PEDIATRICS Vol. 122 No. 6 December 2008, pp. 1196-1203 (doi:10.1542/peds.2007-2231)
ARTICLE |
Descriptive Epidemiological Features of Bronchiolitis in a Population-Based Cohort
a School of Environmental Health
b School of Population and Public Health
e Centre for Health Services and Policy Research, University of British Columbia, Vancouver, Canada; Departments of
c Pediatrics
d Environmental and Occupational Health Sciences, University of Washington, Seattle, Washington
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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OBJECTIVE. The goal was to investigate the epidemiological features of incident bronchiolitis by using a population-based infant cohort.
METHODS. Outpatient and inpatient health records were used to identify incident bronchiolitis cases among 93 058 singleton infants born in the Georgia Air Basin between 1999 and 2002. Additional health-related databases were linked to provide data on sociodemographic variables, maternal characteristics, and birth outcome measures.
RESULTS. From 1999 to 2002, bronchiolitis accounted for 12 474 incident health care encounters (inpatient or outpatient contacts) during the first year of life (134.2 cases per 1000 person-years). A total of 1588 hospitalized bronchiolitis cases were identified (17.1 cases per 1000 person-years). Adjusted Cox proportional-hazard analyses for both case definitions indicated an increased risk of incident bronchiolitis in the first year of life (follow-up period: 2–12 months) for boys, infants of First Nations status, infants with older siblings, and infants living in neighborhoods with smaller proportions of maternal postsecondary education. The risk also was elevated for infants born to young mothers (<20 years of age) or mothers who did not initiate breastfeeding in the hospital. Infants with low (1500–2400 g) or very low (<1500 g) birth weight and those with congenital anomalies also had increased risk. Maternal smoking during pregnancy increased the risk of hospitalized bronchiolitis.
CONCLUSIONS. This population-based study of the epidemiological features of bronchiolitis provides evidence for intervening with high-risk infants and their families. Clinical and public health interventions are recommended for the modifiable risk factors of maternal breastfeeding and smoking and for modification of vulnerable environments where possible (eg, limiting exposure to other young children), during high-risk periods such as the first few months of life or the winter season.
Key Words: bronchiolitis • epidemiological features • cohort studies • population-based studies • Cox proportional-hazards models
Abbreviations: RSV—respiratory syncytial virus
Bronchiolitis is an infection of the lower respiratory tract that usually affects infants in the first year of life.1 The most common cause of bronchiolitis is respiratory syncytial virus (RSV) (
90% of cases in North America).2 However, a number of other respiratory viruses (such as influenza, parainfluenza, rhinovirus, human metapneumovirus, and bocavirus) also can cause bronchiolitis. Bronchiolitis is the leading cause of morbidity among infants <1 year of age in North America and Europe,1,3–6 and hospital admission rates have been increasing over the past 2 decades.1
Given the frequency and burden of illness, there are very few population-based, epidemiological studies of risk factors associated with bronchiolitis. A Medline search identified 1811 articles focused on "bronchiolitis" or "bronchiolitis, viral," of which 468 were focused on "infant" or "child." Of those, 72 were on "risk factors" or "epidemiology" of bronchiolitis. A review of the abstracts for those 72 articles identified 21 that provided epidemiological evidence of risk factors for the primary onset of bronchiolitis, as opposed to articles on clinical outcomes among children with bronchiolitis,7 diagnostic or clinical practice guidelines,8 bronchiolitis as a risk factor for other outcomes such as asthma,9 review articles,10 or editorials.11
Of the 21 articles on the epidemiological features of bronchiolitis, 11 were cross-sectional clinical studies (eg, hospitalized sample),12–22 9 were case-control or case-crossover studies,23–31 and only 1 was a population-based study.32 One additional clinical study was identified from study references.33 The majority of the studies investigated hospitalization or mortality outcomes for bronchiolitis, with 2 exceptions; 1 study included outpatient visits as part of a combined outcome,19 and the population-based study32 investigated RSV-positive test results via outpatient physician visits. The populations for the clinical studies ranged from 89 hospitalized infants20 to 8265 hospitalized infants16 with the exception of a national study of emergency department visits, with almost 2 million hospitalization outcomes over 10 years.22 The case-control studies ranged from 34 pairs30 to 18 595 case subjects with 10 matched control subjects.27
