International Journal of Epidemiology ©International Epidemiological Association 1996 Vol. 25, No. 6 Printed in Great Britain Air Pollution and Mortality in East Berlin during the Winters of 1981-1989 SIBYLLE I RAHLENBECK* AND HERMANN KAHL* Rahlenbeck S I (Gondar College of Medical Sciences, PO Box 196, Gondar, Ethiopia), Kahl H. Air pollution and mortality in East Berlin during the winters of 1981-1989. International Journal of Epidemiology 1996; 25: 1220-1226. Background. The relationship between air pollution and mortality in East Berlin was examined for the winters of 1981-1989. Methods. Regression analysis included daily mean levels of sulphur dioxide (SO2) and suspended particulates (SP), and was controlled for temperature, humidity, week-day, month, and year. Moving averages of previous pollution were also used. Results. Each pollutant was a significant contributor to excess mortality. The strongest association was found for mortality lagged for 2 days, which depended significantly on the level of SP (p for In SP = 0.876; P = 0.008) and SO2 (p for In SO2 = 0.635; P = 0.012), when regressed separately. When omitting days with pollutant concentrations above 150 |ig rrr 3 , the pollutant-mortality relationship was linear, and a 100 ng rrr 3 increase was associated with a 6.1% (SP) and 4.5% (SO2) mortality increase 2 days later, when pollutants were considered separately; this was reduced to 4.6% (SP) and 2.8% (SO2) increase, when both were considered simultaneously. Conclusions. The results show that short-term associations between air pollutants and mortality in East Berlin did exist during the winters 1981-1989. Since the coefficients for SP and SO2 dropped when controlling for the other pollutant species, a similar strength of association with mortality for both pollutants was found. Keywords: air pollutants, air pollution, mortality, particulates, sulphur dioxide Several decades ago high levels of air pollutants were associated with excess mortality in some populations, for example in the Meuse Valley in 1930, Belgium,1 and in London 1952.2 Usually, sulphur dioxide (SO2) and suspended particulates (SP) (US) and black smoke (BS) (UK) have been used as air pollution indices. The World Health Organization summarized in 19873 that short-term mortality excesses might be expected when ambient levels of particulates (measured as BS) and SO 2 exceed 500 )J.g m~3. However, several recent studies indicate that thresholds, if they exist, are much lower.4"15 Using time series techniques and controlling for weather variables, epidemiologists have investigated the classical data sets of London and New York.5-7-16"18 However, no consensus was reached as to which of these primary pollutants was most responsible for causing excess mortality. Because of their high collinearity it is difficult to discriminate their relative contribution. Furthermore, their physico-chemical behaviour and toxicity is influenced by weather variables and the presence of other pollutants. Recently, secondary products such as acid sulphates and sulphuric acid aerosols have increasingly attracted attention, and it has been argued that health effects might be related to these compounds rather than SO2, total suspended particulates (TSP), SP or BS. 718 " 20 Others, however, have found an independent relationship between SP and mortality,5'8'13'15 whereas SO2 seemed to be an indicator of general air pollution. Contrary to the worldwide trend of decreasing air pollution levels, emissions and air pollution levels remained high over the final decades of the former German Democratic Republic.13'21 Due to legal restrictions, the data were previously unavailable for evaluation. In the present investigation, we examined the association between daily concentrations of SO 2 and SP and daily mortality in East Berlin, covering eight and a half winters, from 1 October 1981 to 31 March 1988, as well as from 1 October 1989 to 31 December 1989. Multivariate procedures were applied, controlling for temperature, humidity, week-day, month, and year. MATERIAL AND METHODS East Berlin East Berlin was situated at 53.3° North and 13.3° East in a flat valley of the Spree river, 35 m above sea level, covering an area of 403 km2; the population was * Gondar College of Medical Sciences, P O Box 196, Gondar, Ethiopia. * Senatsverwaltung fuer Stadtentwicklung und Umweltschutz, Lentzeallee. Berlin, Germany. 