Affiliations of authors: Department of Medical Epidemiology and Biostatistics (ETC, KES, H-OA) and Department of Oncology and Pathology (AP-M, BG), Karolinska Institutet, Stockholm, Sweden; Department of Epidemiology Research, Danish Epidemiology Science Center, Statens Serum Institut, Copenhagen, Denmark (HH); Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden (GR); Department of Oncology, Radiology and Clinical Immunology, University of Uppsala, Uppsala, Sweden (BG)
Correspondence to: Ellen T. Chang, ScD, Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Box 281, SE-171 77, Stockholm, Sweden (e-mail: ellen.chang{at}meb.ki.se).
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ABSTRACT |
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INTRODUCTION |
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To investigate risk factors for malignant lymphoma, we assembled a large population-based casecontrol study of NHL and HL. By linking our casecontrol study, the largest such study to date, to the Swedish Multi-Generation Register and the Swedish Cancer Register, we obtained high-quality data on confirmed cancer diagnoses in first-degree relatives of study participants. To our knowledge, no other population-based casecontrol study of lymphoma has used confirmed registry-based data on family history of malignancy. The unique combination of detailed, individualized exposure data and validated information on cancer in first-degree relatives enabled us to examine the associations between family history of cancer and risk of malignant lymphoma, including major NHL subtypes, and also to investigate whether associations of lymphoma risk with environmental exposures varied between individuals with and without a family history of hematopoietic malignancy.
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PATIENTS AND METHODS |
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The Scandinavian Lymphoma Etiology (SCALE) study is a population-based casecontrol study of newly diagnosed malignant lymphoma case patients and population control subjects in Denmark and Sweden [previously described (23)]. For this analysis, however, we included only Swedish residents. The study base included all persons between 18 and 74 years living in Sweden between October 1, 1999, and April 15, 2002. To be eligible, individuals were required to speak Swedish and to have no history of organ transplantation, human immunodeficiency virus infection, or prior hematopoietic malignancy.
Case patients were diagnosed with incident, morphologically verified NHL (International Classification of Diseases, Tenth Revision [ICD-10] codes C82C85, C88.0, C91.35, and C91.7), chronic lymphocytic leukemia (CLL; ICD-10 code C91.1), or HL (ICD-10 code C81) (24). HL case patients diagnosed in 1999 but before the start of enrollment on October 1 were also included but as prevalent case patients. Incident case patients were identified through a rapid case ascertainment network of contact physicians from all departments in which malignant lymphomas are diagnosed and treated and also through continuous collaboration with the Swedish regional cancer registries, with an estimated coverage close to 100% (25).
Control subjects were randomly sampled from the Swedish population by use of a continuously updated, computerized population registry. A subset of control subjects was sampled every 6 months during the study period and was frequency matched to the expected final distribution of NHL case patients on 10-year age intervals and sex.
Within the study base and time period, 85% of all Swedish case patients diagnosed with malignant lymphoma (n = 2347) and 75% of potential control subjects (n = 2001) consented to participate in the study. All participants granted informed consent before the interview. This study was approved by all regional ethics committees in Sweden.
Histopathologic Classification of Case Patients
All specimens from case patients were histopathologically evaluated by one of six senior hematopathologists or cytologists and classified according to the current World Health Organization specifications (26). Those specimens with indeterminate results (8%) were referred to the panel of hematopathologists for final evaluation. Overall, 2312 (98.5%) of the 2347 original tumor slides were reevaluated; for the 35 (1.5%) remaining case patients, the written results of the primary morphologic and immunohistochemical investigation were evaluated.
Registry-Based Data Collection
The Swedish Multi-Generation Register was created by Statistics Sweden in the early 1990s from national registration records and includes individuals (index persons) who were born in 1932 or later and who were still alive in 1961 or who were born in 1961 or later (27). The Register contains information on index persons and their parents, full or half-siblings, and children. Non-biologic (e.g., adoptive) relations are indicated. At present, the Multi-Generation Register includes more than 11 million individuals and approximately 3.2 million nuclear families.
The population-based Swedish Cancer Register, established in 1958, contains individual data on all newly diagnosed malignant tumors in Sweden (25). Tumors are required to be reported to the Cancer Register by both the diagnosing clinician and the responsible pathologist or cytologist, so that nearly 100% of diagnosed cancers are reported.
