Skip Navigation


American Journal of Epidemiology Advance Access originally published online on July 11, 2006
American Journal of Epidemiology 2006 164(7):629-636; doi:10.1093/aje/kwj254
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
164/7/629    most recent
kwj254v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (6)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Wigertz, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wigertz, A.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

Original Contribution

Risk of Brain Tumors Associated with Exposure to Exogenous Female Sex Hormones

Annette Wigertz1, Stefan Lönn1, Tiit Mathiesen2, Anders Ahlbom1, Per Hall3, Maria Feychting1 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

Correspondence to Dr. Annette Wigertz, Institute of Environmental Medicine, Karolinska Institutet, Box 210, S-171 77 Stockholm, Sweden (e-mail: annette.wigertz{at}ki.se).

Received for publication October 14, 2005. Accepted for publication March 20, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
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 20–69 years who had been diagnosed with meningioma or glioma during 2000–2002 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


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
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 (1Go). The etiology of these tumors is mainly unknown. Aside from extremely rare genetic conditions, such as neurofibromatosis and tuberous sclerosis (2Go, 3Go), the only unequivocally identified risk factor is exposure to ionizing radiation (4Go–6Go), 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 (1Go, 3Go, 7Go, 8Go), and an observed growth stimulation during pregnancy and the luteal phase of menstruation (9Go, 10Go) support this hypothesis. A higher incidence of glioma in men 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 (11Go). An observed association between breast carcinoma and meningioma has been reported (12Go, 13Go), 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 (14Go, 15Go). Hormone receptors have also been found in gliomas (16Go, 17Go).

Prior epidemiologic studies have reported contradictory results about the relation between exogenous hormone use and the risk of brain tumors in females (18Go–22Go). 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
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study setting and subjects
The study population consisted of all women aged 20–69 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, 2002. The study was part of INTERPHONE, an international case-control study of adult brain tumors that has been described previously (23Go). 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 2001.

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 = 6) of participating meningioma cases and 13 percent (n = 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 (24Go).

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 9530–9539) or intracranial glioma (ICD-10 code C71; ICD-O-2 codes 9380–9384, 9390–9394, 9400–9401, 9410–9411, 9420–9424, 9430, 9440–9443, 9450–9451, 9460, 9480–9481, 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 (25Go, 26Go).

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.

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 (27Go).

The study was approved by the ethics committees at the Karolinska Institute (Stockholm) and the universities of Göteborg, Umeå, and Lund.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
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.


View this table:
[in this window]
[in a new window]

  		TABLE 1. Descriptive characteristics of meningioma and glioma cases and controls, INTERPHONE Study, Sweden, 2000–2002

 

View this table:
[in this window]
[in a new window]

  		TABLE 2. Adjusted odds ratios for meningioma and glioma according to use of female steroid hormones, INTERPHONE Study, Sweden, 2000–2002

 
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
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
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 dose-response 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 (14Go, 15Go).

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 (20Go), 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 (18Go). 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. (19Go) 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 (19Go), 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. (21Go) 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. (22Go) 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 (22Go).

The effect of female steroid sex hormones is mediated through their receptors, in concert with coactivators and corepressors (28Go, 29Go). 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 (28Go). 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 (30Go). 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 (31Go).

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 (32Go). Antiprogesterone and antiestrogen have also been tried in vivo for unresectable or recurrent meningiomas, with varied results (33Go–35Go). 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 (36Go, 37Go).

Strengths of our study include the population-based design and the rapid case ascertainment. Cases were identified 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 registries; therefore, most cases are reported by both a clinician and a pathologist. This notification system has produced high completeness of coverage (38Go). 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 estrogen-progesterone compounds than for estrogen-only compounds (39Go–42Go). 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 (43Go). Participation of controls in a study is also associated with socioeconomic status (44Go). 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 (45Go). Recall of oral contraceptive use has been studied, and information has been shown to correspond well between interview and pharmacy records (46Go). The correlation coefficient for duration of use was 0.71–0.82, depending on how much time had passed between the use and the interview (46Go). 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-1999-01563); 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 http://www.iarc.fr/ENG/Units/RCAd.html.