1220 AIR POLLUTION AND MORTALITY IN EAST BERLIN 1 284 553 in 1989. About half of the inhabitants lived in the centre (Berlin-Mitte) and the adjacent districts of Prenzlauer Berg, Friedrichshain, and Lichtenberg, that cover 58 km2 or 14% of the East Berlin area. The climate was typically continental with an average daily mean temperature of 5.5°C maximum and 0.0°C minimum for the winter half years. The prevailing wind direction was west-southwest. Domestic coal burning constituted an important emission source, and import of air pollution occurred mainly from southwestern winds from West-Berlin and the industrial areas southeast and southwest of Berlin. Mortality Data Daily deaths in East Berlin were extracted from the mortality records of the former East-German registry. The data set only includes deaths of people aged over one year. Deaths due to accidents and suicides (ICD-9 numbers > 800) were excluded, as were deaths which occurred outside East Berlin. Air Quality and Meteorological Data Data for SO 2 and SP concentrations were collected from one station (Parochialstrasse) in the city centre of East Berlin. SO 2 was measured colometrically on a 30-minute basis (CM5; Zentrum fuer Umweltgestaltung, Wittenberg). Daily mean values expressed in |ig nT 3 were taken for the analysis. SP levels were measured by p-absorption (FH62; Friesicke and Hoepfner, Schweinfurt). Values taken represent daily means (|ig m"3) that were obtained from hourly readings from October 1981-November 1988, and from half-hour readings from December 1988 onwards. Mean daily temperature (°C) and relative humidity (%) were taken as weather variables. Data were obtained from the central station in East Berlin, Alexanderplatz.22 The measurements were made on a 3-hourly basis. Data Analysis Multiple regression models were used to study the relationship between air pollution indices and daily mortality, controlling for weather variables. Though linear regression models assume normally distributed errors with a constant variance, a criterion not met when analysing count data, results from linear regression models do not differ from those obtained by Poisson regression models. 23 ' 24 Models using mortality on the same day, as well as daily mortality lagged for up to 5 days were specified. Differences of daily mortality from its 15- and 29-day moving average were also used as dependent variables. All models included dummy 1221 variables for week-day, month and year. Transformations of the independent pollution variables were used as indicated by plots, obtained when grouping pollutant values in increasing order of 50 adjacent values and plotted against the relevant mortality means (Figure 1); of these, the ones with the highest R2 and lowest Akaike Criteria were selected for the model.5 In order to estimate cumulative pollutant effects, models were also specified with multiple-day moving averages of pollutant concentrations (up to 6 days, including and excluding the concurrent day). All models were controlled for covariates; for temperature and humidity, the moving averages of the same time range as the pollutants were used. Data analysis was carried out using the Statistical Analysis System SAS, Cary, North Carolina, USA. RESULTS Daily numbers of deaths ranged from 17 to 64, and mean number of deaths per day ranged from 36.0 during winter 1988/1989 to 41.5 during winter 1981/1982 (Table 1). Daily mean concentrations of SO 2 ranged from 2 to 997 ug m"3, and those of SP from 10 to 566 ng m~3; mean and median levels of SO 2 and SP are shown in Table 1. As expected, high positive correlations were observed between daily SO2 and SP (Pearson correlation coefficient = 0.75), and negative ones for temperature and SO 2 (Pearson correlation coefficient = -0.47), and SP (Pearson correlation coefficient = -0.32), respectively. When SO2 and SP levels were grouped in increasing order for adjacent values and plotted against mean mortality, lagged for 2 days (Figure 1), the slope obtained decreased at higher levels for both pollutants, thus being compatible with a logarithmic transformation. Since the natural log transformations gave the highest R2 and lowest Akaike Criteria for each, SO 2 and SP concentrations of previous days, they were used for further anaylsis. Since the actual pollutant concentrations on the concurrent day, and—for SO 2 on the third previous day—gave a marginally better fit, they were used (Table 2). For temperature (not shown) the slope was inverse and nearly linear, though slightly decreasing at both ends. As the majority of the values (>95%) were in the linear part of the slope, no transformations were made. When these variables were regressed on daily mortality, and mortality lagged for up to 5 days, SP was a significant predictor of mortality lagged for 1-3 days, while SO 2 was significant in models using mortality lagged for I, 2 and 4 days (Table 2). The highest estimates were observed for the model using mortality 1222 