From the Department of Epidemiology and Medical Statistics, School of Public HealthWHO Collaborating Center, University Bielefeld, 33501 Bielefeld, Germany.
Received for publication January 31, 2002; accepted for publication May 1, 2002.
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ABSTRACT |
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aircraft; aviation; cohort studies; mortality; neoplasms; occupational exposure; radiation
Abbreviations: Abbreviations: AIDS, acquired immunodeficiency syndrome; CI, confidence interval; SIR, standardized incidence ratio; SMR, standardized mortality ratio.
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INTRODUCTION |
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Occupational factors that are potentially relevant for studies of cancer among cabin attendants include exposure to cosmic radiation (7), exposure to environmental tobacco smoke (8, 9), circadian rhythm changes (10), and exposure to onboard pesticides (6). Neutrons contribute a large proportion (up to 60 percent) to the effective dose from cosmic radiation and are considered to have greater biologic effectiveness than gamma radiation. However, there are few available data on the carcinogenic effect of neutrons in humans (11). It would be pertinent to investigate whether this kind of radiation is more effective in causing cancer than other types of radiation.
The excess annual radiation received by a flight crew varies as a function of cumulative flight hours, flight routes, and solar activity. Typically, airline crews flying 700900 hours per year have been estimated to receive effective radiation doses of 25 mSv per year (1214), in addition to approximately 23 mSv from natural background radiation. Flight crews were recently included in European radiation protection regulations (15), which implies a need for further research on cancer risk in this occupational group. Nonoccupational risk factors, among them reproductive factors and particular lifestyles involving increased leisure-time exposure to ultraviolet radiation, additionally influence the cancer patterns of flight personnel.
To evaluate the mortality of male and female cabin attendants in the German airline industry, we conducted a cohort study among cabin attendants employed by two major German airlines between 1953 and 1997. The main topic of interest was patterns of cancer mortality and other important causes of mortality in this occupational group. To our knowledge, this is the first cohort study that has reported mortality patterns among airline cabin crews.
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MATERIALS AND METHODS |
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Follow-up of vital status
The cohort included 20,895 cabin attendants. From company files, 11,285 cabin attendants were identified as still employed on December 31, 1997, and no follow-up was necessary. For the remaining 9,610 persons, including all those with a last known address in Germany, Switzerland, Austria, or the Netherlands, we conducted follow-up for vital status via the compulsory population registry of the municipality of last known residence. This procedure revealed a further 542 persons who were still employed on December 31, 1997. This process was continued until vital status was confirmed as alive on December 31, 1997, or later or until death or emigration was reported. Persons were occasionally lost during the process; however, this happened most often immediately after the end of employment because of insufficient address information. In general, name changes due to marriage did not cause a loss to follow-up. Persons who were lost or who had emigrated were censored at the date of last known vital status.
In cases of death, we requested a copy of the death certificate from the local health authority of the place of death. Since these certificates are kept for different periods of time in various federal states, not all causes of death could be obtained in this way. Wherever possible, we contacted the treating physician or the next of kin of the deceased for information on the underlying cause of death. Death certificates were available for 62.4 percent of female cabin crew and 71.8 percent of male cabin crew, while information from physicians was used for 15.6 percent and 6.5 percent, respectively. For three women (2.1 percent) and five men (2.9 percent), only data from relatives were accessible. In approximately 19 percent of deaths, no information on the underlying cause of death could be established. All causes of death were coded according to the International Classification of Diseases, Ninth Revision, by trained codification staff from the Statistical State Office Saarland. National reference rates were obtained from the World Health Organization mortality database for most causes of death and from the National Statistical Office for causes not available from the World Health Organization.
Exposure assessment
Because company files did not contain information on past individual flights for cabin crew, we used duration of employment as cabin crew as the main variable to assess occupational exposure. In the framework of our study, we showed that duration of employment is highly correlated (r 0.8) with exposure to cosmic radiationat least for pilots for whom more detailed information on job history was available (16). Employment periods were grouped into three categories: 6 months<10 years, 10<20 years, and
20 years. For female staff, the first category was additionally subdivided into 6 months<5 years and 5<10 years, because the majority of women were employed for less than 10 years. Slightly different categories were used for breast cancer to avoid categories with fewer than five cases. Since nonjet planes were gradually phased out in the early 1970s, we conducted separate analyses for the subcohort of cabin crew who had first been employed in 1971 or later. Stratification details were laid out beforehand in the study protocol.
