1 Division of Epidemiology and Medical Statistics, School of Public Health, University of Bielefeld, Bielefeld, Germany.
2 Department of Tropical Hygiene and Public Health, Institute of Hygiene, University of Heidelberg, Heidelberg, Germany.
3 Laboratorio di Igiene Ambientale, Istituto Superiore di Sanità, Rome, Italy.
4 Clinic of Aviation Medicine, University Hospital, Copenhagen, Denmark.
5 Division of Cancer Epidemiology, Danish Cancer Society, Copenhagen, Denmark.
6 Cancer Registry of Norway, Oslo, Norway.
7 Institute for Energy Technology, Kjeller, Norway.
8 Department of Epidemiology, Karolinska University Hospital, Stockholm, Sweden.
9 Institute for Health, Safety and Working Conditions, Athens, Greece.
10 Department of Hygiene and Epidemiology, University of Athens Medical School, Athens, Greece.
11 Department of Epidemiology, School of Public Health, University of Tampere, Tampere, Finland.
12 STUK Radiation and Nuclear Safety Authority, Helsinki, Finland.
13 Finnish Cancer Registry, Helsinki, Finland.
14 Department of Preventive Medicine, Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
15 Department of Oncology, Landspitalinn (National University Hospital), Reykjavik, Iceland.
Received for publication August 23, 2002; accepted for publication November 19, 2002.
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ABSTRACT |
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aviation; cohort studies; cosmic radiation; mortality; neoplasms; occupational exposure
Abbreviations: Abbreviations: AIDS, acquired immunodeficiency syndrome; CI, confidence interval; ESCAPE, European Study of Cancer Risk among Airline Pilots and Cabin Crew; SMR, standardized mortality ratio.
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INTRODUCTION |
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Most scientific and regulatory attention so far has focused on exposure to ionizing radiation of cosmic origin. The highest radiation doses occur at high altitudes and in polar flight routes. Short-haul flights involve lower doses than long-haul flights, and so does traveling in propeller-driven aircraft relative to jet aircraft. Measurement programs (24) and specific software (5, 6) provide relatively precise information on the radiation doses received onboard. For most cabin crew, annual exposure ranges from 1 mSv to 6 mSv (7, 8), as compared with approximately 2.4 mSv annually from background radiation. Cosmic radiation includes a substantial neutron component (2550 percent of effective dose but less than 5 percent of absorbed dose). The fact that this population is the only source of human data on the health effects of exposure to neutron radiation is of interest.
Long-term health consequences associated with this occupation were recently examined in several cohort studies carried out in Nordic countries that included approximately 6,700 cabin crew members in total. Studies conducted in Finland and Iceland (9, 10) suggested a slightly increased risk of breast cancer (standardized incidence ratio = 1.51.9) among female cabin crew, but a study done in Norway (11) did not. An excess of both melanoma and nonmelanoma skin cancer was observed among cabin crew (911). Recently published findings on California cabin crew (12) also showed increases in standardized incidence ratios for breast and skin cancer. However, evaluation of cabin crew mortality and cancer risk according to measured or estimated radiation exposure has not been possible so far.
Little information is available on incidence of and mortality from diseases other than cancer among cabin crew. For pilots and flight engineers, low mortality from cardiovascular diseases and high rates of accidental death due to airplane crashes have been noted (13, 14).
In order to increase study power and to develop common approaches to exposure assessment, study teams from several European countries decided in 1997 to jointly conduct and analyze data from their national cohort studies on mortality among cockpit and cabin crew in a collaborative project, the European Study of Cancer Risk among Airline Pilots and Cabin Crew (ESCAPE). In this paper, we describe the mortality of European airline cabin attendants in eight countries where cabin crew members were studied, focusing on both cancer and noncancer mortality. Data from two recently published cabin crew mortality studies (15, 16) were included in the current analysis.
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MATERIALS AND METHODS |
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The data collected for each individual included name or personal identification number, sex, date of birth, dates of first employment and/or license renewals, and date of end of employment. Detailed job history data, such as annual flight hours and the dates, routes, and duration of flights, were not available for most cohort members. Thus, duration of employment as a flight crew member was used as a proxy for occupational exposure. The employment and licensing information pertained exclusively to flight attendant work, but some time spent as ground staff may have been included. When the total employment/licensing period consisted of several distinct periods, these periods were summed to obtain the overall duration of employment. Information on reproductive history and other potentially relevant cofactors was not available for most cohorts.
