Cancer mortality in workers employed in cattle, pigs, and sheep slaughtering and processing plants
Introduction
Workers in the meat industry include persons who work in abattoirs (slaughterhouses) where cattle, pigs, and sheep are slaughtered for human consumption, and those who work in meat processing plants where no killing is done, but the carcasses of these animals killed elsewhere are brought in for processing (by being cut into special smaller pieces, by being cured, spiced, or cooked into various products, or used to manufacture meat-related products such as meat pies, etc.). In large abattoirs, meat processing is also carried out. These food animals and their raw or inadequately cooked products are naturally infected with viruses that cause cancer in the animals. The viruses include, the bovine leukemia virus (BLV), a retrovirus that causes lymphosarcoma in cattle and sheep (Burny and Mammerickx, 1987); jaagsietke sheep retrovirus (JSRV) that causes adenocarcinoma of the lung in sheep (Palmarini and Fan, 2001); ovine nasal adenocarcinoma virus (ONAV) a retrovirus that causes nasal adenocarcinoma in sheep (Cousens et al., 1999, Cousens et al., 2009); caprine nasal adenocarcinoma virus (CNAV) another retrovirus that causes nasal adenocarcinoma in goats (Ortin et al., 2003); and the bovine papilloma viruses (BPVs) that cause cancer of the alimentary tract, bladder cancer, fibromas, fibrosarcomas, meningiomas and chondromas, and warts, in cattle (Campo, 1987, Lancaster and Olson, 1982). It is not known whether these viral agents cause cancer in humans also.
Workers in these plants have one of the highest human exposures to these viruses, and we therefore reason that if these viruses do cause cancer in humans, this should be readily evident in this highly exposed group. Accordingly, we and others have conducted mortality and cancer incidence studies of butchers and meatcutters, and workers in slaughterhouses and meat processing plants (Besson et al., 2006, Boffetta et al., 2000, Coggon et al., 1989, Coggon and Wield, 1995, Doerken and Rehpenning, 1982, Fox et al., 1982, Fritschi et al., 2003, Griffith, 1982, Guberan et al., 1993, Gustavsson et al., 1987, Johnson et al., 1995a, Lagorio et al., 1995, Lynge et al., 1983, McLean et al., 2004, Milham, 1982, Reif et al., 1989). With the exception of studies by Coggon and Wield, 1995, Milham, 1982, the overwhelming majority of the studies have reported an excess occurrence of various cancers, including cancer of the lung, buccal cavity and pharynx, esophagus, bladder, kidney, bone, stomach, larynx, colon/rectum, and prostate.
We previously studied mortality on two occasions in a cohort of workers employed in abattoirs and meat processing plants where cattle, pigs, or sheep were killed and/or processed. Follow-up was from 1949 to 1980 and 1949 to 1989 (Johnson and Fischman, 1982, Johnson et al., 1986a, Johnson et al., 1986b, Johnson, 1989, Johnson et al., 1995a). An excess of cancers of the lung, buccal cavity and pharynx, esophagus, bladder, kidney, bone, and colon was recorded in the cohort. We describe here a further follow-up of this cohort up to the end of 2006, but this time excluding subjects who worked exclusively in predominantly pork processing plants.
Section snippets
Methods
The cohort was identified from a local meatcutters' union in Baltimore, and consisted of 4996 workers who were employed in plants where cattle, pigs, and sheep were killed or killed and processed (heretofore referred to as abattoirs), and a total of 3642 who worked in processing plants that handled these same animals, but where no killing was performed. Carcasses of animals killed elsewhere several days previously are brought in, to these plants for processing. Workers studied were employed
Results
The number of subjects, deaths, and person-years are given in Table 2. As can be seen, the 8638 workers that comprise the study population contributed a total of 337,854.1 person-years, i.e., each study subject contributed an average of 39.1 person-years of observation, and 62% of them died during the study period. Whites contributed 81.1% of the person-years and non-whites 18.9%; males contributed 74.8% of the person-years and females 25.2%. There were 593 subjects born in 1906 or earlier, who
Discussion
Other than race, there were few missing data (Table 1). The findings of this study are important because 1) the average follow-up for study subjects was 39 years (Table 2), which is adequate for investigating diseases with long latency period such as cancers; 2) more than 60% of the workers studied were deceased, which should give a good and fairly representative pattern of mortality in this occupational group; 3) the union records from which the study population was derived were exceptionally
Acknowledgments
This study was funded by a grant (1 RO1 OH008687) from the National Institute for Occupational Safety & Health. Initial funding was provided by the National Institute of Environmental Health Sciences, and the National Cancer Institute. Other than in providing the funds, these agencies had no involvement in the design, collection, analysis, and interpretation of the data. There are no competing interests.
References (48)
- et al.
Jaagsiekte sheep retrovirus is present at high concentration in lung fluid produced by ovine pulmonary adenocarcinoma-affected sheep and can survive for several weeks at ambient temperatures
Res Vet Sci
(2009) - et al.
Lung cancer in butchers
Lancet
(1982) - et al.
