From the Institute for Social and Preventive Medicine, University of Berne, Berne, Switzerland.
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ABSTRACT |
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brain neoplasms; electromagnetic fields; environmental monitoring; leukemia; occupational exposure
Abbreviations: CI, confidence interval; ELF, extremely low frequency; ICD-8, International Classification of Diseases, Eighth Revision.
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INTRODUCTION |
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In Switzerland, the study of railway workers offers an excellent possibility for investigating the health effects of ELF magnetic fields. Exposures of railway engineers can be measured and extrapolated accurately, since the position of a train's driver is fixed and electromagnetic characteristics stay the same over the lifetime of an engine, thus permitting reliable extrapolation. In addition, the Swiss railways have extensive, mostly electronic records on their employees, which allows cohort studies. An earlier study showed excess mortality from malignancies of the hematopoietic and lymphatic systems for engineers as compared with workers in metal construction and engineering and technical personnel (14). Subsequently, measurements of ELF magnetic fields in Swiss railway engines were made, showing magnetic field strengths in the 36,000 µT range at the workplaces of railway engineers (15
).
The purpose of the present study was to use better methodology to reassess whether, for Swiss railway engineers, exposure to electromagnetic fields is associated with an increased risk for leukemia or brain tumors. In particular, we wanted to investigate the following two hypotheses (adapted from the original project funding proposal from 1991, with slightly changed wording):
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MATERIALS AND METHODS |
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Vital status and cause of death
Mortality follow-up covered the period between January 1, 1972, and December 31, 1993. Probabilistic record linkage (16, 17
) was used to determine the vital status and mortality endpoints of cohort members by linking personnel or pension records to (anonymous) death certificates. Linkage variables used were date of birth, date of death, place of residence, occupation, marital status, and duration of marriage if married. Prior to linking, knowledge of the vital status of cohort members was completed by searching union journals and noting all deaths in the four study job categories. The computerized records of death certificates were then matched by name and date of birth to personnel or pension records. Only deaths with complete agreement regarding dates of birth and death on the personnel or pension record and the death certificate and with an odds ratio for correct linkage (vs. linkage due to random agreement) exceeding 1,024 were accepted. Finally, the vital status of all 123 linked cases with a cause of death of leukemia, other hematopoietic or lymphatic neoplasm, or brain tumor were manually verified against archived pension records. The data sources (personnel records, pension records, and death certificates) and linkage variables used did not differ between occupations.
Outcomes
The main mortality outcomes were leukemia (International Classification of Diseases, Eighth Revision (ICD-8), codes 204207; 37 cases) and brain tumors (ICD-8 code 191; 23 cases) (18). In addition, we analyzed deaths from any cause, all cancer deaths, and lung cancer deaths (ICD-8 code 162) for validation purposes. Table 1 gives the numbers of deaths in each category, including leukemia subtypes.
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Employment data with beginning and ending dates, duration, and job category were available for all cohort members. We assigned each person to the job category last mentioned. With few exceptions, this corresponded to the job held the longest, since there was limited switching between job categories. However, younger line engineers often worked in shunting yards (M. Gerber, Motive Power Construction Division, personal communication, 2001).
Assessment of magnetic field exposure
Swiss trains run on 16-Hz alternating current. For our measurements, we used a device developed by Bramur, Inc. (Lee, Massachusetts). Tests conducted at the technical laboratory of Swisscom (Berne, Switzerland) confirmed that it was reliable for recording magnetic flux density in the frequency range between 0 Hz and 100 Hz. Measurements of root mean square field strength were taken at 10-second intervals and stored in a battery-powered computer. Figure 1 shows the readings from one driving cycle. The raw readings were processed to extract mean exposure, as well as the time fraction with field strength at or above 10 µT. This fraction is a simple measure of exposure dynamics.
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For modified engines in which exposure was not measured, the measurements of the corresponding main type of engine were used.
