Background Recent studies have reported associations betweenparticulate air pollution and daily mortality rates. Population-based,cross-sectional studies of metropolitan areas in the UnitedStates have also found associations between particulate airpollution and annual mortality rates, but these studies havebeen criticized, in part because they did not directly controlfor cigarette smoking and other health risks.
Methods In this prospective cohort study, we estimated the effectsof air pollution on mortality, while controlling for individualrisk factors. Survival analysis, including Cox proportional-hazardsregression modeling, was conducted with data from a 14-to-16-yearmortality follow-up of 8111 adults in six U.S. cities.
Results Mortality rates were most strongly associated with cigarettesmoking. After adjusting for smoking and other risk factors,we observed statistically significant and robust associationsbetween air pollution and mortality. The adjusted mortality-rateratio for the most polluted of the cities as compared with theleast polluted was 1.26 (95 percent confidence interval, 1.08to 1.47). Air pollution was positively associated with deathfrom lung cancer and cardiopulmonary disease but not with deathfrom other causes considered together. Mortality was most stronglyassociated with air pollution with fine particulates, includingsulfates.
Conclusions Although the effects of other, unmeasured risk factorscannot be excluded with certainty, these results suggest thatfine-particulate air pollution, or a more complex pollutionmixture associated with fine particulate matter, contributesto excess mortality in certain U.S. cities.
Several cross-sectional investigations have found associationsbetween mortality rates and particulate air pollution in U.S.metropolitan areas1,2,3. A recent study reported associationsbetween infant mortality and particulate air pollution in theCzech Republic4. These studies have often been criticized becausethey did not control directly for cigarette smoking or othercovariates. Recent daily time-series studies, which are likelyto be free of confounding by individual characteristics, havereported associations between daily mortality rates and changesin air pollution, specifically particulate pollution, in London5and in several cities in the United States6,7,8,9,10,11,12.
Particulate air pollution is a mixture of solid particles andliquid droplets that vary in size, composition, and origin.Because only very small particles can be inhaled into the lungs,U.S. national health standards for the quality of ambient airare based on the mass concentration of "inhalable particles,"defined to include particles with an aerodynamic diameter ofless than 10 microm13. Fine-particulate air pollution includesparticles with an aerodynamic diameter equal to or below 2.5microm. Whereas larger particles are derived chiefly from soiland other crustal materials, fine particles are derived primarilyfrom the combustion of fossil fuels in transportation, manufacturing,and power generation. Fine-particulate pollution typically containsa mixture of particles including soot, acid condensates, andsulfate and nitrate particles. Fine particles are thought topose a particularly great risk to health because they are morelikely to be toxic than larger particles and can be breathedmore deeply into the lungs14.
In this study, a well-characterized cohort of adults participatingin the Harvard Six Cities Study of the health effects of airpollution was followed prospectively, beginning in 197415. Theobjective of this study was to estimate the effects of air pollutionon mortality, with control for individual smoking status, sex,age, and other risk factors.
Methods
Study Population
We selected random samples of adults from six communities15:Watertown, Massachusetts (where study enrollment was conductedin 1974); Harriman, Tennessee, including Kingston (1975); specificcensus tracts of St. Louis (1975); Steubenville, Ohio (1976);Portage, Wisconsin, including Wyocena and Pardeeville (1976);and Topeka, Kansas (1977). The sample was restricted to the8111 white subjects who were 25 through 74 years of age at enrollment,had undergone spirometric testing, and had completed a standardizedquestionnaire. The questionnaire included questions about age,sex, weight, height, education level, complete smoking history,occupational exposures, and medical history.
Informational letters and postage-paid return postcards includinga question on vital status were mailed to the subjects annually.The vital status of the subjects who did not respond was determinedby questioning family members, friends, or neighbors. In addition,we searched the National Death Index16 for the years 1979 through1989. Death certificates were obtained for 1401 of the 1430subjects who had died (98 percent); the causes of death werecoded according to the International Classification of Diseases,9th Revision (ICD-9) by an independent certified nosologistwho was blinded both to pollution levels and to the study designand objectives. The ending date of the study for each city wasMarch or June of 1991, depending on the date of the last follow-upcontact; the total duration of follow-up was 14 to 16 years(111,076 person-years).