Using the individually unique national registration number of each study participant, we linked all participants in the SCALE study born in 1932 or later (1841 case patients [78%] and 1498 control subjects [75%]) to the Multi-Generation Register to identify their first-degree relatives. We then linked all individuals and their relatives, again by national registration number, to the Swedish Cancer Register to identify all cancer diagnoses in first-degree relatives of primary case patients and control subjects. Based on ICD-7 codes (28), we identified all hematopoietic cancers (ICD-7 codes 200209), including NHL (ICD-7 codes 200, 202, 204.0 [CLL], and 205), HL (ICD-7 code 201), multiple myeloma (ICD-7 code 203), and leukemia (ICD-7 codes 204207, excluding 204.0 and 205). Malignant skin neoplasms were identified by ICD-7 codes 190191.
We restricted our study population to individuals for whom both parents were identified within the Multi-Generation Register (n = 1506 case patients and 1229 control subjects, or 82% of both groups) to ensure that we had full information on cancer history in parents and siblings.
Exposure Assessment
All SCALE participants completed a comprehensive telephone interview evaluating known and suspected risk factors for lymphoma, including age, height, normal weight, family background, UV exposure, smoking history, past medication use, occupation, and sexual behavior. Body mass index was calculated as usual weight (in kilograms) divided by height (in meters) squared and categorized as normal weight (<25 kg/m2), overweight (25 to <30 kg/m2), or obese (30 kg/m2), in accordance with World Health Organization standards for adults (29). Family background included country of birth, age at immigration if born elsewhere, and country of mother's and father's birth. Measures of UV exposure, categorized according to the distribution among control subjects, included number of beach and/or sun vacations abroad (0, 15, 620, or
21 total vacations), frequency of sunbathing 510 years ago or at age 20 years (0,
1, 23, or
4 times per week), frequency of sunburns 510 years ago, at age 20 years, or before age 15 years (0, <1, 1, or
2 times per year), and frequency of solarium visits (0, <10, 1049, or
50 times). Smoking was classified as never, former, or current smoking of any cigarettes daily for at least 1 year. Medication use evaluated included total frequency of antibiotic use during adulthood (0, 12, 35, 610, 1120, 2130, 3140, or
41 courses of treatment) and use of immunosuppressive drugs (ever/never use of azathioprine, cyclosporine, methotrexate, cyclophosphamide, or chlorambucil) for conditions other than lymphoma at least 2 years prior to the interview. Occupational data included history of working at a paper factory or sawmill, regular occupational exposure to organic solvents for at least 1 year, and occupational exposure to pesticides at least twice a year for 2 years or more. Sexual behavior included history of heterosexual and/or homosexual intercourse and sexually transmitted disease.
After completing the telephone interview, residents of seven Swedish counties (about half of the country's population) were asked to complete a semiquantitative food-frequency questionnaire. Details of the questionnaire, including its contents and validity, have been described elsewhere (30,31). Individuals were asked how often, on average, they had consumed 137 food and drink items 2 years before the interview. Intake of all food groups and items was converted into number of servings per day and then categorized into tertiles by the distribution in the control population. Alcohol intake overall or from beer, wine, or liquor was converted into grams of ethanol consumed per day (31) and similarly categorized into tertiles by the distribution in the control group, excluding former drinkers. Among eligible participants who were asked to complete the food-frequency questionnaire, 613 (89%) case patients and 480 (85%) control subjects did so. After exclusion of those who were born before 1932, had at least one unidentified parent, and/or left more than half of the food-frequency questionnaire blank, a total of 442 case patients (374 NHL case patients) and 384 control subjects had information on dietary intake. These participants were included in analyses of the association between diet and risk of NHL, stratified by family history of hematopoietic malignancy.
Statistical Analysis
We used unconditional logistic regression to estimate the relative risks, approximated by odds ratios (ORs) and corresponding 95% confidence intervals (CIs) for associations between family history of malignancy and risk of overall NHL, NHL subtypes, and HL. All models were adjusted for 5-year age group, sex, and number of full siblings in the family (none, 1, 2, or 3). Birthplaces of the subject (Sweden or other) and of his/her parents (both born in Sweden or not) were also considered as possible confounders. Tests for linear trend were conducted with the exposure coded as an ordinal variable, with each level defined by the median value within each category. Estimates were stratified by age (<60 years or
60 years for NHL; <45 or
45 years for HL) or sex; heterogeneity of the stratified associations was evaluated by using a likelihood ratio test for the statistical significance of an interaction term between family history of cancer and either age or sex. All statistical tests were two-sided. Analyses were performed with SAS System software, release 8.2 (SAS Institute Inc., Cary, NC, 19992001).
