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Nathaniel C. Briggs, MD, MSc, Robert S. Levine, MD, H. Irene Hall, PhD, Otis Cosby, MD, MSPH, Edward A. Brann, MD and Charles H. Hennekens, MD, DrPH

Nathaniel C. Briggs and Robert S. Levine are with the Division of Preventive Medicine, Department of Internal Medicine, Meharry Medical College, Nashville, Tenn. H. Irene Hall is with the National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Ga. Otis Cosby is with the Division of Occupational Medicine, Department of Family and Community Medicine, Meharry Medical College. Edward A. Brann is with the National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention. Charles H. Hennekens is with the Departments of Medicine and Epidemiology and of Public Health, University of Miami School of Medicine and Mount Sinai Medical Center-Miami Heart Institute, Miami, Fla.

Correspondence: Requests for reprints should be sent to Nathaniel C. Briggs, MD, MSc, Division of Preventive Medicine, Department of Internal Medicine, Meharry Medical College, 1005 Dr DB Todd Jr Blvd, Box 52A, Nashville, TN 37208 (email: nbriggs{at}mmc.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION References

 

Objectives. This study examined occupational risks for non-Hodgkin’s lymphoma, Hodgkin’s disease, and soft-tissue sarcoma among African American and White men.

Methods. Race-specific multivariate logistic regression analyses were conducted using data from a large US population-based case–control study.

Results. Significant occupational risks were limited to African Americans; chromium was associated with non-Hodgkin’s lymphoma (odds ratio [OR] = 3.9, 95% confidence interval [CI] = 1.2, 12.9) and wood dust was associated with Hodgkin’s disease (OR = 4.6, 95% CI = 1.6, 13.3) and soft-tissue sarcoma (OR = 3.7, 95% CI = 1.6, 8.6).

Conclusions. Race-specific occupational risk factors for cancer were evident only among African American men. This may reflect racial disparities in levels of exposure to occupational carcinogens.

	INTRODUCTION

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African American men in the United States have a much higher cancer incidence than White men, but rates among African American and White women are similar.¹ This disparity may be attributable, in part, to disproportionate exposure of African American men to hazardous occupational conditions.^2–4 However, data are sparse on race-specific occupational risk factors for cancer.^4,5 Furthermore, published reports have generally been based on data from death certificates and other secondary sources, which have questionable validity because of racial disparities in accuracy.^6,7

In this exploratory study, we examined race-specific occupational risk factors for non-Hodgkin’s lymphoma, Hodgkin’s disease, and soft-tissue sarcoma using data provided by African American and White men aged 32 to 60 years who participated in the Selected Cancers Study.^8–11

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION References

 
Study Design
The Selected Cancers Study was a large population-based case–control study designed to investigate possible associations between Agent Orange exposure during US military service in Vietnam and the risks of developing non-Hodgkin’s lymphoma, Hodgkin’s disease, sarcoma, nasal cancer, nasopharyngeal cancer, and primary liver cancer. The study’s methods have been described in detail elsewhere.^8–11

Briefly, the study population comprised men who were born between 1929 and 1953, representing the age group that was eligible for service in Vietnam. Eligible case patients were men diagnosed with selected cancers between 1984 and 1988. The case men were identified from 8 US cancer registries (Atlanta, Ga; Connecticut; Detroit, Mich; Iowa; Kansas; Miami, Fla; San Francisco, Calif; and Seattle, Wash). All registries except Miami and Kansas were part of the National Cancer Institute’s Surveillance Epidemiology and End Results program. A common group of living control subjects for all cancers was identified by random-digit telephone dialing.

Control subjects with no history of a selected cancer were frequency matched to presumptive lymphoma case patients (non-Hodgkin’s lymphoma, Hodgkin’s disease, or "lymphoma not otherwise specified") by birth year (1929–1933, 1934–1938, 1939–1943, 1944–1948, and 1949–1953) and geographic region of cancer registry.

