Prospective Study of Occupation and Amyotrophic Lateral Sclerosis Mortality

M. G. Weisskopf1,2, M. L. McCullough3, N. Morozova4, E. E. Calle3, M. J. Thun3 and A. Ascherio1,4,5

1 Department of Nutrition, Harvard School of Public Health, Boston, MA
2 Department of Environmental Health, Harvard School of Public Health, Boston, MA
3 Epidemiology and Surveillance Research, American Cancer Society, Atlanta, GA
4 Department of Epidemiology, Harvard School of Public Health, Boston, MA
5 The Channing Laboratory, Department of Medicine, Harvard Medical School and Brigham and Women's Hospital, Boston, MA

Correspondence to Dr. Marc G. Weisskopf, Harvard School of Public Health, Department of Environmental Health, Landmark Center, 3rd Floor East, PO Box 15697, Boston, MA 02215 (e-mail: mweissko{at}hsph.harvard.edu).

Received for publication May 31, 2005. Accepted for publication August 24, 2005.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Occupational exposures are suspected of contributing to the risk of amyotrophic lateral sclerosis (ALS), but results of epidemiologic studies have been inconsistent. The authors prospectively assessed the relation between occupation and ALS mortality among more than 1 million participants in the Cancer Prevention Study II of the American Cancer Society. Follow-up from 1989 through 2002 identified 507 ALS deaths among men and 430 among women. Adjusted rate ratios were calculated by using Mantel-Haenszel weights and Cox proportional hazards. Among men, elevated ALS mortality was found for programmers (rate ratio = 4.55, 95% confidence interval: 1.46, 14.2; p = 0.009) and laboratory technicians (rate ratio = 1.96, 95% confidence interval: 1.04, 3.66; p = 0.04). Occupations previously associated with increased risk of ALS for which no increased risk was found included farmers, electricians, and welders, although the numbers of electricians (eight ALS deaths) and welders (two ALS deaths) were small. Among women, only machine assemblers had significantly increased ALS mortality (rate ratio = 2.81, 95% confidence interval: 1.05, 7.53; p = 0.04). Results, which suggest that male programmers and laboratory technicians and female machine assemblers may be at increased risk of death from ALS, should be interpreted cautiously, however, because they are based on small numbers.

motor neuron disease; occupations; prospective studies


Abbreviations: ALS, amyotrophic lateral sclerosis; CI, confidence interval; CPS-II, Cancer Prevention Study II; EMF, electromagnetic fields; RR, rate ratio


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
A role for environmental exposures in the etiology of amyotrophic lateral sclerosis (ALS) is suggested by the epidemic occurrence of an ALS-Parkinson's complex in the western Pacific (1Go–3Go), differences in incidence by geographic region (4Go), and results of case-control studies implicating particular environmental or occupational exposures (5Go–14Go). Farming and farming chemicals (9Go, 10Go, 12Go, 15Go, 16Go), exposure to electromagnetic fields (EMF) (17Go, 18Go), welding (8Go, 11Go, 14Go, 19Go), and electrical work or electric shock (8Go, 11Go, 13Go, 20Go–22Go) are occupations or exposures that have been found to be related to risk of ALS. Most of these findings, however, are from case-control studies, which are prone to recall bias and biased control selection (5Go, 6Go, 23Go, 24Go). We therefore undertook a prospective cohort study of occupation and ALS mortality using data from the Cancer Prevention Study II (CPS-II) cohort of the American Cancer Society (25Go).


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Study population
CPS-II is a prospective cohort study of nearly 1.2 million US men and women, begun in 1982. Participants were recruited by American Cancer Society volunteers in 50 states, the District of Columbia, and Puerto Rico (25Go). Families with at least one member over age 45 years, and other family members over age 30 years, were invited to participate. The median age at cohort entry in 1982 was 57 years for men and 56 years for women. In total, 508,308 men and 676,253 women completed a four-page questionnaire at baseline. Because deaths from ALS before 1989 were not coded separately, we restricted our study to the 459,334 men and 639,331 women who were still alive as of January 1, 1989. Furthermore, since CPS-II participants may have had ALS when they responded to the baseline questionnaire in 1982, we excluded the 44,216 men and 65,832 women who reported a major illness at baseline (specific information on ALS status was not available). For an additional 11,329 men and 23,967 women, occupational data were missing. Excluded participants were slightly older than those who were included in the analyses (69.1 (standard deviation, 10.8) vs. 63.4 (standard deviation, 9.7) years for men and 67.7 (standard deviation, 12.3) vs. 62.8 (standard deviation, 10.6) years for women) as expected given the exclusion based on illness, but there was little difference in smoking status, educational level, alcohol intake, body mass index, or race. The follow-up period extended from January 1, 1989, to December 31, 2002.

