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Reproductive Factors and Risk of Intermediate- or High-Grade B-Cell Non-Hodgkin’s Lymphoma in Women

From the Keck School of Medicine of the University of Southern California, Los Angeles, CA 90033.

Address reprint requests to Leslie Bernstein, PhD, University of Southern California/Norris Comprehensive Cancer Center, 1975 Zonal Avenue, KAM 506, Los Angeles, CA 90033; email: lbern{at}hsc.usc.edu

	ABSTRACT

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PURPOSE: The incidence rates of non-Hodgkin’s lymphoma (NHL) unrelated to human immunodeficiency virus infection are lower for women than for men; yet, few factors have been identified that may account for this difference in risk. NHL is difficult to study epidemiologically because this disorder represents a group of malignancies that differ in terms of morphologic presentation, immunologic features, genetic characteristics, prognosis, and etiology.

PATIENTS AND METHODS: We conducted a population-based case-control study in women to determine whether reproductive factors or hormonal exposures might be related to the risk of high- or intermediate-grade B-cell NHL. We interviewed 177 female residents of Los Angeles County who were diagnosed with high- or intermediate-grade B-cell NHL between 1989 and 1992; each case patient was individually matched on age and race to a control subject who lived in her neighborhood.

RESULTS: Women who had used oral contraceptives had significantly lower risk of intermediate- or high-grade NHL (multivariate odds ratio [OR] = 0.47; 95% confidence interval [CI], 0.26 to 0.86) than women who had never used these compounds. Among parous women, those who had used lactation suppressants (which contain high levels of estrogen) had significantly lower risk of NHL (multivariate OR = 0.50; 95% CI, 0.29 to 0.85) than unexposed women. Postmenopausal women had a somewhat greater risk of NHL than premenopausal women, whereas those postmenopausal women who had used hormone replacement therapy (HRT) (primarily estrogen) had somewhat lower risk than those who had not used HRT.

CONCLUSION: Exogenous estrogens seem to have a protective effect on the risk of high- and intermediate-grade B-cell NHL. Although the mechanisms for such protection are not known, alterations in immune reactivity, cytokine expression, or B-cell modulation may play a role.

	INTRODUCTION

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THE INCIDENCE OF non-Hodgkin’s lymphoma (NHL) has been steadily increasing worldwide among both men and women over the past 50 years.¹ Although some of this increase is a result of infection with the human immunodeficiency virus (HIV)¹ or the use of immunosuppressive agents, such as azathioprine and cyclosporine,² few risk factors have emerged to explain the increasing incidence among immunocompetent individuals.

Worldwide, men are reported to have a higher incidence of NHL than women.³ The reasons for the lower NHL rates among females are not known, and few epidemiologic studies have examined factors that might explain this difference in risk. The information currently available suggests oral contraceptive use may lower risk,⁴ and estrogen replacement therapy may increase risk.⁵ Whether parity affects risk is unclear. Olsson et al⁶ found that late age at first full-term pregnancy was associated with increased risk of NHL, whereas Adami et al⁷ observed no such relationship, while also noting a weak, negative association with increasing parity. Tavani et al⁸ observed that for women less than 50 years old, those who reported one or more pregnancies were at an increased risk of NHL compared with nulliparous women. Although of interest, these data are conflicting, perhaps because NHL was considered as one entity with no attempt to look specifically at the various types of lymphoma under study.

We initiated a population-based case-control study of HIV-related and HIV-unrelated high- and intermediate-grade NHL in Los Angeles County to determine the relative impact of potential risk factors in these two groups. We obtained detailed reproductive and hormonal exposure histories from HIV-negative women in this study to determine whether such factors might provide a coherent explanation for the lower risk in women. The results presented below focus on these factors.

	PATIENTS AND METHODS

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As previously described in detail,⁹ newly diagnosed patients with NHL living in Los Angeles County who were between the ages of 18 and 75 at the time of diagnosis were identified by the Cancer Surveillance Program, the population-based cancer registry for Los Angeles County, using a rapid case-reporting mechanism. All case patients diagnosed between April 1989 and November 1992 who were English- or Spanish-speaking residents of Los Angeles County and were diagnosed with high- or intermediate-grade tumors (classified according to the Working Formulation¹⁰) were considered eligible for this study. This report is limited to information collected from female HIV seronegative participants in this study.