For subjects who died, survival times were calculated by subtractingthe date of enrollment from the exact date of death. For survivingparticipants who were not lost to follow-up, censored survivaltimes were defined as the date of the end of the study minusthe enrollment date. For those who were lost to follow-up beforethe period covered by our National Death Index search (i.e.,before 1979), censored survival times were estimated by subtractingthe enrollment date either from the date of the last follow-upcontact plus six months or from the first day of the NationalDeath Index search period (January 1, 1979), whichever camefirst. For those who were lost to follow-up after the NationalDeath Index search period (i.e., after 1989), censored survivaltimes were estimated by subtracting the enrollment date eitherfrom the date of the last follow-up contact plus six monthsor from the last day of the study period, whichever came first.For those who were lost to follow-up during the period coveredby the National Death Index search, the censored survival timeswere estimated by subtracting the date of enrollment from thelast date in the search period (December 31, 1989).
Air-Pollution Data
As part of the original study design, ambient (outdoor) concentrationsof total suspended particulate matter, sulfur dioxide, ozone,and suspended sulfates were measured in each community at acentrally located air-monitoring station15. Size-selective aerosolsamplers were placed at these sites in the late 1970s; datawere collected for two classes of particle: fine particles (aerodynamicdiameter <2.5 microm) and inhalable particles (aerodynamicdiameter, <15 microm before 1984 and <10 microm startingin 1984). In the mid-1980s, supplemental 24-hour integratedsampling of aerosol acidity by the measurement of hydrogen ionconcentrations17 was conducted for approximately one year ineach city. Mean pollution levels for each pollutant were calculatedfor periods that were consistent and comparable among the sixcities.
Statistical Analysis
Life-table survival probabilities for each year of follow-upwere estimated for each city, and differences between city-specificmortality rates were assessed with a log-rank test18. We estimatedadjusted mortality-rate ratios for air pollution by simultaneouslyadjusting for other risk factors in Cox proportional-hazardsregression models18,19,20,21,22. In these models the subjectswere stratified according to sex and five-year age groups, andeach sex-age group had its own base-line hazard. Each modelalso included indicator variables for current or former smokers,the number of pack-years of smoking (evaluated separately forcurrent and former smokers), an indicator variable for lessthan a high-school education, and body-mass index (defined asthe weight in kilograms divided by the square of the heightin meters).
Two approaches were used to evaluate the effects of air pollutionin the Cox proportional-hazards models. First, indicator variablesfor the city of residence were included, with Portage, Wisconsin,the city with the lowest levels of particulate air pollution,as the reference category. Adjusted mortality-rate ratios foreach of the six cities were then compared graphically with themean pollution levels in those cities. Next, adjusted mortality-rateratios were estimated by including city-specific pollution levelsdirectly in the Cox proportional-hazards models. Adjusted rateratios were calculated and reported for a difference in airpollution equal to that between the city with the highest levelsof air pollution and the city with the lowest levels -- thatis, the adjusted rate ratios across the range of exposure foreach pollutant among the six cities.
Analyses were conducted to evaluate the robustness of the modelsand the possibility of residual confounding. Models were estimatedafter the data were separated according to the subjects' smokingstatus, sex, and occupational exposure to dust, gases, or fumes.The effect of the inclusion of different covariates on the estimatedeffect of pollution was evaluated. Models were also estimatedafter the exclusion of subjects who had been treated for highblood pressure within 10 years of enrollment in the study andsubjects who had ever been told by a doctor that they had diabetes,had glucose in their urine, or had too much glucose in theirblood. We also used a variety of approaches to estimate censoredsurvival times.
Mortality-rate ratios from the Cox proportional-hazards models(with adjustment for cigarette smoking, education, and body-massindex) were estimated separately for the following cause-of-deathcategories: cardiopulmonary (ICD-9 codes 400 through 440 and485 through 496), lung cancer (162), and all others. For eachcause-of-death category, data on subjects whose deaths werenot in that specific category were censored at the time of death.
