The objective of this study was to obtain preliminary information on which non-occupational risk factors are responsible for the excess of lung cancer deaths seen in a cohort of workers in poultry slaughtering & processing plants, and to investigate whether established non-occupational risk factors for lung cancer mortality can be replicated. We conducted a pilot case-cohort study within a cohort of 43,904 poultry and non-poultry plant workers alive in 1990 and followed up to the end of 2003. Cases were 125 lung cancer deaths that occurred between 1990-2003 for whom interviews were successfully obtained. Controls (N=152) were derived from a random sample of the cohort in 1990. Statistical analysis was by logistic and Cox proportional hazards regression. The study successfully identified many of the established risk factors for lung cancer, and a few new ones were identified. The study demonstrates that valid case-cohort studies in this occupational group are feasible, and also successfully identified non-occupational risk factors that may need to be adjusted for in future planned large-scale studies of this occupational group.
Chickens; meat; lung cancer; diet; non-occupational
Workers in poultry slaughtering/processing plants have high exposures to oncogenic viruses that naturally infect and cause cancer in poultry. They also have exposures to chemical carcinogens at work. We initially performed three cohort mortality studies of 30,411 poultry workers and 16,405 non-poultry workers who were members of the United Food and Commercial Workers unions in the United States (N=46,816). An excess of lung cancer was consistently observed in the poultry workers [1-4]. We next conducted a pilot case-cohort study of lung cancer within a subset of 43,904 subjects of the 46,816 subjects that were alive in 1990, and followed them up to the end of 2003. The findings for occupational exposures have been published,  and the corresponding literature reviewed . Here we present the results for non-occupational exposures. The study provides a unique opportunity for examining whether established non-occupational risk factors for lung cancer can be replicated in this group of workers who are among the lowest paid workers in industry. Also, if established risk factors for lung cancers are confirmed in this study, this will be strong evidence that future planned large full-scale studies to investigate lung cancer occurrence in this occupational group will give valid results.
Material & Methods
Cases were the first 125 lung cancer deaths out of 552 (23%) that occurred in the cohort between 1990 and 2003, for whom telephone interviews were obtained. Controls were similarly the first 152 subjects (10%) for whom telephone interviews were obtained. They originate from a random sample of 1,516 persons in the cohort that were alive in 1990. A telephone questionnaire was administered to the next-of-kin of study subjects if they were deceased (all cases, and 13% of controls) or to live control subjects themselves. Statistical analyses were conducted using both logistic regression and Cox proportional hazards regression methods as previously described .
Ethics: The study was approved by the University of North Texas Health Science Center’s Institutional Review Board
The results are summarized in Tables 1&2.
Table 1. Poultry associated non-occupational exposures: Associations with lung cancer mortality, 1990-2003
|Adjusted Logistic Regression ORs†||Adjusted Cox Proportional HRs‡|
|OR (95% CI)||HR (95% CI)|
|Ever smoked tobacco||113||135||7.1 (2.8-18.0)||3.7 (1.8-7.4)|
|Mostly prepared own food||118||147||0.5 (0.2-1.1)||0.5 (0.3-0.9)|
|Ever drunk wine||113||146||0.4 (0.2-0.9)||0.6 (0.4-0.9)|
|Swam at least once a month for more than one year||115||147||0.4 (0.1-0.9)||0.5 (0.3-0.9)|
|Regularly performed any exercise||117||147||0.3 (0.1-0.5)||0.5 (0.3-0.7)|
|Ever treated with radiation therapy||106||141||16.6 (6.8-40.8)||5.3 (3.5-8.1)|
|Ever treated with radiation therapy for cancer||67||21||1.6 (0.5-5.4)||1.1 (0.6-1.9)|
