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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptHHS Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
Am J Ind Med. Author manuscript; available in PMC 2009 December 31.
Published in final edited form as:
PMCID: PMC2800169
NIHMSID: NIHMS162792

Shared Occupational Risks for Transitional Cell Cancer of the Bladder and Renal Pelvis among Men and Women in Sweden

Abstract

Background:

Unlike cancer of the bladder, cancer of the renal pelvis is not considered an occupational cancer and little is known about risks among women.

Methods:

Using the Swedish national census and cancer registry-linked data (1971-1989), we identified transitional cell cancers of the renal pelvis (N=1374) and bladder (N=21,591). Correlation between cancer sites for the Standardized Incidence Ratios (SIR) were determined using Pearson's coefficient of the log SIR. Relative risks of job exposure matrix variables were calculated using Poisson regression.

Results:

Both cancer sites were significantly elevated among women and men employed in the machine/electronics industry, sedentary work, and indoor work, as well as among men employed in the shop and construction metal industry, contributing 10-14% of cases among men. Risks by industry were more highly correlated among women (r=0.49, p=0.002) than men (r=0.24, p=0.04).

Conclusion:

Cancers of the renal pelvis and bladder share common occupational risk factors that may be more frequent among women. In addition, there may be several jobs that pose an increased risk specifically for cancer of the renal pelvis but not bladder.

Keywords: epidemiology, bladder neoplasms, kidney neoplasms, occupational exposure, industry

Background

In Sweden, the incidence of bladder cancer has doubled since the 1960s and reasons for this are not entirely clear [National Board of Health and Welfare of Sweden 2000, Thorn, et al. 1997, Mattsson and Wallgren 1984]. In addition, although bladder cancer accounts for a higher proportion of all cancers among men (7.3%) than women (2.9%), women have experienced a comparatively lower survival, and a greater increase in incidence [Ries, et al. 2003, McLaughlin, et al. 1996, Madeb and Messing 2004]. A significant proportion of bladder cancers among men (10-25%) have been attributed to occupational exposures, and changes in the workforce suggest that these exposures are also becoming more relevant for women [Kogevinas, et al. 2003, Vineis and Magnani 1985, Mannetje, et al. 1999].

At the same time, very little is known about occupational risk factors for cancers of the renal pelvis, particularly among women. Cancers of the bladder and renal pelvis are both predominantly of transitional cell origin (90-95%). Secondary cancer studies suggest that these two cancer sites are etiologically related because approximately 1-4% of bladder cancer patients will develop cancers of the renal pelvis and ureter, and 20-50% of renal pelvis cancer patients will also have bladder cancer [Rabbani, et al. 2001, Sharir and Jewett 1999, Kirkali and Tuzel 2003, Huguet-Perez, et al. 2001]. Two known carcinogens that are associated with both cancers include tobacco smoking and ionizing radiation.[Silverman, et al. 2006]

In this study, our purpose is to explore similar occupational risk factors between these two cancer sites among employed Swedish men and women.

Methods

Data

The cohort was defined as all male and female Swedish residents reporting gainful employment at either the 1960-or-1970 censuses, and alive on January 1, 1971. Person-years were accrued for each member of the cohort beginning January 1, 1971 until a diagnosis of cancer, emigration, death or end of follow-up on December 31, 1989, whichever occurred first. We used the Swedish Cancer-Environment Registry (CER), Version III, to determine the incidence of transitional cell cancers of the renal pelvis (International Classification of Diseases, 7th Revision (ICD-7) code 180.1), and bladder (181.0) between 1971-1989. We also investigated mortality from these two cancers, but do not report these results in the tables. Cancers were limited by histology according to the Swedish Cancer Registry PAD (codes 114 and 116). Microscopic confirmation occurred for 97% of cancers in this study. CER III is the linked dataset between the 1960-and-1970 National Population and Housing Censuses and the Swedish cancer registry. The proportion of unlinked cancer cases was less than 1%, and the Census response rate was 99% [Wiklund and Eklund 1986]. Job titles reported to the Census were converted to the three-digit National Swedish Classification of Occupations and Industries, as described elsewhere [Shields, et al. 2002]. Urban residence was defined according to the place of residence at the 1970 Census (i.e. residence in one of the 3 largest Swedish cities of Stockholm, Göteborg, and Malmö).

Job exposure matrices (JEM), developed by American and Swedish experts in occupational medicine, were used to assess risks associated with the following occupational exposures: asbestos, ionizing radiation, low physical activity and indoor work. JEMs for other known or suspected bladder carcinogens have not yet been developed for this dataset. All scoring was blinded to the health status of subjects. Ionizing radiation and asbestos exposures were scored in the categories of probability (none, low, medium, high), intensity (none, low, medium, high), and confidence (low, high) of exposure, and have been used in previous research [Shields, et al. 2002]. Occupational physical activity was categorized as heavy, medium, light, and sedentary. This JEM has been shown to correlate reasonably well with self-reported occupational physical activity (spearman rank coefficient=0.62) [Moradi, et al. 1998] . Work location was classified into 3 categories, (outdoor only, both indoor and outdoor, and indoor only). Individuals were classified into a JEM category according to the occupation held in 1970.

Analysis

We calculated the standardized incidence ratio (SIR), the ratio of observed to expected number of cancers, for each two- and three-digit occupation and industry category. Individuals were assigned to an industry or occupation category in a specified category if they reported employment in either 1960 or 1970. Thus, an individual reporting a different occupation in 1960 than in 1970 would be considered separately for each occupational exposure group. According to our calculations, 34% and 37% of men and 24% and 24% of women with cancer of the bladder and renal pelvis cancer, respectively, held a different occupation in 1960 than in 1970. The expected number of cases was based on the incidence rates in attained age (by 5-year-age groups), sex, site and calendar-year (by 4-year calendar periods from 1971-1989) specific cancer incidence rates. The expected rate was based on cancer incidence rates in the total employed population. The total employed population was defined as those individuals reporting employment at either the 1960 or 1970 census. Autopsy-only reported cases were excluded from both observed and expected rate calculations.

We present SIR results for occupations and industries with at least 3 exposed cases and meeting at least one the following criteria: 1) statistically significant (p<0.05), 2) SIR=2.0 or greater, and 3) a priori risk based on published literature [Kogevinas, et al. 2003]. For completeness, if the SIR met these criteria for renal pelvis cancer, we also reported the SIR value for bladder cancer, even if it did not meet the above criteria.

In order to test the hypothesis that bladder and renal pelvis cancers were similarly elevated in each occupation and industry category, the Pearson's correlation coefficient and two-tailed p-values were calculated from the log of the SIR values, stratified by sex. In addition, because occupational correlations could be related to smoking, we also estimated the correlation for SIR values using a conservative approach to adjust the SIR values for smoking. Using this approach, we identified occupations that were significantly elevated for lung cancer in this dataset as previously reported [Pollan and Gustavsson, 1999]. The list of male occupations elevated for bladder and/or renal pelvis cancer was then reviewed by the authors and placed into the following categories based on knowledge of the existing literature: definitely not tobacco-related only (occupation codes 633, 754, 757, 781, 794 and 826); probably not tobacco-related only (occupation codes 662, 751, 752, 795 and 932); and possibly tobacco-related only (295, 333, 603, 793, 941). The list of female occupations with both bladder and/or renal pelvis cancer elevations occurred in only three occupations (085, 758 and 921) all three of which were categorized as possibly tobacco-related only. Based on the existing literature that reports attenuation of occupation-related risks for cancers of the bladder and lung to range between 5 to 30 percent [Blair, et al. 1985, Siemiatycki, et al., 1988, Haldorsen, et al., 2004, Mannetje, et al., 1999, Richiardi, et al., 2005], we conservatively adjusted the number of observed cancers in each of the occupation groups above by reducing them by 30 percent and then calculated the tobacco-adjusted correlation between bladder and renal pelvis SIR values.