This analysis was limited to non-Hodgkin’s lymphoma, Hodgkin’s disease, and sarcoma because few African American men were diagnosed with the other cancers (nasal: African American = 8, White = 53; nasopharyngeal: African American = 12, White = 50; primary liver: African American = 18, White = 55).

Selection of Case Patients and Control Subjects
Non-Hodgkin’s lymphoma and Hodgkin’s disease. Of 2354 men with a presumptive diagnosis of lymphoma (non-Hodgkin’s lymphoma, Hodgkin’s disease, or "lymphoma not otherwise specified"), 2073 (88%) agreed to participate in the study (Table 1). Pathology specimens were available for 97% of the men. After an independent, blinded review by 3 hematopathologists, consensus diagnoses were reached for 1511 non-Hodgkin’s lymphoma cases, 343 Hodgkin’s disease cases, and 14 unclassifiable lymphoma cases. Non-Hodgkin’s lymphoma was classified by the Working Formulation.¹² Hodgkin’s disease was classified using the International Classification of Diseases for Oncology.¹³

Control Subjects. Of 15 768 households contacted for screening, 14 328 (91%) provided eligibility information, 4381 of 4822 (91%) households with eligible men provided follow-up information, 2299 men were randomly selected for an interview and 1910 men (83%) completed interviews.

Analysis Population
Our analysis was limited to directly-interviewed non-Hispanic African American and non-Hispanic White men for whom interviewers judged interview quality and interviewee cooperation to be good. Men with AIDS or major AIDS risk factors (injection drug use, homosexual/bisexual orientation) and men with Von Recklinghausen’s neurofibromatosis or Gardner’s syndrome were excluded because of strong associations with lymphoma and sarcoma, respectively.

Proxy interviews were excluded because previous Selected Cancers Study findings indicated that proxy data on occupational exposure seriously compromised internal validity.¹⁴ Men with an AIDS history were excluded because AIDS-associated lymphoma is considered to be a unique nosological entity. Moreover, the overwhelming association of AIDS with non-Hodgkin’s lymphoma in our study population (290 case patients and 1 control subject) would have precluded adjustment for confounding.

The final study population included 959 non-Hodgkin’s lymphoma cases (African American = 66, White = 893), 291 Hodgkin’s disease cases (African American = 22, White = 269), 243 soft-tissue sarcoma cases (African American = 38, White = 205), and 1620 control subjects (African American = 132, White = 1488).

Data Collection
Information about demographics, medical history, lifestyle, and occupation was collected by professional interviewers who administered structured questionnaires, generally through telephone interviews lasting about 50 minutes. To increase participation rates, some in-person interviews were also conducted (non-Hodgkin’s lymphoma = 75, Hodgkin’s disease = 8, sarcoma = 25, control subjects = 36).

As part of the occupational history portion of the interview, study participants were asked about every full-time and part-time job held for at least one year since the age of 18 years. In addition, each study participant was specifically queried about all occupational exposures implicated as etiologic determinants for 1 or more of the selected cancers.^8–11

Statistical Analysis
Multivariate unconditional logistic regression was performed using SAS (SAS Institute Inc, Cary, NC) to calculate odds ratios (ORs) and 95% confidence intervals (CIs) adjusted for the matching factors. Because so few African Americans were from Iowa, Kansas, and Seattle, case patients and control subjects from these registries were combined. Cancer-specific analyses were limited to occupational exposures reported by 5 or more African American case patients.

	RESULTS

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Demographics
For each race, the proportions of case patients and control subjects by registry were similar (Table 2). Relative to White men, however, proportionately more African American men were from Atlanta, Detroit, and Miami, and proportionately fewer African American men were from Connecticut, Iowa, Kansas, and Seattle. Control men of both races were slightly younger than men with non-Hodgkin’s lymphoma and slightly older than men with Hodgkin’s disease because of frequency matching that was based on presumptive lymphoma diagnoses.