Case ascertainment
Vital status of the study participants has been determined by automated linkage with the National Death Index through December 31, 2002 (26Go). The National Death Index began providing multiple cause-of-death codes for linked deaths in 1993. Death certificates (1989–1992) or codes for cause of death (1993–2002) have been obtained for over 98 percent of known deaths. The underlying cause of death was coded according to the Ninth or Tenth Revision of the International Classification of Diseases, as appropriate (27Go, 28Go). Prior to and through 1988, deaths from ALS were coded together with rare causes of death and thus cannot be identified. Deaths occurring after 1988 and prior to 1999 were attributed to ALS if International Classification of Diseases, Ninth Revision code 335.2 (motor neuron disease) was listed as either the underlying or a contributing cause of death because, in a review of death certificates, we found that virtually all deaths with this code were diagnosed as ALS (98.3 percent) or bulbar palsy (1.1 percent) (29Go). Similarly, deaths occurring after 1998 were attributed to ALS if International Classification of Diseases, Tenth Revision code G12.2 (motor neuron disease) was listed as either the underlying or a contributing cause of death.

Assessment of exposure
In the baseline questionnaire, participants were asked their current occupation, the job they held for the longest period of time, and the years spent working in each. Retired participants were asked to report their last occupation, but the number of years spent in that occupation was assessed in a subgroup only. Therefore, for all retired participants in our analysis, we assigned as the number of years spent in the occupation from which they retired the median value for that occupation found in our subgroup analysis. The majority of respondents (58.3 percent) reported only one occupation and were assigned accordingly. Two occupations were reported by 40.2 percent, and 1.5 percent reported three occupations. Analyses were based on the job held the longest. Considering the adult working years to be those between age 22 years and the age at the time the questionnaire was completed for nonretired participants, the average percentage of working years that the job held the longest covered was 69.2 percent for men and 67.6 percent for women. Occupations were categorized according to the 1980 Bureau of the Census occupational titles (30Go) and were assigned to one of 13 broad occupational groups. Jobs that could not be classified according to the Bureau of the Census list were assigned to a separate category designated "unclassified."

Statistical analyses
Participants contributed follow-up time from January 1, 1989, to the date of death or December 31, 2002 (the most recent linkage with the National Death Index), whichever came first. Age- (5-year groups) and smoking-adjusted rate ratios were calculated using Mantel-Haenszel weights by dividing the incidence of death from ALS among participants in each category of occupation by the corresponding incidence among those in all other occupations. We used Cox proportional hazards regression to estimate multivariate rate ratios and 95 percent confidence intervals. To obtain a better adjustment, the Cox models were stratified by both age and calendar time in single years.

In primary analyses, respondents were assigned to the occupation in which they spent the greatest number of years (main occupation) and were compared with all workers who had other main occupations. Multivariable models were also run, additionally adjusting for education (some high school, completed high school, vocational/trade, some college, completed college/graduate school), alcohol intake (nondrinkers and quartiles of grams per day), and, among men, military service (yes/no) (31Go) because these variables have been previously suggested to be related to risk of ALS. Further adjustment for use of vitamin E—strongly related to lower ALS mortality in this cohort (32Go)—had no material effect on the rate ratio; therefore, results not adjusted for vitamin E are reported in this paper. Data on all covariates considered in the analyses were obtained from responses to the questionnaire in 1982.