The population-based, 1-year, follow-up study of 1179 healthy infants identified male gender and <1 month of or no breastfeeding as risk factors for RSV infection in multivariate models adjusted for sociodemographic factors.32 It also found a protective interaction effect for breastfeeding among mothers with a lower education level. Studies of clinical populations indicate that native or aboriginal infants (eg, First Nations or Inuit)13,17 have higher rates of hospital admissions related to bronchiolitis, although this may be attributable to unmeasured socioeconomic factors rather than genetic factors. Bronchiolitis (and RSV) is also more common in male infants,13,32 infants of low birth weight or gestational age,14,15,17,18,23,25,30,33 and infants born to young mothers.18,19 It is associated with no breastfeeding or early weaning,23,25,29,32 living in crowded conditions or in the presence of older siblings14,18,30,32,33 or attending day care,14 exposure to secondhand smoke or tobacco during pregnancy,18,19,23,33 and social disadvantage.16,26,32 Case-control studies identified environmental exposures associated with the risk of bronchiolitis, including exposure to wood-burning in the home24 and air quality measures (2.5-µm particulate matter levels).27
The purpose of this study was to conduct a large, population-based, epidemiological study of a comprehensive set of concurrent risk factors for bronchiolitis, including both hospitalizations and outpatient visits to physicians. Although bronchiolitis is common, there are limited population-based studies on the epidemiological features of this condition, and little is known about what causes infants to be susceptible to infection in the general population.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Overview
This was a retrospective cohort study of infants born between 1999 and 2002 in the geographic area defined as the Georgia Air Basin, British Columbia (N = 119 345). The analysis excluded multiple births and births of <25 weeks of gestation (n = 2606). A total of 14 488 births were excluded because of missing data on maternal age or First Nations status and 9193 births because of incomplete residential history (because this cohort was the basis for a study investigating residential air pollution exposures and risk of bronchiolitis), for a final study population of 93 058 births.
Data Sources
Health data are available from the British Columbia Linked Health Database for research purposes, through an approved process34 governed by a data access agreement between the researchers and the data stewards. Medical services and hospitalization data were provided and governed by the Ministry of Health, Government of British Columbia, and vital statistics data by the British Columbia Vital Statistics Agency. These data were merged, through an additional data access agreement, with records in the provincial perinatal database, governed by the British Columbia Reproductive Care Program. The research database was constructed by merging vital statistics birth records (for cohort enumeration according to residential postal codes) with outpatient medical services billing records and inpatient hospital discharge records, for identification of cases for the period of 1999–2003 (allowing a minimum of a 1-year follow-up period for all births). Birth and health records were merged with the provincial perinatal database for maternal characteristics (maternal age, infant age, breastfeeding initiation, smoking during pregnancy, and parity) and birth outcome measures (gestational age, preterm complications, and low birth weight complications). First Nations status was available from hospital discharge records for all births, with socioeconomic indicators for education and household income from Statistics Canada census data. The research database was provided to the research team with all personal identifiers removed and replaced by anonymous study identifiers. The identifiers were unique to each infant and enabled identification of the same infants across data sources. The research protocol was approved by the University of British Columbia Behavioral Research Ethics Committee.