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY TABLE 1 Mean and standard deviation (SD) of daily mortality and daily temperature (° Celsius) and mean and median concentrations (fig m3) of sulphur dioxide and suspended particulates in East Berlin, winters 1981-1989 (1 October-31 March) Winter Mortality Mean (SD) Temperature Mean (SD) SO2 Mean (median) SP Mean (median) 1981-1982 1982-1983 1983-1984 1984-1985 1985-1986 1986-1987 1987-1988 1988-1989 1989a All 41.5(7.1) 38.7(7.1) 38.5 (6.9) 40.8 (7.2) 40.1 (7.9) 38.0 (6.4) 37.1 (6.3) 36.0 (6.3) 35.6 (6.8) 38.6 (7.0) 3.4 (5.6) 5.9 (4.4) 4.6 (4.8) 3.3 (6.6) 2.8 (6.3) 2.6 (6.7) 5.3(4.1) 6.0 (4.0) 7.1 (4.8) 4.4 (5.6) 184(130) 171 (144) 205 (157) 219(182) 157 (126) 173(125) 130(103) 107 (81) 172 (140) 166 (129) 118(93) 94 (87) 120(100) 116(104) 92 (88) 93 (74) 75(71) 73 (58) 91 (71) 97 (82) ' 1 October-31 December 1989. 44CO X42- x • • x • JJ Q 1 < D Z 38< LLJ •* * * w • x • •x * x" 36*• 340 x SO2 • SP ! ,— 100 200 300 400 500 600 700 SO2 and SP (/ug/m3) FIGURE 1 Daily deaths by mean daily concentrations of sulphur dioxide and suspended particulates (fig m~3), grouped for 50 adjacent values of pollutant concentrations, and corresponding mean daily deaths, 2 days later, East Berlin, winters 1981-1989 lagged for 2 days. When including both pollutants simultaneously into those models, where at least one pollutant was a significant predictor in the singlepollutant model (mortality lagged for 1-4 days), the estimates of both pollutants were on average reduced by 40-45%, but there was considerable variation and no consistent pattern for the various lag times (Table 2). While SO 2 concentrations were more robust on days /_, and t_i, SP concentrations were on days t_2 and t_3. Table 3 presents the models with mortality lagged for 2 days, starting with ln(SO2) or ln(SP), and successively adding other variables. Controlling for week-day (model 2) did not result in a considerable improvement of fit, whereas inclusion of dummies for months (model 3) and years (model 4) did. The addition of temperature (model 6) caused a significant improvement, and reduced the coefficient of SO 2 and SP by 40%; thus temperature explains much of the mortality variation attributed to SO 2 or SP in the previous models. Table 4 shows the effect estimates after omission of days with SO2 and/or SP levels > 150 (Xg m"3. In this pollution range the actual concentrations gave a marginally better fit than the log-transformed ones; even in this low range of pollution, each pollutant was significantly associated with excess mortality, being associated with a 6.1% mortality increase per 100 (ig m~3 increase in SP (2.28/37.5), and 4.5% per 100 (ig m"3 increase in SO 2 (1.72/37.5) levels. After control for the other pollutant, the SP estimates dropped by 25%, while that for SO 2 was diminished by 40%; thus, based on the coefficients in the two-pollutant model, an increase in SP concentration of 100 u.g rrT3 would result in about 4.6% increase in mortality 2 days later, compared to a 2.8% mortality increase for a 100 fig m~3 increase in SO 2 (1.71/37.5 and 1.04/37.5). Possibly because of the low numbers of daily deaths, first order autocorrelation was not significant (DurbanWatson statistic). Nevertheless, removal of possibly existing seasonal trends was sought by using differences of mortality from its 15- and 29-day moving averages. Of these, differences of mortality from its 29-day moving average decreased autocorrelation to nearly zero (-0.003). In these models R2 decreased to 3% of its original value, suggesting that, although some shortterm effects, for example epidemics, are controlled for, an underestimation of other 'real' effects, for example high pollution episodes, has also occurred. AIR POLLUTION AND MORTALITY IN EAST BERLIN 1223 TABLE 2 Coefficients of mean daily concentrations of suphur dioxide and suspended particulates and/or their natural logarithm in regression models with daily mortality as dependent variable, lagged for 1-5 days; all models are controlled for temperature, humidity, week-day, month, and year; East Berlin, 1981-1989 Models including single pollutant Daily mortality P so2 t '+i* '+3a ' • / P STE 0.0019 0.0034 0.500* 0.621 0.635* 0.876* 0.0028 0.819* 0.387 0.819* 0.510* 0.566 0.207 0.124 SP ln(SO 2 ) ln(SP) ln(SO 2 ) In(SP) SO 2 C In(SP) ln(SO 2 ) ln(SP) ln(SO 2 ) ln(SP) ln(SO 2 ) ln(SP) Models including both pollutants 0.0015 0.0011 0.335 0.291 0.345 0.590 0.0008 0.694 -0.027 0.841 0.391 0.243 0.246 -0.079 0.0015 0.0030 0.255 0.330 0.254 0.332 0.0015 0.331 0.256 0.331 0.256 0.332 0.257 0.334 % decrease1" STE 0.0021 0.0044 0.331 0.429 0.329 0.427 0.0019 0.427 0.331 0.430 0.332 0.431 0.334 