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RESULTS |
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We performed a secondary analysis limited to participants who were born in Sweden that included 1468 case patients and 1197 control subjects (97% of both groups), because Multi-Generation Register data are incomplete for immigrants. There were no substantial changes in the estimates of association among Swedish-born participants only (data not shown). In another analysis, we restricted the population to those born in 1948 or later, that is, 641 case patients (43%) and 575 control subjects (47%), based on the assumption that their parents would have been born in 1908 or later and would thus have had a diagnosis of cancer after age 50 years recorded in the Cancer Register beginning in 1958. Again, although estimates were less stable due to a smaller sample size, there were no differences in the overall associations between family history of total or hematopoietic malignancy and risk of NHL (data not shown).
To examine whether associations between family history of total or hematopoietic cancer and risk of NHL varied by age or sex, we stratified analyses by age (individuals younger than 60 years old and those 60 years or older) or by sex. There was no statistically significant heterogeneity in the association between family history of any, hematopoietic, or non-hematopoietic cancer and risk of NHL between age groups or between sexes (data not shown), with one exception: the relative risk of NHL associated with having a father with a history of hematopoietic cancer was increased among individuals younger than 60 years of age (OR = 3.0, 95% CI = 1.4 to 6.1) but not among those aged 60 years or older (OR = 0.8, 95% CI = 0.4 to 1.7) (P for test of heterogeneity = .02).
To examine whether risk associations with family history varied by the type of hematopoietic malignancy in family members, we divided all such hematopoietic malignancies into NHLs (including CLL), CLL, HL, multiple myeloma, and leukemias (Table 3). Although numbers were small, it appeared that a family history of NHL was associated with an increased risk of all NHL subtypes and of HL. Similarly, a family history of CLL, in particular, was associated with a statistically significantly elevated risk of overall NHL and especially of CLL and HL. HL was too rare among family members for reliable relative risks to be estimated, although having a family history of HL was statistically non-significantly associated with a threefold-higher risk of HL. Neither a family history of multiple myeloma nor a family history of leukemia was statistically significantly associated with increased risk of NHL, HL, or most NHL subtypes, although relative risk estimates were unstable because multiple myeloma and leukemia were uncommon in family members. However, the risk of follicular lymphoma was increased by more than threefold among those with familial multiple myeloma (OR = 3.6, 95% CI = 1.5 to 8.7).
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DISCUSSION |
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We also found a stronger association of NHL risk with sibling rather than with parental history of hematopoietic malignancy. This observation suggests that a shared environment in childhood and adolescence may contribute to NHL risk, beyond the increased risk conferred by a shared genetic background. In addition, there was an apparently stronger association of paternal, than of maternal, history of hematopoietic malignancy with risk of several lymphoma subtypes and vice versa for risk of CLL. This difference could be explained by sex-linked susceptibility genes. For example, a susceptibility gene on the Y chromosome would be transmitted only from father to son. However, there was no heterogeneity of associations with paternal or maternal history of hematopoietic malignancy between males and females in our study. Alternatively, these differences could be explained by genomic imprinting, by which the expression, and therefore phenotype, of a susceptibility gene in the offspring depends on whether it was inherited from the father or the mother (40). Both of these phenomena could help to explain the approximately 2-to-1 male-female ratio in NHL incidence that is consistently observed worldwide (41). The association with paternal history of malignancy could also arise if risk factors in the offspring's environment, including exposures in childhood and/or adulthood, are more strongly influenced by fathers than by mothers. Finally, the differences in strength of association could be due to chance. In fact, any of the associations that we observed, most of which were modest, could be explained by chance, although the consistency across studies of the positive association between familial hematopoietic cancer and risk of lymphoma argues for a true association.
Likewise, we observed a heterogeneity of the association with paternal history of hematopoietic malignancy between older and younger individuals. This difference could be explained either by chance or by under-ascertainment of cancer in fathers of older individuals. That is, a positive association between paternal hematopoietic malignancy and risk of lymphoma in older persons could have been obscured if their fathers' cancer diagnoses occurred before 1958 and, therefore, were not registered. It is also possible that offspring of fathers with a history of hematopoietic cancer tend to develop malignant lymphoma at an earlier age than do offspring of fathers with no such history, leading to a positive association with paternal hematopoietic cancer only in the younger age group. Such a phenomenon, known as anticipation, has been hypothesized to occur in both familial NHL and HL (42,43).
