American Journal of Epidemiology Advance Access published July 11, 2006

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1 American Journal of Epidemiology Advance Access published July 11, 2006 American Journal of Epidemiology Copyright ª 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A. DOI: /aje/kwj254 Original Contribution Risk of Brain Tumors Associated with Exposure to Exogenous Female Sex Hormones Annette Wigertz 1, Stefan Lönn 1, Tiit Mathiesen 2, Anders Ahlbom 1, Per Hall 3, Maria Feychting 1, and the Swedish INTERPHONE Study Group 1 Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden. 2 Department of Clinical Neuroscience, Karolinska University Hospital, Stockholm, Sweden. 3 Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden. Received for publication October 14, 2005; accepted for publication March 20, The etiology of brain tumors is largely unknown. Prior observations have implicated gender-specific hormones in the pathogenesis of these tumors. In a population-based case-control study, the authors identified all women aged years who had been diagnosed with meningioma or glioma during in four regions of Sweden. Controls were randomly selected from the study base. Detailed information on hormone usage, including use of hormonal contraceptives, hormonal treatment for gynecologic problems, and hormone replacement therapy, was collected from 178 meningioma cases, 115 glioma cases, and 323 controls. Data were analyzed using unconditional logistic regression, adjusting for age, residential area, education, and parity. An increased relative risk of meningioma was found among postmenopausal women for ever use of hormone replacement therapy, with an odds ratio of 1.7 (95% confidence interval: 1.0, 2.8). Women who had used long-acting hormonal contraceptives (subdermal implants, injections, or hormonal intrauterine devices) had an increased risk of meningioma; the odds ratio for at least 10 years of use was 2.7 (95% confidence interval: 0.9, 7.5). Hormone usage was not associated with glioma risk in this study. The findings suggest that the use of female sex steroids may increase the risk of meningioma. case-control studies; contraceptives, oral; estrogens; glioma; hormone replacement therapy; meningioma; progesterone Abbreviations: CI, confidence interval; ICD-10, International Classification of Diseases, Tenth Revision; ICD-O-2, International Classification of Diseases for Oncology, Second Edition. Primary brain tumors are a heterogeneous group of tumors which vary by the tissue of origin. The two most common types are gliomas and meningiomas (1). The etiology of these tumors is mainly unknown. Aside from extremely rare genetic conditions, such as neurofibromatosis and tuberous sclerosis (2, 3), the only unequivocally identified risk factor is exposure to ionizing radiation (4 6), and this explains only a very small fraction of cases. Numerous environmental agents have been implicated as possible causal factors, but no consistent evidence has been shown. It has been suggested that female sex hormones influence the development and growth of brain tumors, particularly meningiomas. A higher female:male ratio (2 3:1) in meningiomas, especially during the female reproductive years (1, 3, 7, 8), and an observed growth stimulation during pregnancy and the luteal phase of menstruation (9, 10) support this hypothesis. A higher incidence of glioma in men Correspondence to Dr. Annette Wigertz, Institute of Environmental Medicine, Karolinska Institutet, Box 210, S Stockholm, Sweden ( annette.wigertz@ki.se). 1

2 2 Wigertz et al. has been shown to be evident around the age of female menarche, reaching a maximum around the age of menopause and diminishing thereafter, suggesting that female hormones may have a protective effect (11). An observed association between breast carcinoma and meningioma has been reported (12, 13), with an elevated risk of meningioma being observed among women who have been diagnosed with breast cancer and an elevated risk of breast cancer being observed among women with a previous meningioma. This suggests a possible overlap in genetic or environmental factors in tumor formation. Hormone receptors are present in brain tumor tissue; progesterone receptors are present in approximately two thirds of meningiomas, estrogen receptors in one tenth, and androgen receptors in two thirds (14, 15). Hormone receptors have also been found in gliomas (16, 17). Prior epidemiologic studies have reported contradictory results about the relation between exogenous hormone use and the risk of brain tumors in females (18 22). We conducted a case-control study in Sweden to analyze possible associations between exposure to exogenous female steroid hormones and the risks of meningioma