We used multivariate Poisson regression to estimate the relative risk of bladder and renal pelvis cancer with respect to the job-exposure matrix (JEM) estimated exposure to asbestos, ionizing radiation, physical activity, and indoor/outdoor work. The JEM variables were adjusted for urban residence, as well as attained age and calendar year.

Results

Among the 4,197,684 employed Swedish residents there were 70,083,912 person-years of follow-up, with a mean follow-up of 16.70 years. There were 1,014 and 360 renal pelvis cancers and 18,244 and 3,347 bladder cancers among men and women, respectively.

Occupation

Among women, there were no occupations with significantly elevated risks for both cancer sites (Table 1). Risk for both cancer sites was significantly reduced among women employed as agriculture and animal management workers. The correlation between bladder and renal pelvis risks was statistically significant, and this correlation was not altered once we adjusted the SIR values for smoking (r=0.47, p=0.02). Occupations which demonstrated excess risk for cancer of the bladder among women included: personnel work, business administration, bank cashier, clerk/secretary/stenographer, insurance clerk, switchboard operator, graphic work, bookbinder, photographic lab work, and waitress. Cancers of the renal pelvis were significantly elevated among women employed as pharmacists, journalists/editors, business executives, food-related workers, food process workers, and chemical/cellulose workers, unspecified. The largest proportion of bladder and renal pelvis cancers occurred among clerk/secretary/stenographers and waitresses combined (16% of bladder cancers and 18% of renal pelvis cancers), data not shown.

Table I
Risk for bladder and renal pelvis cancer among women in Sweden by occupation, 1971-19891

Among men, both cancer sites were elevated for purchasers/office sales people, shop and construction metal work, and, civil security and enforcement. Risks for both cancer sites were significantly reduced among men employed in agriculture and forestry work. The highest proportion of cases occurred in shop and construction metal work, accounting for 12% of bladder and 14% of renal pelvis cancers. There was not a statistically significant correlation between the non-smoking adjusted SIR values for occupation among men (r=0.17, p=0.12). However, once we adjusted SIR values for smoking the correlation increased slightly and became statistically significant (r=0.25, p=0.02).

Industry

Among women, risks for both cancer sites were elevated in the machine/electronics industry, and both cancer sites were significantly reduced in the agriculture and stock raising industry (Table 3). The correlation coefficient for the bladder and renal pelvis SIR industry values was statistically significant among women (r=0.49, p=0.002). Bladder cancer was significantly elevated among women employed in the following industries: graphics and publishing, book binderies, machine/electronics, radio/TV, wholesale durable goods (fuels, chemical, hardware and machines), banking, insurance, state administration (general), universities and higher learning, public functions, and hotel and restaurant work. Renal pelvis cancer was elevated among women employed in the food, chocolate and candy, machine/electronics, transportation equipment construction, hardware and machine business, and drugstore industries.

Table III
Risk for bladder and renal cancer pelvis cancer among women in Sweden by Industry, 1971-19891

Among men, both cancer sites were significantly elevated among men employed in the machine/electronics industry, and both cancer sites were reduced among men employed in agriculture. The correlation coefficient between bladder and renal pelvis cancer risks was statistically significant (r=0.25, p=0.04). Employees in the machine/electronics industry accounted for 10% of bladder and 12% of renal pelvis cancers.

Job-exposure matrix and urban residence

Urban residence was associated with a 26 to 36% elevated risk for cancers of the bladder among men and women, respectively, but was not statistically significant for renal pelvis cancer (Table 5). Among both men and women, sedentary (versus physically active) and indoor (versus outdoor) work were associated with a significantly increased risk of both cancer sites and trends for both sexes and cancer sites were statistically significant (p-trends ranging from <0.001 to <0.03).

Table V
Risk of Incident Bladder Cancer by Job Exposure Matrix Assessment, Sweden, 1971-89

Among men, moderate occupational ionizing radiation exposure was associated with an elevated risk of bladder cancer, however, there was no evidence of a trend. There was also no association with bladder cancer mortality (data not shown).

Summary of Results

Both cancer sites were significantly elevated among workers in the following industries: machine/electronics (men and women), machine (men); and occupations: civil security (men), purchasing and office sales (men), and shop and construction metal (men); as well as indoor and sedentary workers, demonstrating evidence of a trend. Among all industry and occupational categories, shop and construction metal work contributed the highest proportion of cancers among men.

Discussion

Renal Pelvis

Cancer of the renal pelvis occurs less frequently than cancers of the bladder, and unlike bladder cancer, is not generally referred to as an occupational cancer. Our data suggest that among the employed population, the occupation-related correlations between these two cancer sites is moderate (25 percent among men and nearly 50 percent among women) and persists after proportionate adjustment for smoking-related cancers. We also found fewer commonly associated occupations between these two cancer sites than might be expected, given that both cancer sites are associated with tobacco smoking [Silverman, et al. 2006], the fact that cancers of the bladder and renal pelvis frequently occur simultaneously or as secondary cancers in the same individual [Rabbani, et al. 2001, Sharir and Jewett 1999], as well as data from molecular studies of genetic and epigenetic changes in tumors of the bladder and renal pelvis [Vriesema, et al. 2001, Paterson, et al. 2003, Hafner, et al. 2001].

In particular, we identified several jobs for which there was an elevated risk of cancer of the renal pelvis but not bladder. Several of these occupations and industrial groups also had a small number of cases (i.e. 5 or below), suggesting that these results could be due to chance. Those jobs with a significantly elevated risk for renal pelvis cancer, but not bladder cancer, and having more than 5 cases, included: women employed as food processors and employed in the food, transportation and drug store industries; and men employed as insurance clerks, butchers, cleaners and employed in the pulp grinding, metal manufacturing, scientific/surgical instruments, insurance and legal service industries. Cancers of the renal pelvis have been previously associated with work in the dry cleaning and iron and steel industry[McCredie and Stewart 1993]. Other occupational studies have reported an elevated risk of breast cancer in female pharmacists and an elevated risk of bladder cancer in the pharmaceutical industry.[Pelucchi, et al. 2002, Notani, et al. 1993, Baker, et al. 1986] Pharmacologic agents, such as phenacetin-containing analgesics, have been associated with papillary scarring and cancer of the renal pelvis while others are known to significantly alter intra-pelvic pressure as well as the flow rate of urine from the renal pelvis to the ureter[Stewart, et al. 1999, Jung, et al. 2006]. However, the extent of exposure to such agents in our study population is not known. Mycotoxins produced by fungal contamination of grains and cereals have been associated with Balkan endemic nephropathy, and this condition is in turn associated with an elevated risk of transitional cell cancers of the renal pelvis.[Grollman, et al. 2007] Certain mycotoxins, like ochratoxin A, are nephrotoxic and cause renal cell cancer in animal models.[Pfohl-Leszkowicz and Manderville 2007] Exposure to mycotoxins is known to occur in the food processing, meat, and pulp grinding industries[Prazmo, et al. 2003, Thuvander, et al. 2001]. One might hypothesize that that mycotoxin exposure is related to the commonly elevated risk of renal pelvis cancer in these occupational groups, although this is not known.