Relative Magnitude of Race- and Cancer-Specific Odds Ratios
Cancer-specific odds ratios among African American men were greater than corresponding odds ratios among White men for 73% (8 of 11), 100% (4 of 4) and 92% (11 of 12) of occupational exposures reported by 5 or more African American men with non-Hodgkin’s lymphoma, Hodgkin’s disease or soft-tissue sarcoma, respectively. For all cancer types combined, the odds ratios among African American men were increased relative to corresponding odds ratios among White men for 85% (23 of 27) of occupational exposure comparisons (P_{sign test} = .0003).

	DISCUSSION

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Among African American men, chromium was associated with a significantly increased risk of non-Hodgkin’s lymphoma and wood dust was associated with significantly increased risks of both Hodgkin’s disease and soft-tissue sarcoma. Among White men, no associations reached significance.

Chromium as a Race-Specific Risk Factor for Non-Hodgkin’s Lymphoma
The finding that African American men with an occupational exposure to chromium had an increased risk of non-Hodgkin’s lymphoma was unanticipated because chromium is not widely implicated as a lymphomagen. However, hexavalent chromium compounds are well-established human carcinogens and are strongly associated with respiratory cancer.¹⁵

Biological plausibility exists for lymphomagenesis as hexavalent chromium is taken up by alveolar macrophages,¹⁵ has been associated with cytogenetic abnormalities in peripheral lymphocytes of exposed workers,¹⁵ and was used by all but 1 chromium-exposed African American case patient with non-Hodgkin’s lymphoma, for whom chromium was unknown. Specificity of the association for African American men is consistent with findings from a study of male chromate-industry workers showing a proportionate mortality ratio for lymphatic cancer of 3.7 among non-Whites versus 1.1 among Whites.¹⁶

Historical reports of striking racial disparities among chromate-industry workers in relation to risk of respiratory cancer^17,18 also parallel our finding that chromium-exposed African American men have an increased risk of non-Hodgkin’s lymphoma. A large retrospective cohort study of US chromate-industry workers revealed a relative risk of 80.0 for respiratory cancer mortality among non-Whites versus 14.3 among Whites.¹⁸ Because 41% of non-Whites were found to have been assigned to jobs involving exposure to the highest levels of chromate dust,¹⁸ compared with only 16% of Whites, disproportionate exposure to carcinogenically hazardous working conditions was considered a likely contributing factor.⁵ By analogy, the possibility that disproportionately high levels of occupational chromium exposure contribute to a race-specific increase in risk of non-Hodgkin’s lymphoma among African Americans would appear to merit further investigation.

Wood Dust as a Race-Specific Risk Factor for Hodgkin’s Disease and Soft-tissue Sarcoma
Wood dust, like chromium, is well established as a human carcinogen and is strongly associated with respiratory cancer.¹⁹ Wood dust and woodworking occupations also are implicated in Hodgkin’s disease^19,20 and soft-tissue sarcoma.^20–22

It is unclear why wood dust might increase the risks of Hodgkin’s disease and soft-tissue sarcoma among African American men but not White men. However, because African Americans are disproportionately exposed to dusty occupational conditions in general,⁴ racial differences in wood dust exposure levels may be a contributing factor. The small numbers of African American men exposed to wood dust precluded assessment of interaction effects. However, effect modification due to race-specific genetic polymorphisms and lifestyle factors (e.g., smoking) may be important.²³

Pesticide Exposure as a Race-Specific Risk Factor for Soft-tissue Sarcoma
Although many studies have found that occupational pesticide exposure is associated with an increased risk of soft-tissue sarcoma, other studies have failed to detect an association.²⁴ One possible explanation for the inconsistent findings is that effect modification due to racial differences in risk has been overlooked. In previous studies specifically investigating race-specific associations, it has been observed that US minority populations exposed to pesticides have a disproportionately increased risk of cancer.²⁵

This premise is supported by our finding of a nearly threefold increase in risk of soft-tissue sarcoma among African American men exposed to pesticides, compared with a slightly decreased risk among White men. Although the association did not reach significance, this may have been a result of limited study power. Future studies designed to investigate race-specific dose–response associations for pesticide exposure in relation to soft-tissue sarcoma risk may prove fruitful.

