Pollutants and Respiratory Illness in Infants
Fine Particulate Matter Pollution Linked To Respiratory Illness In Infants And Increased Hospital Costs
1Perry Sheffield (perry.sheffield{at}mssm.edu) is an assistant professor at the Mount Sinai School of Medicine, in New York City.
2Angkana Roy is a pediatrician at the Erie Family Health Center, in Chicago, Illinois.
3Kendrew Wong is a research assistant at the Mount Sinai School of Medicine.
4Leonardo Trasande is an associate professor and an assistant attending doctor at the Mount Sinai School of Medicine.
- ↵*Corresponding author
Abstract
There has been little research to date on the linkages between air pollution and infectious respiratory illness in children, and the resulting health care costs. In this study we used data on air pollutants and national hospitalizations to study the relationship between fine particulate air pollution and health care charges and costs for the treatment of bronchiolitis, an acute viral infection of the lungs. We found that as the average exposure to fine particulate matter over the lifetime of an infant increased, so did costs for the child’s health care. If the United States were to reduce levels of fine particulate matter to 7 percent below the current annual standard, the nation could save $15 million annually in reduced health care costs from hospitalizations of children with bronchiolitis living in urban areas. These findings reinforce the need for ongoing efforts to reduce levels of air pollutants. They should trigger additional investigation to determine if the current standards for fine-particulate matter are sufficiently protective of children’s health.
The most common cause of hospitalization for children younger than age one is bronchiolitis, an acute viral infection of the small air passages of the lungs called the bronchioles. The majority of children recover without complications, although the disease accounts for about 100,000 pediatric hospitalizations and 4,500 deaths each year. Inpatient care for this condition costs more than $500 million annually.1 Studies are increasingly documenting evidence of the role of outdoor air pollutants as a risk factor for this ailment.2–9
Previous Studies
Common Pollutants
The many studies linking air pollutants to negative health effects provide the backbone of evidence on which the Environmental Protection Agency (EPA) bases the National Ambient Air Quality Standards under the Clean Air Act.10 The air pollutants linked to pediatric respiratory disease, in general, are particulate matter, ozone, sulfur dioxide, nitrogen dioxide, and carbon monoxide, all of which are regulated by the Clean Air Act. Outdoor air pollution could contribute to the infectious disease bronchiolitis by causing ongoing inflammation in the lungs, which then could contribute to making what can be a mild infection a more severe one.11
Fine particulate matter (particles with a diameter less than 2.5 microns) has been the subject of much health research.12 Fine particulate matter gets into the air through natural processes such as volcanic eruptions, dust storms, and forest fires. Human activities such as burning gasoline, diesel, or other fossil fuels in vehicles, power plants, and other industrial processes also produce fine particulate matter. The smaller the particle, the farther into the lungs it can penetrate when inhaled, thereby affecting more of the lung tissue and potentially being absorbed from the lungs into the blood.
Duration Of Exposure
The duration of exposure may also be important. Acute exposure—a few days or less—to air pollutants has been consistently associated with bronchiolitis-related clinic visits and hospitalizations.5,8,9 However, fewer studies have associated subchronic exposure—more than thirty days—with bronchiolitis episodes. A study in the Czech Republic found that children younger than age two had an increased bronchitis risk from exposure to subchronic fine particulate matter.3 An Italian study identified a positive association between parents who reported increased automotive traffic and the occurrence of bronchiolitis in their children during the first two years of life.2
In North America, studies limited to single geographic areas have found chronic exposures—more than one year—to air pollution to be a health concern. For infants this is typically represented by “lifetime” exposure, which is the average of all daily or monthly averages of various pollutant levels for the lifetime of the infant. Catherine Karr and colleagues6 examined a population of infants in British Columbia and found a positive association of both lifetime and prior-month exposure to nitrogen dioxide, sulfur dioxide, and carbon monoxide with bronchiolitis episodes.
In a western Washington State study that looked at lifetime as well as shorter exposures to fine particulate matter and nitrogen dioxide, positive but nonsignificant associations were seen between these air pollutants and the risk of hospitalization for bronchiolitis among children up to age one.7 Nonsignificant association means that although almost all odds ratios were greater than 1, the 95 percent confidence intervals crossed 1. Thus, there is less than 95 percent confidence that the observed association could have occurred by chance, and the results should be interpreted with caution.