Conversely, it is notable that in our study all occupations and industrial groups which were protective for renal pelvis cancer (i.e. had a SIR value significantly below 1.0, p<0.05), were also protective for bladder cancer. In addition, consistent with an earlier study, we identified a reduced risk for cancer of the renal pelvis for employment in agriculture, which was lower among women than among men[McLaughlin, et al. 1987]. A large proportion of women in our study sample were employed in agriculture, which may explain why trends for outdoor work and occupational physical activity were steeper among women than men, although the confidence intervals among men and women were overlapping.

Differences in risk factors for cancers of the bladder and renal pelvis for certain occupation and industry groups may be explained because certain carcinogens can act selectively or more intensively upon either the bladder or the renal pelvis, as is evidenced by animal studies [Murai, et al. 1993, Bach 1991], and as suggested by differences in genetic instability between bladder and renal pelvis tumors occurring within the same patient [Takahashi, et al. 2001]. In summary, however, our results suggest that while there are a few occupations with shared increased risk, these occupations account for a moderate proportion of the total number of cases in the employed population.

Bladder Cancer

Due to the sparse amount of information on risks for cancers of the renal pelvis, by necessity, the following discussion will focus primarily on the consistency of our findings with other studies of bladder cancer.

Physical Activity

In other studies, greater physical activity has been related to a reduced risk of bladder cancer, although these reports were not-statistically significant [Dosemeci, et al. 1993, Hardman 2001, Hu, et al. 2003, McTiernan, et al. 1998, Mellemgaard, et al. 1995, Severson, et al. 1989, Sommer, et al. 2004, Thune and Furberg 2001, Tripathi, et al. 2002, Brownson, et al. 1991]. While the biologic mechanisms of physical activity in cancer prevention are not clear, it has been hypothesized that moderate physical activity may improve mucosal immunity and alter cytokine expression [Sommer, et al. 2004, Tripathi, et al. 2002, Gleeson, et al. 2004, Bevers, et al. 2004, Griffiths and Mellon 2004, Drela, et al. 2004]. Notably, intravesical administration of Bacillus Calmette-Guerin (BCG) used to treat superficial bladder cancer, results in altered cytokine production (as measured in urine), and in vitro, BCG has been shown to induce T-cell and NK-cell activity [Moldoveanu, et al. 2001, Saint, et al. 2003, Ma, et al. 1987]. In addition, other epidemiologic studies and animal models suggest that other physical-activity related disease pathways, including IGF-1 and diabetes, may also be relevant [Tripathi, et al. 2002, Hursting, et al. 2004, Coughlin, et al. 2004].

Outdoor Work

An association with indoor work has not been previously reported. Sunlight is the major source of vitamin D [Holick 2004]. The active metabolite of Vitamin (1α,25 (OH)2D3) is reported to promote apoptosis in human bladder cancer cell lines, and intravesical administration of vitamin D3 in the bladder has been shown to reduce the incidence of bladder tumors in animal models [Konety, et al. 2001, Yazawa, et al. 2000]. However, it is important to note that most physically active occupations are also outdoors and our study is unable to disentangle the differential relation of outdoor exposure and physical activity. Follow-up in future studies is necessary.

Farm Work

Reduced bladder cancer risk has been frequently found among farmers [McLaughlin, et al. 1987, Lee, et al. 2004, Blair, et al. 1992, Acquavella, et al. 1998, Porru, et al. 1996, Wiklund and Dich 1994]. However, elevated risks have been reported for professional gardeners [Silverman, et al. 1989, Teschke, et al. 1997, Colt, et al. 2004], orchard and greenhouse workers [Kristensen, et al. 1996], nursery workers [Kogevinas, et al. 2003], herbicide applicators [Lee, et al. 2004, Rusiecki, et al. 2004, la Vecchia, et al. 1990], and field crop workers [Mannetje, et al. 1999]. Several other cancers are reduced among farmers, possibly related to the generally lower smoking rate among farmers [Wiklund and Dich 1994, Statistics 1965, Wiklund and Dich 1995], although studies adjusting for smoking still find a reduced risk of bladder cancer among farmers [Barbone, et al. 1994, Folsom, et al. 1996]. Similarities in the risk for bladder cancer among men and women employed in farming and the agricultural sector suggest that non-occupational factors may be important since job-related exposures may be quite different between men and women [Alavanja, et al. 1999].

Urban Residence

Urban residence has been previously associated with higher risk of bladder cancer, possibly related to environmental agents more frequently encountered in urban environments, including chlorination by-products in drinking water, tobacco smoke, and decreased fluid intake [Villanueva, et al. 2004].

Ionizing Radiation

Ionizing radiation is an established cause of bladder cancer, primarily through studies of high-dose radiotherapy, radioactive iodine therapy, and atomic bomb survivors [Silverman, et al. 2006]. Only a few studies have reported excess bladder cancer risk due to ‘low-dose’ ionizing radiation exposures which are generally found in the occupational setting, and most of these studies focus on cancer mortality rather than incidence [McGeoghegan and Binks 2000, Sont, et al. 2001, Cardis, et al. 1995, Ugnat, et al. 2004]. Our study found evidence of an association between ionizing radiation and bladder cancer incidence. However, we did not find a trend with higher exposure, possibly due to the small number of individuals in highly exposed jobs or to exposure misclassification. The plausibility of lower-dose exposure in bladder cancer risk has been suggested by the positive relation between Cs 137 levels in urine, chronic proliferative atypical cystitis (Chernobyl cystitis), and the development of dysplasia and carcinoma in situ of the bladder among individuals living in the Chernobyl region [Romanenko, et al. 2003].

Machine & Electronics

Several studies report elevated risk of bladder cancer among machinists [Kogevinas, et al. 2003, Colt, et al. 2004, Tolbert 1997] and a previous follow-up of this cohort found elevated risk for cancer of the renal pelvis among this occupational group [McLaughlin, et al. 1987]. Metal-workers and machinists account for approximately 15% of occupationally-related bladder cancers in Europe [Kogevinas, et al. 2003]. Other electronics-related work associated with increased bladder cancer risk in this study include: radio and TV, electrical installation, electrical power/gas/waterworks, and electrical work. Electric power plant workers may be at excess risk for kidney and bladder cancer [Mattos, et al. 2002, Mattos and Koifman 1996], although this has not been consistently found [Mattos and Koifman 1996, Baris, et al. 1996, Keller and Howe 1993]. Electricians and electrical workers are exposed to polychlorinated biphenyls, asbestos, and low frequency EMF, none of which have been conclusively linked to occupational bladder cancer. Workers in the semiconductor industry exposed to elemental arsenic and/or gaseous arsenic hydride in the in the manufacture of silicon chips have been shown to have higher urinary metabolites of arsenic [Hwang, et al. 2002]. While arsenic is classified as a known bladder carcinogen, the carcinogenic potential of occupational exposures is not clear [Cancer 2004].