and glioma. MATERIALS AND METHODS Study setting and subjects The study population consisted of all women aged years in the geographic areas covered by the regional cancer registers in Stockholm, Göteborg, Umeå, and Lund. The study period ranged from September 1, 2000, to August 31, The study was part of INTERPHONE, an international case-control study of adult brain tumors that has been described previously (23). The main purpose of INTERPHONE was to test possible associations between use of mobile telephones and brain tumors. During the planning and introduction of the study, additional questions were added to the interview to allow analyses of other risk factors for brain tumors apart from use of mobile phones. A number of different areas were covered by detailed questions, including the use of female sex steroid hormones. The supplementary questions were not introduced until spring During the study period, 231 meningioma cases, 197 glioma cases, and 504 controls were identified. Because of the delayed introduction of the questions concerning hormone usage, we were only able to include 220 meningioma cases, 176 glioma cases, and 495 controls in the study. Of these persons, 185 meningioma cases, 132 glioma cases, and 323 controls agreed to participate, leading to response rates of 84 percent, 75 percent, and 65 percent, respectively. Proxy respondents were interviewed for 3 percent (n ¼ 6) of participating meningioma cases and 13 percent (n ¼ 17) of participating glioma cases. One patient diagnosed with meningioma was suffering from Turner s syndrome (having only one X chromosome) and was therefore not included in the analysis. We decided a priori to exclude the proxy respondents from the analyses, because of the difficulty of a proxy respondent s giving accurate information on someone else s lifetime usage of female hormones (24). Case ascertainment Eligible cases were all women diagnosed during the study period with intracranial meningioma (International Classification of Diseases, Tenth Revision (ICD-10), code C70; International Classification of Diseases for Oncology, Second Edition (ICD-O-2), codes ) or intracranial glioma (ICD-10 code C71; ICD-O-2 codes , , , , , 9430, , , 9460, , and 9505). Cases were identified continuously during the study period through collaboration with departments of neurosurgery, oncology, and neurology at all hospitals within the study areas. Trained research nurses and a psychologist contacted the clinics every week to guarantee fast ascertainment of cases. The regional cancer registries were searched approximately every third month for additional case identification, to ensure that no cases had been missed. The diagnoses were pathologically confirmed for 85 percent of participating meningioma cases and 94 percent of participating glioma cases. A reference date of diagnosis was defined as the date of the first medical examination leading to diagnosis (usually the first radiologic examination). Control selection Control subjects were randomly chosen from the study population, stratified by age (in 5-year groups) and residential area. Controls were selected from the Swedish population registry approximately every second month throughout the study period. The reference date for controls was defined as the date of identification of the control, adjusted for the average time difference between dates of identification and dates of diagnosis of cases. Reference dates for controls were adjusted separately for meningioma cases and glioma cases, because the average time between diagnosis and identification was shorter for glioma cases than for meningioma cases. Data collection All interviews and contacts with cases and controls were made by nurses or a psychologist employed for this purpose. All cases and controls were contacted as soon as possible after identification. Data collection has been described in detail previously (25, 26). Information on hormone usage and other possible risk factors, such as parity and exposure to ionizing radiation, was collected through personal interviews. Interviews were conducted using a computer program that guided the interview, with questions being read by the interviewer from a laptop computer screen. Persons who were unable to participate in a personal interview were offered a telephone interview instead. If a case had died, the closest relative was contacted as a proxy respondent. Exposure information related to exogenous female hormones was ascertained by asking whether the subject had ever used oral contraceptives, other hormonal contraceptives, hormonal treatment for gynecologic problems, or hormone replacement therapy. Affirmative answers were followed by additional questions on the name of the compound and the duration of use.