0.433 -21% -68% -33% -53% ^16% -33% -71% -15% 5100% +3% -23% -57% + 19% 3=100% a Daily mortality lagged for 1,2,3 etc. days. Per cent decrease in the effect estimate in the two-pollutant model compared to the single-pollutant model. ' SO2 gave a slightly better fit than ln(SO2). * Significant at P < 0.05. b TABLE 3 Regression models with the natural logarithm of mean daily concentrations of sulphur dioxide (left side) and suspended particulates (right side), with daily mortality (2 days lagged) as dependent variable, East Berlin, winters 1981-1989 No. of predictors Description 1 2 3 4 5 6 7 one pollutant model 1+weekdays model 2+months model 3+years model 4+humidity model 5+temperat. model 6+ln(SOj/SP) 1 7 12 20 21 22 23 ln(SO 2 ) ln(SP) P SEa R2'b 1.97 2.10 1.54 1.09 1.04 0.64 0.34 0.21 0.22 0.23 0.25 0.25 0.25 0.33 0.058 0.062 0.096 0.135 0.140 0.165 0.165 "CO Model no. SE° R2'b 2.48 2.61 2.22 1.62 1.54 0.88 0.59 0.31 0.31 0.31 0.31 0.32 0.33 0.43 0.039 0.048 0.101 0.140 0.140 0.162 0.165 * SE = standard error of the coefficient. b Adjusted model R2. c Plus inclusion of the other pollutant. When estimating cumulative effects of pollutants, the of the pollutants was significantly associated with an pollutant increase in mortality. When including moving averages concentrations (not transformed) of the previous 4 days of both pollutants, the effect estimates for SP were (not including the concurrent day) gave the best fit reduced considerably to about 40% of their original (Table 5). In models including only one pollutant, each values, while those for SO 2 were reduced to only 70%. model using the moving average of the 1224 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY TABLE 4 Coefficients of mean daily concentrations of SO2 and SP after exclusion of days with mean concentrations of sulphur dioxide and/or suspended particulates exceeding 150 fig m3 (n = 866) in models with daily mortality, lagged for two.days, as dependent variable Mean concentration (Mg m3) SO2/_. SPr, 85.2 66.3 Model including both pollutants Model including one pollutant 0.0172* 0.0228* STE J STE 0.0071 0.0083 0.0104 0.0171 0.0080 0.0094 * Siginificant at P < 0.05. TABLE 5 Coefficients of moving averages of mean daily concentrations mortality as dependent variable Moving average 3 of sulphur dioxide and suspended particulates Models including single pollutant SO 2 SP SO 2 SP SO 2 SP in models with daily Models including both pollutants P STE P STE 0.0039* 0.0070* 0.0040* 0.0110* 0.0044* 0.0078* 0.0016 0.0033 0.0018 0.0035 0.0018 0.0037 0.0030 0.0025 0.0025 0.0041 0.0032 0.0032 0.0025 0.0049 0.0027 0.0054 0.0029 0.0056 a Moving average of pollutant concentration of previous / days. * Significant at P < 0.05. DISCUSSION A significant association was found between ambient SO 2 and SP concentrations and daily number of deaths on the ensuing 4 days in East Berlin during the winters of 1981-1989. In single pollutant models, controlled for covariates, the mortality effect was most pronounced on the second day. Graphic analysis of the relationship (Figure 1) revealed curvilinear functions with steeper slopes at lower mean concentrations that level off with increasing pollutant concentrations. This has been reported previously, as has been the lack of an indication for the existence of a threshold. 5 " 91314 - 24 Previous studies have found, varying with the degree of pollution observed and species measured, mortality increases of about 4-8% per 100 (ig m~3 increase of particulates, 5 ' 913 " 15 - 23 ' 24 and between 0.5 and 5% per 100 fig m"3 increase in SO 2 levels. 6 1 0 " 1 3 This is in agreement with our results. The majority of previous studies, however, which used the same or similar pollution variables, found one of the two to be the major predictor of excess mortality, rendering the other one insignificant when both were included simultaneously. Most recent studies have reported particulates or BS as having a stronger association with excess mortality than SO 2 , for example in Detroit, Philadelphia, Steubenville, Ohio, London, and Erfurt. 