma among cohorts of adolescents and children entering adolescence, who were participating in the Southern California Children’s Health Study. 23
We recruited children in early 1993 from schools in neighborhoods with stable, primarily middle-income populations in 12 communities in Southern California. Approximately 175 fourth graders (age 9–10 years), 75 seventh graders (age 12–13 years), and 75 tenth graders (age 15–16 years) from each community completed a baseline questionnaire with help from their parents, as described previously. 23 An additional cohort of approximately 175 fourth graders from each community was recruited in early 1996. All children from targeted classrooms were invited to participate. Children were followed through the spring of 1998 (or, in the case of tenth graders, until graduation in 1995). The study was approved by the Institutional Review Board at the University of Southern California, and informed consent was obtained from all participants.
Definition of Asthma and Wheeze
We excluded children from the analysis if (1) there was a “yes” answer to the question, “Has a doctor ever diagnosed this child as having asthma?” on the baseline questionnaire sent home to each child’s parents, or (2) if a child answered “yes” to the question, “Has a doctor ever said you had asthma?” on a questionnaire administered by an interviewer in the spring of 1993 (or in 1996 for the more recent cohort). We stratified the population according to history of wheezing, based on the answer in the baseline questionnaire to the question, “Has your child’s chest ever sounded wheezy or whistling, including times when he or she had a cold?” In addition, children were excluded from analysis if there were “don’t know” or missing answers about wheezing, if they did not have at least 1 year of follow-up, or if there was a history of cystic fibrosis or severe chest injury or chest surgery. A total of 3535 children without a history of asthma were available for follow-up, 2752 (78%) of whom had no history of wheezing.
Interviewers administered the questionnaire to participating children in the spring of each subsequent year through 1998 (or until graduation). Those children answering “yes” to the question about doctor-diagnosed asthma were considered to have newly diagnosed asthma. We calculated follow-up age from the time of the first questionnaire administered to the child until 20 June of each following year. Each child who reported physician-diagnosed asthma was also asked whether an inhaler was used.
Information on characteristics of the child’s home environment was also collected in the baseline questionnaire, as has been described previously. 23 Home environmental risk factors included the presence of pets (cats, dogs, gerbils or hamsters, pet mice or rats, guinea pigs, birds, or other) and pests (rats, mice, cockroaches, ants, spiders, termites, or other). The questionnaire included items about other contributors to indoor allergens (eg, water damage, flooding, or mold or mildew on surfaces in the home while the child had lived there; an evaporative cooler or humidifier in the home; number of plants in the home; and carpeting in the child’s bedroom). The following additional exposures were assessed: presence of combustion sources (gas or wood as the primary source of heat; a gas stove or oven); whether a stove or oven was used to heat the home; air conditioning in the home; whether there were any months during the year when the parent tried to keep the home completely closed because of heating or air conditioning; whether the home had been built since 1980 (as there might be more insulation and less ventilation in newer homes); current maternal smoking; and lifetime history of the child’s smoking 100 cigarettes or more.
Additional covariates of interest (from the baseline questionnaire) included gender, age, race and ethnicity (Hispanic, non-Hispanic white, Asian or Pacific Islander, African American, or other), community of residence, family history of asthma in either parent, child’s history of allergy, membership in a health insurance plan, and high or low socioeconomic status (SES) compared with middle-income families. We considered families to be of low SES if family income was less than $15,000 annually (or, if income was not reported, if the responding parent had less than a 12th grade education). High SES was defined by annual family income of $100,000 or more (or, if income was not reported, by graduate training). All other families were considered to be of middle SES, based on income (or education, if income was not reported). We restricted some sensitivity analyses to children without a history at baseline of the following conditions: bronchitis in the previous year, chronic cough that lasted for more than 3 months in the previous 12 months, or frequent congestion in the chest or production of phlegm. Body mass index (BMI; weight/height2 by quartiles) was measured at the time of the administration of the initial interview to the child.
We calculated the unadjusted person-time of follow-up and asthma incidence rates for each indoor exposure of interest. We used multivariate proportional hazards models 24 to evaluate the relative risk of asthma for each exposure, adjusted for ethnicity and community of residence. The models incorporated baseline hazards stratified by age groups and gender. Age groups were less than 9.70 years, 9.70–11.49 years, and greater than 11.49 years; these groups were selected to divide the fourth grade cohorts at the median at study entry and to result in minimal overlap of the fourth grade with the combined seventh and tenth grade age distributions. We evaluated confounding by including additional covariates in the models and assessing whether there was more than a 10% change in the estimates for the effect of each indoor exposure. We conducted all analyses with the Statistical Analysis System (SAS) package, using the PROC PHREG procedure for proportional hazards models. 25
The prevalence of wheeze was slightly higher among males than among females, and there was approximately similar prevalence of wheeze in each of the three age groups examined (Table 1). Caucasian, non-Hispanic children had the highest prevalence of wheeze; rates were low among Asians and intermediate among Hispanic and African American children. (Wheeze rates for Asians and African Americans were based on small numbers of children.)
