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Original Article
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Volume 331:1542-1546 December 8, 1994 Number 23
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Patterns of Asthma Mortality in Philadelphia from 1969 to 1991
David M. Lang, and Marcia Polansky

 

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ABSTRACT

Background The rate of mortality from asthma has increased substantially in the United States since 1978. We analyzed the patterns of the rates of death from asthma in Philadelphia between 1969 and 1991.

Methods The rates of death from asthma were analyzed and compared with trends in the concentrations of major air pollutants: ozone, carbon monoxide, nitrogen dioxide, particulate matter (particles <10 microm in diameter), and sulfur dioxide. Univariate and multivariate analyses were used to study the rates of death from asthma from 1985 to 1991 and their association with race, poverty, sex, and other factors.

Results The rate of death from asthma decreased from 1.68 per 100,000 people in 1969 to 0.68 per 100,000 in 1977, but then increased to 0.92 per 100,000 in 1978 and 2.41 per 100,000 in 1991. Between 1965 and 1990, the concentrations of major air pollutants declined substantially. From 1985 to 1991, 258 people were identified for whom asthma was the primary cause of death. According to multivariate analysis, the rates of death from asthma from 1985 to 1991 were significantly higher in census tracts with higher percentages of blacks (P = 0.032), Hispanics (P = 0.013), female residents (P<0.001), and people with incomes in the poverty range (P<0.001).

Conclusions The rates of death from asthma have increased in Philadelphia, whereas concentrations of major air pollutants have declined. The rates are highest in census tracts with the highest percentages of poor people and minority residents, particularly blacks. Public health efforts should target urban areas where the risk of death from asthma is highest.

Since 1978, the rate of mortality from asthma has increased substantially in the United States1,2,3. Although it has been suggested that this trend may be spurious,4 the rate has also increased in other countries1. Neither more frequent diagnosis nor aging of the population can account for this change1,3,5. In the United States, deaths from asthma occur predominantly in large cities,1,2,6,7 suggesting an association with the urban environment. The prevalence and severity of asthma are also higher among blacks1,2,6,7,8,9,10 and Hispanics11,12 and in association with socioeconomic factors linked to poverty,1,8,9,10,11,13 such as young maternal age, maternal cigarette smoking, low birth weight, crowded living conditions, and living in the inner city, where access to and use of health care may be suboptimal14,15.

In Pennsylvania, a disproportionate number of deaths from asthma occur in Philadelphia16. We analyzed the rate of mortality from asthma from 1969 to 1991 to identify trends in the rate and to determine whether changes in the rate have paralleled changes in the concentrations of major air pollutants. We also analyzed data collected from 1985 to 1991 to identify aspects of the urban environment that were associated with death from asthma.

Methods

The Philadelphia Department of Public Health provided data on deaths from asthma among Philadelphia residents between 1969 and 1991. The criteria listed in the 9th revision of the International Classification of Diseases were used to identify cases in which asthma was the primary cause of death; for data on deaths occurring before 1979, criteria listed in the eighth revision were used. Population estimates were derived from census tables for 1960 to 1990. Additional information, including the date and location of death, age, sex, and race, was also recorded for deaths reported from 1985 to 1991. The Division of Air Management Services, Philadelphia Department of Public Health, provided measurements of the annual concentrations of five ambient air pollutants: ozone, carbon monoxide, nitrogen dioxide, particulate matter (particles <10 microm in diameter), and sulfur dioxide17. To investigate the possibility that the rate of mortality from asthma might be associated with the number of days with high air-pollutant concentrations rather than the average annual concentration, we obtained data on the annual numbers of unhealthful days from the Pollution-Standards Index. This index integrates data on measurements of the five air pollutants into a single figure that represents the worst air quality recorded each day; the air quality of a particular day is defined as unhealthful if the level of any of the pollutants exceeds the air-quality standard17.