Results
Characteristics of the Cohort and Air-Pollution Data
The characteristics of the cohort and the values for air-pollutionmeasures are summarized in Table 1. For all measures of airpollution except the ozone level and aerosol acidity, ambientconcentrations were highest in Steubenville and lowest in Portageor Topeka. The mean acidity of the aerosol was highest in Harriman,but second-highest in Steubenville. The mean ozone concentrationswere highest in Portage and Topeka. The concentrations of totalparticles declined during the study period, especially in Steubenvilleand St. Louis; the annual average concentrations of fine andsulfate particles varied relatively little during the studyperiod (Figure 1). Crude mortality rates (Table 1) and survivalcurves (Figure 2) both show that mortality was highest in Steubenvilleand St. Louis and lowest in Portage and Topeka. Differencesin the probability of survival among the cities were statisticallysignificant (P<0.001).
Figure 2. Crude Probability of Survival in the Six Cities, According to Years of Follow-up.
Adjusted Mortality Rates
On the basis of the proportional-hazards model, mortality wasmost strongly associated with cigarette smoking (Table 2). Increasedmortality was also associated with having less than a high-schooleducation and with increased body-mass index (the latter wasespecially true for women). After simultaneous adjustment forthese other risk factors, the differences in mortality amongthe six cities remained significant.
Table 2. Adjusted Mortality-Rate Ratios Estimated from Cox Proportional-Hazards Models.
City-specific mortality rates, adjusted for a variety of healthrisk factors, were associated with the average levels of airpollutants in the cities (Figure 3). The small differences inozone levels among the cities (Table 1) limited the power ofthe study to detect associations between mortality and ozonelevels. Mortality was more strongly associated with the levelsof inhalable, fine, and sulfate particles than with the levelsof total suspended particles, the sulfur dioxide levels, thenitrogen dioxide levels, or the acidity of the aerosol.
Figure 3. Estimated Adjusted Mortality-Rate Ratios and Pollution Levels in the Six Cities.
Mean values are shown for the measures of air pollution. P denotes Portage, Wisconsin; T Topeka, Kansas; W Watertown, Massachusetts; L St. Louis; H Harriman, Tennessee; and S Steubenville, Ohio.
When the mean concentrations of each pollutant were includedindividually in the proportional-hazards model, we found significantassociations between mortality and inhalable, fine, or sulfateparticles (P<0.005). For a difference in the air-pollutionlevel equal to that between the most polluted city and the leastpolluted city and with inhalable particles (range, 18.2 to 46.5µg per cubic meter), fine particles (range, 11.0 to 29.6µg per cubic meter), and sulfate particles (range, 4.8to 12.8 µg per cubic meter) used as indicators of airpollution, the adjusted rate ratios were nearly equal at 1.27(95 percent confidence interval, 1.08 to 1.48), 1.26 (95 percentconfidence interval, 1.08 to 1.47), and 1.26 (95 percent confidenceinterval, 1.08 to 1.47), respectively.
Sensitivity
Estimates of the association between mortality and fine-particlepollution among subjects with different smoking status and amongmen and women (Table 3) showed only small and nonsignificantdifferences between subgroups. Associations with air pollutionwere somewhat stronger among subjects with occupational exposureto dust, gases, or fumes (Table 3). However, positive associationsbetween mortality and air-pollution levels were observed inall subgroups defined by occupational exposure and sex, anddifferences among the subgroups were not statistically significant.
Table 3. Adjusted Mortality-Rate Ratios for the Most Polluted and Least Polluted Cities Studied, According to Smoking Status, Sex, and Occupational Exposure, with Fine Particles Used as the Indicator of Air Pollution.
Although cigarette smoking and other risk factors were associatedwith mortality, our estimates of pollution-related mortalitywere not significantly affected by the inclusion or exclusionof these variables in the models (Table 4). The estimated associationof air pollution and mortality was unchanged when subjects whohad been treated for high blood pressure or subjects with diabeteswere excluded from the analysis (Table 4). When censored survivaltimes were recalculated as the date of the last follow-up contactminus the enrollment date, or when the analysis was restrictedto data on deaths in 1979 through 1989 (the years of the NationalDeath Index searches), no appreciable differences in the estimatedassociation between air pollution and mortality were observed.