Bladder Cancer among Women

Our results are consistent with previous studies among women finding excess bladder cancer risks among, secretarial and clerical [Zheng, et al. 2002], cashiers [Colt, et al. 2004] [Colt, et al. 2004], education work [Zheng, et al. 2002], sales [Mannetje, et al. 1999, Colt, et al. 2004, Swanson and Burns 1995, Silverman, et al. 1990], graphics and publishing [Bulbulyan, et al. 1999], machine [Barbone, et al. 1994], electronics [Mannetje, et al. 1999, Silverman, et al. 1990, Simpson, et al. 1999], telephone industry [Dosemeci and Blair 1994], and waitresses [Simpson, et al. 1999]. In addition, among women, Gridley et al. (1999) report a 20% elevated risk of bladder cancers among the employed population, compared with the non-employed female population in Sweden [Gridley, et al. 1999]. Because our study was limited to the employed population, this suggests that the occupational bladder cancer risks among women reported in this study may be higher when compared with the general population. We did not confirm observations of significantly elevated bladder cancer risk among women employed in pulp and paper processing [Langseth and Andersen 1999], health services [Colt, et al. 2004, Simpson, et al. 1999, Carpenter and Roman 1999], leather [Garabrant and Wegman 1984], metal work [Mannetje, et al. 1999, Silverman, et al. 1990], chemical [Pelucchi, et al. 2002, Silverman, et al. 1990, Dolin and Cook-Mozaffari 1992], rubber [Swanson and Burns 1995, Silverman, et al. 1990, Simpson, et al. 1999, Carpenter and Roman 1999], and textile [Mannetje, et al. 1999, Simpson, et al. 1999, Carpenter and Roman 1999] industries. A large pooled analysis of case-control studies in Europe among leather and rubber work also did not report elevated risks [Mannetje, et al. 1999]. Elevations in bladder cancer risk among women employed as photographic laboratory workers, book binders, and business administrators, and the radio and TV industry have not been previously reported. Finally, although the relative risks we found in this study among women employed as clerks/secretaries and waitresses were modest, these occupations accounted for a large proportion of the total number of cases.

Bladder Cancer among Men

Our results are similar to research reporting elevated bladder cancer risk among men employed in: administrative and clerical work [Porru, et al. 1996, Schumacher, et al. 1989], artistic work [Brown, et al. 2002], automotive repair [Zheng, et al. 2002], chemical industry [Silverman, et al. 1989, Teschke, et al. 1997, la Vecchia, et al. 1990], electronics and electrical work [Mattos, et al. 2002, Dolin and Cook-Mozaffari 1992, Tynes, et al. 1992], engineering [Dolin and Cook-Mozaffari 1992], electrical power/gas and waterworks [Dolin and Cook-Mozaffari 1992], executives [Dolin and Cook-Mozaffari 1992], food processors [Dolin and Cook-Mozaffari 1992], gas stations [Schoenberg, et al. 1984], glass processing [Dolin and Cook-Mozaffari 1992], health care (including physicians) [Wynder and Goldsmith 1977, Howe, et al. 1980], machine industry [Kogevinas, et al. 2003, Colt, et al. 2004, Tolbert 1997, Dolin and Cook-Mozaffari 1992, Howe, et al. 1980, Claude, et al. 1988], metal work [Silverman, et al. 1989, Zheng, et al. 2002], photographic lab work, printing/graphics work [Lynge, et al. 1995, Pesch, et al. 2000], railroad work [Dolin and Cook-Mozaffari 1992], rubber industry [Vineis and Magnani 1985, Zheng, et al. 2002, Straif, et al. 1998], ship's machine command [Dolin and Cook-Mozaffari 1992], shop and metal industry [Kogevinas, et al. 2003, Teschke, et al. 1997, Colt, et al. 2004, Pesch, et al. 2000], transportation workers [Colt, et al. 2004, Dolin and Cook-Mozaffari 1992, Pesch, et al. 2000, Hoar and Hoover 1985, Silverman, et al. 1983, Guo, et al. 2004], and waiters [Porru, et al. 1996]. This study did not confirm elevations in bladder cancer among men employed as asbestos workers [Ugnat, et al. 2004], dry cleaners [Teschke, et al. 1997, Zheng, et al. 2002, Pesch, et al. 2000, Ruder, et al. 2001, Brown and Kaplan 1987], dyestuffs workers [Vineis and Magnani 1985, Ugnat, et al. 2004, Vineis and Pirastu 1997], hairdressers [Teschke, et al. 1997, Lynge 1990, Miller and Bartsch 2001], leather workers [Dolin and Cook-Mozaffari 1992, Schumacher, et al. 1989, Pesch, et al. 2000, Montanaro, et al. 1997], miners [Teschke, et al. 1997, Dolin and Cook-Mozaffari 1992], painters [Silverman, et al. 1989, Teschke, et al. 1997, Zheng, et al. 2002, Dolin and Cook-Mozaffari 1992], petroleum workers [Teschke, et al. 1997], textile workers [Kogevinas, et al. 2003, Teschke, et al. 1997, Frumin, et al. 1990], or welders [Silverman, et al. 1989]. A large pooled case-control study also reported no association with hairdressing [Mannetje, et al. 1999], and the lack of association during the time period of this study may be related to changes in the constituents of the hair dyes used [Czene et al. 2003]. There may also be unique aspects of the Swedish work environment which might be important in comparing our results with other studies [Kleinman 1984]. Similar to our study, Axelson et al. (1994) did not observe an increased risk of bladder cancer in Swedish dry cleaners [Axelson, et al. 1994]. In addition, while previous studies have found quite high risks associated with dyestuffs work (ranging from 4 to 64-fold), benzidene and 2-naphthylamine are two known carcinogenic compounds which have not been widely used in the dye industry in Nordic countries [Vineis and Magnani 1985, la Vecchia, et al. 1990, Naito, et al. 1995], [Dreyer, et al. 1997].

Strengths and Limitations

The strengths of this study include: a large number of cases in a population with excellent cancer surveillance, the investigation of risk factors among the working population in order to control for the ‘healthy-worker bias,’ and the ascertainment of occupational exposure prior to cancer diagnosis. Important limitations of this study include: 1) no adjustment for the effects of other potential confounding factors in the estimation SIR values (e.g. diet, tobacco use, use of protective equipment on the job), 2) exposure misclassification due to classification of occupational exposures based on job title occurring at one point in time, which may be greater for women than for men [Stewart and Blair 1994]; and 3) the large number of comparisons in this analysis, which increases the possibility that a statistically significant finding is due to chance alone [Law, et al. 2001].

Methodologic studies report that adjustment for tobacco use in occupational studies may alter occupational risk estimates [Shavers, et al. 2005, Ji, et al. 2005, Richiardi, et al. 2005]. Studies using diverse methods including the assessment of confounding in case-control studies using self-reported smoking status, and those employing an a priori correction factor for smoking-related occupations have found adjustment for smoking to result in attenuation of approximately 10 to 25% [Blair, et al. 1985, Siemiatycki, et al., 1988, Haldorsen, et al., 2004, Mannetje, et al., 1999, Richiardi, et al., 2005]. A recent study reports that, among Swedish men employed in 1960 and 1970, the risk for bladder cancer among men was attenuated downwards by a range 5 to 29%, depending upon the occupation [Ji et al., 2005]. Richiardi et al. (2005) adjusted for self-reported smoking status and found lung cancer risk among men employed in metal and machine industry to be attenuated downwards by 6% and for blue collar workers by 11% [Richiardi, et al. 2005]. We used the upper limit of 30% to adjust for the possibility that smoking could be confounding our SIR results. The smoking-adjusted SIR resulted in an increased correlation between bladder and renal pelvis risks among men. This suggests that the correlations we observed between bladder and renal pelvis cancers were not due to tobacco alone. It is likely, however, that our correction may be too stringent as not all occupations with an elevated risk for lung cancer are solely due to smoking, but may be attributed to recognized workplace carcinogens [Siemiatycki et al., 2004, Rousseau et al., 2005].

Conclusions

Our work suggests that there are common occupational risks for cancers of the bladder and renal pelvis, particularly among women. Further research is needed to confirm commonly elevated risks found for the machine/electronics industry, physical inactivity and indoor work. In addition, there may be several jobs that pose an increased risk specifically for cancer of the renal pelvis but not bladder.

