Context. Residential exposures are recognized risk factors for asthma, but the relative contribution of specific indoor allergens and their overall contribution to asthma among older children and adolescents in the United States are unknown.
Objective. To estimate the relative contributions, population-attributable risks, and costs of residential risk factors for doctor-diagnosed asthma.
Design. Nationally representative, cross-sectional survey conducted from 1988 to 1994.
Setting and Participants. A total of 5384 children who were 6 to 16 years old and participated in the National Health and Nutrition Examination Survey III, a survey of the health and nutritional status of children and adults in the United States.
Main Outcome Measure. Doctor-diagnosed asthma, as reported by the parent.
Results. Five hundred three of 5384 children and adolescents (11.4%) had doctor-diagnosed asthma. After adjusting for age, gender, race, urban status, region of country, educational attainment of the head of household, and poverty, predictors of doctor-diagnosed asthma included a history of allergy to a pet (odds ratio [OR: 2.4; 95% confidence interval [CI]: 1.7, 3.3), presence of a pet in the household (OR: 1.5; 95% CI: 1.1, 2.1), and immediate hypersensitivity to dust mite (OR: 1.5; 95% CI: 1.05, 2.0),Alternaria (OR: 1.9; 95% CI: 1.3, 2.8), and cockroach allergens (OR: 1.4; CI: 1.04, 1.9). Family history of atopy (OR: 1.7; 95% CI: 1.1, 2.7) and diagnosis of allergic rhinitis (OR: 2.1; CI: 1.1, 3.7) were also predictors for asthma. The population-attributable risk of having 1 or more residential exposures associated with doctor-diagnosed asthma was 44.4% (95% CI: 29–60), or an estimated 2 million excess cases. The attributable cost of asthma resulting from residential exposures was $405 million (95% CI: $264–$547 million) annually.
Conclusions. The elimination of identified residential exposures, if causally associated with asthma, would result in a 44% decline in doctor-diagnosed asthma among older children and adolescents in the United States.
- National Health and Nutrition Examination Survey
- allergic rhinitis
- pets and environment
Asthma, estimated to affect over 4 million children and adolescents in the United States, has increased dramatically during the past 2 decades.1–3 Numerous risk factors for childhood asthma have been identified. Residential exposures, including indoor allergens, have consistently been shown to be risk factors for the development or exacerbation of asthma.4–20 Studies that have implicated certain risk factors for asthma, however, are often limited by small sample size or a restricted focus on a specific age group, geographic distribution, or socioeconomic strata.4,,10,17,21 Thus, the relative contribution of specific allergens or other residential exposures to asthma for children and adolescents in the United States is poorly defined. Moreover, there has not been any attempt to estimate the overall contribution of indoor allergens or residential exposures to asthma. To develop a national strategy to prevent childhood asthma, it is critical to estimate the contribution of specific risk factors and the overall contribution of residential exposures to asthma.
In a previous analysis, we estimated that residential exposures—including pets in the household, allergy to a pet, exposure to environmental tobacco smoke, and use of gas stove or oven for heat—accounted for 530 000 excess cases (40%) of doctor-diagnosed asthma in children <6 years old.20 Risk factors for asthma in early childhood, however, are often distinct from those that predict asthma in later childhood and adolescence.6,,9Moreover, skin testing was not conducted among children younger than 6 years old in the National Health and Nutrition Examination Survey (NHANES) III, so we could not assess immediate hypersensitivity in the younger children.
The objective of this study was to estimate the relative contributions, population-attributable risks, and costs of residential risk factors, including indoor allergens, for doctor-diagnosed asthma among a representative sample of persons 6 to 16 years old in the United States.
NHANES III, conducted from 1988 to 1994, was the source of data for this study. NHANES III was a cross-sectional, household survey of the civilian, noninstitutionalized population that used a complex, multistage probability-sampling design.
The primary dependent variable in this analysis was doctor-diagnosed asthma. The definition of asthma used in this study was based on parent report, as determined by a positive response to the survey question, “Were you ever told by a doctor that your child had asthma?”
