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American Journal of Epidemiology Advance Access originally published online on January 4, 2007
American Journal of Epidemiology 2007 165(6):652-659; doi:10.1093/aje/kwk044
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American Journal of Epidemiology Copyright © 2007 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Cigarette Smoking, Familial Hematopoietic Cancer, Hair Dye Use, and Risk of t(14;18)-defined Subtypes of Non-Hodgkin's Lymphoma

Brian C.-H. Chiu1,2, Bhavana J. Dave3, Aaron Blair4, Susan M. Gapstur1,2, Joan S. Chmiel1,2, Angela J. Fought1, Shelia Hoar Zahm4 and Dennis D. Weisenburger5

1 Department of Preventive Medicine, Northwestern University Medical School, Chicago, IL
2 The Robert H. Lurie Comprehensive Cancer Center of Northwestern University, Chicago, IL
3 Munroe Meyer Institute for Genetics and Rehabilitation, University of Nebraska Medical Center, Omaha, NE
4 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD
5 Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE

Reprint requests to Dr. Brian C.-H. Chiu, Department of Preventive Medicine, Feinberg School of Medicine, Northwestern University, 680 North Lake Shore Drive, Suite 1102, Chicago, IL 60611-4402 (e-mail: bchiu{at}northwestern.edu).

Received for publication March 27, 2006. Accepted for publication July 28, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Some evidence suggests that smoking, a family history of hematopoietic cancer, and use of hair dyes are associated with t(14;18)-defined subsets of non-Hodgkin's lymphoma (NHL) in men. To further evaluate these associations and to expand them to women, the authors determined t(14;18)(q32;q21) status by fluorescence in situ hybridization in 172 of 175 tumor blocks from a population-based case-control study conducted in Nebraska during 1983–1986. Exposures in 65 t(14;18)-positive cases and 107 t(14;18)-negative cases were compared with those among 1,432 controls. Odds ratios and 95% confidence intervals were calculated using polytomous logistic regression. Among men, smoking was not associated with risk of t(14;18)-positive or -negative NHL. Among women who had ever smoked cigarettes, there was an association with risk of t(14;18)-negative NHL (odds ratio (OR) = 1.9, 95% confidence interval (CI): 1.1, 3.3) but not t(14;18)-positive NHL (p-difference = 0.01). The risks for t(14;18)-negative NHL among women increased with longer duration (>30 years: OR = 2.1, 95% CI: 1.1, 4.1) and early initiation (age ≤20 years: OR = 2.2, 95% CI: 1.1, 4.4) of smoking. A family history of hematopoietic cancer was associated with a twofold higher risk for both t(14;18)-defined NHL subtypes among men and women. Hair dye use was not associated with either subtype. These findings should be interpreted cautiously because of the small sample.

chromosome aberrations; hair dyes; hematologic neoplasms; lymphoma, non-Hodgkin; risk factors; smoking

Abbreviations: CI, confidence interval; FISH, fluorescence in situ hybridization; NHL, non-Hodgkin's lymphoma; OR, odds ratio


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Age patterns and secular trends in the incidence of non-Hodgkin's lymphoma (NHL) vary across different NHL subtypes (1). These subtype-specific NHL incidence rates suggest different etiologies (2). Although the new World Health Organization classification of NHL might be useful for etiologic research (3), genomic studies suggest that many World Health Organization-defined subtypes are heterogeneous at the molecular level (4, 5). Thus, molecular classification of NHL may better define homogeneous disease entities.

Approximately 30 percent of NHL in North America is follicular lymphoma and 40 percent is diffuse large B-cell lymphoma (3). The chromosomal translocation t(14;18)(q32;q21) occurs in approximately 70–90 percent of follicular lymphomas and 20–30 percent of diffuse large B-cell lymphomas (3, 6, 7), and t(14;18)-positive NHL might represent a homogeneous group within these two subtypes. Defining subtypes of NHL according to the t(14;18) translocation may increase the etiologic specificity relative to all NHLs combined. This hypothesis is supported by previous studies (8, 9) which showed a higher risk of NHL associated with pesticide exposure that was limited to t(14;18)-positive NHL cases.

Schroeder et al. (10) further applied this approach in evaluating associations of cigarette smoking, family history of cancer, and hair dye use with NHL risk, because there is evidence that these risk factors are specifically associated with follicular lymphoma (11–19) and diffuse large B-cell lymphoma (14, 15, 17, 20, 21). These researchers found a nonsignificant 70 percent higher risk of t(14;18)-positive NHL, but not t(14;18)-negative NHL, among cigarette smokers (10). Conversely, a family history of hematopoietic cancer was associated with t(14;18)-negative NHL but not t(14;18)-positive NHL, and hair dye use was associated with a twofold higher risk of both t(14;18)-positive NHL and t(14;18)-negative NHL. In that study (10), only men were included and t(14;18) status was assessed by polymerase chain reaction, a process which might miss t(14;18) breakpoints (22).