Outcomes
Infants were monitored from the second to 12th month after birth, and cases were identified from the first health care encounter with an International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis code35 of 466 (acute bronchitis and bronchiolitis) in the outpatient medical charts (general practitioner or specialist visit) or a principal diagnosis code of 466.1 (acute bronchiolitis) in the hospital discharge records. Only the first encounter (either outpatient visit or hospitalization) for each infant was counted as the case. The outpatient medical services records allow for 1 diagnosis code, coded to the first 3 digits only of the International Classification of Diseases, Ninth Revision, Clinical Modification coding system, which necessitated the broader inclusion criteria for this data set. A second case definition was limited to hospitalizations only, with the more-specific diagnosis code of 466.1. Only the first hospitalization was counted as the case. These data do not include emergency department visits unless they resulted in a hospital admission. The databases are considered comprehensive for outpatient and inpatient encounters, given a universal, publicly funded, health care system.
Risk Factors
The analyses investigated the risk of a first clinical encounter related to bronchiolitis associated with infant gender, maternal age (<20 years, 20–29 years, or >29 years), maternal education (in quartiles), household income (in quintiles), urban versus rural residence, maternal smoking during pregnancy, breastfeeding initiation in the hospital, First Nations status, parity (yes or no, as a proxy measure for older siblings), birth weight (normal: 2500–4000 g; low: 1500–2500 g; very low: <1500 g; high: >4000 g), gestational age (25–28 weeks, 29–32 weeks, 33–35 weeks, or 
36 weeks), preterm complications (yes or no), and low birth weight complications (yes or no). Urban residence, based on census data, is defined as living in an area with >400 people per km2.36 Education and household income variables, also based on census data, represent the distribution of median household incomes (in quintiles) and the proportion of the population with postsecondary education (in quartiles) according to neighborhood (ie, census subdivisions). These census variables were assigned to infants on the basis of their mother's postal code of residence within a neighborhood.
Analysis
Follow-up monitoring was from the second to 12th month of life; the first month of life was excluded because bronchiolitis infection is not common among infants in the first month18 and exclusion reduces misclassification of other acute respiratory infections. The Cox proportional-hazard model37 was used to investigate the association between risk factors and an infant's first clinical encounter related to bronchiolitis. Factors associated with bronchiolitis at the bivariate level (95% confidence interval for the hazard rate ratio) were entered into the final multivariate model. Models were constructed for both case definitions of bronchiolitis, for comparison purposes.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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The study cohort included 93 058 singleton births in the Georgia Air Basin between 1999 and 2002 with complete data. The cohort was 48.6% female, 1.2% of First Nations status, and 45.9% firstborn. Eighty-two percent of infants had a normal birth weight (2500–4000 g), and 89.0% were born at term (gestational age of >38 weeks). Less than 10% of infants had complications related to either preterm status (7.1%) or low birth weight (6.7%). Less than 1% of the study cohort had congenital anomalies. Maternal smoking during pregnancy was recorded for 9% of the birth cohort, and lack of breastfeeding initiation at the hospital was recorded for 7.5% of the cohort. The majority (57.3%) of infants were born to mothers
29 years of age. The excluded population had similar proportions of female infants (48.5%) and mothers in the lowest education quartile (25.9% vs 24.0%) and household income quintile (21.9% vs 21.6%) but a larger proportion of infants of First Nations status (2.9%). A total of 12 474 incident bronchiolitis cases (134.1 cases per 1000 person-years) were identified from outpatient and inpatient encounters among cohort infants during the first year of life (second to 12th month). A total of 1588 bronchiolitis cases were identified from hospitalizations only (17.1 cases per 1000 person-years). The rates of bronchiolitis were higher in the excluded population (146.1 and 23.1 cases per 1000 person-years, respectively).
An analysis of bronchiolitis cases according to calendar month of diagnosis (Fig 1) and age of diagnosis (Fig 2) indicated that incident cases occurred more frequently during the winter months (December through March) and in the first months of life. The same trends were observed for bronchiolitis defined on the basis of outpatient visits as noted for hospitalizations.