5 ' 6 ' 8 ' 913 Spix et al.u have recently examined the association of daily air pollution and mortality in Erfurt, which is located about 200 km southwest of Berlin. SO 2 levels, available from 1980 until 1989, were in general, much higher than in Berlin, with a winter median of 364 u.g m"3. Daily mortality in Erfurt, lagged for 2 days, increased by 10% for an increase in SO2 from 23 to 929 ng m"3 (5th to 95 lh percentile); this is comparable to our results. Only for the years 1989 and 1990 were SP data available in Erfurt and the SP levels were comparable to those in Berlin. During these 2 years, the effect of SP was stronger than that of SO 2 , with an increase from 15 to 331 |ig m -3 being associated with a 22% increase in mortality on the same day. Though SO 2 levels were high during these AIR POLLUTION AND MORTALITY IN EAST BERLIN two years (winter medians of 275 and 208 jig m 3 ), their mortality effect was very small then, and reduced to nearly zero, when SP was considered simultaneously, while the effect of SP was only slightly decreased in the two-pollutant model. Therefore, the authors conclude, as have others who found similar results in other locations,5>6>8>9 that the mortality effect is caused by particluates, while SO2 acts as a proxy of another pollution agent or as a mere indicator for general air pollution. While our results agree with those from Erfurt and other sites regarding the logarithmic nature of the relationship, the magnitude of the effects, and the higher effect estimates for SP than for SO 2 , there are remarkable differences. Firstly, SP mortality effects were lagged in Berlin, as has also been reported from other locations,5'14'15'24 while they occurred on the concurrent day in Erfurt. Secondly and more importantly, when considering SO 2 and SP simultaneously in Berlin, SP effect estimates were—on average—destabilized by the same amount as were SO 2 estimates. Though, when considering the day with the maximum effect, that is after 2 (and 3) days, the SP mortality association was robuster than the SO 2 one, the former was severely diminished after control for SO2, when mortality was lagged for 1 or 4 days. In models using moving averages of pollutant concentrations over the previous 2-4 days, when controlling for the other pollutant, mortality associations were stronger with SO 2 than with SP. Therefore, the strong and superior effect of SP over SO2 found in Erfurt and elsewhere, 5 ' 14 ' 15 was not seen in Berlin during the winters 1981-1989. There is certainly some collinearity problem here that makes it difficult to discriminate their relative contribution. Furthermore, the physico-chemical behaviour as well as toxicity at a given site, are modified by temperature, humidity, distribution of existing particle sizes, and the presence of other pollutants.3'19 Several recent reports have emphasized the importance of acidic aerosols and acidic particulates 16,18-20 as more plausible candidates for causing health effects than the pollutants measured routinely. The notion that the observed associations in East Berlin are probably confounded by other co-existing pollutants cannot be excluded from the data. However, causality of the relationships—at least in part—is supported by studies relating these air pollutants to cause-specific-mortality11 and morbidity. At ambient concentrations of < 100 |ig m"3 for SO 2 and BS, significant associations between pollutant levels and emergency room admissions for chronic pulmonary diseases have been reported from Barcelona, Spain.12 Similar TSP levels were associated with increased incidence of croup cases in German cities, 25 and hospital admissions from respiratory conditions were associated with PMIO 1225 levels in Utah, USA.26 The relative contribution of these, and the importance of other existing pollutants, remains to be investigated in further studies. Constraints of the present study include the imprecise exposure data, derived from only one sampling point (the only one existing over the whole period), the lack of information on other pollutants existing, and finally, the use of a rather crude measure of health effects. Despite these constraints however, significant associations were found between SO2 and SP levels, and mortality in East Berlin. These associations were significant at concentrations well below air pollution standards. In summary, the association between air pollutants and daily mortality in East Berlin is quantitatively similar to results of other recent studies, though the often reported stronger mortality association of particulates compared to SO 2 was not found here. It would be of great value to investigate these issues in greater detail, covering more pollutants, and their possible interactions. ACKNOWLEDGEMENTS The authors thank Dr D Obrikat, Institut fuer Strahlenschutz, Berlin, Dr Casper, and Dr W Mehnert, Robert-Koch-Institut, Berlin for co-operation and Dr J Stolwijk, Yale University for advice. Thanks are extended to Dr J Hanley, McGill University and Dr Eshetu, Dept. of Statistics, Addis Ababa University for computational help, Dr R Waller, Dept. of Health, London, Dr K Katsouyanni, Athens, K Salmon, Belfast and Dr Prinz, Marburg for valuable comments. REFERENCES ' Firket J. 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