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Occupational Medicine Advance Access published online on February 22, 2007
Occupational Medicine, doi:10.1093/occmed/kqm002
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© The Author 2007. Published by Oxford University Press on behalf of the Society of Occupational Medicine. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Occupational female breast and reproductive cancer mortality in British Columbia, Canada, 1950–94

Amy C. MacArthur1, Nhu D. Le1,2, Zenaida U. Abanto1 and Richard P. Gallagher1,3

1 Cancer Control Research Program, BC Cancer Agency, Vancouver, BC, Canada
2 Department of Statistics, University of British Columbia, Vancouver, BC, Canada
3 Department of Health Care and Epidemiology, University of British Columbia, Vancouver, BC, Canada

Correspondence to: Amy C. MacArthur, Cancer Control Research Program, BC Cancer Agency, 675 West 10th Avenue, Vancouver, BC V5Z 1L3, Canada. Tel: +1 604 675 8000; fax: +1 604 675 8180; e-mail: amacarthur{at}bccrc.ca


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conflicts of interest
 References
 
Background It has been postulated that recent increases in female breast and reproductive cancers may be, in part, attributable to occupational exposures.

Aim We aimed to identify occupational associations with female breast and reproductive cancer mortality among women living in British Columbia (BC), Canada.

Methods Case–control methods were used to calculate mortality odds ratios for occupation and cause of death information obtained from the provincial death registry. Cases included women 20 years of age or older who died from breast or reproductive cancer between 1950 and 1994 and resident in BC, Canada. Controls were randomly selected from non-cancer deaths, matched according to age at death and year of death. In a subsequent, stratified analysis, we also identified changes over time to breast and reproductive cancer mortality among each worker group.

Results There was excess mortality from breast and ovarian cancer among teachers, nurses, secretaries, librarians, retail sales clerks and religious workers. An elevated risk of breast cancer mortality was also found among professionals employed as owners, managers and government officials, financial saleswomen, scientists, physicians, medical and dental technicians and accountants. Secretaries, telephone operators and musicians were at increased risk of death from endometrial cancer. Cervical cancer mortality was not significantly increased for any occupational classification.

Conclusions Our study was aimed primarily at hypothesis generation. More systematic reviews, including cancer registry studies, will prove useful for confirming the relationships we have observed, including a possible increase in the risk of breast and ovarian cancer mortality among women employed in professional occupations.

Keywords      Cervical cancer; endometrial cancer; female breast cancer; mortality odds ratio; occupational mortality; ovarian cancer


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conflicts of interest
 References
 
Breast cancer is the most commonly occurring cancer in women, accounting for 21% of all incident cancer diagnoses, with the highest rates observed in Europe and North America. Although incidence rates for other female reproductive cancers are lower than those for breast cancer, they constitute a major fraction of cancer incidence and mortality among women worldwide [1]. In Canada, the incidence of female breast and reproductive cancers combined has been steadily increasing, most markedly during the last several decades [2].

With more women participating in the paid workforce [3], it has been postulated that increases in these cancer rates may be, in part, attributable to occupational exposures. The magnitude of occupationally related cancer mortality has been estimated to range between 4 and 10% [4]. However, these estimates may not reflect current workforce demographics with respect to gender distribution. Exposures, including level and duration of exposure, may differ between men and women holding the same job title if gender differences persist in the tasks performed. Furthermore, biologic differences may exist leading to different levels of susceptibility or disease outcome when external factors are comparable [5,6].

Several epidemiologic studies have examined occupational breast cancer mortality patterns across parts of the USA and Europe with inconsistent findings [7–14]. A review of more than 100 published reports found limited evidence for specific occupational associations with breast cancer, but the majority of studies had limited data on employment history, individual-level exposures and confounding factors [15]. Studies which utilized mortality data, including death registrations, most commonly reported elevated breast cancer mortality among women professional, managerial and clerical workers, teachers, registered nurses, clinical laboratory technicians, social workers and food processing workers [12,14].

Cancer registry studies have also provided information on occupations with elevated breast cancer rates. A study examining cancer incidence in Canada showed excess risk among women employed as hairdressers, material processors and dry-cleaners, as well as women in the food, clothing, chemical and transportation industries [7]. Data from US, Swedish and Chinese cancer registries further suggest that pharmacists, teachers, librarians, administrative and clerical workers, telephone operators, metal workers and women employed in professional occupations may be at excess risk of breast cancer [9,16,17]. Conversely, a registry-based study of work-related cancer incidence in the Nordic countries reported elevated breast cancer risk only for the nursing occupation [18].