Calculation of historical exposure. Swiss line engineers switch engines several times daily, and over time they drive a changing mix of engines. We obtained the numbers of engines in service every 5 years from 1905 to 1995 and estimated the ELF magnetic field load for each 5-year calendar period by calculating weighted averages of engine-specific exposures. A similar approach was used to estimate the historical exposure of shunting yard engineers, including an average of 36 percent steam-powered engines (19051965) and later diesel-electric engines (19541995). We assumed that steam-powered and diesel-electric engines gave zero exposures (diesel-electric engines being direct-current engines).
For independent validation of the historical exposure reconstruction, we assembled the engine sequences of the daily service tours of 52 line and 14 shunting yard engineers for several weeks in 1993 (19).
Exposure assessment for train attendants and station masters. Train attendants and station masters do not work at the same location for extended periods of time. Therefore, spot measurements lasting for 230 minutes were taken at their most frequent places of work (train attendants: various positions within the coaches; station masters: platform and office). Exposure was then estimated as a time-weighted average of location-specific field strengths. The weights were estimated in close collaboration with railway authorities, taking into account the fractions of air-conditioned and electrically powered coaches.
Calculation of historical exposure. For train attendants and station masters, only recent measurements were available. Historical exposures were linearly interpolated between 0 µT for 1900 and the exposure level of 1993.
Data analysis
Data were analyzed using SAS (20) and Stata (21
). Record linkage was carried out using probabilistic linkage with the LinkPro subroutine package (17
). For cohort analysis, we used Clayton's algorithm as described by Breslow and Day (22
), with 5-year age groups/5-year periods/exposure categories as units of analysis. The cumulative exposures were classified into three categories: 04.99 µT-years, 5.0074.99 µT-years, and
75 µT-years. We determined these cutoffs from the empirical frequency distribution of cumulative exposure to obtain an approximately equal distribution of person-years across the exposure categories. Similarly, the time fractions of each year spent under ELF magnetic field exposures of
10 µT were cumulated over life. These were aggregated into the following groups:
0.099 years, 0.1000.499 years, and
0.50 years (feet:
0.199 years, 0.20.499 years, and
0.5 years).
To estimate mortality rate ratios and their 95 percent confidence intervals, we carried out Poisson regressions using number of deaths from leukemia or brain cancer per unit of analysis (see above) as the dependent variable and 5-year age group, 10-year calendar period, and job or exposure category as the independent variables. For estimation of the dose-response curves, we classified exposures into five classes by subdividing the lowest class and the middle class. The number of person-years at risk was included as an offset in the models. We carried out trend analyses using weighted regression with mortality rate ratios as dependent variables and job-related exposures as independent variables.
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RESULTS |
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Each cohort member was assigned the job he held when he left the cohort. Job changes were not frequent. Fifteen percent of shunting yard engineers were promoted to the position of line engineer. Fewer than 2 percent of line engineers changed to shunting yard engineer, and none became train attendants or station masters. Fewer than 2 percent of station masters and train attendants changed their job category.
Accuracy of exposure information
Treating the engine mix driven by each line engineer as a random sample of all engines available at the time, the coefficient of variation of the cumulative occupational exposure reconstruction was estimated at 18 percent for the head, 25 percent for the thorax, and 40 percent for the feet. For shunting yard engineers, the coefficient of variation of the reconstructed estimate of cumulative exposure was estimated to be 26 percent regardless of body location. Estimates of cumulative exposure obtained by reconstructing average exposure using the daily work plans of 52 line engineers and 14 shunting yard engineers over a 2-week period were within 10 percent of the historical reconstruction estimates described above. For station masters, the coefficient of variation of the reconstruction was approximately 40 percent. For train attendants, the coefficient varied from 25 percent at the head and thorax levels to 60 percent at the feet.
Table 3 shows the exposure characteristics of the four occupations for the years 1930, 1960, and 1990. There was a fairly steady increase in the estimated exposure levels.