In Southern California (including Orange County and parts of Los Angeles, San Bernardino, and Riverside Counties), an area of higher ambient air pollution levels, infant bronchiolitis requiring hospitalization was associated with lifetime and month-prior-to-hospitalization average exposures to fine particulate matter but not carbon monoxide or nitrogen dioxide exposures.4
This Study’s Approach
A major limitation of past studies is their focus on one geographic area, especially because, as a result of regional variation, findings from the western United States and southwestern Canada may not be generalized to the entire United States. Fine particulate matter has been documented to have varying effects on hospital admissions for cardiovascular disease among adults, based on season and location within the United States. These varying effects may represent the different chemical composition of particulate matter in different parts of the country. This increases concern about the accuracy of extrapolating results from single-region studies.11,13
We therefore decided to link two nationally representative data sets on hospitalizations and air quality to better explore the association between outdoor air pollution and bronchiolitis.14,15 Our analysis also assessed the variable effect of differing lengths of exposure to fine particulate matter on bronchiolitis.
Study Data And Methods
We undertook a multiyear, cross-sectional study, including hospitalizations between 1999 and 2007 for children ages one month to one year with a primary diagnosis of bronchiolitis. Hospitalizations with no corresponding air pollutant data were excluded.
The Institutional Review Board/Program for the Protection of Human Subjects at our institution deemed that this study was not considered human research according to federal regulations and was exempt from review. The study analyzed data from a previously collected, publicly available, deidentified data set.
Databases
The hospitalization data came from the 1999–2007 Nationwide Inpatient Sample. This sample is the largest data set available to measure the costs of bronchiolitis hospitalization in the United States.14 It is a valuable tool for examining health care resource use at the national level. The air pollution data came from the largest national data set on air pollution: the EPA’s Air Quality System.15
These data sets were merged, representing a unique opportunity to examine the national economic costs of health care resource use in association with air pollution. Because the Nationwide Inpatient Sample does not contain identifying information about patient residence, air pollutant levels were determined for a defined area surrounding hospitals where infants with bronchiolitis were admitted. The Appendix contains more detailed information regarding these databases and calculations.16
Outcomes: Hospitalization Data
Outcomes in this study included length-of-stay, total charges, and total costs for infant bronchiolitis hospitalizations. The length-of-stay for each admission was provided in days. Total charges represent the amount billed for each hospitalization. Charges were controlled for inflation by adjusting to 2005 dollars using the Medical Care Consumer Price Index from the Bureau of Labor Statistics.17 Costs represent the amount of money actually paid to the hospital, which, in general, is much less than the hospital’s charges.
Because data on costs are not directly collected, cost estimates were created using specific files that accompany the Nationwide Inpatient Sample, called group-weighted cost-to-charge ratio files.18 Further details are provided in the Appendix.16
Predictor Variables: Air Pollutants
The main predictor of infant bronchiolitis hospitalizations was the average level of ambient fine particulate matter. To calculate monthly average air pollutant levels, we averaged data from all monitors located within ten miles of the hospital at which each hospitalization occurred. Specifically for fine particulate matter, personal air monitoring has shown high correlation with ambient levels within an approximately twelve-mile (twenty-kilometer) radius of the central monitor.19,20
We performed correlations among the pollutants to determine which ones to include in multivariable analyses. Any two pollutants correlated with each other very strongly were not included together in multivariable models. We prioritized the inclusion of fine particulate matter and ozone, which are the pollutants with the strongest evidence linking them to adverse respiratory outcomes.
In our preliminary analyses using three pollutants (fine particulate matter, ozone, and nitrogen dioxide), we identified a positive association with exposure to fine particulate matter. We explored this association further by examining the effect of increasing durations of exposure to fine particulate matter, also known as increasing chronicity of exposure. Fine particulate matter two-month averages (which included the month of admission and the month prior) as well as three- to eleven-month averages were calculated and linked to the hospital data. To calculate the lifetime average of fine particulate matter, the monthly averages for as many months as the child was old were averaged and then also linked to the hospital data.
Statistical Analyses
Because of a skewed distribution, we calculated the logarithm of total charges and costs to base ten, which changes the distribution of those variables to be more appropriate for use in our model. Air pollutants determined from our initial analysis were included in the regression models.