The estimated twofold increase in risk of NHL among first-degree relatives of individuals with hematopoietic malignancy is similar to that reported in other studies (615). However, the magnitude of increased HL risk in those with a family history was also twofold in our study, whereas the estimated relative risk has generally been higher in other studies (7,11,1620). This discrepancy could be due to the low numbers of HL case patients in our study, especially those with a family history of hematopoietic malignancy, which limited our ability to estimate the relative risk precisely. The association of HL risk with a family history of NHL or CLL has been reported previously (20), whereas the association of follicular lymphoma risk with a family history of multiple myeloma has not. One other study corroborates our finding of increased risks of overall NHL, diffuse large B-cell lymphoma, and follicular lymphoma among individuals with familial NHL, as well as an increased risk of CLL among those with a family history of CLL (15).
Contrary to prior reports, in this large study, we found no evidence that associations with a range of environmental risk factors vary between familial and nonfamilial NHL. Our results indicate that body mass index, cigarette smoking, occupational contaminants, homosexual activity, and alcohol intake play no role in either type of NHL and that the roles of UV exposure, medication use, and diet are the same in both familial and nonfamilial NHL. These findings suggest that putative susceptibility genes do not interact with these exposures in the pathogenesis of NHL. Previous studies that detected statistically significant heterogeneity in risk associations between NHL case patients with and without a family history of hematopoietic malignancy relied on self-reported data of familial cancer (12,21,22). It could be that individuals who reported a family history of hematopoietic cancer were also more or less likely to report certain other risk factors. If, as expected, more case patients than control subjects reported a family history of hematopoietic malignancy and if those reporting such a history had a greater tendency to recall harmful exposures, this tendency could lead to spurious positive associations with risk of familial, but not nonfamilial, NHL.
Although our study was relatively large, there were only 166 diagnoses of hematopoietic malignancy among relatives of our study participants, and fewer than one-third of these familial diagnoses were among control subjects. The low prevalence of familial hematopoietic cancer limited the precision of our relative risk estimates, especially for NHL subtypes and HL, and for associations with family history of NHL, HL, multiple myeloma, and leukemia. Sample size restrictions also prevented us, for example, from examining whether family history of a particular NHL subtype was specifically associated with an increased risk of the same subtype.
One factor that reduced our study sample size was the restriction of the analysis to individuals with both parents who could be identified in the Multi-Generation Register, which enabled us to identify all siblings and then all parent and sibling cancer diagnoses. This restriction should not have introduced any bias to our analysis, because an equal proportion of case patients and control subjects had identifiable parents. Likewise, an equal proportion of case patients and control subjects were born in Sweden, making it unlikely that differences in immigration influenced our results; indeed, there were no changes in our findings when we restricted the analysis to individuals born in Sweden. Although the percentages of case patients and control subjects born after 1948 were different, with a higher percentage of case patients being born earlier, our overall results also remained the same when we restricted the analysis to persons born after 1948. Thus, the positive association between parental history of hematopoietic malignancy and risk of lymphoma is probably not due to more complete recording of diagnoses among the parents of case patients after the Swedish Cancer Registry was established in 1958. If anything, the case patientswho were on average older than the control subjectsshould have had older parents, whose diagnoses would be less likely to be registered, which would bias the association downward toward the null.
Because we used validated, registry-based data on family history of cancer, our results were not vulnerable to the problem of recall bias that can invalidate casecontrol studies of self-reported family medical history. By combining confirmed family history data with detailed interview-based data, we were able to examine the association between family history of hematopoietic malignancy and risk of lymphoma in further depth than would be possible in a study using registry data alone. In summary, we substantiated the positive association between family history of hematopoietic cancer and risk of malignant lymphoma and estimated the increase in relative risk to be about twofold for both NHL and HL. Furthermore, we found no differences in the associations between certain environmental exposures and risk of familial versus nonfamilial NHL. The particular genes that account for the increased genetic risk of NHL, and any other environmental factors with which they may interact, remain to be identified.
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NOTES |
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Manuscript received March 29, 2005; revised July 18, 2005; accepted August 5, 2005.
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