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
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 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.
  2. Inskip PD, Linet MS, Heineman EF. Etiology of brain tumors in adults. Epidemiol Rev 1995;17:382–414.[Free Full Text]
  3. Wrensch M, Minn Y, Chew T, et al. Epidemiology of primary brain tumors: current concepts and review of the literature. Neuro-Oncol 2002;4:278–99.[Abstract]
  4. Ron E, Modan B, Boice JD Jr, et al. Tumors of the brain and nervous system after radiotherapy in childhood. N Engl J Med 1988;319:1033–9.[Abstract]
  5. Karlsson P, Holmberg E, Lundell M, et al. Intracranial tumors after exposure to ionizing radiation during infancy: a pooled analysis of two Swedish cohorts of 28,008 infants with skin hemangioma. Radiat Res 1998;150:357–64.[ISI][Medline]
  6. Preston DL, Ron E, Yonehara S, et al. Tumors of the nervous system and pituitary gland associated with atomic bomb radiation exposure. J Natl Cancer Inst 2002;94:1555–63.[Abstract/Free Full Text]
  7. Helseth A. Incidence and survival of intracranial meningioma patients in Norway 1963–1992. Neuroepidemiology 1997;16:53–9.[CrossRef][ISI][Medline]
  8. Klaeboe L, Lonn S, Scheie D, et al. Incidence of intracranial meningiomas in Denmark, Finland, Norway and Sweden, 1968–1997. Int J Cancer 2005;117:996–1001.[CrossRef][ISI][Medline]
  9. Bickerstaff ER, Small JM, Guest IA. The relapsing course of certain meningiomas in relation to pregnancy and menstruation. J Neurol Neurosurg Psychiatry 1958;21:89–91.[Medline]
  10. Michelsen JJ, New PF. Brain tumour and pregnancy. J Neurol Neurosurg Psychiatry 1969;32:305–7.[ISI][Medline]
  11. McKinley BP, Michalek AM, Fenstermaker RA, et al. The impact of age and sex on the incidence of glial tumors in New York State from 1976 to 1995. J Neurosurg 2000;93:932–9.[ISI][Medline]
  12. Schoenberg BS, Christine BW, Whisnant JP. Nervous system neoplasms and primary malignancies of other sites. The unique association between meningiomas and breast cancer. Neurology 1975;25:705–12.[Abstract/Free Full Text]
  13. Custer BS, Koepsell TD, Mueller BA. The association between breast carcinoma and meningioma in women. Cancer 2002;94:1626–35.[CrossRef][ISI][Medline]
  14. Sanson M, Cornu P. Biology of meningiomas. Acta Neurochir (Wien) 2000;142:493–505.[CrossRef][Medline]
  15. Blankenstein MA, Verheijen FM, Jacobs JM, et al. Occurrence, regulation, and significance of progesterone receptors in human meningioma. Steroids 2000;65:795–800.[CrossRef][ISI][Medline]
  16. Carroll RS, Zhang J, Dashner K, et al. Steroid hormone receptors in astrocytic neoplasms. Neurosurgery 1995;37:496–503.[ISI][Medline]
  17. Khalid H, Shibata S, Kishikawa M, et al. Immunohistochemical analysis of progesterone receptor and Ki-67 labeling index in astrocytic tumors. Cancer 1997;80:2133–40.[CrossRef][ISI][Medline]
  18. Preston-Martin S, Monroe K, Lee PJ, et al. Spinal meningiomas in women in Los Angeles County: investigation of an etiological hypothesis. Cancer Epidemiol Biomarkers Prev 1995;4:333–9.[Abstract]
  19. Schlehofer B, Blettner M, Preston-Martin S, et al. Role of medical history in brain tumour development. Results from the international adult brain tumour study. Int J Cancer 1999;82:155–60.[CrossRef][ISI][Medline]
  20. Jhawar BS, Fuchs CS, Colditz GA, et al. Sex steroid hormone exposures and risk for meningioma. J Neurosurg 2003;99:848–53.[ISI][Medline]
  21. Huang K, Whelan EA, Ruder AM, et al. Reproductive factors and risk of glioma in women. Cancer Epidemiol Biomarkers Prev 2004;13:1583–8.[Abstract/Free Full Text]
  22. Hatch EE, Linet MS, Zhang J, et al. Reproductive and hormonal factors and risk of brain tumors in adult females. Int J Cancer 2005;114:797–805.[CrossRef][ISI][Medline]
  23. Cardis E, Killkenny M. International case-control study of adult brain, head and neck tumours: results of the feasibility study. Radiat Protect Dosimetry 1999;83:179–83.
  24. Poulter NR, Chang CL, Farley TM, et al. Reliability of data from proxy respondents in an international case-control study of cardiovascular disease and oral contraceptives. World Health Organization Collaborative Study of Cardiovascular Disease and Steroid Hormone Contraception. J Epidemiol Community Health 1996;50:674–80.[Abstract]
  25. Lonn S, Ahlbom A, Hall P, et al. Mobile phone use and the risk of acoustic neuroma. Epidemiology 2004;15:653–9.[CrossRef][ISI][Medline]
  26. Lonn S, Ahlbom A, Hall P, et al. Long-term mobile phone use and brain tumor risk. Am J Epidemiol 2005;161:526–35.[Abstract/Free Full Text]
  27. SAS Institute, Inc. SAS statistical software. Cary, NC: SAS Institute, Inc, 2001.
  28. Dickson RB, Stancel GM. Estrogen receptor-mediated processes in normal and cancer cells. J Natl Cancer Inst Monogr 2000(27):135–45.
  29. Mulac-Jericevic B, Conneely OM. Reproductive tissue selective actions of progesterone receptors. Reproduction 2004;128:139–46.[Abstract/Free Full Text]
  30. Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321–33.[Abstract/Free Full Text]
  31. Lundgren CI, Hall P, Ekbom A, et al. Incidence and survival of Swedish patients with differentiated thyroid cancer. Int J Cancer 2003;106:569–73.[CrossRef][ISI][Medline]
  32. Matsuda Y, Kawamoto K, Kiya K, et al. Antitumor effects of antiprogesterones on human meningioma cells in vitro and in vivo. J Neurosurg 1994;80:527–34.[ISI][Medline]
  33. Grunberg SM, Weiss MH, Spitz IM, et al. Treatment of unresectable meningiomas with the antiprogesterone agent mifepristone. J Neurosurg 1991;74:861–6.[ISI][Medline]
  34. Lamberts SW, Tanghe HL, Avezaat CJ, et al. Mifepristone (RU 486) treatment of meningiomas. J Neurol Neurosurg Psychiatry 1992;55:486–90.[Abstract]
  35. Goodwin JW, Crowley J, Eyre HJ, et al. A phase II evaluation of tamoxifen in unresectable or refractory meningiomas: a Southwest Oncology Group study. J Neurooncol 1993;15:75–7.[CrossRef][Medline]
  36. Hsu DW, Efird JT, Hedley-Whyte ET. Progesterone and estrogen receptors in meningiomas: prognostic considerations. J Neurosurg 1997;86:113–20.[ISI][Medline]
  37. Roser F, Nakamura M, Bellinzona M, et al. The prognostic value of progesterone receptor status in meningiomas. J Clin Pathol 2004;57:1033–7.[Abstract/Free Full Text]
  38. Mattsson B, Wallgren A. Completeness of the Swedish Cancer Register. Non-notified cancer cases recorded on death certificates in 1978. Acta Radiol Oncol 1984;23:305–13.[ISI][Medline]
  39. Chlebowski RT, Hendrix SL, Langer RD, et al. Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women: The Women's Health Initiative Randomized Trial. JAMA 2003;289:3243–53.[Abstract/Free Full Text]
  40. Beral V. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 2003;362:419–27.[CrossRef][ISI][Medline]
  41. Li CI, Malone KE, Porter PL, et al. Relationship between long durations and different regimens of hormone therapy and risk of breast cancer. JAMA 2003;289:3254–63.[Abstract/Free Full Text]
  42. Anderson GL, Limacher M, Assaf AR, et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004;291:1701–12.[Abstract/Free Full Text]
  43. Finley C, Gregg EW, Solomon LJ, et al. Disparities in hormone replacement therapy use by socioeconomic status in a primary care population. J Community Health 2001;26:39–50.[CrossRef][ISI][Medline]
  44. Richiardi L, Boffetta P, Merletti F. Analysis of nonresponse bias in a population-based case-control study on lung cancer. J Clin Epidemiol 2002;55:1033–40.[CrossRef][ISI][Medline]
  45. Strom BL, Schinnar R. An interview strategy was critical for obtaining valid information on the use of hormone replacement therapy. J Clin Epidemiol 2004;57:1210–13.[CrossRef][ISI][Medline]
  46. Norell SE, Boethius G, Persson I. Oral contraceptive use: interview data versus pharmacy records. Int J Epidemiol 1998;27:1033–7.[Abstract/Free Full Text]