To confirm the associations reported by Schroeder et al. (10) and to expand them to women, we evaluated the t(14;18) translocation by interphase fluorescence in situ hybridization (FISH) in a population-based case-control study conducted in Nebraska. FISH is considered the "gold standard" test for detecting specific chromosomal abnormalities.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study population
The study population and methods have been reported in detail elsewhere (23, 24). Briefly, cases of NHL, Hodgkin's disease, multiple myeloma, and chronic lymphocytic leukemia diagnosed between 1983 and 1986 among White men and women aged 21 years or older who resided in one of 66 counties in eastern Nebraska were identified through the Nebraska Lymphoma Registry and Tissue Bank and area hospitals. The current study included only cases of NHL. A total of 426 histologically confirmed cases were identified.

Controls without hematopoietic cancer were randomly selected from the same 66-county area through 3:1 frequency matching by sex, vital status, and age (5-year age groups) to the combined age distribution of the four cancer case types. Controls for living cases under 65 years of age were randomly selected by two-stage random digit dialing as described by Waksberg (25). For living cases aged 65 years or older, controls were selected at random from the Medicare records of the Health Care Financing Administration. Controls for deceased cases were selected from the Nebraska state mortality files using the additional matching factor of year of death. A total of 1,655 controls were identified.

Exposure assessment
Telephone interviews were conducted directly with the subjects or their next of kin (if the subject was deceased or incapacitated). Interviews were obtained for 385 cases (201 males, 184 females) and 1,432 controls (725 males, 707 females), yielding response rates of 90 percent and 87 percent, respectively. Proxy interviews were obtained in 40.5 percent of cases and 43.6 percent of controls. The questionnaire collected information on demographic factors, smoking history, use of hair dye, occupational history, medical history, history of cancer among first-degree relatives, and the frequency of consumption of 31 food items.

Ascertainment of the t(14;18)(q32;q21) translocation by FISH analysis
Paraffin-embedded tumor blocks were obtained through the statewide Nebraska Lymphoma Registry and Tissue Bank for 175 of the 385 NHL cases (45.5 percent) in the parent case-control study. Other specimens were not available because of the length of time since case diagnosis, which exceeded the average time most hospitals and laboratories keep their blocks (approximately 10–15 years). We evaluated potential selection bias by comparing the distributions of exposures of interest between NHL cases with available tumor blocks and those whose tumor blocks could not be retrieved. We found that selection bias was unlikely because the availability of tumor blocks did not differ by exposures of interest, and it is unlikely that t(14;18) status is related to tumor block availability.

The method used for FISH analysis in this study has been described in detail elsewhere (8). Tissue microarrays were prepared from archival paraffin-embedded tissue. Four representative 0.6-mm cores were obtained from each case and inserted in a grid pattern into a recipient paraffin block using a tissue arrayer (Beecher Instruments, Silver Spring, Maryland). FISH studies were performed on 4-µm tissue microarray sections. We used the commercially available LSI IGH/BCL2 dual-color, dual-fusion probe to define the t(14;18) translocation and the centromeric enumeration probe of chromosome 18 to define the number of chromosome 18's present in the cell (Abbott-Vysis, Inc., Downers Grove, Illinois). The tissue sections were pretreated using VP2000 (Abbott-Vysis, Inc.), following the manufacturer's standard protocol for paraffin-embedded tissue sections, with minor modifications. The probe mixture was placed on the tissue sections, cover-slipped, and sealed. Co-denaturation of probes and target DNA at 75°C for 5 minutes was followed by overnight hybridization at 37°C using an automated hybridization chamber (HYBrite; Abbott-Vysis, Inc.). The slides were then washed with standard posthybridization washes, and the nuclei were counterstained with 4,6-diamidino-2-phenylindole. Analysis was performed on an Olympus BX51 microscope equipped with appropriate filters, and images were captured with CytoVision image capture software (Applied Imaging, Santa Clara, California).