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Study hypotheses
To assess the occupational hypothesis (see Introduction), we calculated mortality rate ratios for five causes of death and three job categoriesline engineers, shunting yard engineers, and train attendantseach compared with station masters (table 4). No differences between occupations were apparent for all-cause mortality or lung cancer mortality. However, there appeared to be differences in leukemia mortality between engineers on the one hand and train attendants and station masters on the other, although statistical significance was not attained. Risk of brain tumor mortality appeared to be elevated for shunting yard engineers and train attendants, but only the shunting yard engineers' risk relative to that of station masters was significant.
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To assess the dose-response hypothesis (see Introduction), we estimated a dose-response curve by including all occupations together in a Poisson regression with number of leukemia (or brain tumor) deaths as the dependent variable, offset person-years at risk (22, p. 137), and the independent variables age group, calendar period, and exposure category. The results are shown in table 5 for various measures of exposure. For leukemia, there was an excess risk in the highest exposure category regardless of the way exposure was assessed. This excess attained significance for time spent under ELF magnetic fields 10 µT at the thorax level; it did not reach significance at the other body sites or for mean exposure. For brain tumors, no consistent increase in risk with dose was visible, regardless of the measure used. However, the lowest category seemed to have a lower risksignificantly so for time spent under ELF magnetic fields
10 µT at the level of the feet.
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DISCUSSION |
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Brain tumors seemed to aggregate in the occupations of shunting yard engineer and train attendant. These two occupational groups may have a common exposure that causes brain tumors. However, it is unlikely that electromagnetic fields are solely responsible for this finding. We did not find a dose-response relation between exposure to ELF magnetic fields and risk of brain tumor mortality. Speculatively, the results shown in table 5 could be interpreted to mean that risk of brain tumor mortality exhibits a threshold with respect to ELF magnetic field exposure. We found elevated brain tumor rates for occupations that in other studies had been found to entail exposure to the highest electric fields: shunting yard engineers and train attendants. Hence, our results fit in with Guénel et al.'s (23) conclusion that brain cancer risk relates more to electric field exposure than to magnetic field exposure. However, Guénel et al.'s findings were not confirmed by Miller et al. (24
).
Limitations
In this study, there was potential for exposure bias from several sources. Measurements were done in different ways for the four occupational groups. The effect of this was probably minor, since the largest potential for bias was with the occupations of generally low exposure: These were measured least precisely. Historical extrapolation could be based on erroneous judgment about past exposures, either over- or underestimating exposures. It is hard to assess the possible effect of this, except that the relative order of occupations with respect to exposure would probably be preserved. In view of the above discussion, the nonassessment of electric field exposure must be considered a weakness.
Ascertainment of death
Probabilistic record linkage poses the problem of false positives (false links) and false negatives (missed links). With the restrictive strategy we used, the numbers of deaths and causes linked to the wrong person were certainly small. From the manual verification of cancer deaths, in which we found one person still alive among 122 deaths checked, we estimate it to have been less than 1 percent. On the other hand, we probably missed some deaths, which reduced the power of our study as well as the size of the estimated effects of ELF magnetic fields. The number of deaths missed was probably less than 4 percent, since most of these deaths would have been found among the 147 additional deaths linked when less restrictive linkage rules were applied. We can discern no reason why these losses should have differed according to occupation. Ascertainment of causes of death such as leukemia and (especially) brain cancer may be subject to errors. A validation study showed that the quality of cause-of-death data was good for leukemia and fairly good for brain tumors (see Materials and Methods section).
Exposure assessment
We had employment data, including duration and type of activity, for all members of our cohort. All of the major engines that had ever been in use were measured repeatedly so that exposure could be assessed precisely, and extrapolation was fairly straightforward. Taken together, this means that in the present study, accurate exposure assessment was possible for the highly exposed group. For the less exposed groups of station masters and train attendants, the relative accuracy is lower. Because newer electric and electronic equipment, most notably air conditioning in coaches (since 1964) and computers in station offices (since 1985), was introduced rather recently, the linear historical interpolation used probably led to an overestimate of the historical exposure of these groups, decreasing any estimate of the effects of ELF magnetic fields. However, for these occupations as well, the absolute level of exposure was determined fairly accurately (±1 µT-years).