|Ever treated with radiation therapy for skin/scalp conditions||68||20||1.0 (0.1-11.9)||1.5 (0.6-3.9)|
|Ever treated with radiation therapy for arthritis||70||20||0.5 (0.1-1.9)||0.8 (0.4-1.5)|
|Tuberculosis||102||144||9.0 (0.3-304.9)||2.2 (0.9-5.4)|
|Cirrhosis||112||147||7.8 (0.7-82.6)||2.0 (0.8-5.0)|
|Pancreatic inflammation||111||146||6.2 (0.7-55.5)||1.2 (0.5-2.8)|
|Infectious mononucleosis||109||147||3.6 (0.3-51.5)||1.7 (0.4- 6.9)|
|Cold sores on lip||114||145||0.6 (0.3-1.2)||0.6 (0.4-0.9)|
|Diabetes||114||148||0.3 (0.1-0.8)||0.4 (0.2-0.9)|
|Allergic to pollen||113||145||0.2 (0.1-0.5)||0.3 (0.2-0.7)|
|Allergy to drug medications||110||144||0.1 (0.0-0.4)||0.2 (0.1-0.5)|
|Ate beef once every two weeks for most of life||114||144||14.9 (1.8-123.0)||9.6 (1.3-69.0)|
|Ate bacon every week for most of life||112||141||12.1 (4.2-35.1)||5.1 (2.4-11.2)|
|Ate uncooked fish/shellfish every week for most of life||111||142||2.0 (0.4-10.0)||1.4 (0.5-3.8)|
|Ate spicy foods every week for most of life||110||142||1.7 (0.9-3.4)||1.3 (0.9-1.9)|
|Ate chicken once every two weeks for most of life||116||144||1.7 (0.4-7.4)||1.5 (0.6-3.6)|
|Ate pork once every two weeks for most of life||114||144||1.6 (0.7-3.6)||1.4 (0.8-2.4)|
|Ate lamb once every two weeks for most of life||115||144||1.6 0.5-5.2)||1.1 (0.6-2.2)|
|Ate turkey once every two weeks for most of life||115||144||1.0 (0.5-1.9)||1.0 (0.7-1.5)|
|Ate fruits every week for most of life||108||143||0.8 (0.3-2.0)||0.9 (0.5-1.5)|
|Ate freshwater fish at least once a month||115||142||0.7 (0.4-1.4)||0.8 (0.5-1.2)|
|Ate cheese every week for most of life||109||142||0.7 (0.3-1.7)||0.8 (0.5-1.4)|
|Ate raw eggs at least once every two weeks for most of life||114||143||0.6 (0.1-3.9)||0.7 (0.3-2.1)|
|Ate veggies every week for most of life||111||143||0.5 (0.3-1.1)||0.6 (0.2-1.7)|
|Ate seafood once every two weeks for most of life||111||144||0.5 (0.2-0.9)||0.7 (0.4-1.0)|
|Ever ingested herbal leaves, drinks, medications at least once a week for >1yr||111||140||0.3 (0.1-0.9)||0.4 (0.2-1.0)|
|Ever adhered to a vegetarian diet for more than a year||114||143||0.2 (0.0-3.8)||0.3 (0.0-2.1)|
|Method of cooking meats|
|Ate meat fried at least once every two weeks for most of life||113||144||2.6 (1.0-6.6)||1.9 (1.0-3.8)|
|Ate meat salted at least once every two weeks for most of life||109||144||2.4 (1.2-4.8)||1.5 (1.0-2.2)|
|Ate meat raw at least once every two weeks for most of life||111||144||1.6 (0.2-11.3)||1.9 (0.7-5.3)|
|Ate meat barbequed at least once every two weeks for most of life||112||144||1.5 (0.8-2.9)||1.1 (0.7-1.6)|
|Ate meat smoked at least once every two weeks for most of life||110||144||1.3 (0.6-2.8)||1.0 (0.6-1.6)|
|Use vitamins at least every week for more than a year||103||140||0.4 (0.2-0.8)||0.6 (0.4-1.0)|
|Ever had general anesthesia during surgery||108||140||0.4 (0.2-0.7)||0.6 (0.4-0.9)|
|Ever used hormone replacement therapy continuously for at least a year||24||57||0.2 (0.0-0.8)||0.3 (0.1-0.9)|
|FAMILY HISTORY OF CONDITIONS|
|Reported cancer in children||114||139||1.7 (0.5-6.4)||1.1 (0.6-1.9)|
|Reported cancer in parents||107||135||0.8 (0.4-1.6)||0.8 (0.5-1.2)|
|Reported cancer in spouse||113||139||0.8 (0.3-2.0)||1.1 (0.7-1.8)|
|Typhoid||46||127||2.1 (0.8-5.5)||1.4 (0.7-2.7)|
|Pneumococcal infections||48||127||1.7 (0.6-4.3)||1.4 (0.7-2.7)|
|Yellow fever||41||127||1.7 (0.5-5.6)||0.9 (0.4-2.2)|
|Ever received gamma globulin||56||131||1.6 (0.3-8.7)||1.8 (0.6-6.0)|
|Measles||42||124||1.5 (0.6-3.5)||1.0 (0.5-2.0)|
|Small pox||64||128||1.4 (0.6-3.1)||1.0 (0.6-1.7)|
|Diphtheria||55||120||1.3 (0.6-3.2)||1.0 (0.5-1.8)|
|Mumps||43||123||1.3 (0.5-3.0)||0.9 (0.5-1.7)|
|Ever owned a cell phone||115||141||0.2 (0.1-0.4)||0.3 (0.1-0.6)|
† Odds ratios (OR) were adjusted for smoking, gender, and age by the Logistic Regression Method
‡ Hazard ratios (HR) were adjusted for smoking, gender, and”> age by the Cox Proportional Hazard Method
@ For ever smoked tobacco, adjustment was for age and gender.