3 Brain Tumors and Exogenous Female Sex Hormones 3 A woman was defined as postmenopausal if she had had her last menstrual period or a bilateral oophorectomy at least 1 year prior to the reference date. Women whose menopausal status was unknown because of hormonal treatment or prior hysterectomy were considered postmenopausal if they had reached 55 years of age (the age of natural menopause in 90 percent of control subjects). For 11 percent of the meningioma cases, 11 percent of the glioma cases, and 7 percent of the controls, menopausal status was unknown and was therefore assessed by imputation of age. Statistical analysis Odds ratios and 95 percent confidence intervals were used as measures of relative risk. These were computed from multivariate logistic regression models and estimated by the unconditional maximum-likelihood method. Adjustments for the stratification variables (age and residential area), parity, and education (compulsory school, vocational or secondary school, upper secondary school, and university) were made in all analyses. Additional analyses were conducted for investigation of possible confounding from marital status, smoking, or previous radiotherapy exposure. These variables did not affect the results and therefore were not included in the final models. All analyses were performed using SAS statistical software, version 8.2 (27). The study was approved by the ethics committees at the Karolinska Institute (Stockholm) and the universities of Göteborg, Umeå, and Lund. RESULTS The characteristics of participating subjects are summarized in table 1. Table 2 displays the results for various categories of hormone usage. There was no clear association between the use of oral contraceptives and meningioma or glioma risk. For the use of other hormonal contraceptives (subdermal implants, injections, or hormonal intrauterine devices), the relative risk of meningioma was estimated to be 1.5 (95 percent confidence interval (CI): 0.9, 2.6). For use for 10 or more years, the risk estimate increased to 2.7 (95 percent CI: 0.9, 7.5). No consistent pattern was seen for glioma. Only a very small number of women had used hormones for gynecologic problems, and the relative risk estimates for both meningioma and glioma were statistically unstable. Among postmenopausal women, the use of hormone replacement therapy was associated with an elevated risk of meningioma; for ever use, the risk estimate was 1.7 (95 percent CI: 1.0, 2.8), and for use of 10 or more years duration, the risk estimate was 1.9 (95 percent CI: 1.0, 3.8). However, no consistent dose-response relation was observed. The risk estimates for glioma were close to or below unity. DISCUSSION In this population-based case-control study, we found an elevated risk of meningioma associated with the use of hormone replacement therapy, though with no consistent doseresponse relation. We found no association for use of oral contraceptives, and no noteworthy associations were seen for glioma. The results correspond with the hypothesis of a late-acting hormonal influence on meningioma risk and the existence of progesterone receptors in most meningiomas (14, 15). The few prior studies of exogenous hormones have shown contradictory results. One cohort study found an elevated risk of meningioma among postmenopausal women who used hormone replacement therapy (20), similar to the results in our study. The risk increase was confined to current hormone replacement users, whereas no association was found among past users. In our study, we were not able to make the distinction between current use and past use. Contrary to these findings, a study of spinal meningiomas showed a reduced risk for current use of hormone replacement therapy and a reduced risk of spinal meningioma after 3 years of oral contraceptive use (18). The relevance of comparing spinal and intracranial meningiomas may be questionable, however. In a case-control study focusing on the role of medical history in brain tumor development, Schlehofer et al. (19) reported a decreased risk of glioma associated with the use of steroid hormones (oral contraceptives and/or hormone replacement therapy). The authors mentioned briefly in their Discussion that no effects were seen for meningioma (19), but no actual numbers were presented; the results are therefore difficult to interpret. The authors did not analyze different types of hormones separately, and they probably included all women regardless of menopausal status; effects of exogenous hormones were not the main hypothesis examined in their study. This makes comparisons with our study difficult, since our results differed for oral contraceptive use and hormone replacement therapy, and we restricted analyses of the latter hormone type to postmenopausal women. In a study of glioma and reproductive factors, Huang et al. (21) reported a reduced risk of glioma among women who had ever used hormone replacement therapy. In a recent hospital-based case-control study of meningioma and glioma, Hatch et al. (22) reported similar findings; reduced risks of glioma were seen for both oral contraceptive use and hormone replacement therapy. Overall, they found little evidence that use of hormone replacement therapy or oral contraceptives was associated with meningioma, but they cautioned that this may have been a result of low statistical power (22). The effect of female steroid sex hormones is mediated through their receptors, in concert with coactivators and corepressors (28, 29). The hormones regulate proliferation and cell cycle progression through transcriptional mechanisms involving the receptors. In addition, estrogens have been postulated to influence the regulation of cell death and the genomic instability of cells (28). Cancers with a large female:male ratio seem to be influenced by female sex hormones. It is beyond doubt that hormone replacement therapy increases the risk of breast cancer (30). As with meningiomas, differentiated thyroid cancer, with a female: male ratio of approximately 3:1, has been shown to be more prevalent among women during their fertile years (31).