Expected ALS deaths in different occupational groups were calculated on the basis of the age- (5-year groups) and smoking-adjusted rate ratios for each job or job category compared with all others. We do not report in the tables individual occupations with fewer than three observed ALS deaths, except for electricians and welders, because several previous studies have suggested an increased risk of ALS among these workers. Because duration of work or particular tasks within individual jobs may be quite different between men and women, we considered men and women separately. SAS version 8 software (SAS Institute, Inc., Cary, North Carolina) was used for all analyses.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Between 1989 and 2002, we documented 507 deaths from ALS during 4,913,369 person-years among men and 430 deaths from ALS during 7,081,569 person-years among women. Among men, a significantly increased age- and smoking-adjusted rate of ALS mortality was observed for technicians (broad category) and programmers, although the numbers of ALS deaths were small for this latter occupation (table 1). The average number of years worked in these jobs were 20.6 (standard deviation, 10.1) for technicians and 18.1 (standard deviation, 8.9) years for programmers. Neither electricians, welders, nor farmers had significantly elevated rates of ALS mortality (table 1). These results were not substantially altered by additional adjustment for education, alcohol intake, and military service (table 1). Because comorbidities would be more likely at older ages, we repeated the analyses with follow-up until age 75 years only (data not shown). Results of these analyses were similar, except that farmers appeared to have a marginally decreased ALS mortality rate (adjusted rate ratio (RR) = 0.46, 95 percent confidence interval (CI): 0.22, 0.98; p = 0.05). Results of analyses based on any mention of a particular job rather than the job held the longest were also similar (data not shown), except again that farmers appeared at marginally decreased risk of ALS mortality (adjusted RR = 0.66, 95 percent CI: 0.44, 0.99, p = 0.05).


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TABLE 1. Adjusted rate ratios of amyotrophic lateral sclerosis mortality by longest-held occupation among male participants in the Cancer Prevention Study II, United States, 1989–2002

 
Among women, no broad occupational category was associated with statistically significant increased ALS mortality (table 2). The only individual occupation to show a significantly increased risk was machine assembler. The average number of years worked as an assembler was 12.8 (standard deviation, 8.2). There were many fewer women farmers, electricians, and welders than there were men in these occupations. In contrast, more women were programmers (23Go,907 person-years of follow-up, one ALS death; not shown in table 2). None of these individual occupations showed increased ALS mortality. Results of analyses with follow-up to age 75 years only were similar. These results differed slightly when the analyses were based on any mention of a specific job (data not shown). In particular, in this analysis, the broad category of professionals showed elevated ALS mortality rates (adjusted RR = 1.35, 95 percent CI: 1.05, 1.75; p = 0.02), as did the individual occupations of nurse (adjusted RR = 1.61, 95 percent CI: 1.18, 2.21; p = 0.003) and welder (adjusted RR = 8.32, 95 percent CI: 1.17, 59.3; p = 0.03). However, this latter result was based on only one death from ALS.


View this table:
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TABLE 2. Adjusted rate ratios of amyotrophic lateral sclerosis mortality by longest-held occupation among female participants in the Cancer Prevention Study II, United States, 1989–2002

 
In analyses of main occupation that combined data for men and women, only nurses had increased ALS mortality (adjusted RR = 1.45, 95 percent CI: 1.00, 2.09; p = 0.05). The average number of years worked as a nurse was 17.2 (standard deviation, 10.4) for women and 17.2 (standard deviation, 10.1) for men. Data for male nurses are not shown in table 1 because there was only one ALS death. This ALS death occurred during 4,255 person-years of follow-up, however, so the adjusted rate ratio was elevated (RR = 2.93, 95 percent CI: 0.41, 20.9), although not significantly (p = 0.28). Too few deaths were associated with any given job to adequately assess the relation between duration of employment and ALS mortality.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In this large prospective study, we did not find an association between death from ALS and the occupations of electrician, welder, or farmer, each of which has been associated with ALS in previous studies. Among men, we found increased ALS mortality for programmers and laboratory technicians. Among women, we found increased ALS mortality for machine assemblers and a marginally significant increase for nurses. These results were based on a small number of cases in each occupational category, however, and should be interpreted cautiously. Furthermore, for programmers and laboratory technicians, the results were not consistent between men and women, and we could not determine from our data the extent to which this inconsistency might be the result of men and women performing different jobs or tasks within a given individual occupational group.