We also included other factors associated with bronchiolitis outcomes and hospital charges: age; race or ethnicity (white, black, Hispanic, Asian/Pacific Islander, Native American, or other); sex; income; insurance (Medicare, Medicaid, private, self-pay, no charge, or other); hospitals’ US region (Northeast, South, Midwest, or West); hospitals’ location (urban, rural); hospitals’ teaching status; and month of admission. As a proxy for income, we used a variable included in the Nationwide Inpatient Sample, which is the median household income quartile for a patient’s ZIP code.
To validate findings between air pollutants and bronchiolitis outcomes, we ran similar multivariable models for the infectious diarrheal illness gastroenteritis, which is a frequent cause of infant hospitalization that should have no association with changes in air pollutant levels. We hypothesized that no significant relationships would be found between air pollutants and gastroenteritis.
Limitations
One limitation of this approach is that patients’ addresses were not available in the Nationwide Inpatient Sample; therefore, we used hospital ZIP codes to determine location, which is not an exact measure of personal exposure. However, previous studies have shown that fine particulate matter levels measured at central monitoring sites correlate well with average personal exposure.19–21
Results
Hospital Admissions
Between 1999 and 2007, there were 70,052,217 hospital admissions in the Nationwide Inpatient Sample; 156,889 were for infants, ages one month to one year, with a primary diagnosis of bronchiolitis. Hospital admissions with no corresponding air pollutant data were excluded, resulting in a final sample of 47,822 hospitalizations.
Compared to all infant bronchiolitis hospitalizations, hospitalizations included in the analysis had more patients who were black or Hispanic, were more likely to be in teaching hospitals, were almost exclusively located in urban settings, and were less likely to be in the South and Midwest (Exhibit 1). However, these differences were attributed to the national distribution of air monitors, which are more numerous in more densely populated areas. Many states do not report race data to the Nationwide Inpatient Sample, and this variable was unreported for a large percentage of patients.22,23
View this table:
Exhibit 1
Characteristics Associated With Infant Bronchiolitis Hospitalizations In The Nationwide Inpatient Sample, 1999–2007
Hospital Charges And Costs
The mean total charge for infant bronchiolitis hospitalizations was $14,027, with a maximum charge of $967,799. The median charges and interquartile range were $7,909 and $9,268, respectively. The mean total cost was $5,493; the maximum cost was $446,077. The median costs and interquartile range were $3,173 and $3,513, respectively.
Air Quality Monitoring
Regarding the air monitoring around the hospitals, 1,309 of 2,426 hospitals in the sample from the years 1999–2007 had at least one fine particulate matter monitor for at least one year. Of those hospitals, the median number of air monitors within ten miles was 2, with a mean of 2.9, a maximum of 18, and a standard deviation of 2.8. The average distance of air monitors to the hospitals was 5.5 miles. Although it was difficult to make direct comparisons to national air quality standards because of different averaging times, the mean fine particulate matter and nitrogen dioxide levels (monthly averages) were slightly above the annual standard (as defined by the EPA), and the maximum monthly ozone level was below the eight-hour maximum standard, as shown in the Appendix.16
Among the different air pollutants, fine particulate matter and particulate matter with a diameter less than ten microns were most highly correlated. Sulfur dioxide and carbon monoxide were negatively correlated with ozone, and fine particulate matter and carbon monoxide were positively correlated, as shown in the Appendix.16 As mentioned above, we prioritized fine particulate matter and ozone for inclusion in final models because of a priori hypotheses about bronchiolitis morbidity. Therefore, after excluding one from each pair of highly correlated pollutants, we included fine particulate matter, ozone, and nitrogen dioxide in the multivariable analyses.
In multivariable analyses, the one-month averages of the three pollutants and the lifetime average of fine particulate matter were not significant predictors (defined as ) of length-of-stay. Monthly fine particulate matter was nearly significant as a predictor of charges and was weakly significant for costs. Neither ozone nor nitrogen dioxide was significantly associated with charges or costs.
Duration Of Exposure
To examine the effect of increasing durations of exposure, we explored the association of increasing months of exposure to fine particulate matter and increasing incremental hospitalization charges (Exhibit 2). Monthly averages and associations of one to eleven months are shown in the Appendix.16
Exhibit 2
Association Of Exposure To Outdoor Fine Particulate Matter And Bronchiolitis Hospital Charges For Infants
SOURCE Authors’ analysis of data from the Agency for Healthcare Research and Quality Nationwide Inpatient Sample and the Environmental Protection Agency Air Quality System (see Notes 14 and 15 in text). NOTES Dollar amounts represent additional charges per each microgram/cubic meter increase in fine particulate matter. Sample sizes and p values are as follows: 1: , ; 2: , ; 3: , ; 4: , ; 5: , ; lifetime: , .