FISH probes are approved by the US Food and Drug Administration as analyte-specific reagents. FISH analyses were performed in a blinded manner, with the unique identifiers being unknown to the laboratory personal involved in the analyses. Blind replicates of approximately 5 percent of the specimens were analyzed for quality control. In addition, classical cytogenetic analysis was performed in 5 percent of the samples. The t(14;18) status determined by FISH was validated by means of these two quality control measures. The upper limit for false-positive results for the t(14;18) probes was 5 percent. A minimum of 100 interphase nuclei were independently examined by two people, a cytotechnologist and an expert cytogeneticist (B. D.), for the presence of the t(14;18) translocation and the number of chromosome 18's. Agreement between the two readers was 100 percent.

Statistical analysis
Smoking status was categorized as never smoker, former smoker, or current smoker. Never smokers were defined as subjects who had never used any tobacco product for 6 months or longer. Current smokers were defined as those who had smoked cigarettes for a continuous period of 6 months or longer and were also smoking within 2 years preceding the telephone interview. Former smokers were defined as those who had quit smoking cigarettes 2 or more years prior to the interview. Total lifetime cigarette smoking was estimated in pack-years and was calculated by dividing the average number of cigarettes smoked per day by 20 and then multiplying by the number of years smoked. Age at initiation of smoking, duration, amount smoked per day, and pack-years of smoking were classified as never, less than or equal to the median, and greater than the median.

The presence of hematopoietic cancer, including leukemia, myeloma, or lymphoma, in at least one first-degree relative was considered a positive family history of hematopoietic cancer. We used hematopoietic cancer rather than NHL alone as the definition of a positive family history because: 1) hematopoietic stem cells are the common cell of origin for a variety of hematopoietic cancers, including NHL; 2) hematopoietic cancers share some common risk factors; and 3) respondents may not be able to distinguish between the various types of hematopoietic cancer when they report a family history of NHL or other related cancers.

Information collected on hair dye use included the ages of first and last use of products that gradually change hair color, as well as use of nonpermanent, semipermanent (defined as products that rinse out after a few shampoos), and permanent (defined as products that last until the hair grows out) hair-coloring products.

Odds ratios and 95 percent confidence intervals for subtypes defined by t(14;18) status were derived from multivariate polytomous logistic regression, where the dependent variable was treated as a three-level variable (i.e., t(14;18)-positive NHL, t(14;18)-negative NHL, and controls), and the logit estimator always compared t(14;18)-defined NHL subtypes with controls. This allowed comparison of odds ratios for t(14;18)-positive NHL with odds ratios for t(14;18)-negative NHL. Risk estimates for NHL subtypes defined by the new World Health Organization classification (3) were derived from multivariate logistic regression. We report point estimates only for comparisons where there were at least three exposed cases in the t(14;18)-defined subtype of NHL. The reported p values are two-sided. Indicator variables for age (21–44, 45–64, 65–74, and ≥75 years), type of respondent (direct or proxy interview), and sex were included in the final model because controls were frequency-matched by these variables to cases in the parent case-control study. Other potential confounders were considered based on prior knowledge of risk factors for NHL, as well as change-in-estimate criteria (26). Information on human immunodeficiency virus infection was not available. However, it is unlikely that human immunodeficiency virus infection was a significant confounder or risk factor for NHL in the present study, given the time period (i.e., the early to mid-1980s), the location (i.e., a Midwestern state where human immunodeficiency virus infection and acquired immunodeficiency syndrome were not common), and the age of the participants (i.e., 88 percent of the cases and 87 percent of the controls were older than 50 years of age). Analyses were conducted using PROC CATMOD in the SAS 9.1 statistical software package (SAS Institute, Inc., Cary, North Carolina).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Of the 175 cases with tumor blocks available for the current study, 65 (37.1 percent) were positive for the t(14;18) translocation, 107 (61.1 percent) were negative for the t(14;18) translocation, and in three cases t(14;18) status could not be determined (table 1). Compared with controls, t(14;18)-negative cases were more likely to be female (p = 0.04). There were no significant differences regarding age (data not shown), education, and respondent status between t(14;18)-positive NHL, t(14;18)-negative NHL, and controls. Consistent with previous reports (3, 7), the t(14;18) translocation occurred in 67 percent of follicular lymphomas and 32 percent of diffuse large B-cell lymphomas.