Philadelphia was divided into 365 census tracts in the 1990 Census18. The Delaware Valley Regional Planning Commission provided demographic data according to the census tract on race, ethnicity, median age of homes, level of education, and sex. The Philadelphia City Planning Commission provided data on median age, degree of crowding, and socioeconomic status. The degree of crowding was defined as the percentage of housing units per census tract with at least 1.01 persons per room. Persons living in poverty were identified with a standard used by federal government agencies: total income is adjusted to a poverty threshold that varies depending on the size and composition of a family. The average poverty threshold in 1990 was $13,359 for a family of four13.

The census tracts were divided into equal-sized groups (those with low proportions of the variable, those with average proportions, and those with high proportions) for each of the following independent variables: black race, Hispanic ethnicity, poverty, residents without a high-school diploma, median age of homes, crowding, median age of residents, and female sex. The rate of mortality from asthma per census tract was the dependent variable. Data were analyzed for each census tract with the Kruskal-Wallis test for univariate analyses (SAS Institute, Cary, N.C.)19. Forty-seven census tracts with fewer than 1000 residents were excluded from the analysis. A standard Poisson multiple-regression model20 was used for multivariate analyses (Egret, Statistics and Epidemiology Research Corporation, Seattle) to adjust for confounding and to determine independent risks. Independent variables were analyzed in the Poisson regression as ordinal terms and their interactions. Calculated P values are two-tailed, with values below 0.05 considered to indicate statistical significance.

Results

Rate of Mortality from Asthma: 1969 to 1991

The rate of mortality from asthma decreased from 1.68 per 100,000 people in 1969 to 0.68 per 100,000 in 1977, but then increased to 0.92 per 100,000 in 1978 and 2.41 per 100,000 in 1991. The annual rates of death from asthma for 1969 to 1991 are shown in Figure 1. The rate among persons 5 to 34 years of age, for whom certification of asthma as the cause of death is considered the most reliable,1,2 also increased during the latter period.


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  		Figure 1. Annual Rates of Death from Asthma in Philadelphia from 1969 to 1991.

Data were obtained from the Philadelphia Department of Public Health18.

 
Between 1965 and 1990, the concentrations of major air pollutants declined substantially in Philadelphia (Figure 2). The concentrations of ozone (initially measured in 1970) and carbon monoxide exceeded U.S. national standards for the quality of ambient air in 1989 and 1990; however, these concentrations were lower than those recorded in the 1970s, when the rates of death from asthma were low. According to the Pollution-Standards Index,17 Philadelphia averaged 15.3 unhealthful days from 1979 to 1984 and 9.9 days from 1985 to 1991.


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  		Figure 2. Concentrations of Major Air Pollutants in Philadelphia from 1965 to 1990, as a Percentage of the U.S. National Air-Quality Standard.

The peak asthma mortality rate in 1989 was not associated with a substantial worsening of air quality. Over the past 25 years, the concentrations of the indicated pollutants have declined markedly. In 1990 the national standards for quality of ambient air were as follows: sulfur dioxide, 0.03 ppm (annual average); particulate matter, 50 µg per cubic meter (annual arithmetic mean); nitrogen dioxide, 0.05 ppm (annual average); carbon monoxide, 9 ppm (eight-hour average); and ozone, 0.12 ppm (one-hour average). For each year, values from the monitoring station in Philadelphia that recorded the highest concentrations were used. Data were obtained from the Philadelphia Department of Public Health.

 
Rate of Mortality from Asthma: 1985 to 1991

We identified 258 people (average [±SD] age, 54 ±21 years) for whom asthma was the primary cause of death. No relation between death and the season or month in which death occurred was found. The majority of deaths occurred in hospitals (65.1 percent) and among nonwhites (Figure 3), as has been found in other studies1,3,6. From 1985 to 1991, the average annualized rate of death from asthma was 3.35 per 100,000 among nonwhites and 1.44 per 100,000 among whites; from 1979 to 1984, the rates were 2.13 per 100,000 and 1.14 per 100,000, respectively. Among persons 5 to 34 years of age, the average annualized rate of death from asthma from 1985 to 1991 was 1.57 per 100,000 among nonwhites and 0.49 per 100,000 among whites.


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  		Figure 3. Annual Rates of Death from Asthma in Philadelphia among Whites and Nonwhites from 1985 to 1991.