Table II
Risk for bladder and renal pelvis cancer among men in Sweden by occupation, 1971-19891
Table IV
Risk for bladder and renal pelvis cancer among men in Sweden by Industry, 1971-19891

Acknowledgements

The authors would like to thank Drs. Debra Silverman, Wong-Ho Chow, Sheila Zahm, and Mitchell Gail of the National Cancer Institute, United States, for their thoughtful review of the manuscript; and Drs. Nils Plato and Tahereh Moradi of Karolinska Institutet, Stockholm, Sweden for the development of Job Exposure Matrices. The authors also appreciate the clerical assistance of Ms. Aimee Seisay, Ms. Barbara Hynum and Ms. Diane Pague in the preparation of the tables and manuscript and the computer programming assistance of Ms. Heather Morris, Information Management Services, Inc. This research was supported by the Intramural Research Program of the National Cancer Institute.

Grant Sponsor: This work was conducted as part of a Post-Doctoral Fellowship at the National Cancer Institute, Division of Cancer Epidemiology and Genetics

Footnotes

Institutions where statistical analysis performed: National Cancer Institute and Pennsylvania State University

Conflict of Interest

The authors do not presently have affiliations with organizations that have a direct financial interest in the subject matter or materials discussed.

References

  • Acquavella J, Olsen G, Cole P, Ireland B, Kaneene J, Schuman S, Holden L. Cancer among farmers: a meta-analysis. Ann Epidemiol. 1998;8:64–74. [PubMed]
  • Alavanja MC, Sandler DP, McDonnell CJ, Mage DT, Kross BC, Rowland AS, Blair A. Characteristics of persons who self-reported a high pesticide exposure event in the Agricultural Health Study. Environ Res. 1999;80:180–186. [PubMed]
  • Axelson O, Selden A, Andersson K, Hogstedt C. Updated and expanded Swedish cohort study on trichloroethylene and cancer risk. J Occup Med. 1994;36:556–562. [PubMed]
  • Bach PH. A molecular basis for target-cell toxicity and upper urothelial carcinoma in analgesic abusers and patients with Balkan endemic nephropathy. IARC Sci Publ. 1991:215–227. [PubMed]
  • Baker CC, Russell RA, Roder DM, Esterman AJ. A nine year retrospective mortality study of workers in a British pharmaceutical company. J Soc Occup Med. 1986;36:95–98. [PubMed]
  • Barbone F, Franceschi S, Talamini R, Bidoli E, La Vecchia C. Occupation and bladder cancer in Pordenone (north-east Italy): a case-control study. Int J Epidemiol. 1994;23:58–65. [PubMed]
  • Baris D, Armstrong BG, Deadman J, Theriault G. A mortality study of electrical utility workers in Quebec. Occup Environ Med. 1996;53:25–31. [PMC free article] [PubMed]
  • Bevers RF, Kurth KH, Schamhart DH. Role of urothelial cells in BCG immunotherapy for superficial bladder cancer. Br J Cancer. 2004;91:607–612. [PMC free article] [PubMed]
  • Blair A, Zahm SH, Pearce NE, Heineman EF, Fraumeni JF., Jr. Clues to cancer etiology from studies of farmers. Scand J Work Environ Health. 1992;18:209–215. [PubMed]
  • Blair A, Hoar SK, Walrath J. Comparison of crude and smoking-adjusted standardized mortality ratios. J Occup Med. 1985;27:881–4. [PubMed]
  • Brown DP, Kaplan SD. Retrospective cohort mortality study of dry cleaner workers using perchloroethylene. J Occup Med. 1987;29:535–541. [PubMed]
  • Brown LM, Moradi T, Gridley G, Plato N, Dosemeci M, Fraumeni JF., Jr Exposures in the painting trades and paint manufacturing industry and risk of cancer among men and women in Sweden. Journal of Occupational & Environmental Medicine. 2002;44:258–264. [PubMed]
  • Brownson RC, Chang JC, Davis JR, Smith CA. Physical activity on the job and cancer in Missouri. Am J Public Health. 1991;81:639–642. [PubMed]
  • Bulbulyan MA, Ilychova SA, Zahm SH, Astashevsky SV, Zaridze DG. Cancer mortality among women in the Russian printing industry. American Journal of Industrial Medicine. 1999;36:166–171. [PubMed]
  • Cancer IAfRo Some Drinking-water Disinfectants and Contaminants, including Arsenic: World Health Organization. 2004
  • Cardis E, Gilbert ES, Carpenter L, Howe G, Kato I, Armstrong BK, Beral V, Cowper G, Douglas A, Fix J, et al. Effects of low doses and low dose rates of external ionizing radiation: cancer mortality among nuclear industry workers in three countries. Radiat Res. 1995;142:117–132. [PubMed]
  • Carpenter L, Roman E. Cancer and occupation in women: identifying associations using routinely collected national data. Environmental Health Perspectives. 1999;107(Suppl 2):299–303. [PMC free article] [PubMed]
  • Claude JC, Frentzel-Beyme RR, Kunze E. Occupation and risk of cancer of the lower urinary tract among men. A case-control study. Int J Cancer. 1988;41:371–379. [PubMed]
  • Colt JS, Baris D, Stewart P, Schned AR, Heaney JA, Mott LA, Silverman D, Karagas M. Occupation and bladder cancer risk in a population-based case-control study in New Hampshire. Cancer Causes Control. 2004;15:759–769. [PubMed]
  • Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ. Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. American Journal of Epidemiology. 2004;159:1160–1167. [PubMed]
  • Dolin PJ, Cook-Mozaffari P. Occupation and bladder cancer: a death-certificate study. Br J Cancer. 1992;66:568–578. [PMC free article] [PubMed]
  • Dosemeci M, Blair A. Occupational cancer mortality among women employed in the telephone industry. J Occup Med. 1994;36:1204–1209. [PubMed]
  • Dosemeci M, Hayes RB, Vetter R, Hoover RN, Tucker M, Engin K, Unsal M, Blair A. Occupational physical activity, socioeconomic status, and risks of 15 cancer sites in Turkey. Cancer Causes Control. 1993;4:313–321. [PubMed]
  • Drela N, Kozdron E, Szczypiorski P. Moderate exercise may attenuate some aspects of immunosenescence. BMC Geriatr. 2004;4:8. [PMC free article] [PubMed]
  • Dreyer L, Andersen A, Pukkala E. Avoidable cancers in the Nordic countries. Occupation. APMIS Suppl. 1997;76:68–79. [PubMed]
  • Folsom AR, Zhang S, Sellers TA, Zheng W, Kushi LH, Cerhan JR. Cancer incidence among women living on farms: findings from the Iowa Women's Health Study. Journal of Occupational & Environmental Medicine. 1996;38:1171–1176. [PubMed]
  • Frumin E, Velez H, Bingham E, Gillen M, Brathwaite M, LaBarck R. Occupational bladder cancer in textile dyeing and printing workers: six cases and their significance for screening programs. J Occup Med. 1990;32:887–890. [PubMed]