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The distributions of risk factors between infants with and without bronchiolitis, by outpatient and inpatient case definitions, are shown in Table 1. Because of quantitative correlations or conceptual overlap between the measures of maternal education and household income (Spearman's
= 0.43), gestational age and birth weight (Spearman's = 0.30), congenital anomalies and preterm complications (Spearman's = 0.32), and low birth weight complications and preterm complications (Spearman's = 0.97), only maternal education, birth weight, and congenital anomalies were entered in the final multivariate models.
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In the final regression models adjusted for covariates (Table 2), the risk of incident bronchiolitis in the first year of life remained elevated for male infants, infants of First Nations status, infants with older siblings, and infants living in neighborhoods with smaller proportions of maternal postsecondary education (lowest quartile, compared with highest quartile). The risk was also elevated for infants born to young mothers (<20 years versus 20–29 years of age) and mothers who did not initiate breastfeeding in the hospital. Infants with a low (1500–2400 g) or very low (<1500 g) birth weight and those born with a congenital anomaly also had an increased risk of bronchiolitis. The hazard rate ratios for all of the preceding risk factors were higher in the model of hospitalized bronchiolitis cases, compared with the combined inpatient and hospitalized definition, with an approximately twofold increased risk observed for infants with older siblings and a congenital anomaly, a threefold increased risk associated with First Nations status, and a sixfold increased risk associated with very low birth weight (<1500 g, compared with 2500–4000 g). An elevated risk of bronchiolitis associated with maternal smoking during pregnancy remained significantly elevated in the model for hospitalized bronchiolitis only (hazard rate ratio: 1.49; 95% confidence interval: 1.27–1.72).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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This is the first study to evaluate the epidemiological features of bronchiolitis in Canada by using a population-based cohort, a comprehensive set of risk factors through linkage of several longitudinal and retrospective databases, and the inclusion of outpatient visits in the case definition. Our data suggested that 13.4% of singleton infants born in the Georgia Air Basin had incident bronchiolitis requiring a clinical encounter within the first year of life and 1.7% of cases were serious enough to warrant hospitalization. This rate is lower than previously reported rates of acute hospitalized bronchiolitis for Canadian infants5,38 and for infants in other countries,16,22 although the lowest rates were reported in the province of British Columbia (2.5%).38 The previous studies were not limited to first encounters for calculation of hospitalization rates, and others studies tended to use a broader definition of hospitalized bronchiolitis.22 The prevalence of hospitalized bronchiolitis in this study is closer to bronchiolitis rates in other studies that used a confirmed RSV lower respiratory tract infection outcome.32,38 However, 2.3% of our excluded population met the hospitalized case definition, an estimate closer to previous reports for British Columbia,38 which may indicate a conservative bias in the current findings. Comparable population-based studies are limited, but one using physician visits as the first point of contact32 indicated a comparable overall bronchiolitis rate of 10.4% in a study of 1179 infants.
Our study used administrative health records to capture outpatient visits and hospitalizations for bronchiolitis, as well as administrative databases for infant and maternal characteristics. An assessment of the validity and reliability39 of key variables captured in the perinatal database (relative to patient charts) indicated good sensitivity and specificity for maternal smoking status (79% and 98%, respectively) and breastfeeding initiation (95% and 73%, respectively). In addition, the breastfeeding initiation rate of 92.5% in the current study parallels the population estimates for breastfeeding (of any duration) reported by women in the Canadian Community Health Survey for the province of British Columbia (93.1%) and the city of Vancouver (90.4%),40 the most densely populated area of the study region. The survey data also indicated that the majority (81.8%) of women in Vancouver who breastfeed do so for 6 months.