Statistical methods
Standardized mortality ratios (SMRs) for predefined causes of death were computed according to person-years methods (17). According to the protocol, we restricted the SMR analysis to the period 19601997. We calculated person-years for each subject, commencing on the first day of employment or on January 1, 1960, whichever was later, and ending on the date of last known vital status, emigration, or death or on December 31, 1997, whichever came first. Expected numbers of deaths in 5-year age and calendar intervals were calculated on the basis of German population mortality rates. In analyses conducted according to duration of employment, person-years were dynamically allocated to the respective employment time categories.
To account for missing causes of death, we corrected the observed number of deaths for specific causes with a proportional correction factor, (18). Basically, the "corrected observed" number of deaths, Oc, was calculated as Oc = O/
, where
is the proportion of known causes among all causes, stratified by sex (and SMR = uncorrected SMR/
= Oc/E). The 95 percent confidence interval of the SMR was calculated by approximate methods (16) for 100 or more observed cases or by exact methods if the number of observed cases was smaller. If p were known, the confidence interval of the corrected SMR could be calculated by dividing the upper and lower limits of the uncorrected SMR by p. Since
is an estimate of p, we used the confidence limits of
(19) to calculate appropriate 95 percent confidence intervals for the corrected SMR. This means that our confidence intervals are rather wide. In addition to the SMR analysis, we used Poisson regression models to further evaluate the role of length of employment for all-cause mortality, all-cancer mortality, and breast cancer mortality. Age-adjusted parameter estimates for categories of employment time were calculated, with the lowest category used as the reference group. We used SAS, version 6.12 (SAS Institute, Inc., Cary, North Carolina) for all statistical analyses.
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RESULTS |
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A total of 311 deaths were confirmed in the total cohort, of which 141 occurred among women and 170 among men. A total of 1,020 persons (820 female, 200 male) were lost to follow-up in the population registries, while 640 cohort members (488 female, 152 male) emigrated to foreign countries. Table 1 gives an overview of the cohort size and follow-up results.
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Tables 2 and 3 show observed numbers of deaths and calculated expected numbers of deaths by cause of death for women and men, respectively. Among female cabin attendants, the SMR for all causes of death was significantly decreased (SMR = 0.79, 95 percent confidence interval (CI): 0.67, 0.94), while the decrease in the all-cancer SMR was of the same size but not statistically significant (SMR = 0.79, 95 percent CI: 0.54, 1.17). The SMR for breast cancer mortality was 1.28 (95 percent CI: 0.72, 2.20). SMRs were decreased for most other cancers. Among noncancer deaths, the very low SMR for cardiovascular disease was statistically significant. The observed number of deaths caused by aircraft accidents was 13 (16.2 corrected). Since comparison rates were available only from 1980 onwards, the expected number of deaths and the SMR for aircraft accidents must be interpreted with particular caution.
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A separate evaluation of cabin crew first employed after 1970 (table 4) revealed no deviation from the overall cohort SMRs, with the exception that the SMR for all-cause mortality among men was significantly increased (SMR = 1.56, 95 percent CI: 1.26,1.91). We performed SMR analyses according to duration of employment for all causes of death and for the two major causes of cancer death (breast cancer for women and lung cancer for men) for which at least five deaths were recorded (tables 5 and 6). No differences in the SMRs were seen for all causes or for all cancers in the different employment categories. For breast cancer among women, there was no pattern by duration of employment: The SMR was nonsignificantly increased among women employed for less than 10 years (both categories) but not for those with a longer duration of employment. Results from the Poisson regression analysis (table 7) indicated nonsignificant decreases in all-cause and all-cancer mortality with increasing length of employment among women. The age-adjusted rate ratio for breast cancer among women employed for 5<10 years versus those employed for 0.5<5 years was 1.05 (95 percent CI: 0.42, 2.62); among women employed for 10 or more years, the rate ratio was 0.60 (95 percent CI: 0.21, 1.65). For all causes of death, the highest SMR in men was observed among those who had been employed for 1020 years (see table 6), while no pattern with duration of employment was seen for either all cancer or lung cancer. Results were similar for the Poisson regression.