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  		TABLE 1. Characteristics of controls and non-Hodgkin's lymphoma cases by t(14;18) chromosomal translocation status, Nebraska, 1983–1986

 
Among men, there was a weak inverse association between smoking and the risks of both t(14;18)-positive NHL and t(14;18)-negative NHL (table 2). However, none of the point estimates were statistically significant, and there was no clear dose-response effect. Among women, compared with those who had never used any tobacco products, women who had ever smoked cigarettes had a significantly higher risk of t(14;18)-negative NHL (odds ratio (OR) = 1.9, 95 percent confidence interval (CI): 1.1, 3.3) but a statistically nonsignificant deficit of t(14;18)-positive NHL (p-difference = 0.01). There were positive dose-response associations of cigarette smoking with risk of t(14;18)-negative NHL based on current smoking status, age at which the subject had first started smoking, and duration of smoking. None of these smoking factors was associated with t(14;18)-positive NHL, although numbers were low. Analysis of histologic subtypes defined by the new World Health Organization classification (3) showed no association of cigarette smoking with follicular lymphoma or diffuse large B-cell lymphoma in either sex (data not shown).


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  		TABLE 2. Associations between tobacco use and risk of non-Hodgkin's lymphoma according to t(14;18) chromosomal translocation status, by sex, Nebraska, 1983–1986

 
In both men and women, a positive family history of hematopoietic cancer among first-degree relatives was nonsignificantly associated with an approximately twofold higher risk of both t(14;18)-positive NHL and t(14;18)-negative NHL, compared with subjects with no family history of cancer (table 3). The point estimates did not materially change in analyses combining men and women (for t(14;18)-positive NHL, OR = 2.1, 95 percent CI: 0.8, 5.2; for t(14;18)-negative NHL, OR = 1.9, 95 percent CI: 1.0, 3.8). Analysis by histologic subtype showed that a family history of hematopoietic cancer was associated with a higher risk of follicular lymphoma (for men, OR = 3.5, 95 percent CI: 0.9, 13.3; for women, OR = 3.9, 95 percent CI: 1.2, 12.8) but not diffuse large B-cell lymphoma (data not shown). There were too few cases for meaningful analysis of hair dye use among men. Among women, hair dye use was not associated with either t(14;18)-positive NHL or t(14;18)-negative NHL. However, the use of permanent dyes was associated with a 40 percent higher risk of t(14;18)-negative NHL. Hair dye use was not associated with follicular lymphoma or diffuse large B-cell lymphoma in either sex (data not shown).


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  		TABLE 3. Associations between family history of hematopoietic cancer, hair dye use, and risk of non-Hodgkin's lymphoma according to t(14;18) chromosomal translocation status, by sex, Nebraska, 1983–1986

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
We found that cigarette smoking was associated with a higher risk of t(14;18)-negative NHL among women, and the risk increased with early initiation of smoking and the duration of smoking. However, there was no clear association between smoking and t(14;18)-positive or t(14;18)-negative NHL in men. A family history of hematopoietic cancer was associated with twofold higher risks of t(14;18)-positive and t(14;18)-negative NHL in both men and women. We found no association between hair dye use and t(14;18)-defined subtypes of NHL, but the statistical power of the analysis was limited.

Epidemiologic studies have linked cigarette smoking with increased risks of follicular lymphoma (12, 13, 27) and diffuse large B-cell lymphoma (20). In a recent pooled analysis of 6,594 NHL cases and 8,892 controls, cigarette smoking was significantly associated with a higher risk of follicular lymphoma (11). Therefore, we might expect to find a positive association between cigarette smoking and t(14;18)-positive NHL, because the translocation occurs in 70–90 percent of follicular lymphomas and 20–30 percent of diffuse large B-cell lymphomas (3, 7). In contrast, we found that smoking was associated with a higher risk of t(14;18)-negative NHL but not t(14;18)-positive NHL in women, and there was no clear association between smoking and t(14;18)-positive or t(14;18)-negative NHL in men. In the only other population-based study that evaluated associations of smoking with NHL in men by t(14;18) status (10), smoking was associated with a nonsignificant 70 percent higher risk of t(14;18)-positive NHL, but the odds ratios decreased as smoking increased. Explanations for the differences between our study and the other study of men (10) and for the results for men and women in this report are unclear. Because the samples in these studies were not large, the findings could simply have been due to chance variation. However, it is possible that smoking-associated risk varies according to chromosomal abnormalities. A study of acute myeloid leukemia found that smoking was positively associated with the t(8;21)(q22;q22) subgroup but inversely associated with the t(15;17)(q22;q12) subgroup (28). It remains possible that smoking may be associated with chromosomal abnormalities other than the t(14;18) translocation which might be distributed differently among men and women. Unfortunately, we did not have data with which to assess this possibility.