Lifetime average exposure to fine particulate matter was positively associated with both charges and costs. A one-unit (micrograms per cubic meter) increase—approximately 3 percent above the twenty-four-hour fine particulate matter standard (thirty-five micrograms per cubic meter) and 7 percent above the annual standard (fifteen micrograms per cubic meter)—in lifetime fine particulate matter led to a $285 increase in charges and a $127 increase in costs (Exhibit 3; see the Appendix for comparison with National Ambient Air Quality Standards).16
View this table:
Exhibit 3
Multivariable Results For Infant Bronchiolitis Hospitalization Charges And Costs As Predicted By Increase In The Level Of Fine Particulate Matter
These findings support the hypothesis not only that short-term exposure to particulate matter (the one-month average) is associated with more severe bronchiolitis, but that the longer duration—the average over the lifetime of the infant—shows a stronger effect. Monthly ozone and nitrogen dioxide averages were not significant predictors of charges or costs. Possible reasons for this lack of association are discussed below. Other significant predictors of charges included race or ethnicity (Hispanic, Asian, or Pacific Islander) and hospital location in the South ( for all associations). This last finding could be indicative of increased vulnerability among certain populations or in certain geographic areas, although exploration of the underlying reasons for these associations was not possible with this data set.
To examine the association between air pollutants and gastroenteritis-related hospital charges, we ran the same analyses as for bronchiolitis. As we hypothesized, we found no significant association with fine particulate matter.
Discussion
Drawing from a national sample of hospital discharge data, we found a statistically significant association between lifetime levels of fine particulate matter around hospitals and total charges and costs for infant bronchiolitis hospitalizations. We interpret these findings to reflect greater use of health care resources as the result of more severe cases of bronchiolitis. As mentioned above, fine particulate matter could contribute to smoldering inflammation in the lungs of exposed infants and result in a more severe illness when these infants contract bronchiolitis.
We found no association between monthly averages of exposure to fine particulate matter and gastroenteritis charges, thereby supporting the hypothesis that the association seen between air pollution and bronchiolitis is not spurious. Also of interest is the lack of statistically significant association seen between monthly averages of exposure to fine particulate matter and length-of-stay. A possible explanation for this last observation might be that length-of-stay measures are too coarse (measured in days, not hours) to be associated with small changes in monthly fine particulate matter. Although length-of-stay contributes to overall charges, other factors such as kinds of procedures performed, medication used, and intensity of care likely contribute more to the differences in charges between hospitalizations. Unfortunately, variables for assessing these factors are limited or not available in the Nationwide Inpatient Sample.
Our sample differed, as stated, from the entire sample of infant bronchiolitis hospitalizations because it represented primarily a bicoastal urban population, which should be considered when generalizing these findings. The race or ethnicity (more black or Hispanic) and type of hospital (more teaching hospitals) differences of our sample compared to all infant bronchiolitis hospitalizations are thought to be primarily a result of demographics and hospital characteristics within dense urban settings.
A major strength of this study is that our results are based on a large amount of data that are nationally representative of urban area hospitals. Although these results cannot be translated to nonurban areas, 80 percent of bronchiolitis hospitalizations do occur in urban areas.24 Substantial health care dollars are spent each year on bronchiolitis,1 and better control of fine particulate matter levels may result in considerable savings.
We found that for every level of increase in fine particulate matter, infant bronchiolitis hospitalization costs increased on average by $127. At first this may not seem like a lot, but there are approximately 150,000 infant bronchiolitis hospitalizations in the United States annually. If we extrapolate our findings to urban infant bronchiolitis hospitalizations (80 percent of 150,000 equals 120,000), reducing the average level of fine particulate matter by just one unit—or 7 percent below the current annual standard— could save about $15 million annually.