Even less consideration has been conferred to cancers of the female reproductive system as separate outcomes, likely due to their low incidence rates [19–26]. An early study that utilized population-level census data from the UK found excess mortality due to cancers of the breast, ovary or uterine body among women employed as teachers, secretaries, nurses, social workers and management and sales professionals [25]. A registry-linkage study conducted in Denmark reported that ovarian cancer incidence was significantly elevated among clerks, while hairdressers, nurses, furriers and saleswomen had an excess of endometrial cancer [24]. Mortality data from US death certificates also showed that service and apparel manufacturing workers may be at elevated risk for cervical cancer [26].

Some reports speculate that high rates of breast and female reproductive cancers might be related to occupational exposure to electromagnetic fields (EMFs), ionizing radiation, low physical activity, organic solvents and dyes, hydrocarbons, styrene, metals or selected pesticides [6,15,21,27–29]. However, owing to inconsistency of the study results and methodological weaknesses, including lack of exposure information, no tangible conclusions can be drawn from the information reported to date. The purpose of this study was to examine occupational associations with female breast and reproductive cancer mortality from 1950 to 1994 among women living in British Columbia (BC), Canada.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conflicts of interest
 References
 
Female residents of the province of BC, Canada, who were 20 years of age or older and died between 1950 and 1994 were included in our analyses. Deaths at ages younger than 20 years were excluded because it is unlikely they could be attributable to occupational exposures. All data were obtained on file from the BC Vital Statistics Agency. Death certificates were reviewed for information on usual occupation and cause of death. A trained nosologist translated underlying cause of death information into standard codes of the Ninth Revision of the International Classification of Diseases system [30], assigning one underlying cause of death code per death certificate. Usual occupation, as recorded in the death certificate, was reviewed and assigned a code from the 1980 Canadian Standard Occupational Classification (SOC) system [31]. A coding schema was developed by a scientific review committee at the BC Cancer Agency to account for changes in job titles over time and merge classifications reported in earlier versions of the SOC with those listed in the 1980 update. In particular, obsolete occupational codes were recoded to an appropriate job classification listed in the current SOC. This was necessary to ensure comparability across time, as well as to produce a cumulative mortality risk estimate during a period when substantial changes to job descriptions had occurred. Coding of occupations was done by computer using a validated Automated Coding by Text Recognition system developed by Statistics Canada. For those codes that could not be classified due to unrecognizable text, manual coding was completed by two trained personnel and reviewed for inaccuracies. We excluded records with invalid occupation or cause of death codes. We also excluded any records that had missing or inconsistent data. After applying these criteria, there was a total of 9524 female reproductive (5070 ovarian, 1986 endometrial and 2468 cervical) and 15 049 breast cancer deaths eligible for inclusion in our study. The number of deaths due to chorioepithelioma and cancers of other female genital organs (vagina, labia majora, labia minora, clitoris, vulva, pudendum and female genital organs not otherwise specified) was small (n = 403) and not included in the analysis. Controls were randomly sampled from all other deaths in the same file and matched on 5-year age groups and year of death. A maximum of four controls were selected for each case.

We conducted separate case–control analyses for each occupation and corresponding cause of death pair [32]. Conditional logistic regression modeling techniques [33] were used to compute mortality odds ratios (MORs) separately for each occupation and disease pair. MORs serve as reliable risk estimates and allow for the simple interpretation of observed-to-expected ratios under the assumption that mortality due to other causes is unrelated to the exposure [20]. MORs and 95% confidence intervals (CIs) are reported for all statistically significant (P < 0.05, two-sided test) occupations with at least five cases for the overall study period. Risk stratified according to three distinct calendar periods was also examined, with time periods chosen to represent intervals with relatively equal proportions of deaths (1950–68, 1969–82 and 1983–94).


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conflicts of interest
 References
 
The proportion of total deaths due to cancer among women living in BC has progressively increased between 1950 and 1994. The greatest proportion of cancer deaths (60%) occurred among women not in the paid workforce. Among women working outside the home, the largest number of cancer deaths occurred among those employed in ‘traditional’ female occupations, including secretaries (n = 1868), clerical workers (n = 1837), nurses (n = 1659) and schoolteachers (n = 1576). When breast and reproductive cancers were examined independently, the number of deaths as a proportion of all-cause mortality has remained fairly constant at ~7–8%, for a total of 24 976 deaths during the study period.