Several studies have examined the associations between ALS and occupation. Most have been case-control studies, which have implicated primarily the occupations of farming (9Go, 10Go), electrical work (8Go, 11Go, 13Go, 22Go), and welding (8Go, 11Go, 14Go). A population-based case-control study in Washington State supplemented self-reported history of occupational exposures with exposure assessed by a panel of industrial hygienists (12Go). In that study, the strongest association, a twofold increase in risk, was found for exposure to agricultural chemicals. A positive association between ALS and agricultural work or exposure to agricultural chemicals has also been found in other studies (9Go, 10Go, 15Go, 16Go, 20Go, 33Go), but not all (11Go, 14Go, 34Go). EMF exposure was also found in multiple studies to be associated with ALS risk (17Go, 18Go). In particular, this exposure has been studied among cohorts of utility company and engineering industry workers in the United States, Denmark, and Sweden (19Go, 21Go, 35Go–37Go), although a case-control study in southern California not restricted to a particular occupation found an even stronger association (7Go).

Our results are consistent with some previous findings, but not others. The increased risk for laboratory technicians and machine assemblers could be consistent with an association with EMF because workers in these occupations can have increased exposure to EMF (38Go, 39Go). One report suggests that keypunch (data entry) operators can have high exposures to EMF (34Go); another suggests that computer operators have a wide range of exposures, with the higher end being greater than that for most other occupations surveyed (40Go). On the other hand, although EMF strength at the surface of the screen of video display terminals can be high, the field amplitude decreases rapidly with distance from the source, and such terminals have generally been thought to be a minor source of EMF exposure (41Go). In addition, electrician and welder are two occupations that also can entail high exposures to EMF (39Go, 42Go) yet, except for our analysis of any mention of welding among women, these occupations were not associated with increased ALS mortality in our study. These null findings in our study should be viewed cautiously, however, because the expected numbers of ALS deaths in these occupations were small.

We found marginally increased ALS mortality among female nurses, a finding consistent with a previous study that found an increased risk of ALS among females in medical services (10Go), although, in that study, the increased risk appeared more related to nurses' assistants than to nurses. This finding is also intriguing in light of recent suggestions of a possible infectious etiology for ALS (43Go). The lack of association with farming, although based on somewhat larger numbers, should also be interpreted cautiously because we cannot exclude the possibility of underreporting of ALS on death certificates in this group characterized by rural living and possibly lower access to specialized health care (44Go). Furthermore, in our cohort, this job category includes rancher and fisherman, so we do not know the extent to which participants in these jobs may dilute an effect among farmers.

Strengths of our study include its large size, the ability to control for other risk factors for ALS, and the prospective assessment of occupation prior to disease onset, which eliminates the problem that disease status may influence participation in the study or reporting of occupation. There are also several limitations. First, follow-up of the CPS-II cohort was limited to mortality and did not directly measure ALS incidence. However, bias from this source is likely to be small because median survival with ALS is short (1.5–3 years) (45Go–49Go) and mortality is thus a good surrogate for incidence.

A second issue is the validity of the ALS diagnosis reported on death certificates. The diagnosis becomes manifest as the disease progresses, and it is unlikely that a diagnosis of ALS would be made on the death certificates of patients who did not have the disease. In contrast, death certificate data have been estimated to accurately identify 70–90 percent of ALS or motor neuron disease cases (50Go–53Go). Thus, a small number of ALS deaths will have been attributed to other causes in CPS-II. If people in lower socioeconomic status occupations tended to be less likely to have ALS reported on their death certificates, then ALS mortality could be underestimated in these groups. The general validity of our ALS assessment is supported by the fact that age-specific mortality rates in our population are very similar to incidence rates found in a study in Washington State with a slight lag, because mortality reflects the incidence at younger ages, as we have reported previously (29Go).

Lastly, we did not have complete occupational histories of the participants, and our analysis is based on only that job held the longest. Although the percentage of adult working years that the job held the longest represented was nearly 70 percent, this analysis necessarily missed jobs held for shorter periods of time—some of which can be those with the highest chemical exposures. Potential bias from this limitation would most likely be toward the null.

In summary, in this large prospective study, we found increased ALS mortality for the occupations of programmer and laboratory technician among men and machine assemblers—and possibly nurses—among women. However, these few significant associations are based on small numbers and could be due to chance. In contrast, we did not find evidence of increased ALS mortality among farmers, electricians, or welders.


    ACKNOWLEDGMENTS
 
Conflict of interest: none declared.


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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