© 1994 by Oxford University Press
Journal of the National Cancer Institute, Vol. 86, No. 7, 527-537,
April 6, 1994
© 1994 Oxford University Press
Endometrial Cancer in Tamoxifen-Treated Breast Cancer Patients: Findings From the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14*
Department of Surgery, University of Pittsburgh Pa
Department of Biostatics, University of Pittsburgh Pa
Shadyside Hospital Pittsburgh
Correspondence to: Bernard Fisher, M.D., Department of Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA 15261.
BACKGROUND: Tamoxifen is advantageous in treating all stages of breast cancer. However, studies have suggested that incidence and severity of endometrial cancer increase in women treated with tamoxifen.
PURPOSE: We compared rates of endometrial and other cancers in tamoxifen- and non-tamoxifen-treated patients and described the pathologic characteristics of the endometrial cancers.
METHODS: Data were analyzed on 2843 patients with node-negative, estrogen receptor-positive, invasive breast cancer randomly assigned to placebo or tamoxifen (20 mg/d) and on 1220 tamoxifen-treated patients registered in NSABP B-14 subsequent to randomization. Average time on study is 8 years for randomly assigned patients and 5 years for registered patients.
RESULTS: The incidence rates of liver, gastrointestinal, urinary tract, and nonuterine genital tumors were not increased by tamoxifen treatment. Twenty-five endometrial cancers were originally reported, one of which was reclassified after subsequent review. Two cases occurred in the placebo group in patients whose medical status subsequent to random assignment had required tamoxifen treatment. Twenty-three occurred in the tamoxifen groups. Twenty-one of the 24 originally reported endometrial cancers were FIGO stage 1; 18 of 23 gradable cases were of good to moderate histologic grade. Four tamoxifen-treated women died of uterine cancer. The average annual hazard rate of endometrial cancer as a first event within the first 5 years of follow-up in the randomized, tamoxifen-treated group was 1.2/1000 patient-years; the cumulative hazard rate was 6.3/1000. Findings for the registered, tamoxifen-treated group were similar. Including all originally reported endometrial cancers, the annual hazard rate through all follow-up was 0.2/1000 in the placebo group and 1.6/1000 in the randomized, tamoxifen-treated group; the relative risk of endometrial cancer for the latter versus the former group was 7.5. Again for the latter group, using population-based rates of endometrial cancer from SEER data and information from another NSABP (B-06) trial, relative risks were 2.2 and 2.3, respectively. The 5-year cumulative hazard rate for disease-free survival in the randomized tamoxifen group was 38% less than that in the placebo group. Some data in this paper were provided by an investigator who submitted fraudulent data to the NSABP [see the "News" section]; therefore, the reader must read the entire text including Table 10 and the Editor‘s notes. In brief, data on 182 of the 2843 randomly assigned patients and 37 of the 1220 registered patients were provided by the investigator in question. After review, 24 of the 182 records showed falsification, all involving characteristics of patients prior to random assignment. Of the 37 registered-patient records, 8 showed falsification.
CONCLUSIONS: Risk of endometrial cancer increases following tamoxifen therapy for invasive breast cancer; however, net benefit greatly outweighs risk. Endometrial cancers occurring after tamoxifen therapy do not appear to be of a different type with a worse prognosis than are such tumors in non-tamoxifen-treated patients.
