Community urbanization and hospitalization of adults for asthma.

Introduction

It is estimated that 150 million people world-wide are living with asthma, including 15 million people in the United States (Mannino et al., 2002). Asthma has been defined as a "chronic inflammatory disease of the airways that involves many cells and cellular elements" (National Institutes of Health [NIH], 2003). The inflammation is accompanied by increased airway hyper-responsiveness to a variety of environmental stimuli that include airborne allergens, viruses, tobacco smoke, and particulate matter (Etzel, 2003; Sotir, Yeatts, & Shy, 2003). In Healthy People 2010, asthma is cited as a major clinical and public health problem (U.S. Department of Health and Human Services, 2000). One of the key objectives identified by that government document is reduction of environmental exposures that contribute to events, such as asthma hospitalization, associated with diminished lung function.

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Risk factors for asthma include

* gender and prior diagnosis of allergies (Arif, Declos, Lee, Tortolero, & White-head, 2003; National Center for Environmental Health [NCEH], 2003);

* communities with large populations, high household density, or both (Crain et al., 2002);

* proximity to heavy traffic patterns, although the extent to which such proximity contributes to asthma hospitalizations is not known (English et al., 1999; Garshick, Laden, Hart & Caron, 2003; Kim et al., 2004); and

* chronic exposure to nitrogen oxides and carbon monoxide, which have been documented to exacerbate the inflammatory response in asthmatics (Delfino, Gong, Linn, Pellizzari, & Hu, 2003; Ford, Heath, Mannino, & Redd, 2003; Gehring et al., 2002; Lin, Munsie, Hwang, Fitzgerald, & Cayo, 2002; Nicolai et al., 2003; U.S. Environmental Protection Agency [U.S. EPA], 2005).

Traffic-related air pollution accounts for much of the diminished air quality seen, especially in urban areas (Kunzli et al., 2003). Although emission standards are regulated by U.S. EPA, traffic volume and type are not (U.S. EPA, 2005). Heavy traffic patterns are a problem not only in large city centers, but also in areas of rapid suburban growth (Tibbetts, 2002). Thus, traffic "corridors" are becoming more common irrespective of their proximity to pre-existing communities (Lwebuga-Mukasa, Oyana, Thenappan, & Ayirookuzhi, 2004).

In the past decade, there has been a surge in adult asthma and associated complications. The factors contributing to this increase are poorly understood, although environmental factors associated with urbanization are suspect. Measurement of "urbanization" is, however, difficult. The study reported here assessed community urbanization by population size and density, the amount of vehicular traffic per day, and the total number of roads and highways. The authors tested the hypothesis that the degree of urbanization of six Pennsylvania counties, as measured by these criteria, is an environmental risk factor for adult asthma hospitalization.

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Methods

Selection of Counties

The Pennsylvania counties selected for this study were Allegheny, Dauphin, Erie, Fayette, Lancaster, and York. These counties were selected primarily as a sample of their varied distances to major urban centers (i.e., urban, suburban, rural). The authors further typified urbanization by considering both the population and the motor vehicle characteristics of an urban community. Four measures were used: total population, population density (persons/[mi.sup.2]), miles of roads/highways, and daily vehicle miles traveled. The population data were obtained from Census 2000, published by the U.S. Census Bureau (2005). The traffic-related information, obtained from the Pennsylvania Department of Transportation, consisted of miles of roads and highways and daily vehicle miles traveled in each county. The counties were ranked for urbanization on a scale of 1 to 6 with respect to population size and density, daily traffic density, and total miles of roads and highways. The overall urbanization rank of each county was determined by averaging of the scores for each of the four measures. The air quality of each county was evaluated with data from U.S. EPA's Toxic Release Inventory (U.S. EPA, 2000).

Case Definitions

Hospitalization data for adults 19-64 years of age were obtained from the Pennsylvania Health Care Cost Containment Council (PHC4) (PHC4, 2005). During this three-year period, asthma (ICD Code 493) was the primary diagnosis upon admission in 5,650 cases. To control for patients hospitalized more than once during a calendar year, the authors used the patient identifier code (a randomly generated number unique to each individual in the data set). Thus, the rate analysis used only one event per patient identifier code. The data set also included demographic descriptors that allowed calculation of age-specific and gender-specific asthma hospitalization rates.

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Data Analysis

Hospitalization rates per 10,000 people, age-standardized with respect to population data from Census 2000 (U.S. Census Bureau, 2005), were determined for asthma causes. Age-specific rates were calculated with the population counts also provided in the Census 2000. To make the data consistent with age-specific data published by the Centers for Disease Control and Prevention, the authors stratified population ages into three groups: 19-34, 35-44, and 45-64 years of age (NCEH, 2003). Poisson regression analysis was used to assess statistically significant contributions to the adult asthma hospitalization rates by each of the independent covariates (county rank, gender, and age). Previous studies have cited factors related to income and educational attainment as contributing to poor health outcomes (Boudreaux, Emond, Clark, & Camargo, 2003). Since the authors did not have such data for the individuals in the study population, the study employed graphical methods using Excel to describe the distribution of socioeconomic data for each county and the relationship of such data to adult asthma hospitalization rates within the county. Statistical analyses were performed with Stata 8.0 and Excel for determination of relative risk. All estimates of significance were at p = .05.