Interviews were completed with 203 female patients. We were unable to interview 134 female patients who had died, 14 who were too ill to be interviewed, 26 who were lost to follow-up, and 54 who refused to participate. Physicians denied permission to contact an additional 17 patients. Thus, 45% of the eligible female patients were actually interviewed for this study.

Two expert hematopathologists reviewed diagnostic biopsy materials for all potentially eligible case patients to allow for a uniform classification of disease and to restrict eligibility to those with confirmed diagnoses of high- or intermediate-grade B-cell NHL. Seven interviewed patients were determined to be ineligible for the study based on this pathologic review. The remaining 196 were confirmed to have high- or intermediate-grade B-cell lymphomas.

Although we had information on HIV status from patients or their physicians at the time of interview, we obtained a blood sample from each patient to confirm this status. HIV status was determined by enzyme-linked immunosorbent assay, with confirmatory Western blot, performed by standard methods. Of the 196 eligible female NHL patients interviewed, 193 were confirmed to be HIV seronegative. The remaining three patients were HIV positive and were not included in this report.

One female control subject was individually matched to each interviewed female HIV-negative NHL patient on the basis of date of birth (within 3 years), race/ethnicity (non-Hispanic white, Hispanic white, black, or Asian), language of interview (English or Spanish), and neighborhood of residence of the case at diagnosis. We selected control subjects by canvassing housing units in the neighborhood where the case patient lived at the time of diagnosis using a predefined walk pattern based on the geographic configuration of streets around the patient’s residence. We canvassed each housing unit until a woman who matched the case subject on the matching criteria was located and interviewed. Matching on neighborhood of residence provides matching of most cases and controls within one or two block groups and provides close matching on socioeconomic status. Personal interviews conducted with each case and control subject obtained information on the respondent’s lifetime history of medication usage, medical history (immunizations, chronic and infectious diseases, or other medical conditions), hospitalizations and special treatments, such as radiotherapy, blood transfusions, and anesthetic exposures, smoking and alcohol intake history, use of recreational drugs, family medical history, and occupational and household exposure to a series of substances. In addition, soon after we initiated the study, we added a section to the questionnaire that queried women about details of their reproductive histories including experiences during all pregnancies, age at last menstrual period, and the use of hormonal contraceptives and hormone replacement therapy (HRT). We had complete data on these factors for both cases and controls of 177 (of the 193) female case-control pairs.

This report focuses on reproductive and hormonal exposure factors reported by the female participants and examines the risk of high- and intermediate-grade B-cell NHL associated with pregnancy history (including parity, number of pregnancies, age at first full-term pregnancy, number of full-term pregnancies, history of induced abortion and miscarriage, treatment for nausea or vomiting during pregnancy, and use of hormones to induce labor), lactation history and use of lactation suppressants, oral contraceptive use, menopausal status, age at menopause, and use of HRT. For each NHL patient, exposure information was collected up to the date that was 12 months before the date of NHL diagnosis. The same reference date was used for a patient’s matched control. Age at menopause was recorded as the age at last menstrual period for women considered as postmenopausal. Because age at menopause is inversely related to the likelihood that a woman would be prescribed HRT, it is necessary to adjust for age at menopause in analyses evaluating the effects of use on cancer risk. To do this, it is preferable to consider women who began HRT before their last menstrual period or who had a hysterectomy without bilateral oophorectomy while still menstruating as having unknown age at menopause.¹¹ We conducted analyses with and without such women.

Before the interview, each participating subject provided her informed consent. Study procedures were approved by the University of Southern California Institutional Review Board in accordance with assurances approved by the United States Department of Health and Human Services.