 
The association between demographic factors and death from asthma was evaluated with data for the 318 census tracts in Philadelphia with populations of at least 1000, according to the 1990 census. The average population of these census tracts was 4945 (range, 1009 to 17,971). According to univariate analyses, black race, poverty, lack of a high-school diploma, crowding, and female sex were associated with a significantly increased rate of death from asthma (Table 1). According to multivariate analysis, the rate of death from asthma was significantly increased in census tracts in which greater proportions of residents were black, Hispanic, female, or poor (Table 1). Black race, however, was only associated with an increased rate of death from asthma in census tracts with higher poverty rates (Figure 4). An interaction term between poverty and black race was significant (rate ratio, 1.32; 95 percent confidence interval, 1.01 to 1.72; P = 0.043) when it was added to the multivariate model. Census tracts categorized as being in the top 10 percent for death from asthma (average annual rate, 11.69 per 100,000) accounted for only 6.3 percent of Philadelphia residents but for 30.2 percent of deaths from asthma from 1985 to 1991. These census tracts, as compared with those in the lowest 10 percent for death from asthma (average annual rate, 0), were areas in which greater proportions of residents were black (70.1 percent vs. 0.2 percent), Hispanic (6.8 percent vs. 1.3 percent), less well educated (percent without high-school diploma, 40.7 vs. 35.1 percent), young (mean age, 33.0 vs. 38.0 years), female (55.1 percent vs. 53.3 percent), living in crowded conditions (7.6 percent vs. 1.6 percent), and poor (34.0 percent vs. 7.9 percent).

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  		Table 1. Influence of Demographic Factors on the Rate of Death from Asthma in Philadelphia.

 

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  		Figure 4. Mean (+SE) Annualized Rates of Death from Asthma in 318 Census Tracts in Philadelphia from 1985 to 1991, According to the Percentage of Residents Living in Poverty and the Percentage of Blacks.

 
Discussion

The rates of death from asthma in Philadelphia have increased since 1978 in parallel with increases in national rates1,2,3. The last year for which mortality data in Philadelphia are complete is 1991; preliminary data indicate that the rate of death from asthma was at least 2.04 per 100,000 in 1992 and 2.18 per 100,000 in 1993 (Tillack W: personal communication). The number of deaths from asthma is disproportionately high in poorer areas of Philadelphia. High mortality rates have previously been reported in large cities such as New York6 and Chicago,7 but not2,3 in the states -- Mississippi, Louisiana, and West Virginia -- with the highest poverty rates13. In contrast to cities, rural areas have both a low prevalence of asthma and a lower incidence of severe asthma2,21. This phenomenon has also been observed in Africa, where the prevalence of asthma increases among people who migrate from rural regions to urban areas22. In Philadelphia, black race was correlated with an increased rate of death from asthma in poorer areas of the city, but not in affluent areas. Our results emphasize the need to characterize more fully the aspects linked to urban poverty that we measured (level of overcrowding, median age of dwellings, and level of education) as well as the ones we did not measure,1,23,24,25 such as exposure to dust-mite and cockroach allergen and the level of physical decay, crime, illicit drug use, family dysfunction, hopelessness, and despair.

Blacks and Hispanics are less likely to receive regular medical care than whites, and such care is essential for optimal control of asthma. Blacks and Hispanics are more likely than whites to obtain care for asthma in an emergency department11. They are also more likely to be less educated than whites,11 to be younger,11,13 and to live in more crowded conditions and thus to have more respiratory tract infections26.

In Philadelphia, the rates of death from asthma were significantly associated with census tracts in which greater proportions of blacks or Hispanics reside. This association was independent of the level of poverty (as shown by multivariate analysis in Table 1); however, a portion of this independent risk may be artifactual. The undercounting of blacks and Hispanics in the census inflates death rates among these groups to some degree11,13. Since the extent of poverty among these groups may also be underestimated, within a single income category census tracts with high proportions of black and Hispanic residents may in fact have more poor residents than census tracts with high proportions of white residents11,13. This may explain why we found that race or ethnicity was associated with an independent risk of death from asthma -- a finding in agreement with some reports9 but not others8,10.