4 4 Wigertz et al. TABLE 1. Descriptive characteristics of meningioma and glioma cases and controls, INTERPHONE Study, Sweden, Characteristic Meningioma cases (n ¼ 178) Glioma cases (n ¼ 115) Controls* (n ¼ 323) No. % No. % No. % Region Stockholm Göteborg Umeå Lund Age (years) at reference date /177 54/ /85 27/26 Educationy Compulsory school Vocational/secondary school Upper secondary school University Unknown Marital status Single Married Separated or divorced Widowed Parity Menopausal status Premenopausal /139 42/43 Postmenopausal /184 58/57 Smoking history Never smoker Former smoker Current smoker Prior radiotherapy treatmentz * Numbers and percentages vary for controls because of the use of different reference dates in analyses of meningioma or glioma. y The highest level of education completed, as translated from the Swedish educational system. z Radiation directed toward the head or neck. The association between steroid hormones and brain tumors, especially meningiomas, has raised the question of whether antihormonal treatment of meningiomas is possible. Two antiprogesterone agents, mifepristone and onapristone, have exhibited cytostatic and cytocidal effects against cultured meningioma cells, however, regardless of the presence or absence of progesterone receptors (32). Antiprogesterone and antiestrogen have also been tried in vivo for unresectable or recurrent meningiomas, with varied results (33 35). The varying results could possibly be explained by dissimilarity in receptor status, making some tumors less sensitive to antiendocrine treatment. The presence of progesterone receptors in combination with a low proliferative index has been shown to predict a better outcome (36, 37). Strengths of our study include the population-based design and the rapid case ascertainment. Cases were identified

5 Brain Tumors and Exogenous Female Sex Hormones 5 TABLE 2. Adjusted odds ratios for meningioma and glioma according to use of female steroid hormones, INTERPHONE Study, Sweden, No. of cases No. of controls* Meningioma ORy,z 95% CIy No. of cases No. of controls* Glioma ORz 95% CI Use of oral contraceptives Never Ever , , 1.4 Duration of use (years) < , , , , , , , , 1.5 Missing data Use of other hormonal contraceptives Never Ever , , 2.1 Duration of use (years) < , , , , , , , , 5.7 Missing data Hormones given for gynecologic problems{ Never Ever , , 1.1 Duration of use (years) < , , , , 3.1 Missing data Hormone replacement therapy# Never Ever , , 1.7 Duration of use (years) < , , , , , , , 2.0 Missing data * Because of missing information on education, three controls were excluded from the analyses. y OR, odds ratio; CI, confidence interval. z Adjusted for age, residential area, education, and parity. Including subdermal implants, injections, and hormonal intrauterine devices. { Hormones for treatment of gynecologic problems such as bleeding and irregular menstruation. # Analyses were restricted to postmenopausal women. Numbers of controls varied because of the use of different reference dates in analyses of meningioma or glioma. continuously during the study period through collaboration with the treating clinics. To ensure that no cases were missed, we searched the regional cancer registries to identify additional cases. Notification to these cancer registries is compulsory for every physician in Sweden, and all pathologists are required to submit separate reports to the

6 6 Wigertz et al. registries; therefore, most cases are reported by both a clinician and a pathologist. This notification system has produced high completeness of coverage (38). Controls were randomly selected from the Swedish Register of the Total Population, which is operated and continuously updated by Statistics Sweden. All contacts and personal interviews were performed by trained nurses and a psychologist, ensuring standardized treatment of cases and controls. Participation rates were comparable to what has been generally found in recent Swedish case-control studies. A weakness of our study is the lack of detailed information on when in time the patients had taken hormones and what types of compounds they had used. During the interview, participants who gave an affirmative answer to questions on ever usage of hormone replacement therapy or oral contraceptives were asked about the names of the compounds used, but approximately two thirds of cases and controls did not mention any names. Therefore, we were not able to evaluate differential effects for use of estrogens alone versus combined estrogen and progesterone or use of high-dose estrogens versus low-dose estrogens. However, the importance of progesterone may be indicated by the fact that, up to the time of the study, the group of hormones here called