Statistical Methods
We retained the individual pair matching in the statistical analyses of factors that were not dependent on parity status. Odds ratios (ORs) were estimated using conditional logistic regression methods.¹² Analyses of breast feeding, use of lactation suppressants, and hormones used to induce labor were restricted to parous women. The ORs for these analyses were estimated using unconditional logistic regression methods, adjusting for reference age. Unconditional logistic regression with adjustment for reference age was also used in the analysis of HRT that was restricted to women with known age at menopause. Ninety-five percent confidence intervals (CI) for the OR were estimated using the logarithm of the OR and its standard error. A single degree of freedom test was used to assess the significance of linear trend across categories of increasing exposure where relevant.

	RESULTS

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The average age of high- and intermediate-grade B-cell NHL patients at the time of diagnosis was 53.3 years (SD = 14.8); control subjects’ average age at reference date was 53.1 years (SD = 14.9). The majority of patients were white (including Hispanic) (n = 159, 90%), 12 (7%) were African-Americans, and six (3%) were Asian. The majority of participants were born in the United States (135 cases v 148 controls). The numbers of foreign-born cases and controls were comparable for most countries except that controls from Central America were underrepresented (11 cases v three controls). Cases and controls did not differ in terms of religious affiliation. We did find, however, that cases were less likely than controls to have a high school diploma (142 cases v 155 controls who graduated high school). Because of these differences, we adjusted for level of education (high school graduate v nongraduate) and place of birth (United States v elsewhere) in multivariate analyses to account for potential confounding effects of these factors on the risk of high- or intermediate-grade NHL. Specific aspects of pregnancy history were not associated with risk of high- or intermediate-grade B-cell NHL in this study, although most ORs were greater than 1.0 ( Table 1).

Among parous women, NHL risk was not associated with a history of taking hormones to induce labor, receiving treatment for nausea or vomiting during pregnancy (symptoms associated with higher first trimester estrogen levels¹³), or history of breast feeding ( Table 2). Parous women who had used lactation suppressants had a statistically significant, substantially reduced risk of NHL (multivariate OR = 0.50; 95% CI, 0.29 to 0.85). Thirty of the 35 case patients and 47 of 59 control subjects who had taken lactation suppressants had at least two full-term pregnancies, and 27 of the case patients and 38 of the control subjects had taken these medications for at least two of their full-term pregnancies (data not shown). All but one of these subjects had their first exposure to lactation suppressants before 1980.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Although pregnancy, with its associated increase in circulating estrogen levels, was not associated with NHL risk, use of oral contraceptives and use of lactation suppressants, two factors associated with increased estrogen exposure, seemed to be protective against high- and intermediate-grade B-cell NHL in the current study. Oral contraceptive use was associated with a 50% reduction in NHL risk. Although the trend in risk was statistically significant, we were unable to show that the risk estimates for women with at least 5 years of use differed statistically from that for women with less than 5 years of use. Those women who first began using oral contraceptives before 1970, when the concentration of estrogen in oral contraceptives was higher than in more recent formulations, seem to have gained somewhat greater protection against NHL; however, we had limited statistical power to demonstrate a significant difference in the estimated relative odds of NHL according to first use before and after 1970.

Women who used lactation suppressants also had a 50% lower risk of high- and intermediate-grade B-cell NHL. We did not collect information on type of lactation suppressant used. However, lactation suppressants generally in use before 1980 (quinestrol, diethylstilbestrol, and chlorotrianisene) contained high levels of long-acting estrogens to suppress lactation by inhibiting the production of prolactin. All but one subject who had used lactation suppressants had their first exposure before 1980, the year when the first major non–estrogen-containing product, bromocriptine (a dopamine agonist) was marketed for this purpose in the United States (Novartis-Sandoz Pharmaceuticals, personal communication, November 1998). Other factors associated with greater estrogen exposure, such as use of HRT and being premenopausal, were also associated with decreased NHL risk, although these results were not statistically significant.

It is possible that the relationship between hormonal factors and NHL risk in women may be mediated through the release of cytokines. Increased levels of interleukin 6 (IL-6), prostaglandin 17ß-oestradiol, and granulocyte-macrophage–colony-stimulating factor have been documented in marrow cultures of women who were within 5 years of natural menopause¹⁵ and may explain the increased bone loss seen in this setting. Of importance, however, is the fact that IL-6 has been shown to be a paracrine growth factor for intermediate- and high-grade NHL.^16-19 The documentation of lower secretion of IL-6 by marrow stroma from women receiving estrogen replacement therapy²⁰ suggests a potential biologic mechanism for the protective effect of estrogen replacement therapy and oral contraceptives on the development of intermediate- or high-grade NHL, as shown in the current study.