A review of the literature on the cause of asthma was conducted to identify environmental and residential risk factors for childhood asthma. We focused on modifiable factors that could be investigated by using NHANES III. These included housing features, such as age of residence, urban or nonurban setting, cotinine and reported exposure to environmental tobacco smoke, presence of pets, given up or avoided a pet because of allergies, type of heating and heating fuel, and use of a gas stove or oven for heat.4–20
Immediate hypersensitivity to standardized indoor allergens (cat, dust mite, and German cockroach) was measured by skin test, using the prick-puncture technique. Standardized outdoor allergens (Bermuda grass, perennial rye, short ragweed, white oak, Russian thistle, andAlternaria alternata) were also measured by skin test. We included all indoor allergens and Alternaria in this analysis. The flare and wheal areas were delineated with a marking pen 15 minutes after the skin was punctured and the allergens were applied. Allergen mean wheal diameter was calculated as the longest diameter of the reaction. We considered a skin test to be valid if the wheal from the positive control (histamine) was at least 1 mm larger than that of the negative control wheal.21 A skin test response was considered positive if the panel was valid and if the mean wheal diameter of the allergen test was at least 2 mm larger than that of the negative control wheal.21
We were primarily interested in environmental risk factors, but we included host and demographic variables to adjust for possible confounding. These variables include child's age, gender, race, and history of allergic rhinitis or hay fever. Measures of socioeconomic status, such as poverty income ratio and educational achievement of the head of household, were also included in the analyses. Finally, we used parental history of atopy (defined as history of asthma or allergic rhinitis) as a measure of genetic predisposition to asthma.
Bivariate analyses were conducted to determine associations with asthma. Variables found to be associated with asthma based on χ2 and Student's t tests (P < .20) were included in logistic regression analyses. Variables were also included if previous studies consistently indicated that they were risk factors for childhood asthma, including gender, race, age, urban residence, region of country, poverty income ratio, and education level of the head of household. Poverty income ratio was computed as a total household income divided by the poverty threshold for the year of the interview.22 Logistic regression analysis was conducted with SUDAAN software to account for the complex, multistaged sampling design of the survey.23Because asthma was present in >10% of the sample population, the odds ratio (OR) was modified to better represent the relative risk.24 Sample weights were used to produce national estimates by adjusting for the oversampling of young children and minority groups.
Population-attributable risk was calculated for factors independently associated with asthma. Population-attributable risk estimates were derived using Levin's formula: Population-attributable risk %where prevalence is the prevalence of the risk factor in the population and relative risk is estimated using the observed OR.25 Population-attributable risk was calculated for each predictor variable and separately for children having ≥1 identified residential exposure.
We used published data on the economic cost of asthma to estimate the cost attributable to residential factors.26 Direct costs included clinic and emergency department visits, hospital outpatient services, hospitalization, and medications. Indirect costs included loss of work because of school absence and illness days. We presented costs inflated to 1997 dollars using inflation factors for each direct and indirect cost category.27 Because there was no significant difference in health service use for children who had asthma associated with a residential exposure compared with those who did not have a residential exposure, we assumed that health service use was similar for the 2 groups. The cost of residential asthma was the product of the fraction of cases attributable to residential exposures and the total cost.
Overall, 503 of the 5384 children (11.4%) surveyed had doctor-diagnosed asthma (Table 1). This translates to 4.6 million children or adolescents in the United States with a history of doctor-diagnosed asthma.
We identified several residential exposures associated with childhood asthma after adjusting for potential confounders in a logistic regression analysis (Table 2). Children who had a history of allergies to a pet—defined as having ever given away or avoided pets because of allergies—were 2.4 times more likely to have doctor-diagnosed asthma (OR: 2.4; 95% confidence interval [CI]: 1.7, 3.3). Presence of a pet in the house was also a risk factor for asthma (OR: 1.5; 95% CI: 1.1, 2.1). In contrast, exposure to environmental tobacco smoke, as measured by either parent report or serum cotinine, was not associated with asthma.