Results

The degree of urbanization of each county was evaluated according to the four measures described above. The results (Table 1) indicate that the rankings were consistent irrespective of the measure used. Allegheny County ranked first in each of the four categories. Fayette County ranked sixth in three of the four categories and fifth in the category of miles of roads and highways.

Age-adjusted adult asthma hospitalization rates (X/10,000) for each county are shown in Figure 1. The counties are ordered from left to right by decreasing rank of urbanization. The hospitalization rate initially decreases with decreasing urbanization, then increases as urbanization further decreases. Fayette County, which ranked as the least urbanized county, had an asthma hospitalization rate greater than that of Allegheny County, the most urbanized county.

Gender is recognized as a risk factor for asthma incidence and severity (Arif et al., 2003; Brogger et al., 2003), and the authors examined adult asthma hospitalization rates of males and females in each county (Figure 2). In all counties, females had higher hospitalization rates than males. In addition, an age-related trend of increasing hospitalizations was observed for females. Using Poisson regression, the authors assessed urbanization, gender, and age individually for their contribution to the adult asthma hospitalization rate within each county (Table 2). The results indicated that urbanization rank was not a significant contributor to the model (RR = 1.04, p = .131). Gender (RR = 3.34, p = .0001) and age (RR = 1.17, p = .016), however, were both statistically significant. A statistical model that included all three of the covariates was validated with a Chi-square goodness-of-fit test ([chi square] = 46.12, p = .0518, [r.sup.2] = .38), which indicated that the model was appropriate.

Socioeconomic factors have been associated with the frequency of asthmatic attacks (Boudreaux et al., 2003). Although individual data for these factors were not available, aggregate data at the county level were obtained from the 2000 U.S Census (U.S. Census Bureau, 2005). The county-specific profiles of these factors in relation to adult asthma hospitalizations are shown in Figure 3. There was a correlation between the hospitalization rate and the percentage of the population living below the federal poverty level (Figure 3A). An inverse relationship was observed for hospitalization and both median income and median property value (Figure 3B, Figure 3C). Although low education has been cited as a risk factor for poor disease management, the profiles of educational attainment in the six counties were similar.

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Discussion

Traditionally regarded as a childhood disorder, asthma has in recent years emerged as a public health concern for adults 19-64 years of age. Unlike childhood asthma, adult asthma affects more females than males and tends to be more difficult to treat (Dolan et al., 2004).

Abundant roads and highways whose purpose is to accommodate heavy traffic often characterize an urban community. Most studies that address the relationship of this urban characteristic with the frequency and severity of asthma symptoms have focused on children (Nicolai et al., 2003). For example, Kim and co-authors (2004) examined the proximity of roads to schools and the relationship of that proximity with asthma symptoms. They found spatial variability in traffic-related pollutants and an influence by this variability on the frequency of asthma symptoms in children.

Other studies have shown that emissions from trucks are more detrimental than car emissions with respect to respiratory symptoms (Janssen et al., 2003; van Vliet et al., 1997). The authors of the study reported here were able to obtain vehicular traffic counts from the Pennsylvania Department of Trans-portation (PennDOT). Since the PennDOT traffic count does not distinguish between car and truck traffic, however, the study was unable to assess the effect of truck traffic on asthma hospitalization rates. Previous studies have noted a disparate prevalence of commercial trucking routes in geographical areas with low socioeconomic status (SES) (Brown et al., 2003; Lwebuga-Mukasa et al., 2004). This phenomenon may explain why Fayette County, the area that ranked as least urbanized--but was characterized by low SES--had the highest adult asthma hospitalization rate.

U.S. EPA collects and monitors information regarding the geographic distribution of facilities that release known respiratory irritants and toxins (Trasande & Thurston 2005; White, Berger-Frank, Middleton, & Falk, 2002). In addition, prevailing wind patterns in the area of the emission sources contribute to reduced regional air quality (Peled et al., 2005). Geographical information systems (Nuckols, Ward, & Jarup, 2004; Vine, Degnan, & Hanchette, 1997) can be used to visualize wind patterns for the Commonwealth of Pennsylvania (Figure 4) (Pennsylvania State University, 1999; U.S. EPA, 2000; U.S. EPA, 2004). Because the authors did not have addresses for the study population, however, their ability to assess the relationship between pollutant releases and individual health outcomes was limited.

Epidemiological studies have suggested that a rural environment confers protection against the development of childhood asthma (von Mutius, 2001). More recent reports from China and Europe have indicated a reduction in the prevalence of childhood asthma in rural settings (Chan-Yeung et al., 2002; Waser et al., 2005). This "hygiene hypothesis" suggests that exposures from farming and livestock tend to protect children from the development of asthma. The authors of the study reported here, however, did not observe a protective effect of a farming environment for adult asthmatics. Lancaster County and Erie County both have substantial agricultural industry, but their adult asthma hospitalization rates were substantially different.