  • Garabrant DH, Wegman DH. Cancer mortality among shoe and leather workers in Massachusetts. Am J Ind Med. 1984;5:303–314. [PubMed]
  • Gleeson M, Pyne DB, Callister R. The missing links in exercise effects on mucosal immunity. Exerc Immunol Rev. 2004;10:107–128. [PubMed]
  • Gridley G, Nyren O, Dosemeci M, Moradi T, Adami HO, Carroll L, Zahm SH. Is there a healthy worker effect for cancer incidence among women in Sweden? Am J Ind Med. 1999;36:193–199. [PubMed]
  • Griffiths TR, Mellon JK. Evolving immunotherapeutic strategies in bladder and renal cancer. Postgrad Med J. 2004;80:320–327. [PMC free article] [PubMed]
  • Grollman AP, Shibutani S, Moriya M, Miller F, Wu L, Moll U, Suzuki N, Fernandes A, Rosenquist T, Medverec Z, Jakovina K, Brdar B, Slade N, Turesky RJ, Goodenough AK, Rieger R, Vukelic M, Jelakovic B. Aristolochic acid and the etiology of endemic (Balkan) nephropathy. Proc Natl Acad Sci U S A. 2007;104:12129–12134. [PubMed]
  • Guo J, Kauppinen T, Kyyronen P, Heikkila P, Lindbohm ML, Pukkala E. Risk of esophageal, ovarian, testicular, kidney and bladder cancers and leukemia among finnish workers exposed to diesel or gasoline engine exhaust. Int J Cancer. 2004;111:286–292. [PubMed]
  • Hafner C, Knuechel R, Zanardo L, Dietmaier W, Blaszyk H, Cheville J, Hofstaedter F, Hartmann A. Evidence for oligoclonality and tumor spread by intraluminal seeding in multifocal urothelial carcinomas of the upper and lower urinary tract. Oncogene. 2001;20:4910–4915. [PubMed]
  • Haldorsen T, Andersen A, Boffetta P. Smoking-adjusted incidence of lung cancer by occupation among Norwegian men. Cancer Causes Control. 2004;15:139–47. [PubMed]
  • Hardman AE. Physical activity and cancer risk. Proc Nutr Soc. 2001;60:107–113. [PubMed]
  • Hoar SK, Hoover R. Truck driving and bladder cancer mortality in rural New England. J Natl Cancer Inst. 1985;74:771–774. [PubMed]
  • Holick MF. Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease. Am J Clin Nutr. 2004;80:1678S–1688S. [PubMed]
  • Howe GR, Burch JD, Miller AB, Cook GM, Esteve J, Morrison B, Gordon P, Chambers LW, Fodor G, Winsor GM. Tobacco use, occupation, coffee, various nutrients, and bladder cancer. J Natl Cancer Inst. 1980;64:701–713. [PubMed]
  • Hu G, Qiao Q, Silventoinen K, Eriksson JG, Jousilahti P, Lindstrom J, Valle TT, Nissinen A, Tuomilehto J. Occupational, commuting, and leisure-time physical activity in relation to risk for Type 2 diabetes in middle-aged Finnish men and women. Diabetologia. 2003;46:322–329. [PubMed]
  • Huguet-Perez J, Palou J, Millan-Rodriguez F, Salvador-Bayarri J, Villavicencio-Mavrich H, Vicente-Rodriguez J. Upper tract transitional cell carcinoma following cystectomy for bladder cancer. 2001;40:318–323. [PubMed]
  • Hursting SD, Lavigne JA, Berrigan D, Donehower LA, Davis BJ, Phang JM, Barrett JC, Perkins SN. Diet-gene interactions in p53-deficient mice: insulin-like growth factor-1 as a mechanistic target. J Nutr. 2004;134:2482S–2486S. [PubMed]
  • Hwang YH, Lee ZY, Wang JD, Hsueh YM, Lu IC, Yao WL. Monitoring of arsenic exposure with speciated urinary inorganic arsenic metabolites for ion implanter maintenance engineers. Environ Res. 2002;90:207–216. [PubMed]
  • Ji J, Granstrom C, Hemminki K. Occupation and bladder cancer: a cohort study in Sweden. Br J Cancer. 2005;92:1276–1278. [PMC free article] [PubMed]
  • Jung HU, Frimodt-Moller PC, Osther PJ, Mortensen J. Pharmacological effect on pyeloureteric dynamics with a clinical perspective: a review of the literature. Urol Res. 2006 [PubMed]
  • Keller JE, Howe HL. Cancer in Illinois construction workers: a study. Am J Ind Med. 1993;24:223–230. [PubMed]
  • Kirkali Z, Tuzel E. Transitional cell carcinoma of the ureter and renal pelvis. 2003;47:155–169. [PubMed]
  • Kleinman GD. Occupational health and safety. The Swedish model. J Occup Med. 1984;26:901–905. [PubMed]
  • Kogevinas M, t Mannetje A, Cordier S, Ranft U, Gonzalez CA, Vineis P, Chang-Claude J, Lynge E, Wahrendorf J, Tzonou A, Jockel KH, Serra C, Porru S, Hours M, Greiser E, Boffetta P. Occupation and bladder cancer among men in Western Europe. Cancer Causes Control. 2003;14:907–914. [PubMed]
  • Konety BR, Lavelle JP, Pirtskalaishvili G, Dhir R, Meyers SA, Nguyen TS, Hershberger P, Shurin MR, Johnson CS, Trump DL, Zeidel ML, Getzenberg RH. Effects of vitamin D (calcitriol) on transitional cell carcinoma of the bladder in vitro and in vivo. J Urol. 2001;165:253–258. [PubMed]
  • Kristensen P, Andersen A, Irgens LM, Laake P, Bye AS. Incidence and risk factors of cancer among men and women in Norwegian agriculture. Scand J Work Environ Health. 1996;22:14–26. [PubMed]
  • la Vecchia C, Negri E, D'Avanzo B, Franceschi S. Occupation and the risk of bladder cancer. Int J Epidemiol. 1990;19:264–268. [PubMed]
  • Langseth H, Andersen A. Cancer incidence among women in the Norwegian pulp and paper industry. American Journal of Industrial Medicine. 1999;36:108–113. [PubMed]
  • Law GR, Cox DR, Machonochie NES, Simpson J, Roman E, Carpenter LM. Large Tables. Biostatistics. 2001;2:163–171. [PubMed]
  • Lee WJ, Hoppin JA, Blair A, Lubin JH, Dosemeci M, Sandler DP, Alavanja MC. Cancer incidence among pesticide applicators exposed to alachlor in the Agricultural Health Study. Am J Epidemiol. 2004;159:373–380. [PubMed]
  • Lynge E, Rix BA, Villadsen E, Andersen I, Hink M, Olsen E, Moller UL, Silfverberg E. Cancer in printing workers in Denmark. Occupational & Environmental Medicine. 1995;52:738–744. [PMC free article] [PubMed]
  • Lynge E. Occupational mortality and cancer analysis. Public Health Rev. 1990;18:99–116. [PubMed]
  • Ma CP, Yu DS, Yeh MY, Chang SY, Han SH. Natural killer cell activity in patients with urologic cancer. European Urology. 1987;13:397–400. [PubMed]
  • Madeb R, Messing EM. Gender, racial and age differences in bladder cancer incidence and mortality. Urol Oncol. 2004;22:86–92. [PubMed]
  • Mannetje A, Kogevinas M, Chang-Claude J, Cordier S, Gonzalez CA, Hours M, Jockel KH, Bolm-Audorff U, Lynge E, Porru S, Donato F, Ranft U, Serra C, Tzonou A, Vineis P, Wahrendorf J, Boffetta P. Occupation and bladder cancer in European women. Cancer Causes & Control. 1999;10:209–217. [PubMed]
  • Mannetje A, Kogevinas M, Chang-Claude J, et al. Smoking as a confounder in case-control studies of occupational bladder cancer in women. Am J Ind Med. 1999;36:75–82. [PubMed]
  • Mattos IE, Koifman S. Cancer mortality among electricity utility workers in a the state of Sao Paulo, Brazil. Rev Saude Publica. 1996;30:564–575. [PubMed]