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DISCUSSION |
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Cancer mortality
Our mortality data showed a decrease in all-cancer mortality, which contrasts with the findings from studies of Nordic cabin crews (24), where the SIR for cancer was slightly increased. However, the precision of published SIR and SMR estimates (including ours) is still rather low. It currently seems premature to conclude that cabin crews have an overall cancer risk which is materially different from that of the general population, since this cohort is very young and further follow-up is needed.
In the Finish (2) and Icelandic (3) cohort studies, as well as in the Danish (5) and US (6) data reported in letters, an excess incidence of breast cancer was observed. Results from the larger Norwegian cohort study (4) did not confirm this finding. Our SMR was slightly lower than the risk estimates from the incidence studies. However, the low number of deaths resulted in a wide confidence interval for the SMR. We did not observe any pattern of mortality increase across categories of duration of employment, which contrasts with data from Finland (2) and Iceland (3), where elevated risks (expressed as SIRs) were seen with increasing duration of employment. The influence of risk factors associated with duration of employment remains unclear.
Possible explanations for the observed small increase in breast cancer risk among female cabin attendants (in comparison with the general population) have focused thus far on cosmic radiation, differences in reproductive factors, and the contribution of socioeconomic differentials. Although data on individual radiation measurements or flight hours were not available, it can be calculated that cabin crews flying for an average of 700 hours per year are exposed to an average of 25 mSv annually (20), resulting in a lifetime occupational dose that is usually below 100 mSv. Ionizing radiation is an established risk factor for breast cancer (21); however, a relative risk of 1.01.1 for a 100-mSv exposure obtained between ages 20 and 40 years would be expected if BEIR V risk estimates were applied (22). Our study had little power to detect a small excess relative risk of this magnitude.
Reproductive factors such as a late first birth and a lower-than-average number of children increase the risk of breast cancer (23). The risk increases observed in the Icelandic cohort did not seem to be explainable by confounding due to reproductive factors (3), while in Finland, a risk difference of 23 percent was attributed to reproductive factor differentials (2). No information on reproductive history is currently available for German cabin crews. It seems reasonable to assume, however, that postponement of childbearing is common in this occupational group, since child-rearing is not easily combinable with the work patterns of airline cabin attendants. The higher social class of this group may also contribute partly to the increase compared with the general population. Since detailed data are not available for this cohort, we are planning a survey to further explore issues concerning reproductive and socioeconomic factors in this population. Given the limits of the available data, our study could not specifically address the influence of other occupational factors, such as exposure to electric and magnetic fields, engine fumes, or pesticides used for insect vector control on selected flights. It is likely that there are circadian rhythm disturbances with associated changes in melatonin homeostasis among airline cabin crews (10), but their importance for breast cancer development is still unclear (2426).
Since one of the main exposures of interest in our study was ionizing radiation, the results for leukemia are of special importance. The study had sufficient power to detect an approximate twofold increase in mortality. The additional lifetime exposure of most cabin crew members is below 100 mSv based on standard weighting factors for neutrons (27). Although these weighting factors for neutrons may not be accurate for the evaluation of leukemia risk, a rough estimate of lifetime risk can be calculated on the basis of epidemiologic studies carried out in populations exposed to gamma radiation. For example, from studies of nuclear power workers, a 22 percent increase in risk has been reported for a 100-mSv lifetime dose (28). In our cohort, no mortality increases were seen for all types of leukemia combined. Subdivision of leukemia cases into chronic lymphoid leukemia and nonchronic lymphoid leukemia was not consistently possible from the death certificates. Given the power of our study and the relative rarity of hematologic tumors in the population, informatively raised leukemia rates in the cohort could only be expected if large deviations from previous risk estimates were to occur. This was not the case.
An increased risk of melanoma has been the most consistent finding in cancer studies conducted among airline crews (29). However, there were no deaths attributed to melanoma in our cabin-crew cohort (number expected: 1.6 in women, 0.9 in men). One possible explanation for the difference between our results and those of the incidence studies is early diagnosis due to regular medical checkups and subsequent more successful treatment in this occupational group. The question of whether ionizing radiation may also be an independent risk factor for melanoma (30, 31) or may modify the risk associated with exposure to ultraviolet radiation (32) requires further investigation.