Breast cancers accounted for the second largest proportion of cancer-related deaths among women between 1950 and 1994 in BC, surpassed only by lung cancer. Increased risk of mortality from breast cancer was observed among several traditional female occupations, including schoolteachers, nurses, librarians, bookkeepers and cashiers, secretaries, other clerical workers and retail sales clerks (Table 1). An elevated risk of breast cancer mortality was also found among professionals employed as owners, managers and government officials, scientists, physicians, medical and dental technicians and accountants. Over 3-fold risks were observed among communications inspectors, policewomen, brokers and financial saleswomen and postal workers, although some were based on small numbers of cases. Risk estimates for breast cancer mortality among schoolteachers, nurses, secretaries and other clerical workers remained elevated during each calendar period in the stratified analysis, although some did not reach statistical significance for the earliest time period. For owners, managers and government officials, religious workers and musicians, the MOR increased over time. Conversely, scientists and medical and dental technicians experienced a steady decline in risk of breast cancer mortality during the study period. Significantly decreased risks of mortality from breast cancer were observed among women working as domestics, cooks, bartenders or waitresses and fish canners or packers, as well as women not in the paid labour force.


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  		Table 1. Risk of death due to female breast cancer for selected occupationsa, BC, 1950–94

 
Occupational associations with ovarian cancer mortality closely paralleled those observed for breast cancer mortality (Table 2). Specifically, there was an increased risk of death from ovarian cancer among owners, managers and government officials, schoolteachers, nurses, religious workers, secretaries, other clerical workers, retail sales clerks and housekeepers and travel attendants. Greater than 2-fold risks were observed for brokers and financial saleswomen, purchasing agents and buyers, food processing workers, scientists and librarians. The period-stratified analysis showed more than a 3-fold increase in the risk of ovarian cancer death among food processing workers and brokers or financial saleswomen from 1983 to 1994. Nursing aides and hairdressers experienced significantly increased mortality from ovarian cancer between 1950 and 1968, as well as social workers for the most recent calendar period, but these associations did not persist in the overall analysis (data not shown). Only schoolteachers and secretaries consistently reported elevated ovarian cancer mortality for each of the stratified calendar periods, although risk estimates were elevated above one for clerical workers, nurses and retail sales clerks at each time interval. Domestic workers had a deficit of ovarian cancer mortality, as well as women not in the paid labour force.


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  		Table 2. Risk of death due to female ovarian and endometrial cancers for selected occupationsa, BC, 1950–94

 
Elevated risks of death from endometrial cancer were observed among musicians, secretaries and telephone operators (Table 2). Mortality rates were noticeably higher prior to the 1970s than during more recent periods. An increased risk of death among schoolteachers was evident only for the period 1969–82 (data not shown). Women not in the paid labour force were at a decreased risk of endometrial cancer, but protective effects were not evident for any other occupational classification.

No occupations were at a significantly increased risk of death from cervical cancer in the overall analysis (data not shown). However, the period-specific analyses suggested increased cervical cancer mortality among domestic workers, bookkeepers and cashiers and women not in the paid labour force prior to the 1980s. Conversely, schoolteachers and nurses were found to have significant deficits of mortality from cervical cancer, which was more pronounced prior to the 1970s.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conflicts of interest
 References
 
In accordance with previous reports [7,8,10–13,23,34–38], our study suggests an association between cancers of the breast and ovary among women working as schoolteachers, nurses, secretaries, clerical workers, librarians and retail sales clerks. We have also detected novel associations among women working in contemporary professions, such as owners, managers and government officials, accountants, brokers and financial saleswomen, journalists and purchasing agents and buyers. Women in professional occupations appeared to have higher associated risks when compared with women holding more traditional roles, and the risks generally increased over time. This trend was also observed for female musicians and religious workers. In contrast, risk of breast and ovarian cancer mortality for teachers, nurses, secretaries, clerical workers, medical and dental technicians and retail sales clerks has either remained stable or decreased over time. Variations in mortality rates over time may be due to changes in workplace exposures, job tasks, screening and reporting of disease, treatment and survival or other potentially confounding reproductive and lifestyle factors. Also, due to the number of statistical comparisons that were made, some findings may be due to chance alone.

Due to a lack of information on personal risk factors, it is difficult to isolate reasons for the increased female breast and ovarian cancer mortality we detected among professional workers. There is some evidence that exposure to ionizing radiation among nurses, physicians and surgeons and medical and dental technicians may lead to increased rates of breast and ovarian cancers [29,39,40]. These occupations are also characterized by light at night, which may disrupt the normal secretion of the hormone melatonin and modify breast cancer risk [39]. Increased mortality among communications inspectors or telephone operators could be attributed to occupational EMF exposure [41]. Conversely, the higher mortality observed for many professional occupations may not be directly attributable to work-related exposures but due to confounding from reproductive, socio-economic or other lifestyle factors [42]. Parity and age at first birth are well-established risk factors for breast and ovarian cancers. Since it is also well documented that women who are gainfully employed have fewer children and give birth to their first child at an older age than those who do not work outside the home [6], these reproductive factors may account for the observed increase in breast and ovarian cancer mortality [5,28]. Compounded by increasing physical inactivity at work, career-dictated lifestyle factors could also contribute to increased cancer susceptibility among women professionals.