Table 2. Lung cancer mortality associated with frequent consumption of Beef and Bacon, adjusted for occupational exposures, meat preparation type, tobacco smoking, age, gender, and union site – (1990-2003)
|Ate a lot of Beef||Ate a lot of Bacon|
|Case/control||HR (95% CI)||Case/control||HR (95% CI)|
|History of working in stockyard||56/99||—||56/98||2.7 (1.1-6.7)|
|Ever killed chickens at work||105/143||8.9 (1.2-64.6)||103/140||4.7 (2.1-10.3)|
|History of working in deli department||66/99||—||66/98||3.1 (1.3-7.4)|
|History of working in meat department||66/99||—||66/98||3.1 (1.3-7.1)|
|Ate a lot of meat raw||109/144||9.8 (1.3-71.1)||108/141||4.8 (2.2-10.5)|
|Ate a lot of meat fried||111/144||8.9 (1.2-64.8)||110/141||4.7 (2.1-10.3)|
|Ate a lot of meat BBQ||111/144||9.7 (1.3-70.4)||109/141||5.0 (2.3-10.9)|
|Ate a lot of meat smoked||109/144||9.5 (1.3-69.0)||109/141||5.1 (2.3-11.2)|
|Ate a lot of meat salted||107/144||8.5 (1.2-62.0)||106/141||4.5 (2.0-10.1)|
*HR = hazard ratio; CI = confidence interval; NOTE: Questionnaire defined a lot as “once every two weeks for most of life”
With regard to lifestyle, established associations in the literature with cigarette smoking, drinking of wine and exercise were confirmed [7-9]. The significant association with radiation exposure may be real and consistent with well-documented reports of this association [7,10]; but it is also likely that it reflects using radiation treatment for the lung cancer, since no significant associations were seen for treating other conditions with radiation. The elevated but not statistically significant risk for tuberculosis seen is consistent with the findings of a comprehensive review . Protective effects were seen for history of cold sores, diabetes, and allergy to pollen and medications. These are consistent with reports of allergies being protective risk factors for the disease [12-14].
Frequent consumption of beef and bacon were significantly associated with increased lung cancer risk, and the risks persisted after adjusting for occupational exposures that were associated with increased risks  Table 2. The risks also persisted irrespective of whether the beef or bacon was eaten raw, fried, barbecued, smoked, or salted – Table 2. The method of preparation of any of the different meats (beef, pork, poultry, etc.) was not an independent risk factor for lung cancer (data not shown) except for salted chicken, turkey and lamb for which the hazard ratios were 1.4 (95% CI, 1.0-2.2), 1.5 (95% CI, 1.0-2.2) and 1.5 (95% CI, 1.0-2.2), respectively. These associations with beef and bacon and salted meats are well documented in the literature [7,15-18], and mere consumption of these meats seem to be the most important factor.
Risk estimates for eating of seafood, ingestion of herbal leaves, drinks or medications, adherence to vegetarian diet, vitamin intake, hormone replacement therapy, and history of diabetes and general anesthesia were all below the null. These protective associations have been previously reported [7,19-21], except for history of diabetes and general anesthesia for which we have no explanation. The results for cellphone use are likely due to systematic bias resulting from cases (all deceased) dying during earlier periods when cellphone use was not in existence or infrequent while controls most of whom were alive, lived long enough into the more recent period of popular use; moreover, this reduced risk was also seen for the other cancers (liver, pancreas, brain) investigated [22,23].
The findings in this study are important for three reasons: 1) in spite of its small size, the study remarkably was able to confirm many of the reported non-occupational risk factors in the literature for lung cancer in this low-income population. This indicates that future planned case-cohort studies nested within occupational cohorts of workers in poultry slaughtering and processing plants that are assembled to investigate cancer occurrence in this industry, are feasible and capable of giving valid results. Such studies can provide valuable information on both occupational and non-occupational risk factors for various cancers. Secondly, this study has successfully identified non-occupational exposures that are risk factors for lung cancer in this specific population of poultry workers. These constitute some important potential confounding factors that may need to be adjusted for when investigating the role of occupational carcinogenic exposures (especially oncogenic viruses) in the occurrence of lung cancer in poultry slaughtering & processing plant workers in future full-scale large case-cohort studies. Finally, this small study indicates that established risk factors for lung cancer are equally applicable for this group of minimum-wage workers who belong to the lowest socioeconomic group.
Our appreciation and thanks go to the United Food & Commercial Workers International Union for their continuing support and collaboration over the years without which this research would not have been possible.
The study was funded by a grant 1 RO1 OH008071 from the National Institute for Occupational Safety & Health.
Competing interests: None
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