We found a rather remarkably low SMR for lung cancer among female cabin attendants and no increase for male cabin attendants, indicating that smoking and exposure to passive smoking may not play an important role in mortality in this group. Smoking during airplane flights was permitted in Germany until the mid-1990s, and smoking is still not banned on all charter flights.
Noncancer mortality
The risk of cardiovascular disease mortality for male and female air crew was surprisingly low (reaching statistical significance among women). This is a clear indication of a healthy worker effect, wherein selection for employment and ongoing monitoring lead to a very low prevalence of cardiovascular disease risk factors such as obesity and hypertension. Since the expected number of deaths was also small, this finding should be confirmed in cohorts with a higher proportion of older persons. On the other hand, current evidence can serve to inform cabin attendants of their advantageous cardiovascular mortality profile and increase their motivation to maintain a healthy lifestyle.
Among male cabin attendants, we found a high number of AIDS deaths. Airline personnel and employers in Germany were aware of this situation prior to our study. The number of AIDS deaths peaked in the early 1990s and has decreased steadily since then. Pukkala et al. (2) reported two cases of Kaposis sarcomapresumably AIDS-associatedamong the three cancers observed in their small male cabin-crew cohort in Finland. Our data and further in-depth analyses of this issue could be used to promote AIDS prevention among cabin attendants.
Aviation accidents are a specific hazard for airline crews, not only as an occupational risk factor but also because airline employees frequently fly for nonoccupational reasons. A considerable number of accidents reported to us were not occupational accidents but rather were small private airplane crashes that occurred during leisure tours. It would be informative to further analyze these data so that airline companies could adequately advise their employees.
Strengths and limitations
To our knowledge, the present study was the largest cohort study performed among airline cabin crews to date. Mortality data for male cabin attendants have not been reported previously. Enumeration of our cohort was based on company files that were carefully checked and validated with Federal Aviation Authority data. We consider it nonselective and highly complete. Unfortunately, the company files did not contain any information on health-related factors, including reproductive history, or on individual annual flight hours, which have only been systematically registered in recent years. Therefore, dose-response analyses could only be carried out using duration of employment. This may have introduced some misclassification, since we could not take into account the fact that some persons were employed only part-time.
Limitations of this study also include loss to follow-up and missing information on causes of death. The occupational group studied here is highly mobile, and these workers may temporarily or permanently migrate to foreign countries. This led to some losses in the population registration system on which the follow-up of cohort members relied. Since we censored persons at the date of loss or migration, the person-year calculations in our study were correct; the main consequence of the losses was a decrease in statistical power.
Because our study included all deaths that had occurred since 1960, a number of original death certificates were not available at the offices of local health authorities. In a few cases, we were able to obtain information on cause of death from physicians or relatives, but a considerable gap in the completeness of cause-specific death data remained. On the basis of the assumption that cause-of-death information was missing at random, we believe that the extrapolation method used for the SMR analysis provides a valid estimate of the SMR if the numbers are not too small. However, this imputation may yield incorrect values for categories with only a few cases. Missing only one case of leukemia among male cabin crew, for example, would change the SMR from 0.78 to 1.25. This uncertainty is partly accounted for in the enlarged confidence intervals. Nevertheless, SMRs based on small numbers should be interpreted with great caution.
Overall, our results regarding cancer mortality among cabin attendants correspond well with the findings of the few other studies published so far (26), whose main finding was increased breast cancer mortality among women. Our study provides new data on noncancer mortality in this population. Notable findings include low mortality from cardiovascular causes and a high risk of death from AIDS among men employed as airline cabin attendants. Our data are being included in an ongoing pooled analysis of nine European cohort studies (33), which will provide more stable risk estimates for specific causes of death. Information from the current study can be used to educate airline staff and employers and to devise appropriate strategies to reduce occupational and individual health risks for airline cabin attendants.
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ACKNOWLEDGMENTS |
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The authors are grateful to all Lufthansa and LTU staff, particularly Barbara Reck (Lufthansa). The authors also thank Dorothea Niehoff for data management in the early phases of the study.
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NOTES |
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REFERENCES |
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