Few occupations were associated with increased endometrial cancer mortality, with inconsistent trends across the study period. Conversely, there appears to be a protective effect for cervical cancer mortality among women in the paid labour force, particularly for those employed in traditional female occupations such as teachers and nurses. Our results have been replicated previously, but may have been confounded by lifestyle-associated factors, including infection with human papilloma virus, Chlamydia infection, multiple sexual partners, oral contraceptive use, smoking, parity, marital status and a family history of cervical cancer [2,20,34,38,43,44].

Contrary to reports in the epidemiologic literature, we found no evidence for an association between female breast, ovarian or endometrial cancer and occupations characterized by exposure to organic solvents or dusts, hydrocarbons, pesticides and other chemicals, including the agriculture, textile, leather, fur, rubber, plastics or industrial manufacturing industries [6,15,21,27–29,45–47]. Increased risks of breast and ovarian cancers have also been reported among female hairdressers, beauticians and cosmetologists, ascribed to hair dyes [7,11,15,48,49]. However, our results do not support these relationships.

Our study was conducted over the period 1950 through 1994, during which time many job descriptions were modified and women entered the workforce in newly established roles. Unlike most previous analytic studies, we were able to conduct case–control analyses for each female reproductive cancer site and provide risk estimates for precise occupational classifications (to the level of 3-digit SOC codes). Furthermore, we used a population-based sampling frame. This approach, as suggested by Miettinen and Wang [50], provides reliable mortality risk estimates and affords the opportunity to compare risks across different occupations or across time periods for the same occupation. Our study also benefited from a large sample size that enabled us to calculate period-specific and site-specific odds ratios with adequate power.

Interpretation of our findings should be considered in light of several limitations. The use of the MOR assumes independence of exposure (occupation) and is dependent upon the fatality rate of the condition examined [32]. It is possible that other causes of death, including both cancer and non-cancer causes, may be related to the exposure of interest. However, any bias introduced would be conservative and would direct risk estimates towards null. While the use of the proportional mortality ratio as an alternative statistical method would be appropriate for analysis of our data, it has the disadvantage of being mutually dependent, such that a proportionate increase in death for any one occupational group may actually be a reflection of decreased mortality from other causes [32,51,52]. Bias may also have been introduced if other causes of death shared similar aetiology to female breast and reproductive cancer deaths, but this could occur had we selected either cancer-related deaths or non-cancer deaths as controls.

The inclusion of women not in the paid labour force in our analysis would influence risk estimates if a higher background rate of disease, including certain cancers, is preventing these women from participating in the workforce [33,51–53]. Similarly, given the known associations between breast and female reproductive cancers and reproductive factors which may impact on a woman's ability to undertake paid employment, including parity and age at first birth, we could expect further confounding. However, in addition to home-makers, women not in the paid labour force comprised both students and retired women in our study, and there is no evidence to presume that reproductive histories of these women would impact on their ability to participate in paid employment.

Our study employed mortality data from death registrations, which could be a poor indicator of risk for several types of cancer, including those that are not fatal. For instance, the high survival rate for breast cancer indicates that mortality studies could miss some incident cases, thereby abating the magnitude of the association observed for some occupations [54]. While it would have been desirable to examine cancer incidence data, occupational information is not available from the provincial cancer registry. Therefore, the use of death certificates as the principal data source for both disease and occupational information may have led to reporting or misclassification bias. The accuracy of our results is dependent upon the validity and completeness of the occupation and cause of death information listed in the death registrations. Furthermore, because death registrations only record the usual occupation at the time of death, we could not examine risk in relation to changes in the type or duration of a job over time and we may have misclassified some cases as unexposed. Nor could we assess the extent to which changes in mortality may have been influenced by changes in screening and reporting practices, changes in treatment, or access to health care during our study period. However, it is expected that issues surrounding accessibility to screening or health care services would not influence our study results due to Canada's publicly funded health care system.

Our study was further limited by the absence of individual-level data on the prevalence of personal risk factors, such as smoking, diet and physical activity. Our results may have been confounded by socio-economic or reproductive factors associated with female breast and reproductive cancers, including age at first menstruation, later age at first childbirth, fewer children and lower probability of breast-feeding [39]. For future studies, it would be desirable to employ incidence data, as well as collect information at the individual level on work history and personal risk factors.

In conclusion, our study identified a small increase in the risk of breast and ovarian cancer mortality among women employed in the professional workforce. However, specific occupational exposures remain unidentified and the potential for confounding by reproductive histories and other lifestyle factors preclude a causal relationship. While our study was aimed primarily at hypothesis generation, additional studies, including systematic reviews, will prove useful for confirming the relationships we have observed.


   Conflicts of interest
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conflicts of interest
References
 
None declared.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conflicts of interest
 References
 

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