Table 4. Estimated Mortality-Rate Ratios for the Most Polluted City as Compared with the Least Polluted City, with Fine Particles Used as the Indicator of Air Pollution, in Selected Models.
Causes of Death
The estimated effects of air pollution on mortality varied amongcauses of death (Table 5). For comparison, rate ratios wereestimated for current smokers and for former smokers with approximatelythe average number of pack-years of smoking at enrollment (Table 5).Smoking was most strongly associated with mortality dueto lung cancer, significantly associated with mortality dueto cardiopulmonary disease, but not associated with mortalityfrom all other causes. Similarly, air pollution was positivelyassociated with mortality due to lung cancer and cardiopulmonarydisease but not with mortality from all other causes. Only 98deaths were coded on the death certificates as due to nonmalignantrespiratory disease (ICD-9 codes 485 through 496), as comparedwith 646 deaths due to cardiovascular disease (codes 400 through440). An analysis restricted to deaths from nonmalignant respiratorydisease produced unstable and statistically nonsignificant estimatesof the association with air pollution. When mortality from allcauses was considered, or when deaths due to cardiovascularand respiratory diseases were grouped together, the effectsof air pollution were consistent and the association was robust.
Table 5. Adjusted Mortality-Rate Ratios for Current and Former Cigarette Smokers and for the Most Polluted City as Compared with the Least Polluted, According to Cause of Death.
Discussion
In this prospective cohort study, the mortality rate, adjustedfor other health risk factors, was associated with the levelof air pollution. Mortality was more strongly associated withthe levels of fine, inhalable, and sulfate particles than withthe levels of total particulate pollution, aerosol acidity,sulfur dioxide, or nitrogen dioxide. As with all other epidemiologicstudies, it is possible that the observed association was dueto confounding -- that is, that it resulted from a risk factorthat was correlated with both exposure and mortality. Potentialconfounders of the effects of air pollution include cigarettesmoking and occupational exposure to pollutants. In our study,however, the association of air pollution with mortality wasobserved even after we directly controlled for individual differencesin other risk factors, including age, sex, cigarette smoking,education level, body-mass index, and occupational exposure.
The estimated effect of air pollution on mortality was not alteredby the inclusion or exclusion of indicator variables for otherrisk factors in our models. Analyses were conducted for subgroupsdefined according to sex, smoking status, and occupational exposure.Although the effects of pollution were somewhat stronger amongsubjects occupationally exposed to dust, gases, or fumes, positiveassociations between mortality and air pollution were observedamong all the smoking-status, occupational-exposure, and sexgroups, and the differences among these subgroups were not statisticallysignificant. The estimated association of pollution and mortalityremained essentially unchanged when subjects who had been treatedfor high blood pressure or who had diabetes were excluded fromthe analysis.
In our analysis, the mortality-rate ratios have been expressedin terms of the range of exposure to air pollutants in the sixcities. When the range of exposure was used, the estimated relativerate ratios for inhalable, fine, and sulfate particles werenearly equal at 1.27 (95 percent confidence interval, 1.08 to1.48), 1.26 (95 percent confidence interval, 1.08 to 1.47),and 1.26 (95 percent confidence interval, 1.08 to 1.47), respectively.Because the six cities were selected as representative of therange of particulate air pollution in the United States, theserate ratios roughly represent the relative risk associated withthat range.
In this study, exposure to air pollution was estimated by monitoringoutdoor air pollution at a central site in each of the six cities.Long-term transport and large-scale mixing of combustion productsplay a large part in establishing the levels of sulfate andfine-particulate air pollution. Therefore, concentrations ofsulfates and fine particles are relatively uniform within eachof these communities23. Furthermore, sulfate and fine-particulateair pollution penetrates indoors, resulting in strong correlationsbetween indoor and outdoor concentrations24,25,26. Thus, measurementsof the outdoor concentrations of sulfate and fine particlesmay be better indicators of individual exposure than the otherpollutants we considered.