Study Strengths
Our study has several unique strengths. First, population-based cancer registries were used to identify a comparatively large number of African American men with non-Hodgkin’s lymphoma, Hodgkin’s disease, or soft-tissue sarcoma who provided detailed information on occupational exposures. Previous studies of race-specific occupational risk factors for cancer among African American men have been limited almost exclusively to analyses of death certificate data, or data from small occupational cohorts that are not generalizable to the rest of the population. Second, random-digit telephone dialing was used to identify population-based control subjects. Third, participation rates were high for both case patients and control subjects. Fourth, pathology specimens were obtained for nearly all participating case patients, and diagnoses were confirmed by consensus after independent and blinded reviews by pathologists with expertise in diagnosing each cancer type.

Study Limitations
Several potential limitations also need to be considered. First, chance may explain the statistically significant associations for African American men. Specifically, confidence intervals around the odds ratios were wide due to small sample sizes, multiple comparisons were made, and race-specific hypotheses were not defined a priori because this was an exploratory study. Nonetheless, the associations were strong, lower bounds of the confidence intervals were well above unity, there was decreased statistical power to detect significant associations among African American men compared with White men due to the small size of the African American sample, and disproportionate exposure of minority populations to occupational carcinogens has been documented in previous studies.^2–4,17,18 Therefore, chance would appear to be an unlikely explanation for our findings. Plausibility for wood dust as a race-specific cancer risk factor among African American men is enhanced because significant increases in risk were found for both Hodgkin’s disease and soft-tissue sarcoma.

Second, recall bias could have influenced our findings if racial differences in recall of occupational exposures existed for case patients relative to control subjects. Third, selection bias could have arisen during recruitment of study participants. This possibility was reduced by using population-based cancer registries to identify case patients and by using random-digit dialing to select control subjects, although racial differences in study participation cannot be ruled out. Fourth, because control subjects included men with a history of cancers other than those of interest in the Selected Cancers Study, the estimates of risk could have been biased toward the null for 1 or both races if occupational risk factors were common to other cancer types. Fifth, our analysis was limited to dichotomous exposure information. Because dose–response analyses provide stronger support for causality, such studies are needed in the future.

Conclusions
To our knowledge, this is the first US population-based case–control study to look at occupation as a risk factor for cancer among living African American and White men. Across 13 occupational exposures investigated, significantly increased risks for non-Hodgkin’s lymphoma, Hodgkin’s disease, and soft-tissue sarcoma were evident only among African American men. Moreover, for each type of cancer, risks among African American men were greater than among White men for the majority of occupational exposures. This raises concern that preventable disparities in cancer risk may exist for African American men as a consequence of disproportionately increased exposure to carcinogens on the job.

Cancer incidence and mortality rates among African American men are higher than for any other US population group.¹ Given the paucity of information on underlying determinants, particularly in relation to cancer incidence, our findings underscore the need to identify occupational exposures associated with race-specific increases in cancer risk among African American men. This would allow for implementation of targeted industrial surveillance programs that can identify racial disparities in hazardous workplace exposures, thereby providing a framework for intervention to eliminate any disparities that are found.

	Acknowledgments

 
This work was supported in part by the Health Resource Services Administration (grant US2 MP99002) and the Agency for Healthcare Research and Quality (grant R24 HS11640).

The authors wish to thank William P. Haliburton, Dr E. Warren Lambert, and Dr Myron B. Towns for their thoughtful comments on this paper and the US Centers for Disease Control and Prevention and the Selected Cancers Cooperative Study Group for collecting the original data.

Human Participant Protection
The Selected Cancers Study was approved by the institutional review board at the Centers for Disease Control and Prevention.

	Footnotes

 
Contributors
N. C. Briggs was responsible for study conception, data analysis, and review of the literature. R. S. Levine was responsible for obtaining funding for the study. All authors were involved in the interpretation of results and writing of the article.

Peer Reviewed

Accepted for publication March 6, 2003.

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