Follow-up
The cohort inclusion time and the period of mortality follow-up differed between countries, depending on the availability of data (table 1). Most cohorts contributed mortality data for a period of more than 30 years. Follow-up for the vital status of each individual started at the first date of employment or licensing, at immigration, or on the technical starting date of follow-up as given in table 1, whichever was latest. Follow-up ended at the date of death, the date of loss to follow-up, or the date of emigration or study closing (table 1). Follow-up was done through centralized or local population registries in most countries. In Greece, social security records were used to establish vital status; these records also contained details on the cause of death for deceased cohort members. In Italy, Denmark, Finland, Iceland, Norway, and Sweden, causes of death were established via record linkage with national death statistics. Death certificates were obtained from local health offices in Germany, and the information was complemented by data obtained from the last treating physician or relatives in some cases where the death certificate was not available.
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Statistical analysis
All analytical steps were laid out in the analysis plan written by the study group prior to analysis. Person-years at risk were calculated in 5-year age and calendar intervals according to standard methods. Expected numbers of deaths were calculated using age, sex, and calendar-period-specific population mortality rates for each participating country from the World Health Organization mortality database or from the national statistical offices. For a small set of causes for which no age-specific Greek data were available (nonmelanoma skin cancer, chronic lymphocytic leukemia, unclear accidental lesions), we used the age distribution of southern Italy to distribute the total annual numbers of Greek cases into 5-year age groups. The standardized mortality ratio (SMR) was then calculated by dividing the number of observed cases by the number of expected cases. We computed 95 percent confidence intervals for the SMR based on an exact Poisson distribution when the observed number of deaths was less than 100 and the approximation given by Breslow and Day (17) for more frequent causes. For approximately 11 percent of the deaths overall, we could not obtain information on the cause of death because death certificates or registry data were not available. There were wide variations in the percentage of missing causes of death, from zero in Iceland, Finland, and Sweden to approximately 8 percent in Italy, 11 percent in Denmark, and 19 percent in Germany. We corrected for these missing causes by using a proportional correction factor in the SMR analysis (18, 19). This factor was estimated separately for each national cohort and represents the proportion of decedents for whom the cause of death was known. Thus, the observed cases were corrected on a country-specific level and then summed for the combined SMR estimate. We performed appropriate 2 tests for heterogeneity (17) and also plotted the SMR and 95 percent confidence interval for each country to allow graphical inspection of the heterogeneity of SMRs. SMR analyses stratified according to employment in the pre-jet age or the jet age (total employment before, across, or after 1971), duration of employment/licensing, and time since first employment/licensing were carried out for grouped causes of death, for some large individual cancer sites (10 or more cases), and for leukemia. To address the independent effects of work-related variables, we also used multivariate Poisson regression adjusted for the effects of age, calendar period, and country, but the results did not add new information and are not shown.
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RESULTS |
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During follow-up, 441 deaths were recorded in the female cohort (SMR = 0.80, 95 percent confidence interval (CI): 0.73, 0.88) (table 2). A total of 171 deaths were due to cancer (SMR = 0.78, 95 percent CI: 0.66, 0.95). Mortality was not statistically significantly increased for any of the primary cancer sites studied. Mortality from breast cancer was slightly but not significantly above population rates (SMR = 1.11, 95 percent CI: 0.82, 1.48). Lung cancer mortality tended to be slightly reduced (SMR = 0.82, 95 percent CI: 0.48, 1.41). No differences were seen for leukemia mortality, regardless of subtype. All countries except Germany and Greece provided mortality data by leukemia subtype, which enabled us to conduct a separate analysis of leukemia excluding chronic lymphocytic leukemia. The SMR for non-chronic lymphocytic leukemia was 1.20 (95 percent CI: 0.49, 2.73), based on seven cases.
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In the male cabin crew cohort, there were 571 deaths (SMR = 1.09, 95 percent CI: 1.00, 1.18) (table 3). Mortality from all cancer was similar to population rates (SMR = 0.90, 95 percent CI: 0.74, 1.12). Increased mortality was found for malignant melanoma (SMR = 1.93, 95 percent CI: 0.70, 4.44) and other skin cancer (SMR = 9.67, 95 percent CI: 1.98, 30.45); both observations were based on fewer than four excess cases. Mortality was also slightly but not significantly increased for cancer at several other sites, including the buccal cavity and pharynx, the pancreas, and the kidney. Mortality from non-Hodgkins lymphoma among male cabin crew was increased twofold (SMR = 2.28, 95 percent CI: 1.04, 4.56). The SMR for non-chronic lymphocytic leukemia (excluding Germany and Greece) was 1.57 (95 percent CI: 0.50, 3.81), based on five cases. As in the female cohort, rates of cardiovascular disease death were reduced (SMR = 0.62, 95 percent CI: 0.48, 0.83). Overall, 103 of 571 deaths (18 percent) were due to external causes. Excess mortality was found for aircraft accidents (SMR = 24.7, 95 percent CI: 13.8, 41.0) and for acquired immunodeficiency syndrome (AIDS) (SMR = 19.6, 95 percent CI: 15.2, 23.3), as well as for unclear accidental deaths.