Our study findings are consistent with some studies that point to an association between bronchiolitis severity and particulate matter. The lack of association observed in some of the other studies between bronchiolitis and fine particulate matter could reflect a lack of regional variability, as all previous studies examined only a single airshed or region; overall lower particulate matter levels; or variations in the actual toxicity of the specific type of particulate matter in that region, as discussed in other studies.6
The lack of association that we found with bronchiolitis and ozone was consistent with the two prior studies in which this pollutant was included.4,6 In contrast to some other studies discussed at the beginning of this article, we found a lack of association between nitrogen dioxide and bronchiolitis charges and costs. These differing results could reflect a true lack of association, or they could reflect limitations of the exposure metric. One explanation is that as shown in previous studies, ambient ozone levels measured at central monitoring sites might not be representative of personal exposure, in contrast to ambient fine particulate matter levels, which are highly correlated with personal exposure.19–21
These estimates represent only a small fraction of potential health care savings that might result from reduced fine particulate matter levels, given that there are a number of other illnesses, such as cardiac mortality, associated with this pollutant.25–27 One study quantified the affect of deaths associated with fine particulate matter from traffic congestion in eighty-three major US cities. It estimated that the public health impact from this outcome alone was valued at $31 billion.28 Our study underscores the economic impacts of particulate matter on the use of health care resources. Furthermore, the findings indicate that fine particulate matter could have far-reaching environmental health effects for children, but the extent is still unknown based on this preliminary study.
Studies such as ours merit further research, using more rigorous exposure assessments and data sets containing more detailed information about the specifics of health care use. Our findings should stimulate further research into the role of air pollution in infectious disease severity, to confirm and better understand the disease mechanism that underlies the association of fine particulate matter and increased bronchiolitis and therefore increased costs for bronchiolitis care. Additional research could encourage regulatory agencies such as the EPA to more fully consider the effect of long-term exposure to air pollutants when reevaluating air pollutant standards. Our results provide economic data to reinforce the need for ongoing efforts to reduce levels of air pollutants in the United States.
Acknowledgments
Angkana Roy and Perry Sheffield were funded by the National Institutes of Health Research Training Grant in Environmental Pediatrics (NIH 5T32 HD0049311). The study was funded by the Mount Sinai Children’s Environmental Health Center.
ABOUT THE AUTHORS: PERRY SHEFFIELD, ANGKANA ROY, KENDREW WONG & LEONARDO TRASANDE
In this issue of Health Affairs, Perry Sheffield and her coauthors report on their study of the relationship between the presence of air pollutants and the development of bronchiolitis in young children. This acute viral infection of the bronchioles in the lungs leads to 100,000 pediatric hospitalizations annually. They found that as the average amount of pollution increased, so did hospital charges and health care costs associated with the ailment.
The authors were surprised to learn that the association between fine particulate matter and bronchiolitis hospitalization costs grew stronger as the duration of exposure increased. Although air pollution is also associated with chronic illnesses, bronchiolitis is a disease of relatively short duration. Sheffield believes that the discovery should lead researchers to think more broadly about the impact of environmental exposures on health and health care costs.
Sheffield and her colleagues Angkana Roy and Leonardo Trasande came to this project because, as pediatricians, they are acutely aware of the burden of bronchiolitis on infants and on the health care system.
Sheffield is an assistant professor in the Mount Sinai School of Medicine’s Departments of Pediatrics and Preventive Medicine. She received her medical degree from the Medical College of Georgia and a master of public health degree from the Mount Sinai School of Medicine.
Roy, a pediatrician at the Erie Family Health Center, in Chicago, is on the faculty at Northwestern University and Children’s Memorial Hospital as a clinical pediatrician. She received her medical degree from the Columbia University College of Physicians and Surgeons and a master of public health degree from the Mount Sinai School of Medicine.
Kendrew Wong served as a research assistant on this study. He graduates in the spring of 2011 from Boston College with a bachelor’s degree in mathematics and economics.
Trasande is an associate professor and an attending doctor at Mount Sinai School of Medicine, where he specializes in preventive medicine and pediatrics. He has served as the codirector of the Children’s Environmental Health Center at Mount Sinai, and he sat on the steering committee of the National Institute for Child Health and Human Development’s National Children’s Study, a longitudinal study of environmental exposure on children that is sponsored by the National Institutes of Health.
Trasande is lead author of another article in this issue of Health Affairs, addressing the costs of environmental diseases in children. He received both his medical degree and a master’s degree in health care policy from Harvard University.
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Published online before print May 2011, doi: 10.1377/hlthaff.2010.1279 Health Aff May 2011 10.1377/hlthaff.2010.1279
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