In addition, a recent study conducted by Medina et al²¹ showed that estrogen modulates the differentiation, proliferation, and survival of early B-cell precursors, with decreased B lineage precursors, and decreased proliferation of early B lineage cells in mouse models. As such, estrogen could potentially influence the pathogenesis or eventual development of lymphoma, thus providing additional biologic credence to our epidemiologic findings.

It is not known why exogenous hormones (oral contraceptives, lactation suppressants, and possibly HRT) seem to reduce the risk of NHL, whereas characteristics of pregnancy history, such as number of pregnancies, number of full-term pregnancies, and age at first full-term pregnancy, which are associated with exposure to high levels of endogenous estrogen and progesterone, do not. These latter findings are potentially important because they suggest that the immunologic changes that occur during pregnancy¹⁴ do not contribute to the risk of NHL. For example, it is possible that, during pregnancy, higher interleukin-10 levels, which are known to be a potent growth factor for high- and intermediate-grade NHL,²² may cause a transient increase in risk of lymphoma during gestation; however, interleukin-10 may also inhibit the synthesis of IL-6,²³ thus serving to diminish the potential for any relationship between pregnancy and development of NHL.

A relationship between immune function and reproductive hormones is well established^14,24-26 and may also serve to influence the development of malignant disease. Thus, multiple changes in immune reactivity have been described in women during pregnancy^14,24,27 and also in the nonpregnant state.^25,26 The protective effect of oral contraceptives or HRT on development of NHL could potentially result from some of these immunologic changes.

Preliminary analyses of an earlier study published by our group⁵ indicated an increased risk of NHL with a history of at least 1 year of use of estrogen replacement therapy. This result is inconsistent with the current data. However, in the earlier study,⁵ we made no restriction in terms of menopausal status nor did we adjust for age at menopause. Furthermore, our earlier study included patients with all grades and types of NHL, whereas the current study is restricted to patients with high- or intermediate-grade B-cell disease. Because low-grade lymphoma is a different disease, biologically, than intermediate- and high-grade B-cell lymphoma, it would seem most appropriate to perform epidemiologic studies on specific subtypes of lymphoma rather than considering NHL as one entity.

It is important to point out that because only 45% of those case patients ascertained were actually interviewed, the generalizability of these results may be limited. The primary reason for nonresponse in the patients was that they died before interview. This situation raises the possibility that these estrogenic exposures may influence NHL survival as well as NHL incidence. Another limitation of this study is that analyses of the effects of exogenous hormone exposures were based on few subjects and are therefore less robust. In addition, age at menopause was unknown for many of the participants, which reduced the power to detect an effect in these analyses. Thus, the possibility that our results may be caused by chance should be considered.

In conclusion, we found that history of exogenous estrogen exposure was associated with a decreased risk of high- or intermediate-grade B-cell NHL among HIV-negative women. Because few studies have examined the relationships between reproductive and hormonal exposure factors and risk of NHL in women, additional larger studies are clearly needed. Future studies may also benefit by examining the role of these factors on women’s risk of other types of NHL.

	ACKNOWLEDGMENTS

 
Submitted January 19, 2000; accepted November 16, 2000.

Supported by National Cancer Institute grant nos. CA-50850 and CA-17054 and the California Public Health Foundation (subcontract 050-F-8709), which is supported by the California Department of Health Services as part of its statewide cancer reporting program mandated by Health and Safety Code Sections 210 and 211.03.

	NOTES

 
The ideas and opinions expressed herein are those of the authors, and no endorsement by the State of California, or the California Public Health Foundation is intended or should be inferred.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Nelson, R. A. Articles by Bernstein, L. Search for Related Content PubMed PubMed Citation Articles by Nelson, R. A. Articles by Bernstein, L.