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Concerning differences between national subcohorts (see figures 1, 2, 3, and 4), there were two main deviations in all-cause mortality, namely the low mortality among Greek males and the relatively high mortality among Danish males. In the cause-specific results, we found significant heterogeneity for several causes of death (tables 2 and 3). For these causes, the pooled ESCAPE SMR must be viewed with particular caution. Note that the heterogeneity test has low statistical power when it is based on low numbers of observed and expected cases.
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DISCUSSION |
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Breast cancer incidence among female cabin crew has previously been studied in Finland (9), Denmark (24), Iceland (10), Norway (11), and the United States (12). Several studies have shown an increased risk of breast cancer among women with a long duration of employment, but the results have not been consistent. All of the above Northern European countries also contributed to the current analysis, which did not show significantly increased mortality from breast cancer in the overall cohort. SMR elevations were not confined to Nordic countries, as indicated by the absence of heterogeneity. However, increased incidence of breast cancer does not necessarily result in mortality increases, partly because women from higher social classes tend to have their cancers diagnosed in early stages, and their stage-adjusted survival rates are higher than those of women from lower social strata (25). In general, the potential insensitivity of mortality studies for relatively nonfatal cancers such as breast cancer should be kept in mind. However, our results are consistent with both the 40 percent increase in breast cancer risk reported from the Nordic countries and no excess.
Ionizing radiation could contribute to an excess risk of breast cancer among cabin crew, but the association may be confounded by differences in reproductive factors or other lifestyle factors. Retired personnel in our study had worked for a relatively short time (the mean duration of employment was 7.5 years among women). The corresponding cumulative radiation dose probably did not exceed 2030 mSv. Therefore, any effect of ionizing radiation on breast cancer mortality in our cohort is likely to have been very small and not detectable in an epidemiologic study, even a study of this size (26). Disruption of circadian rhythms has been cited as a further possible breast cancer risk factor. An alteration in melatonin metabolism decreasing the oncostatic function of this hormone has been hypothesized to be a potential biologic mechanism (27). Studies carried out among blind and visually impaired persons, in whom melatonin production is not suppressed by light (2830), and among shift-working women (31, 32) support a possible role for melatonin in breast cancer development. Beyond showing the absence of any substantial breast cancer mortality increase among female cabin crew, our study did not contribute new data to the ongoing discussion on melatonin.
Reproductive factors and social class as potential confounders could not be directly assessed in most cohorts contributing to our study. Previous studies have reported conflicting findings regarding reproductive history among cabin crew relative to the general population: No differences were found in an Icelandic study (10), while a lower number of children and a higher age at first birth were reported in the Finnish cabin crew cohort (9). A major effort would be required to further disentangle the relative contributions of occupational, reproductive, and other factors associated with breast cancer mortality.
We also found increased mortality from malignant melanoma and other skin cancer among male cabin crew, which is consistent with incidence results from Norway (11) (for melanoma, the standardized incidence ratio was 2.9; for other skin cancer, it was 9.9). All melanoma deaths were observed in Nordic countries, but because of the rarity of melanoma death, the test for heterogeneity was nonsignificant. Exposures of cabin crew to ultraviolet light onboard aircraft are minimal (33), so recreational ultraviolet light exposure or factors related to skin type might cause these increases. The apparent mortality difference between men and women was not statistically significant and may be a chance finding, but it should be investigated further. Additional studies in which more detailed data are collected on occupational and nonoccupational covariates should be considered for both melanoma and breast cancer.
Observations from the United States (12) and Finland (9) suggest that AIDS-associated Kaposis sarcoma probably contributed to the excess of nonmelanoma skin cancer, as does the fact that AIDS was a frequent cause of death among male cabin crew in the ESCAPE cohort. The rate of mortality from non-Hodgkins lymphoma among male cabin crew was twofold that of population rates, but there was no increase among women. A possible explanation is the relatively large number of AIDS deaths observed in the male cohort. Some of the deaths diagnosed as being caused by non-Hodgkins lymphoma could have been related to AIDS but not coded as such.
The increased mortality from cancers of the buccal cavity and pharynx is largely based on the four cases from Norway, where an excess in upper respiratory and gastric tract cancer incidence has also been reported (11). These are cancers associated with tobacco or alcohol consumption. However, no similar increases were seen for cancers with similar risk factors, that is, lung and liver cancer.