other hormonal contraceptives, including subdermal implants, injections, and hormonal intrauterine devices, included only progesterones in Sweden. Only a small number of women had used these kinds of hormones, so the results are unstable and need to be confirmed in other studies before any conclusions can be drawn. There is convincing evidence that breast cancer risk associated with hormone replacement therapy increases with duration of use and that the risk is substantially greater for combined estrogenprogesterone compounds than for estrogen-only compounds (39 42). If a higher risk of meningioma is found after combined hormone replacement treatment, our results could be an underestimation of the true association. Our inability to distinguish between past use and current use would also have resulted in underestimation of meningioma risk associated with hormone replacement therapy if the risk were truly confined to current users. Nonparticipation is always a source of potential selection bias. Prior studies have shown an association between socioeconomic position and the use of hormone replacement therapy (43). Participation of controls in a study is also associated with socioeconomic status (44). In our study, this would mean that participating controls probably had used hormone replacement therapy more frequently than the general population, possibly decreasing the risk estimate. However, adjustment for education as an indicator of socioeconomic status should have reduced the effect of this potential source of bias. In the analyses, we did not use proxy data and thereby avoided the potential inaccuracies associated with that type of information. This also means that we missed a few cases who had died before the interview. Another possible limitation of our study involves the risk of misclassification of exposure history. Cases may recall suspected exposures more accurately than controls; such recall bias may lead to a false elevation of the risk estimate. When cases and controls were initially contacted and informed about the study, the interest in hormones as a potential risk factor was not mentioned, and the risk of recall bias was therefore diminished. The fact that risk estimates were elevated for meningioma but not for glioma also speaks against an effect of recall bias. On the other hand, the nature of the disease, with its often rapidly debilitating course, may have caused impaired memory among cases, especially for glioma. A study of recall of hormone replacement therapy showed relatively good remembrance overall, but the recall of duration of use was poor (45). Recall of oral contraceptive use has been studied, and information has been shown to correspond well between interview and pharmacy records (46). The correlation coefficient for duration of use was , depending on how much time had passed between the use and the interview (46). Nondifferential exposure misclassification of hormone use would lead to a dilution of the risk estimates. Our study supports the hypothesis that exogenous female steroid hormones may play a role in the occurrence of meningioma. Further studies are needed to confirm these results and to make distinctions between progesterone and estrogen usage. Whether steroid hormones influence the growth of tumors or are involved in tumorigenesis remains to be elucidated. ACKNOWLEDGMENTS The authors received funding from the European Union Fifth Framework Programme, Quality of Life and Management of Living Resources (contract QLK4-CT ); the International Union Against Cancer (UICC); the Swedish Research Council; and the Swedish Cancer Society. The UICC received funds for this purpose from the Mobile Manufacturers Forum and the GSM Association. Provision of funds to the INTERPHONE Study investigators via the UICC was governed by agreements that guaranteed INTERPHONE s complete scientific independence. These agreements are publicly available at The Swedish INTERPHONE Study Group consists of the authors and the following contributors: Drs. T. Bergenheim, L. Damber, and B. Malmer (Umeå University Hospital); Drs. J. Boethius, O. Flodmark, A. Lilja, I. Ohlsson-Lindblom, and H. Stibler (Karolinska University Hospital); Drs. J. Lycke, A. Michanek, and L. Pellettieri (Sahlgrenska University Hospital); and Drs. T. Möller and L. Salford (Lund University Hospital). The authors thank the regional cancer registries for their collaboration. They also thank the research nurses for their skillful work. Conflict of interest: none declared. REFERENCES 1. Kleihues P, Cavenee WK. World Health Organization classification of tumours. Pathology and genetics: tumours of the nervous system. 2nd ed. Lyon, France: IARC Press, 2000.

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