The validity and reliability of coding for bronchiolitis have not been established for these data sources, but the consistency of findings between the more-specific hospitalized bronchiolitis definition and the bronchiolitis definition that included outpatient visits supports the validity of using outpatient records to capture cases. In addition, bronchiolitis cases followed recognized seasonal6 and temporal41 patterns for infection for both outpatient and inpatient case definitions. Higher risk estimates for all significant variables for hospitalized bronchiolitis may indicate greater specificity for more-severe inpatient cases and some misclassification of respiratory illness by using the outpatient administrative data records. However, we conclude from our results that outpatient visits provide a reasonable measure of bronchiolitis in the general population and that estimates based on only clinical populations and hospitalized cases may underestimate the incidence and burden of disease in the general population (13.4%, compared with 1.7%, in the current study), even with a degree of misclassification with the 3-digit diagnostic code of 466 in the present study.
We did not have confirmation of RSV infection among bronchiolitis cases. Therefore, our case definition represents the multitude of viral causes. We were interested in the outcome of bronchiolitis in general, as a public health burden, and not risk factors for a specific etiologic agent.
Our data confirm previous findings, based on smaller clinical populations, that the risk of bronchiolitis is seasonal and is associated with male gender, younger maternal age, lower maternal socioeconomic status, low birth weight, parity (as a surrogate measure for older siblings in the home), no breastfeeding initiation at the hospital, and First Nations status. Maternal smoking during pregnancy and congenital anomalies also were associated with increased risk of bronchiolitis, but only for cases severe enough to result in hospitalization.
An increased risk of bronchiolitis for First Nations infants is consistent with previous findings of higher hospitalization rates for bronchiolitis among Native American and Alaskan infants13,16 and among Inuit infants.17 It is not clear, on the basis of previous studies, whether this increased risk is attributable to cultural differences (ie, differences in breastfeeding patterns), reduced access to health care in remote areas,42 or environmental exposures such as indoor air pollution (wood smoke).24 However, an independent effect for First Nations status was found in the current study after adjustment for breastfeeding and socioeconomic factors, in an area with a universal health care system. The observed increased risk may still be attributable to residual confounding or unmeasured covariates, including respiratory system or immune system susceptibility. Infants with compromised physiological features,43 as indicated by the presence of congenital anomalies, had an increased risk of hospitalized bronchiolitis in the current study.
It is important to note that our study variable identified only individuals with First Nations status (registered with the Canadian government for services and benefits) and underrepresented individuals who identified themselves as native or aboriginal persons. According to 2001 statistics, 1.9% of the population in the greater Vancouver region is aboriginal (including North American Indian, Métis, and Inuit persons), compared with 1.2% with First Nations status for those <1 year of age in the study cohort, and the proportion of aboriginal persons <4 years of age is probably greater, given a younger age distribution than in the overall population.44 Indeed, we observed a larger proportion of infants of First Nations status (and a higher rate of bronchiolitis) in the excluded population, which indicates that hazard rate ratios may be underestimated in the current study.
We observed an elevated risk for younger gestational age in the bivariate regression analyses and for the correlated variable of birth weight in the multivariate analyses. Younger infants, including premature infants, are thought to be susceptible to viral infections as a result of missing the transplacental transfer of antibodies.45–47 Our finding of a protective effect for mothers who reported breastfeeding initiation is consistent with the importance of the transfer of maternal antibodies to infants for reducing the risk of infection.45,48 Lower birth weight and young gestational age also may indicate a relatively immature immune or respiratory system, increasing susceptibility to infection.4,33
Maternal characteristics of younger age and lower socioeconomic status were identified previously but may be explained by reduced access to health care services,42 or lower rates of breastfeeding and smoking status49 among disadvantaged mothers. The current study identified an independent effect of younger maternal age after adjustment for breastfeeding initiation and an independent effect of socioeconomic status (education level) after adjustment for smoking status during pregnancy, among a cohort of mothers and infants with universal access to health care services. Although the independent effect of maternal age may be attributable to other, unmeasured, socioeconomic factors, it also may suggest a biological mechanism related to maternal nutrition, health status, or stress that alters the development of the respiratory system of the fetus. The independent effect of socioeconomic status may be a surrogate measure for important environmental exposures for infant respiratory outcomes27 worthy of further investigation, including both outdoor (eg, living near major highways, with increased exposure to poor air quality) and indoor (eg, wood smoke) air quality exposures. Measures of socioeconomic status (education level) were aggregate, neighborhood-level variables based on Census data and residence. This may result in some misclassification but is considered to be nondifferential in the current study and probably an issue of a 1-category difference, rather than misclassification from the lowest quartile to the highest quartile.