Immediate hypersensitivity to allergens was also associated with doctor-diagnosed asthma. Children who had positive skin tests toAlternaria (OR: 1.9; 95% CI: 1.3, 2.8), dust mite (OR: 1.5; 95% CI: 1.05, 2.0), and cockroach (OR: 1.4; 95% CI: 1.04, 1.9) were at increased risk for asthma. An individual who had positive skin tests to all 3 allergens was 4 times more likely to have doctor-diagnosed asthma compared with individuals who were not skin test-positive. An estimated 1 590 000 of children and adolescents (4.5%) in the United States have positive skin tests to all 3 allergens. In contrast, a positive skin test to cat allergen was not associated with asthma in adjusted analysis (OR: 1.3; 95% CI: 0.8, 2.2).
Host factors associated with asthma in adjusted analyses included a parental history of atopy (OR: 1.7; 95% CI: 1.1, 2.7). Children who had a history of allergic rhinitis were 2.4 times more likely to have doctor-diagnosed asthma (95% CI: 1.1, 3.7; Table 2). Black children were not at increased risk for having doctor-diagnosed asthma compared with white children (OR: 1.1; 95% CI: 0.8, 1.4), but poverty was a risk factor.
We conducted sensitivity analyses to examine the robustness of the model. There was no change in predictors when we examined persons who reported wheezing in the previous 12 months instead of ever had doctor-diagnosed asthma. Skin test sensitization to cat allergen did not reach statistical significance as a risk factor for asthma when the 2 variables for pets were removed from the model. Because there was not an ideal variable for inner-city residence, we explored various interactions of poverty income ratio by urban residence, but these interactions did not achieve statistical significance. Similarly, there was no association of asthma and central-city residence for phase I (1988–1991) of NHANES III (the variable central city was only available in phase I). Other interactions were examined, including child's history of allergic rhinitis with skin test sensitization to cat, dust mite, cockroach, and Alternaria, but none achieved statistical significance.
Over 330 000 excess cases of childhood asthma were attributable to having an allergy to a pet (Table 3). Having a household pet accounted for 900 000 excess cases of doctor-diagnosed asthma. Immediate hypersensitivity to dust mite allergen accounted for 520 000 excess cases, and immediate hypersensitivity to cockroach allergen accounted for 375 000 excess cases. Immediate hypersensitivity to Alternaria—a fungi generally regarded as an outdoor allergen—accounted for 600 000 excess cases of asthma.
Next, we estimated the population-attributable risk of having ≥1 residential risk factor for doctor-diagnosed asthma. Of the 4.6 million cases of doctor-diagnosed asthma in persons 6 to 16 years old, we estimate that 44.4%, or 2 million (95% CI: 1.3–2.75 million) were attributable to residential exposures. In contrast, having a parent with a history of atopy—a surrogate marker for the genetic contribution of asthma—accounted for 750 000 cases (Table 3).
There was no significant difference in health services use by residential exposure status. Five percent of children with a residential risk factor were hospitalized in the past 12 months, compared with 6.1% of children without a recognized residential risk factor (P = .79). Forty percent of children with a residential risk factor had ≥1 emergency department visit or clinic visit for wheezing in the past 12 months, compared with 32.9% for children without a recognized residential risk factor (P = .34). We assumed that the costs of asthma attributable to residential exposures were proportional to the attributable risk fraction because there were no differences in health services use for children with or without an identified residential exposure.
Next, we calculated the direct and indirect costs of asthma attributable to residential risk factors. Based on a population-attributable risk of 44.4%, we estimate that the total cost of asthma attributable to residential risk factors was $405 million (95% CI: $264–$547 million) annually in 1997 dollars for children and adolescents 6 to 16 years old. If we include the costs of asthma for children <6 years old,20 the total cost of asthma attributable to residential risk factors increases to $807 million annually.