  • Mattos IE, Sauaia N, Menezes PR. A cancer mortality pattern in Brazilian electrical workers. Cad Saude Publica. 2002;18:221–233. [PubMed]
  • Mattsson B, Wallgren A. Completeness of the Swedish Cancer Register. Non-notified cancer cases recorded on death certificates in 1978. Acta Radiol Oncol. 1984;23:305–313. [PubMed]
  • McCredie M, Stewart JH. Risk factors for kidney cancer in New South Wales. IV. Occupation. Br J Ind Med. 1993;50:349–354. [PMC free article] [PubMed]
  • McGeoghegan D, Binks K. The mortality and cancer morbidity experience of workers at the Capenhurst uranium enrichment facility 1946-95. J Radiol Prot. 2000;20:381–401. [PubMed]
  • McLaughlin JK, Blot WJ, Devesa SS, Fraumeni JF., Jr Cancer epidemiology and prevention. 2nd ed. Oxford University Press; New York: 1996. Renal cancer; pp. 1142–1155.
  • McLaughlin JK, Malker HS, Stone BJ, Weiner JA, Malker BK, Ericsson JL, Blot WJ, Fraumeni JF., Jr Occupational risks for renal cancer in Sweden. Br J Ind Med. 1987;44:119–123. [PMC free article] [PubMed]
  • McTiernan A, Ulrich C, Slate S, Potter J. Physical activity and cancer etiology: associations and mechanisms. Cancer Causes Control. 1998;9:487–509. [PubMed]
  • Mellemgaard A, Lindblad P, Schlehofer B, Bergstrom R, Mandel JS, McCredie M, McLaughlin JK, Niwa S, Odaka N, Pommer W. International renal-cell cancer study. III. Role of weight, height, physical activity, and use of amphetamines. 1995;60:350–354. [PubMed]
  • Miller AB, Bartsch H. Hair dye use and bladder cancer. Int J Cancer. 2001;94:901–902. [PubMed]
  • Moldoveanu AI, Shephard RJ, Shek PN. The cytokine response to physical activity and training. Sports Med. 2001;31:115–144. [PubMed]
  • Montanaro F, Ceppi M, Demers PA, Puntoni R, Bonassi S. Mortality in a cohort of tannery workers. Occupational & Environmental Medicine. 1997;54:588–591. [PMC free article] [PubMed]
  • Moradi T, Nyren O, Bergstrom R, Gridley G, Linet M, Wolk A, Dosemeci M, Adami HO. Risk for endometrial cancer in relation to occupational physical activity: a nationwide cohort study in Sweden. Int J Cancer. 1998;76:665–670. [PubMed]
  • Murai T, Mori S, Machino S, Hosono M, Takeuchi Y, Ohara T, Makino S, Takeda R, Hayashi Y, Iwata H, et al. Induction of renal pelvic carcinoma by phenacetin in hydronephrosis-bearing rats of the SD/cShi strain. Cancer Res. 1993;53:4218–4223. [PubMed]
  • Naito S, Tanaka K, Koga H, Kotoh S, Hirohata T, Kumazawa J. Cancer occurrence among dyestuff workers exposed to aromatic amines. A long term follow-up study. Cancer. 1995;76:1445–1452. [PubMed]
  • National Board of Health and Welfare of Sweden CfE Cancer Incidence in Sweden 1998 Stockholm. 2000
  • Notani PN, Shah P, Jayant K, Balakrishnan V. Occupation and cancers of the lung and bladder: a case-control study in Bombay. Int J Epidemiol. 1993;22:185–191. [PubMed]
  • Paterson RF, Ulbright TM, MacLennan GT, Zhang S, Pan CX, Sweeney CJ, Moore CR, Foster RS, Koch MO, Eble JN, Cheng L. Molecular genetic alterations in the laser-capture-microdissected stroma adjacent to bladder carcinoma. Cancer. 2003;98:1830–1836. [PubMed]
  • Pelucchi C, La Vecchia C, Negri E, Dal Maso L, Franceschi S. Smoking and other risk factors for bladder cancer in women. Preventive Medicine. 2002;35:114–120. [PubMed]
  • Pesch B, Haerting J, Ranft U, Klimpel A, Oelschlagel B, Schill W. Occupational risk factors for urothelial carcinoma: agent-specific results from a case-control study in Germany. MURC Study Group. Multicenter Urothelial and Renal Cancer. Int J Epidemiol. 2000;29:238–247. [PubMed]
  • Pfohl-Leszkowicz A, Manderville RA. Ochratoxin A: An overview on toxicity and carcinogenicity in animals and humans. Mol Nutr Food Res. 2007;51:61–99. [PubMed]
  • Prazmo Z, Dutkiewicz J, Skorska C, Sitkowska J, Cholewa G. Exposure to airborne Gram-negative bacteria, dust and endotoxin in paper factories. Ann Agric Environ Med. 2003;10:93–100. [PubMed]
  • Porru S, Aulenti V, Donato F, Boffetta P, Fazioli R, Cosciani Cunico S, Alessio L. Bladder cancer and occupation: a case-control study in northern Italy. Occupational & Environmental Medicine. 1996;53:6–10. [PMC free article] [PubMed]
  • Rabbani F, Perrotti M, Russo P, Herr HW. Upper-tract tumors after an initial diagnosis of bladder cancer: argument for long-term surveillance. 2001;19:94–100. [PubMed]
  • Richiardi L, Forastiere F, Boffetta P, Simonato L, Merletti F. Effect of different approaches to treatment of smoking as a potential confounder in a case-control study on occupational exposures. Occup Environ Med. 2005;62:101–104. [PMC free article] [PubMed]
  • Ries LAG, Eisner MP, Kosary CL, Hankey BF, Miller BA, Clegg L, Mariotto A, Fay MP, Feuer EJ, Edwards BK. SEER Cancer Statistics Review, 1975-2000, National Cancer Institute. National Cancer Institute; Bethesda, MD: 2003.
  • Romanenko A, Morimura K, Wanibuchi H, Wei M, Zaparin W, Vinnichenko W, Kinoshita A, Vozianov A, Fukushima S. Urinary bladder lesions induced by persistent chronic low-dose ionizing radiation. Cancer Sci. 2003;94:328–333. [PubMed]
  • Rousseau MC, Straif K, Siemiatycki J. IARC carcinogen update. Environ Health Perspect. 2005;113(9):A580–1. [PMC free article] [PubMed]
  • Ruder AM, Ward EM, Brown DP. Mortality in dry-cleaning workers: an update. Am J Ind Med. 2001;39:121–132. [PubMed]
  • Rusiecki JA, De Roos A, Lee WJ, Dosemeci M, Lubin JH, Hoppin JA, Blair A, Alavanja MC. Cancer incidence among pesticide applicators exposed to atrazine in the Agricultural Health Study. J Natl Cancer Inst. 2004;96:1375–1382. [PubMed]
  • Saint F, Kurth N, Maille P, Vordos D, Hoznek A, Soyeux P, Patard JJ, Abbou CC, Chopin DK. Urinary IL-2 assay for monitoring intravesical bacillus Calmette-Guerin response of superficial bladder cancer during induction course and maintenance therapy. Int J Cancer. 2003;107:434–440. [PubMed]
  • Schoenberg JB, Stemhagen A, Mogielnicki AP, Altman R, Abe T, Mason TJ. Case-control study of bladder cancer in New Jersey. I. Occupational exposures in white males. J Natl Cancer Inst. 1984;72:973–981. [PubMed]
  • Schumacher MC, Slattery ML, West DW. Occupation and bladder cancer in Utah. Am J Ind Med. 1989;16:89–102. [PubMed]
  • Severson RK, Nomura AM, Grove JS, Stemmermann GN. A prospective analysis of physical activity and cancer. Am J Epidemiol. 1989;130:522–529. [PubMed]