A family history of NHL or other hematopoietic cancer in close relatives has consistently been associated with a two- to threefold higher risk of NHL overall (14–17) and of NHL subtypes, including follicular lymphoma (14–17), diffuse large B-cell lymphoma (14, 15, 17, 21), and chronic lymphocytic leukemia (15, 17). In our data, a family history of hematopoietic cancer was associated with a nonsignificant twofold higher risk of NHL among men and women for both the t(14;18)-positive and t(14;18)-negative subtypes, suggesting that defining NHL by t(14;18) status does not improve the specificity of this risk factor. The only other study that evaluated the familial cancer-NHL association according to t(14;18) status found that a family history of hematopoietic cancer among first-degree relatives was associated with t(14;18)-negative NHL (OR = 2.4, 95 percent CI: 1.4, 3.9) but not t(14;18)-positive NHL (OR = 1.3, 95 percent CI: 0.5, 3.3) (10). Specific translocations have not been reported as a feature of familial lymphoma (29). It is possible that a shared environmental exposure among family members could increase the likelihood of susceptibility to specific chromosomal abnormalities and risk of NHL.

We found little evidence for an association between ever using hair dye and risk of either t(14;18)-positive NHL or t(14;18)-negative NHL. Schroeder et al. (10) reported that hair dye use was associated with both t(14;18)-positive NHL (OR = 1.8, 95 percent CI: 0.9, 3.7) and t(14;18)-negative NHL (OR = 2.1, 95 percent CI: 1.3, 3.4) among men. Some chemical components of hair dyes have been reported to induce chromosome aberrations in animal cell lines (30). However, a study of 10 volunteers with dyed hair and 10 controls found no difference in the incidence of chromosomal aberrations between the two groups (31).

In the current study, the odds ratios for t(14;18)-positive and t(14;18)-negative NHL associated with cigarette smoking, family history of hematopoietic cancer, and hair dye use did not differ significantly, except for smoking in women. This contrasts with the findings of other studies (8, 9) in which pesticide exposure was significantly and consistently associated with t(14;18)-positive NHL but not t(14;18)-negative NHL. This observation suggests that defining subtypes of NHL according to t(14;18) status might have limited use for etiologic research if an exposure is not genotoxic or does not involve the development of NHL through a pathway involving the t(14;18) translocation. However, results of analyses by histologic subtype are not entirely consistent with those observed using subsets defined by t(14;18) status, suggesting that defining subsets of NHL by t(14;18) status might still be useful for etiologic research. It is possible that, because our sample was small, grouping NHL cases into two subtypes by t(14;18) status limited our power to observe meaningful associations.

Our findings should be interpreted cautiously, because the low numbers limited our ability to fully explore the hypothesized associations, and risk estimates might have been imprecise. In addition, information on exposures was obtained from proxies for about 40 percent of the cases and controls. When analyses were limited to direct respondents, the odds ratios were smaller than those obtained including proxies; however, the directions of association were consistent regardless of the inclusion or exclusion of proxy respondents. There was also no significant difference regarding respondent status between t(14;18)-positive NHL, t(14;18)-negative NHL, and controls. These observations suggest that information bias, should it exist, would not have created spurious associations. Finally, tumor blocks were available for only 45.5 percent of the cases, although there is little evidence for selection bias or survival bias.

One of the major strengths of this study was our use of FISH, which is highly sensitive and specific and is considered the gold standard for detecting specific chromosomal abnormalities in paraffin-embedded tissue. Other strengths were the inclusion of only newly diagnosed, histologically confirmed cases of NHL that occurred in a defined time period (1983–1986) and randomly selected controls who were representative of the population at large.

In summary, these data suggest that smoking is associated with a higher risk of t(14;18)-negative NHL among women and that a family history of hematopoietic cancer is associated with a higher risk of both t(14;18)-positive NHL and t(14;18)-negative NHL among both men and women. Our finding of this positive association with risk of t(14;18)-negative NHL requires confirmation. Our sample was small, and the risk estimates might have been imprecise. These results suggest that future epidemiologic studies should investigate exposures that are likely to be genotoxic, as well as other chromosomal abnormalities in addition to the t(14;18) translocation.


   ACKNOWLEDGMENTS
 
This research was supported by grant CA94770 from the National Cancer Institute and, in part, by the Intramural Research Program of the National Institutes of Health (Division of Cancer Epidemiology and Genetics of the National Cancer Institute). The authors thank Martin Bast of the Nebraska Lymphoma Registry and Tissue Bank for coordinating the retrieval of the tumor blocks and Smarti Jain for her help with the fluorescence in situ hybridization.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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The Utility of t(14;18) in Understanding Risk Factors for Non-Hodgkin Lymphoma
J Natl Cancer Inst Monographs, July 1, 2008; 2008(39): 69 - 73.
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