The data logging at 10-second intervals permitted us to quantify and investigate the health effects of length of time spent under magnetic fields of 10 µT, in addition to the more customary cumulative exposure. In a crude way, this measure describes the dynamics of the exposure process. We neglected leisure time and home exposures, because we judged them to be negligible in comparison with occupational exposures.
Confounder assessment
From the information obtained about the substances used for cleaning and maintenance, there seems to be no reason to suspect any confounding effect. A substudy showed that line engineers smoked less than either shunting yard engineers or train attendants. Line engineers, working mostly alone in their driver's stands, tend to have fewer contacts with other people than workers in the other occupations investigated. Both of these characteristics reduce the exposure of line engineers to two suspected (but not well established) causes of leukemia.
Comparison with literature
Comparison of our study with other occupational or residential studies in the literature is complicated somewhat by the fact that most other studies were concerned with the effects of 50- or 60-Hz alternating current on health, while in our study, 16 Hz was the frequency assessed. It is instructive to compare our study with three other studies (7, 25, 26) of railway personnel exposed to 16
-Hz ELF magnetic fields. Table 7 provides a comparison with these studies.
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We are aware of two occupational studies besides this one that permit the estimation of a dose-response relation (4, 10
). Table 8 summarizes the findings of these studies. There is no statistical disagreement between the findings of the present study and those of Floderus et al. (4
), but there is statistical disagreement with the findings of Tynes et al. (10
). However, the latter study reported results on exposure that are difficult to reconcile with each other: A yearly average exposure of 20 µT (10, p. 647) would necessitate 95 years of exposure for accumulation of 1,900 µT-years, which is the border between the highest and second highest exposure categories in Tynes et al.'s table 3 (10, p. 650).
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The findings of the present study do not result from data-dredging, because we evaluated two hypotheses formulated a priori (see Introduction).
The frequency of 16 Hz has some special interest in view of findings on a frequency-dependent calcium efflux from cells at the frequency of 15 Hz and multiples thereof (27
). Another mechanism of cancer promotion being discussed is based on melatonin, since melatonin appears to be involved in modulation of the immune system (28
) and has oncostatic properties (29
). In a related study, the melatonin metabolism of locomotive engineers was investigated (19
). This study showed a suppression effect after onset of exposure which could not be explained by the shift work. Comparable findings were reported by Burch et al. (30
). Thus, a possible pathway of leukemia causation is a disturbance of melatonin metabolism.
Conclusions
This study contributes to the evidence that exposure to ELF magnetic fields in high dosages over prolonged time promotes or generates leukemia. The best estimate of the dose-mortality relation is an increase of approximately 1 percent per µT-year of cumulative thorax exposure. On a methodological level, this study reinforces the impression that accurate assessment of electromagnetic field exposure through historical reconstruction is crucial. With the moderate size of the risks involved and the rarity of leukemia and brain tumors, even moderate exposure misclassification will invariably lead to insignificant results.
What are the consequences of this study and similar studies with respect to prevention? We believe that monitoring of electromagnetic field exposure is indicated for railway personnel, both to maintain their health and to prevent an accentuation of risk through further increases in exposure.
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ACKNOWLEDGMENTS |
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The authors thank N. Antille, M. Bräuchi, G. Burkard, T. Furrer, M. Gerber, Dr. R. Gränicher, P. Kurth, E. Mathez, D. Reichen, D. Schneider, and J. P. Terrapon of the Swiss Federal Railways for their help with data access and data acquisition. They acknowledge the various Swiss tumor registries and hospital pathology centers for verifying the diagnoses. The authors also thank Drs. T. Abelin, M. Egger, R. Gugelmann, G. Schüler, and A. Stuck for their many valuable comments and suggestions.
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NOTES |
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Editor's note: An invited commentary on this article appears on page 836, and the authors' response appears on page 839.
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REFERENCES |
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