  • Sharir S, Jewett M. Genitourinary cancers. In: Neugut AI, Meadows AT, Robinson E, editors. Multiple Primary Cancers. Lippincott, Williams & Wilkins; Philadelphia: 1999.
  • Shavers VL, Lawrence D, Fagan P, Gibson JT. Racial/ethnic variation in cigarette smoking among the civilian US population by occupation and industry, TUS-CPS 1998-1999. Prev Med. 2005;41:597–606. [PubMed]
  • Shields T, Gridley G, Moradi T, Adami J, Plato N, Dosemeci M. Occupational exposures and the risk of ovarian cancer in Sweden. Am J Ind Med. 2002;42:200–213. [PubMed]
  • Siemiatycki J, Wacholder S, Dewar R, et al. Degree of confounding bias related to smoking, ethnic group, and socioeconomic status in estimates of the associations between occupation and cancer. J Occup Med. 1988;30:617–25. [PubMed]
  • Siemiatycki J, Richardson L, Straif K, Latreille B, Lakhani R, Campbell S, Rousseau MC, Boffetta P. Listing occupational carcinogens. Environ Health Perspect. 2004;112(15):1447–59. [PMC free article] [PubMed]
  • Silverman DT, Devesa SS, Moore LE, Rothman N. Bladder Cancer. In: Schottenfeld D, Fraumeni JF Jr, editors. Cancer Epidemiology and Pevention. Third Edition Oxford University Press; New York: 2006.
  • Silverman DT, Hoover RN, Albert S, Graff KM. Occupation and cancer of the lower urinary tract in Detroit. J Natl Cancer Inst. 1983;70:237–245. [PubMed]
  • Silverman DT, Levin LI, Hoover RN, Hartge P. Occupational risks of bladder cancer in the United States: I. White men. J Natl Cancer Inst. 1989;81:1472–1480. [PubMed]
  • Silverman DT, Levin LI, Hoover RN. Occupational risks of bladder cancer among white women in the United States. Am J Epidemiol. 1990;132:453–461. [PubMed]
  • Simpson J, Roman E, Law G, Pannett B. Women's occupation and cancer: preliminary analysis of cancer registrations in England and Wales, 1971-1990. American Journal of Industrial Medicine. 1999;36:172–185. [PubMed]
  • Sommer F, Klotz T, Schmitz-Drager BJ. Lifestyle issues and genitourinary tumours. World Journal of Urology. 2004;21:402–413. [PubMed]
  • Sont WN, Zielinski JM, Ashmore JP, Jiang H, Krewski D, Fair ME, Band PR, Letourneau EG. First analysis of cancer incidence and occupational radiation exposure based on the National Dose Registry of Canada. Am J Epidemiol. 2001;153:309–318. [PubMed]
  • Statistics CBo Smoking habits in Sweden: A mail survey--Spring 1963 Stockholm. Survey Research Center of the Central Bureau of Statistics; Sweden: 1965.
  • Stewart JH, Hobbs JB, McCredie MR. Morphologic evidence that analgesic-induced kidney pathology contributes to the progression of tumors of the renal pelvis. Cancer. 1999;86:1576–1582. [PubMed]
  • Stewart PA, Blair A. Women in the formaldehyde industry: their exposures and their jobs. J Occup Med. 1994;36:918–923. [PubMed]
  • Straif K, Weiland SK, Werner B, Chambless L, Mundt KA, Keil U. Workplace risk factors for cancer in the German rubber industry: Part 2. Mortality from non-respiratory cancers. 1998;55:325–332. [PMC free article] [PubMed]
  • Swanson GM, Burns PB. Cancer incidence among women in the workplace: a study of the association between occupation and industry and 11 cancer sites. J Occup Environ Med. 1995;37:282–287. [PubMed]
  • Takahashi T, Kakehi Y, Mitsumori K, Akao T, Terachi T, Kato T, Ogawa O, Habuchi T. Distinct microsatellite alterations in upper urinary tract tumors and subsequent bladder tumors. J Urol. 2001;165:672–677. [PubMed]
  • Teschke K, Morgan MS, Checkoway H, Franklin G, Spinelli JJ, van Belle G, Weiss NS. Surveillance of nasal and bladder cancer to locate sources of exposure to occupational carcinogens. Occup Environ Med. 1997;54:443–451. [PMC free article] [PubMed]
  • Thorn M, Bergstrom R, Johansson AM, Ramstrom L, Persson I, Malmstrom PU. Trends in urinary bladder cancer incidence in Sweden 1960-93 with special reference to histopathology, time period, birth cohort, and smoking. Cancer Causes Control. 1997;8:560–567. [PubMed]
  • Thune I, Furberg AS. Physical activity and cancer risk: dose-response and cancer, all sites and site-specific. Med Sci Sports Exerc. 2001;33:S530–550. discussion S609-510. [PubMed]
  • Thuvander A, Moller T, Barbieri HE, Jansson A, Salomonsson AC, Olsen M. Dietary intake of some important mycotoxins by the Swedish population. Food Addit Contam. 2001;18:696–706. [PubMed]
  • Tolbert PE. Oils and cancer. Cancer Causes Control. 1997;8:386–405. [PubMed]
  • Tripathi A, Folsom AR, Anderson KE. Risk factors for urinary bladder carcinoma in postmenopausal women. The Iowa Women's Health Study. Cancer. 2002;95:2316–2323. [PubMed]
  • Tynes T, Andersen A, Langmark F. Incidence of cancer in Norwegian workers potentially exposed to electromagnetic fields. Am J Epidemiol. 1992;136:81–88. [PubMed]
  • Ugnat AM, Luo W, Semenciw R, Mao Y. Occupational exposure to chemical and petrochemical industries and bladder cancer risk in four western Canadian provinces. Chronic Dis Can. 2004;25:63–71. [PubMed]
  • Villanueva CM, Cantor KP, Cordier S, Jaakkola JJ, King WD, Lynch CF, Porru S, Kogevinas M. Disinfection byproducts and bladder cancer: a pooled analysis. Epidemiology. 2004;15:357–367. [PubMed]
  • Vineis P, Magnani C. Occupation and bladder cancer in males: a case-control study. Int J Cancer. 1985;35:599–606. [PubMed]
  • Vineis P, Pirastu R. Aromatic amines and cancer. Cancer Causes & Control. 1997;8:346–355. [PubMed]
  • Vriesema JL, Aben KK, Witjes JA, Kiemeney LA, Schalken JA. Superficial and metachronous invasive bladder carcinomas are clonally related. 2001;93:699–702. [PubMed]
  • Wiklund K, Dich J. Cancer risks among female farmers in Sweden. Cancer Causes Control. 1994;5:449–457. [PubMed]
  • Wiklund K, Dich J. Cancer risks among male farmers in Sweden. Eur J Cancer Prev. 1995;4:81–90. [PubMed]
  • Wiklund K, Eklund G. Reliability of record linkage in the Swedish Cancer-Environment Register. Acta Radiol Oncol. 1986;25:11–14. [PubMed]
  • Wynder EL, Goldsmith R. The epidemiology of bladder cancer: a second look. Cancer. 1977;40:1246–1268. [PubMed]
  • Yazawa Y, Yokota M, Sugiyama K. Antitumor promoting effect of an active component of Polyporus, ergosterol and related compounds on rat urinary bladder carcinogenesis in a short-term test with concanavalin A. Biol Pharm Bull. 2000;23:1298–1302. [PubMed]
  • Zheng T, Cantor KP, Zhang Y, Lynch CF. Occupation and bladder cancer: a population-based, case-control study in Iowa. Journal of Occupational & Environmental Medicine. 2002;44:685–691. [PubMed]