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Increased asthma morbidity in adult females has been reported (NIH, 2003). The authors found that asthma hospitalization rates in all six counties were higher for females than for males. This finding is consistent with NIH's finding that 61 percent of adult asthmatics are female (NIH, 2003). A recent European study found that females, regardless of their geographic location, had higher indices of chronic disease severity than males (European Network for Understanding Mechanisms of Severe Asthma, 2003). Biological mechanisms, such as the endocrine shift during the menstrual cycle, or menopause, have been suggested as responsible for this gender disparity (Haggerty, Ness, Kelsey, & Waterer, 2003; Vrieze, Postma, & Kerstjens, 2003). It has also been hypothesized that differences in the health care--seeking behavior of women and men may explain gender disparities in chronic disease (McCance-Katz, Carroll, & Rounsaville, 1999; Meyer-Weitz, Reddy, Van den Borne, Kok, & Pietersen, 2000). Further cohort studies are needed for a better understanding of the gender disparity in adult asthma hospitalization rates.

Age has been identified as a risk factor for asthma complications in adults (Bellia et al., 2000). The authors found that older adults (45-64 years of age) were 1.2 times more likely than younger adults to be hospitalized for asthma. This finding is consistent with a report that older adults tend to have more difficulty managing their asthma (NIH, 2003). It is unclear if the age-related trend is due to the age at disease onset or the duration of disease in an individual (Burrows, Barbee, Cline, Knudson, & Lebowitz, 1991; Busse, Banks-Schlegal, & Wenzel, 2000; Lange, Parner, Vestbo, Schnohr, & Jensen, 1998; Peat, Woolcock, & Cullen, 1987).

The study reported here had some limitations. The first was a lack of individual data related to socioeconomic status, educational attainment, environmental exposure, and behavioral risk factors (e.g., smoking). Variability among individuals in each county or between counties was not assessed. These limitations are inherent in epidemiological studies that are ecological since such studies consider group characteristics when assessing an association between exposure and disease process (Gordis, 2000). Another limitation was the absence of information related to health care coverage and use of preventive health services. Such information would be useful for assessing the extent to which primary health care services for asthma management are used as opposed to care being sought only in acute situations.

The study is the first to address measures of urbanization and the influence of urbanization on adult asthma hospitalization rates. The Commonwealth of Pennsylvania contains areas with high population density and areas with low population density. It also has a stable population that tends to relocate infrequently. This stability is important in the assessment of change over time in hospitalization frequency. The unexpected trend of increased hospitalization with decreasing population size and decreasing urbanization suggests a strong influence of demographic and socioeconomic factors. These factors should be further explored for a better understanding of their influence on human respiratory health.

Acknowledgments: The study was supported by funds from the Pennsylvania/NASA Space Grant Consortium. The authors thank Bernard D. Goldstein, M.D., and Bruce R. Pitt, Ph.D., for their support in obtaining these funds.

Corresponding Author: Rosemarie Ramos, Postdoctoral Fellow, University of Pittsburgh, Graduate School of Public Health, Department of Environmental and Occupational Health, Bridgeside Point, Suite 300, 100 Technology Drive, Pittsburgh, PA 15219-3130. E-mail: [e-mail].

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Rosemarie G. Ramos, Ph.D., M.P.H.

Evelyn O. Talbott, Dr.P.H., M.P.H.

Ada Youk, Ph.D., M.S.

Meryl H. Karol, Ph.D.

TABLE 1 Measures of Urbanization and Urbanization Rankings of Six
Pennsylvania Counties (a)

                                                   Population
                                                   Density (c) (persons/
County     Overall Rank (b)  Total Population (c)  [mi.sup.2]

Allegheny  1                 1,270,612 (1)         1755 (1)
Lancaster  2                   474,601 (2)         496 (2)
York       3                   386,299 (3)         422 (4)
Erie       4                   279,636 (4)         350 (5)
Dauphin    4                   251,316 (5)         479 (3)
Fayette    6                   147,367 (6)         188 (6)

                                        Daily Vehicle Miles
County     Miles of Roads/Highways (d)  Traveled (d)

Allegheny  5688 (1)                     25,154,896 (1)
Lancaster  3821 (2)                     10,429,462 (2)
York       3691 (3)                      8,462,878 (3)
Erie       2564 (4)                      6,280,805 (5)
Dauphin    1866 (6)                      8,166,979 (4)
Fayette    2075 (5)                      2,744,746 (6)

(a) The rank of the county with respect to each measure of urbanization
is shown in parentheses.
(b) Average of the four measures of urbanization.
(c) Data obtained from the U.S. Census Bureau.
(d) Data obtained from the Pennsylvania Department of Transportation.

TABLE 2 Results of Statistical Analysis*

Covariate    Relative Risk  p-Value  Confidence Interval

Gender       3.34           0.0001   2.60-4.31
Age group    1.17           0.016    1.03-1.33
County rank  1.05           0.131    0.99-1.12

*Goodness of fit for model: [chi square] = 46.02; p = .0518.