Numerous asthma risk factor exposures, including pets (specifically dogs and cats), pests (specifically ants and spiders), water damage, mildew, a home humidifier, carpeting in the child’s room, maternal smoking, and the use of wood for heat, were associated with wheezing history (Table 2).
A total of 265 children reported a new diagnosis of asthma during the follow-up period of up to 5 years (10,944 person-years of follow-up; incidence rate 2.4% per year). Of these, 163 cases occurred among those with no wheeze at baseline (8607 person-years of follow-up; incidence rate 1.9% per year) and 102 among those with wheeze (2337 years of follow-up; incidence 4.4% per year). The relative risk (RR) of asthma, comparing those with and without a history of wheeze, adjusted for ethnicity, community, and baseline age and gender, was 2.4 (95% confidence interval [CI] =1.8–3.0).
Among children with no history of wheeze at baseline, the presence of any pet or dog, a humidifier, and more than four house plants in the home was associated with a modest increased risk for newly reported asthma during follow-up of this cohort (Tables 3–4). There was no evidence for a dose-response relation as number of plants increased from none to 13 or more (results not shown). The estimated RRs for each pet did not change by more than 10% after simultaneously adjusting for every other pet, nor did the RRs for each pest change appreciably after adjustment for every other pest.
Among children with a history of wheeze at the beginning of the study, an increased risk of asthma was associated with gerbils or hamsters and birds as pets, and a decreased risk was associated with any pest in the home and with mildew (Tables 3–4).
For those associations for which the 95% confidence interval did not include 1.0, each model was further adjusted for baseline BMI, maternal smoking, history of allergies, family history of asthma, membership in an insurance plan, and SES. There was evidence of confounding only among children with a history of wheeze at study entry, for whom the RR associated with pet gerbils or hamsters increased to 3.1 (95% CI = 1.6–6.0), and the RRs associated with a pet bird and mildew decreased to 1.4 (95% CI = 0.8–2.4) and 0.5 (95% CI = 0.3–0.8), respectively.
Although genetic predisposition to asthma is well recognized, 10,26 genetics alone cannot explain the apparent increase in asthma prevalence during the past 20 years. The role of environmental factors in asthma is further supported by the large differences in the prevalence of asthma and wheeze in different countries, and between groups of similar ethnicity within countries. 27,28
Our results suggest that there are identifiable indoor environmental exposures that increase the risk of development of asthma among adolescents. Among children with no prior history of wheeze at baseline, there can be little doubt as to the temporal association between exposure and asthma, because children with no history of wheeze were unlikely to have had undiagnosed asthma at study entry. The association with pets, and particularly dogs, is consistent with those of some cross-sectional and case-control studies. 15,29 Other cross-sectional studies, in which allergen in house dust was measured, have found either no association with pet (or any other indoor allergen) exposure in children, 19 or a protective effect. 30 These results might have resulted from families getting rid of pets when the child developed asthma. However, two prospective studies of young children have also not found pets to be associated with asthma. 21,22
One explanation for the inconsistencies among studies might be that pets have different effects at different ages. For example, an exposure early in life to endotoxin associated with pets might result in a protective shift in the immune system from a T-helper-2 cell to a T-helper-1 cell response, 31,32 whereas exposure to pets later in life might be associated with asthma. Other immunologic mechanisms for the development of tolerance at high allergen exposure among children have also been proposed. 33 In adults, a pet in the home has been associated with increased risk of pet-specific sensitization, but pet ownership in childhood has been associated with less atopy and less pet-specific sensitization in adulthood, an observation which would be consistent with different risks of pet exposure for allergic disease at different ages. 34,35 Although we had good information on age of onset of asthma in this study, participants were not asked at what age the child was first exposed to pets.
A potential explanation for the absence of an association of cats with asthma in our study is the misclassification of cat allergen exposure based on questionnaire, because cat allergen is likely to be found in public places and in homes without cats. 36
The increased risk associated with humidifier use, also observed in previous epidemiologic studies of children, 17,37 could have been caused by an increase in house dust mite allergen, which is common in humid homes, 38–41 or by conditions which may favor the growth of mold in the home environment or in the humidifier itself. 41 Clinical and limited laboratory studies have established the potential of humidifiers to grow mold 42 and to exacerbate asthma both in the occupational 43 and in the home environment. 44 Humidifiers have also been associated with endotoxin exposure in the home. 13 We considered the possibility that homes may have had humidifiers to treat symptoms of children with other early respiratory manifestations of asthma, but in whom wheezing had not been recognized or reported at baseline. The association with humidifier use persisted in our study after restricting the analysis to children who did not have a history of other respiratory illness (bronchitis or chronic cough that lasted for more than 3 months in the previous year, or frequent congestion in the chest or production of phlegm) at baseline. In addition, the risk associated with a humidifier in the home in children with newly diagnosed asthma in the first year of follow-up (RR = 1.9), who may have been more likely to have already had asthma at baseline, differed little from that in children diagnosed in later years (RR = 1.6). Therefore, it seems unlikely that a humidifier in the home was an indicator of undiagnosed asthma at baseline.