We found a significant risk of death from asthma for Hispanics in our multivariate model, but not in our univariate analysis; this difference probably reflects confounding by blacks in census tracts where few Hispanics live. A relatively small number of Hispanics -- 89,193 persons mainly of Puerto Rican descent -- live in Philadelphia18. Among Hispanics in the United States, those of Puerto Rican descent are the most impoverished and have the highest cumulative prevalence of asthma11,12.

Women have a greater prevalence of asthma than men27. In the Philadelphia metropolitan area, increased morbidity among women with asthma has been reported28. We found that the rate of death from asthma was significantly increased in census-tract areas with higher proportions of female residents. Substantially more men than women are undercounted in the census, and this undercounting is greater for black men than for other groups of men13. We believe that the association between death from asthma and female sex may in part be spurious, because of potential confounding by inaccurate census data.

Air pollutants may impair respiratory function1,29,30. In 1967, Girsch et al.31 reported an association between visits to emergency departments for asthma in Philadelphia and the number of days with high barometric pressure and elevated concentrations of air pollutants. A more recent study also showed an association between air-pollutant concentrations and the number of visits to emergency departments for asthma32. The concentrations of ambient air pollutants in Philadelphia have declined dramatically since the mid-1960s, a trend also observed in other cities in the United States17. Data on particulate pollutants measuring less than 10 microm in diameter, which are likely to cause adverse health effects, have only been available since 198817. Therefore, determination of the potential relevance of particulate pollutants17,32 to the increasing rates of mortality from asthma in Philadelphia must await future studies. Since we did not measure outdoor or indoor allergens, the importance of exposures to allergens1,23 and their interactive effects with air pollutants33 also cannot be evaluated from our data. Residents of urban areas spend the majority of their time indoors30; consequently, measurements of outdoor air pollutants may not accurately reflect the typical degree of exposure in urban areas. Studies that examine the quality of both indoor and outdoor air will be important in clarifying the role of air quality in the increasing rate of death from asthma in urban areas.

Between 1985 and 1991, the average age of people who died of asthma in Philadelphia was 54 years. Although the use of death-certificate data to identify the number of people who died of asthma has been considered most reliable for the subgroup of people who died of asthma between the ages of 5 and 34,1,2 Hunt et al. recently found that the use of these data had a specificity of 99 percent for 339 people with an average age of 72 years5. They concluded that the rates of mortality from asthma as determined by death-certificate data are most likely underestimates. We believe that measurement error, either from erroneous listing of the cause of death on death certificates or from inaccurate measurements of covariates resulting in misclassification and incomplete adjustment for confounding,34 is an unlikely explanation for our findings.

In conclusion, the rates of death from asthma increased in Philadelphia between 1978 and 1991, a period during which the concentrations of major air pollutants declined. The rates were highest in the census tracts with the highest percentages of poor people and minority residents, particularly blacks. Our findings suggest that aspects of the urban environment increase the severity, and conceivably the prevalence, of asthma and that public health efforts should target urban areas where the risk of death from asthma is highest.

Supported in part by the Hahnemann University Allergy and Asthma Center Research and Education Fund.

We are indebted to Warner Tillack and Arnold Selig (Division of Information Management, Philadelphia Department of Public Health), David Lewis (U.S. Census Bureau in Philadelphia), David Segal (Philadelphia City Planning Commission), and Thomas Weir (Division of Air Management Services, Philadelphia Department of Public Health) for providing data; to Edward S. Schulman, M.D., for reviewing the manuscript; to Eric Vonderheid, M.D., for collaboration in statistical analyses; and to Ms. Donna Thompson for assistance in the preparation of the manuscript.


Source Information

From the Department of Medicine, Division of Allergy and Immunology (D.M.L.), and the Department of Humanities, Social Sciences, and Biometrics (M.P.), Hahnemann University Hospital, Philadelphia. Presented in part at the annual meeting of the American Academy of Allergy and Immunology, Chicago, March 16, 1993.

Address reprint requests to Dr. Lang at Hahnemann University, Mail Stop 107, Division of Allergy and Immunology, Broad and Vine Sts., Philadelphia, PA 19102-1192.

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