The results of these analyses indicate that eliminating exposures to indoor allergens and pets, if they are indeed causal, could prevent over 2 million (44.4%) of the 4.6 million cases of doctor-diagnosed asthma among persons 6 to 16 years old in the United States. The effect of eliminating these risk factors would, therefore, have a profound impact on hospitalization rates, emergency and clinic visits, costs, school absences, and health and functioning of children and adolescents.28
Having a household pet or an allergy to a pet (defined as “given up or avoided a pet because of allergies”) were major risk factors for doctor-diagnosed asthma. Pet allergens are risk factors for asthma.4,,10,2029–32 Consistent with our earlier report and surveys conducted in Europe and the United States, this present analysis indicates that exposure or allergic reactions to pets were the predominant risk factor for asthma among children and adolescents.20,29–31 These variables may overestimate the risk of asthma from pet exposure, however, because the temporal relationship of these exposures with the onset of asthma was unknown.33
Immediate hypersensitivity to dust mite and cockroach allergens was a major risk factor for doctor-diagnosed asthma. Numerous studies indicate that immediate hypersensitivity to indoor allergens is a risk factor for asthma, but the specific allergen(s) implicated is often dependent on geography, urban residence, or socioeconomic status.4,,10,17,21 Our findings from a nationally representative survey indicate that sensitization to dust mite accounted for ∼520 000 excess cases, whereas sensitization to cockroach allergen accounted for ∼375 000 excess cases.
Sensitization to cat allergen was not a predictor for asthma. There are at least 2 reasons for this conflicting finding. First, families with a history of asthma or other allergic conditions may selectively avoid cats.33 Second, the variable “avoid or have allergies to pets” may be a marker for sensitization to cat allergen, but we were not able to distinguish between allergic reactions to cats and dogs for “avoiding or having allergies to pets.”
Immediate hypersensitivity to indoor allergens is considered to be causally associated with asthma exacerbations. The Institute of Medicine concluded that there is sufficient evidence of a causal relation between exposure to allergens produced by house dust mites, cockroaches and cats, and exacerbations of asthma in sensitized individuals.34 They also concluded that there is sufficient evidence of an association between exposure to dog allergens and exacerbations of asthma in sensitized individuals.34Still, it is not entirely certain that eliminating exposure to indoor allergens will prevent the development of asthma.
Exposure to environmental tobacco smoke is a potent risk factor for asthma in early childhood.8,,911–14,20In contrast, we found no association of exposure to environmental tobacco smoke with asthma in older children and adolescents. We did not, however, have a measure of maternal smoking—the most consistent marker for the adverse effects of exposure to environmental tobacco smoke.5,,9,11,14 Instead, we relied on serum cotinine levels and reported smoking for any adult in the household. Thus, these differences may either represent problems with the measurement of exposure to environmental tobacco smoke or a lack of any association of environmental tobacco smoke and asthma in older children.
Host factors associated with asthma included history of allergic rhinitis in the index child and family history of atopy. Allergic rhinitis, as measured by a history of hay fever or nasal eosinophilia, is a risk factor for the subsequent development of asthma.18,,35 Still, it is difficult to disentangle the diagnosis of allergic rhinitis as a risk factor for asthma or the result of environmental exposure that predisposes to both allergic rhinitis and asthma. Similarly, family history of atopy may represent shared genes or common environmental exposures that predispose to asthma. If susceptible children develop asthma only if they are exposed to allergens, then our estimates of the population-attributable risk for such exposures are low.
Black race was not a risk factor for asthma in this analysis. Some researchers found that black race was a risk factor for a higher prevalence of asthma,3,,20,36 whereas others reported that it was not a risk factor.37,,38 There are numerous potential confounders to explain these discrepant findings, such as access to health services and urban status that were not adequately measured in this survey.37 Additional research to address this complex question is warranted.
These results indicate that residential risk factors account for 44.4% of doctor-diagnosed asthma among older children and adolescents. Taken together, these and other data clearly show that asthma in childhood is inextricably linked with residential exposures. The elimination of residential risk factors, if causally associated with asthma, would have a profound effect on medical costs of asthma and, more importantly, on the health of children.
This work was funded by the US Department of Housing and Urban Development (Healthy Home Initiative) and by the Institutional National Research Service Awards 1T-32 PE-10027 and 2T-32 PE-12002 from the Bureau of Health Professions, Health Resources and Services Administration, Public Health Service, Department of Health and Human Services.
- Received October 3, 2000.
- Accepted January 29, 2001.
Reprint requests to (B.P.L.) Children's Hospital Medical Center, 3333 Burnet Ave, Cincinnati, OH 45229-3039. E-mail:
- NHANES =
- National Health and Nutrition Examination Survey •
- OR =
- odds ratio •
- CI =
- confidence interval
- Centers for Disease Control and Prevention
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- Copyright © 2001 American Academy of Pediatrics