Although this study is prospective, the temporal relation of observed associations between risk factors and asthma among children with a history of wheezing at study entry may not be clear. Associations with asthma observed in this group may have resulted from families with more symptomatic children at baseline having intervened to reduce exposures which they believed exacerbated wheeze. For example, these families may have substituted unusual pets, such as gerbils, hamsters, or birds, for dogs. The evidence for effect modification by wheeze is not altogether convincing, because the estimated effects of indoor risk factors had wide and overlapping confidence intervals among wheezy and never wheezy children; nonetheless, these results suggest that prospective studies of the primary causes of asthma should examine children with and without wheeze at study entry separately.
The incidence of newly reported asthma at 2.4% per year is substantial. It may be compared with the cumulative incidence of 12.0% observed among a slightly younger cohort of children followed between ages 6 and 11 in Tucson, Arizona. 8 In a 25-year follow-up, self-reported asthma during the previous 12 months was reported by 10.8% of adults who had no history of asthma or wheezy illness at age 7. 6 However, in other studies of adolescents considerably lower incidence of asthma has been found. 2,45,46 As different methods have been used for ascertainment of asthma in these various studies, it is difficult to determine whether reported differences reflect the true variation in asthma incidence in the various populations.
The many indoor exposures evaluated were selected because they have been reported to be associated with prevalent asthma, or with incident asthma at young age. 14,16,17 The cross-sectional associations of history of wheeze at study entry with pets, pests, and other indicators of indoor allergens, as well as current maternal smoking and the use of wood for heating, suggest that there may be associations of these risk factors with a history of undiagnosed asthma in this population. In contrast, we identified relatively few predisposing indoor risk factors for the new diagnosis of asthma in adolescence. It may be that indoor environment is less important in the etiology of asthma in adolescence than it is in younger years, or it may be that power was too limited because of a small number of new diagnoses. For many risk factors examined in this study, very large (or small) proportions of children were exposed (for example, to carpet and gas stoves), limiting the power to detect an increase in asthma. In addition, the measurement of exposures to indoor pollutants by questionnaire may be relatively imprecise. 19 However, it is likely that the result of questionnaire assessment of indoor exposure in this study would have been nondifferential (at least among parents of children with no history of wheeze at baseline), and it is possible that more precise measurement of exposure would have identified additional associations or strengthened the observed associations.
Another limitation to this study is potential misclassification of asthma, which could be affected by access to care and differences in diagnostic practice between physicians, 47 or by poor reporting by children or parents. However, subject report of physician-diagnosed asthma has been widely used in epidemiologic studies of children, 28 and the validity as assessed by repeatability of response is good. 48,49 Self-report has been found to reflect what physicians actually reported to patients, at least in adults, 50,51 and physician assessment of asthma has been recommended as the gold standard for this disease, for which a more precise diagnosis is not available. 52 Nevertheless, it is also possible that classification of individuals based on measurement of physiologic responses characteristic of asthma, such as bronchial hyperreactivity, or based on a standardized clinical examination, might have strengthened observed associations with indoor risk factors. When we limited the analysis to those cases of asthma for which an inhaler was reportedly used (and which may, therefore, have been more severe, or more likely to be true cases of asthma), the observed associations with indoor risk factors were, in general, stronger. The RRs increased slightly for presence of dogs (to 1.6) and humidifier use (to 2.1) among children without wheeze.
The strength of this study was the ability to identify indoor risk factors for the development of asthma among adolescents with no baseline history of wheezing. This population is also one for which there are few previous prospective studies that could identify risk factors amenable to preventive efforts. Among children without wheeze, there was an increased risk of asthma associated with a humidifier or a pet, especially a dog, in the home. These potentially remediable causes of childhood asthma were common in this population; thus, 32% of asthma among children with no history of wheeze at baseline was attributable to pets, a proportion similar to that estimated from a recent analysis of the Third National Health and Nutrition Examinations Survey. 15
We thank David Bates for his advice and thoughtful comments, and the External Advisory Committee, composed of Morton Lippmann, Jonathan Samet, John Spengler, Frank Speizer, James Whittenberger, Arthur Winer, and Scott Zeger, for its input. We acknowledge the hard work of the study field team and the cooperation of the 12 communities, the school principals, the many teachers, the students, and their parents. Programming support was provided by Isabelo Manila.
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asthma; etiology; indoor allergen; pets; dog; humidity
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