Lung cancer in butchers
Lancet
(1982) - et al.
Development of a food database of nitrosamines, heterocyclic amines, and polycyclic aromatic hydrocarbons 1
J Nutr
(2004) - et al.
Cancer mortality among butchers and slaughterhouse workers
Lancet
(1982) - et al.
Lung cancer in Danish butchers
Lancet
(1983) - et al.
Airborne bacteria and carcass contamination in slaughterhouses
J Food Protect
(1997) Oral squamous cell carcinoma; from an hypothesis about a virus, to concern about possible sexual transmission
Oral Oncol
(2002)- et al.
Cancer mortality among butchers: a 24-state death certificate study
J Occup Environ Med
(2006) - et al.
Adult-onset acute leukemia and employment in the meat industry: a New Zealand case–control study
Cancer Causes Control
(2001)
Employment as a butcher and cancer risk in a record-linkage study from Sweden
Cancer Causes Control
Humans have antibodies reactive with bovine leukemia virus
AIDS Res Hum Retroviruses
Laceration injuries among workers at meatpacking plants
Am J Ind Med
Papillomas and cancer in cattle
Cancer Surv
Occupational exposure to poultry and prevalence of antibodies against Marek's disease virua and avian leukosis retroviruses
Occup Environ Med
Lung cancer in the meat industry
Br J Ind Med
Mortality of butchers and cooks identified from the 1961 census of England and Wales
Occup Environ Med
Complete sequence of enzootic nasal tumor virus, a retrovirus associated with transmissible intranasal tumors of sheep
J Virol
A prospective study of red and processed meat intake in relation to cancer risk
PLoS Med
Mortality and cancer incidence in a cohort of meatworkers
Occup Environ Med
Papillomaviruses and their association with cancer in animals and in man
Cancer Surv
Lung cancer in butchers
Lancet
Mortality and incidence of cancer among a cohort of self employed butchers from Geneva and their wives
Br J Ind Med
Cited by (19)
Spatial interaction between breast cancer and environmental pollution in the Monterrey Metropolitan Area
2021, HeliyonCitation Excerpt :The food cooking byproducts had been linked to cancer, but also the meat processing. Johnson (2011) showed an excess of death from several cancers, including BC, in meat processing industry workers from slaughters, butchers, meat cutters, and meat processors. Processed meat may also constitute a risk for BC and this products are highly consumed by the study population.
Food of animal origin and risk of non-Hodgkin lymphoma and multiple myeloma: A review of the literature and meta-analysis
2016, Critical Reviews in Oncology/HematologyCitation Excerpt :Likewise, the causes of multiple myeloma remain largely unknown despite some evidence concerning a few occupational exposures (like benzene and ethylene oxide (Cogliano et al., 2011) and ionizing radiation (Schubauer-Berigan et al., 2015) and overweight and obesity (Hofmann et al., 2013). The hypothesis that foods of animal origin may increase the risk of haematological malignancies originated from the frequent finding of an increased incidence among people who are occupationally exposed to animals and meats, like livestock and poultry farmers, butchers and abattoir workers (Metayer et al., 1998; Moore et al., 2007; t Mannetje et al., 2008; Johnson, 2011; Beane Freeman et al., 2012). Several studies have investigated the possible link between the consumption of foods of animal origin and the risk of non-Hodgkin lymphoma and multiple myeloma in the general (i.e., non-occupationally exposed) population.
Non-cancer mortality in workers in the meat and delicatessen departments of supermarkets (1950-2006)
2015, Environmental ResearchCancer mortality in the meat and delicatessen departments of supermarkets (1950-2006)
2015, Environment InternationalCitation Excerpt :Occupational cohorts are ideal for this purpose because meat and poultry workers in cattle, pigs, sheep, and poultry slaughterhouses and processing plants who handle these animals have the highest human exposures to these viruses. Important epidemiologic evidence accumulating from occupational cohort studies with these types of workers from all over the world have consistently reported an excess occurrence of certain cancers in these workers (Boffetta et al., 2000; Coggon et al., 1989; Guberan et al., 1993; Johnson, 2011; Johnson et al., 1986a,b, 2010a,b; McLean et al., 2004; McLean and Pearce, 2004). We report here on cancer mortality in a cohort of meat cutters and meat wrappers in the meat and delicatessen departments of supermarkets that has been previously followed-up on two occasions.
Pathological and Aetiological Studies in Sheep Exhibiting Extrathoracic Metastasis of Ovine Pulmonary Adenocarcinoma (Jaagsiekte)
2013, Journal of Comparative PathologyMortality in workers employed in pig abattoirs and processing plants
2011, Environmental ResearchCitation Excerpt :The SMR is the total observed number of deaths divided by the total expected. We investigated a total of 185 separate causes of death, and these have been listed elsewhere (Johnson et al., 2009; Johnson, 2011). While all 231 deceased subjects had complete information on race, gender, and date of birth, the remaining 279 subjects (55%) not identified as deceased had no information on race, and their race was imputed based on the racial distribution of deceased subjects.