Mortality from leukemia was of particular interest, since leukemia is the most important malignancy related to ionizing radiation. We found no substantial increases in leukemia mortality among cabin crew. However, the point estimates for non-chronic lymphocytic leukemia indicated a 1.2- to 1.6-fold higher mortality in the cohort than in the general population. Given that most crew members were employed for less than 20 years, the maximum cumulative individual cosmic radiation exposure was well below 100 mSv. Among nuclear industry workers, a relative risk of 1.22 (90 percent CI: 1.0, 1.6) has been estimated for a 100-mSv protracted dose as compared with 0 mSv (34). Our data appear to be consistent with this dose-response relation between cosmic radiation and leukemia. However, even this comparatively large study did not have sufficient power to detect small risk increases for leukemia. A further note of caution relates to the validity of mortality statistics for the evaluation of hematologic tumors. The reliability of death certificates regarding diagnosis and subtype of leukemia may be low (35). If available, registry-based incidence data are certainly more useful for risk evaluation of these cancers, even though inaccuracies persist (36).
From a radiation epidemiology perspective, it would be of scientific interest to assess the relative biologic effectiveness of neutrons in cancer induction, since quality factors in the range 110 have been suggested for neutrons in calculation of effective dose. However, our study was limited to the extent that no estimation of this aspect was meaningful.
Among noncancer deaths, the low cardiovascular disease mortality in the cohort was striking. Beyond the workforce selection issues, cabin crew have a persistent cardiovascular "health advantage." Medical surveillance schemes might contribute to this, as well as issues of social class and health-conscious behavior. Male cabin crew members were found to have excess mortality from AIDS. AIDS was the most frequent single cause of death in this group, even though we may have missed AIDS cases not coded as such. No AIDS deaths were reported from Greece and Finland. In California, male cabin crew members had an 8- to 9-fold increased risk of Kaposis sarcoma, a sentinel cancer for AIDS (12). Thus, human immunodeficiency virus infection/AIDS has been an important health problem among male cabin crew in many countries in the past and may continue to be of concern.
A typical feature of mortality studies of cockpit crew is the excess mortality from aircraft accidents, many of which are not linked to occupational flying (13, 37). Our pooled study also showed markedly increased mortality from aircraft accidents among cabin crew, but no information on type of flying (i.e., commercial vs. private) was available.
The current study covered several decades, and in most subcohorts we attained a high degree of completeness of cohort compilation, follow-up, and cause-of-death ascertainment. Cohort enumeration was not uniform in the national cohorts. However, multiple data sources were used in all countries, ensuring a high degree of completeness. Automatic registry linkage was used for follow-up in most countries, and in the remaining countries, standard follow-up procedures for retrieval of information from local population and health offices were used. Causes of death were missing in the subcohorts to a varying extent. Rather than disregard this problem, we used a subcohort-specific correction approach that avoided the potential SMR underestimation associated with incomplete cause-specific information and accounted for the distribution of mortality causes in the cohorts. The extent of this correction was rather small, however, so possible errors in the correction method had no marked effect on the SMR.
Because very similar study approaches were used in the national cohort studies, the heterogeneity observed between cohorts was probably not due to methodological differences. It is more likely that differences in underlying disease and mortality rates, in hiring and health examination policies, and in health behavior contributed to the heterogeneity.
We took into account the high rate of migration in this young and very mobile study population by censoring cohort members at the date of migration, irrespective of whether they later returned to their country of origin. This approach slightly decreased the overall power of the analyses, but we avoided the potential bias due to back-migration related to health status. A shortcoming of the study was the lack of detailed occupational exposure information, that is, annual working hours and routes flown. These data have only been collected more recently by employers and licensing authorities and thus could not be used in the current study. Therefore, we used duration of employment or licensing as a proxy for occupational exposure. Because neither detailed job-history information nor individual measurement data were available for our cohort, quantification of radiation doses in particular was not possible.
In summary, the main findings of this European cohort investigation were decreases in mortality for most causes of death among cabin crew. A notable exception was the high mortality due to AIDS and AIDS-associated cancers among male crew members. Similar to cockpit personnel, airline cabin crew have a comparatively high relative risk of death from aircraft accidents, but there were only 48 such deaths during 655,000 person-years at risk. We conclude that the impact of ionizing radiation and other occupational factors on the mortality of European cabin crew is not substantial.
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ACKNOWLEDGMENTS |
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The authors acknowledge the contributions and suggestions of David Irvine, Dr. Harald Eliasch, and Dr. Alexandra Paridou. The support of crew associations, airline staff, and registry personnel in the participating countries is gratefully acknowledged.
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NOTES |
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REFERENCES |
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