The finding that exposure to maternal smoking was associated with the risk of hospitalized bronchiolitis is in agreement with previous studies33 and specifically findings for more-severe infections.18,50 Maternal and paternal environmental tobacco smoke has been linked to reduced lung function and increased airway responsiveness, which may predispose infants to more-severe infections.51 Although it is likely that a large proportion of mothers who smoke during pregnancy continue to do so after birth, we had only a measure of maternal smoking during pregnancy. Although this is a potential limitation, our finding is consistent with a previous study linking maternal smoking during pregnancy with severe bronchiolitis outcomes (death)18 and provides evidence that smoking during pregnancy is itself associated with bronchiolitis.
We also found that a higher birth order (or parity) among infants was associated with bronchiolitis in the first year of life. Higher birth order is likely associated with having older siblings and/or sharing a room with siblings, which increases the likelihood of viral infection transmission. These specific factors were identified previously as risks for bronchiolitis and other respiratory tract infections6,33 and have some public health relevance for reducing risks associated with crowding during peak periods, especially in public facilities such as day care centers.
One of the main strengths of our study is the large sample that is representative of the population of British Columbia. Unlike most other studies, we investigated the epidemiological features of bronchiolitis by using a population-based sample and a wide range of variables concurrently. The comprehensive risk profile provides direction for recommendations to reduce the incidence and burden of bronchiolitis in the general population. From a public health perspective, interventions are warranted to increase breastfeeding initiation and to reduce maternal smoking (especially for reducing the numbers of more-severe, hospitalized cases). Clinicians can support parents to alter these modifiable risk factors, especially for high-risk infants (such as those born with low birth weight or born to young mothers) and during periods of higher risk (such as the first few months after birth and the winter season). In addition, public health practitioners and clinicians need to be aware of the entire environment of the infant and to advise families on making changes that might reduce the risk or severity (hospitalization) of bronchiolitis, such as limiting exposure to other young children or outdoor/indoor air pollution for at-risk infants during high-risk periods.
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ACKNOWLEDGMENTS |
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Dr Koehoorn was supported in part by the Michael Smith Foundation for Health Research Scholar Award. The research was supported in part by Health Canada via an agreement with the British Columbia Centre for Disease Control to the Border Air Quality Study, and by the Center for Health and Environment Research (CHER) at the University of British Columbia. CHER is funded by the Michael Smith Foundation for Health Research.
The linked research database was provided by the Centre for Health Services and Policy Research, University of British Columbia via the British Columbia Linked Health Database. Medical services and hospitalization data were provided by the Ministry of Health, Government of British Columbia; Vital Statistics data by the British Columbia Vital Statistics Agency; and perinatal data by the British Columbia Reproductive Care Program.
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FOOTNOTES |
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Accepted Mar 3, 2008.
Address correspondence to Mieke Koehoorn, PhD, Department of Health Care and Epidemiology, University of British Columbia, 5804 Fairview Ave, Vancouver, British Columbia, Canada V6T 1Z3. E-mail: mieke.koehoorn{at}ubc.ca
The authors have indicated they have no financial relationships relevant to this article to disclose.
| What's Known on This Subject In clinical populations bronchiolitis is associated with socio-demographic, clinical and environmental factors.
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| What This Study Adds To our knowledge, this is the first population-based study of bronchiolitis risk in Canada and one of few in the world. Cases included outpatient visits and hospitalizations.
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