The associations observed in this study between air pollutionand mortality are consistent with associations observed in recenttime-series studies, including studies from three of these sixcities5,6,7,8,9,10,11,12. Because the daily time-series studiesevaluated only the effect of short-term changes in pollutionlevels, whereas our study evaluated associations with long-termexposure (including recurring episodes of relatively high pollution),quantitative comparisons with these investigations are difficultto make. Nevertheless, as was found in the time-series studies,particulate air pollution was associated with death due to cardiopulmonarycauses. In our study, in which we evaluated the effects of long-termexposure, lung cancer was associated with particulate air pollution;such an association with lung cancer was not observed in thedaily time-series studies. Little or no association with othercauses of death was evident in our study or the time-seriesstudies. The small number of reported deaths due to nonmalignantrespiratory disease and the potential for misclassificationof primary causes inherent in the use of death-certificate datalimited our ability to evaluate cause-specific mortality inmore detail.
The pollution concentrations used in our analysis representonly exposures monitored during the study period. Increasedmortality, however, may reflect the cumulative burden of a lifetimeof exposure. Concentrations of total particles clearly declinedduring the study period (especially in Steubenville and St.Louis), whereas concentrations of fine particles and sulfateparticles were relatively stable. Given the lack of data onpollution levels before the study period and in view of thefact that the relative ranking of the cities in terms of air-pollutionlevels did not change during the study period, it is not possibleto differentiate the influences of historical exposure fromthose of recent exposure. The observed association between mortalityand mean exposure to fine-particulate and sulfate air pollutionduring the study period may also partially reflect exposureto air pollution before the study period.
The strength of the observed association between air pollutionand mortality is confirmed by previous observations of associationsbetween particulate air pollution and other health end points.Elevated levels of particulate air pollution have been associatedwith declines in lung function or with increases in respiratorysymptoms such as cough, shortness of breath, wheezing, and asthmaattacks27,28,29,30,31,32,33,34,35,36. Other studies have foundassociations between particulate air pollution and rates ofhospitalization,37,38,39,40,41 chronic obstructive pulmonarydisease,42 and restricted activity due to illness43,44.
A large and growing body of literature documents the adversehealth effects associated with particulate air pollution. Althoughthe effects of unmeasured risk factors cannot be controlledfor, in this prospective cohort study we observed significanteffects of air pollution on mortality even when we controlledfor sex, age, smoking status, education level, and occupationalexposure to dust, gases, and fumes. The compatibility of theeffects of air pollution on mortality in this study with thoseobserved in population-based cross-sectional studies and dailytime-series studies provides further evidence for the conclusionthat exposure to air pollution contributes to excess mortality.This study, therefore, provides additional impetus to the developmentof strategies to reduce urban air pollution.
Supported in part by grants (ES-01108 and ES-00002) from theNational Institute of Environmental Health Sciences, by cooperativeagreements (CR-811650 and CR-818090) with the EnvironmentalProtection Agency, and by a contract (RP-1001) with the ElectricPower Research Institute.
Source Information
From the Environmental Epidemiology Program (D.W.D., C.A.P., X.X., M.E.F., B.G.F., F.E.S.), the Exposure Assessment and Engineering Program (J.D.S.), and the Interdisciplinary Program in Health (C.A.P.), Department of Environmental Health, and the Department of Biostatistics (J.H.W.), Harvard School of Public Health, Boston; the Channing Laboratory, Brigham and Women's Hospital and Harvard Medical School, Boston (D.W.D., F.E.S.); and the Economics Department, Brigham Young University, Provo, Utah (C.A.P.). Presented in part at the annual meeting of the American Thoracic Society, San Francisco, May 19, 1992, and at the Aerosols in Medicine Congress of the International Society for Aerosols in Medicine, Garmisch-Partenkirchen, Germany, April 1, 1993.
Address reprint requests to Dr. Dockery at the Environmental Epidemiology Program, Department of Environmental Health, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115.
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