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Eur J EndocrinolHome page
A. Mueller and L. Gooren
Hormone-related tumors in transsexuals receiving treatment with cross-sex hormones
Eur. J. Endocrinol., September 1, 2008; 159(3): 197 - 202.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
S. Blitshteyn, J. E. Crook, and K. A. Jaeckle
Is There an Association Between Meningioma and Hormone Replacement Therapy?
J. Clin. Oncol., January 10, 2008; 26(2): 279 - 282.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
E. B. Claus, P. J. Park, R. Carroll, J. Chan, and P. M. Black
Specific Genes Expressed in Association with Progesterone Receptors in Meningioma
Cancer Res., January 1, 2008; 68(1): 314 - 322.
[Abstract] [Full Text] [PDF]

Home page
 Ann OncolHome page
G. Corrao, A. Zambon, V. Conti, F. Nicotra, C. La Vecchia, C. Fornari, G. Cesana, P. Contiero, G. Tagliabue, R. E. Nappi, et al.
Menopause hormone replacement therapy and cancer risk: an Italian record linkage investigation
Ann. Onc., January 1, 2008; 19(1): 150 - 155.
[Abstract] [Full Text] [PDF]

Home page
 NEJMHome page
R. Gazzeri, M. Galarza, and G. Gazzeri
Growth of a Meningioma in a Transsexual Patient after Estrogen-Progestin Therapy
N. Engl. J. Med., December 6, 2007; 357(23): 2411 - 2412.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
164/7/629    most recent
kwj254v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (6)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Wigertz, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wigertz, A.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?