IMPLICATIONS: Tamoxifen treatment for breast cancer should continue. In addition, the relative risk of endometrial cancer observed in B-14 tamoxifen-treated patients is consistent with the twofold relative risk used in the initial risk-benefit computation for the NSABP breast cancer prevention trial. [J Natl Cancer Inst 86: 527–537, 1994]
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L. M. Greenberger, T. Annable, K. I. Collins, B. S. Komm, C. R. Lyttle, C. P. Miller, P. G. Satyaswaroop, Y. Zhang, and P. Frost A New Antiestrogen, 2-(4-Hydroxy-phenyl)-3-methyl-1-[4-(2-piperidin-1-yl-ethoxy)-benzyl]-1H-indol-5-ol hydrochloride (ERA-923), Inhibits the Growth of Tamoxifen-sensitive and -resistant Tumors and Is Devoid of Uterotropic Effects in Mice and Rats Clin. Cancer Res., October 1, 2001; 7(10): 3166 - 3177. [Abstract] [Full Text] [PDF]
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V. G. Vogel Reducing the Risk of Breast Cancer With Tamoxifen in Women at Increased Risk J. Clin. Oncol., September 15, 2001; 19(90001): 87s - 92. [Abstract] [Full Text] [PDF]
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A. Guerrieri-Gonzaga, L. Baglietto, H. Johansson, B. Bonanni, C. Robertson, M.-T. Sandri, L. Canigiula, C. Lampreda, S. Diani, E. A. Lien, et al. Correlation between Tamoxifen Elimination and Biomarker Recovery in a Primary Prevention Trial Cancer Epidemiol. Biomarkers Prev., September 1, 2001; 10(9): 967 - 970. [Abstract] [Full Text] [PDF]
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J. F. Robertson, R. I. Nicholson, N. J. Bundred, E. Anderson, Z. Rayter, M. Dowsett, J. N. Fox, J. M. W. Gee, A. Webster, A. E. Wakeling, et al. Comparison of the Short-Term Biological Effects of 7{alpha}-[9-(4,4,5,5,5-pentafluoropentylsulfinyl)-nonyl]estra-1,3,5, (10)-triene-3,17{beta}-diol (Faslodex) versus Tamoxifen in Postmenopausal Women with Primary Breast Cancer Cancer Res., September 1, 2001; 61(18): 6739 - 6746. [Abstract] [Full Text] [PDF]
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 K. Fong, R. Kung, A. Lytwyn, M. Trudeau, W. Chapman, P. Nugent, P. Glanc, L. Manchul, D. Szabunio, and T. Myhr Endometrial Evaluation with Transvaginal US and Hysterosonography in Asymptomatic Postmenopausal Women with Breast Cancer Receiving Tamoxifen Radiology, September 1, 2001; 220(3): 765 - 773. [Abstract] [Full Text] [PDF]
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 L. E. Hann, E. M. Gretz, A. M. Bach, and S. M. Francis Sonohysterography for Evaluation of the Endometrium in Women Treated with Tamoxifen Am. J. Roentgenol., August 1, 2001; 177(2): 337 - 342. [Abstract] [Full Text] [PDF]
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C. L. Shapiro and A. Recht Side Effects of Adjuvant Treatment of Breast Cancer N. Engl. J. Med., June 28, 2001; 344(26): 1997 - 2008. [Full Text] [PDF]
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P. W. Fan and J. L. Bolton Bioactivation of Tamoxifen to Metabolite E Quinone Methide: Reaction with Glutathione and DNA Drug Metab. Dispos., June 1, 2001; 29(6): 891 - 896. [Abstract] [Full Text]
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D. H. Phillips Understanding the genotoxicity of tamoxifen? Carcinogenesis, June 1, 2001; 22(6): 839 - 849. [Abstract] [Full Text] [PDF]
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J. S. Abrams Tamoxifen: Five Versus Ten Years--Is the End in Sight? J Natl Cancer Inst, May 2, 2001; 93(9): 662 - 664. [Full Text] [PDF]
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A. McDougal, M. Wormke, J. Calvin, and S. Safe Tamoxifen-induced Antitumorigenic/Antiestrogenic Action Synergized by a Selective Aryl Hydrocarbon Receptor Modulator Cancer Res., May 1, 2001; 61(10): 3902 - 3907. [Abstract] [Full Text]
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S. Shibutani, A. Ravindernath, I. Terashima, N. Suzuki, Y. R. Santosh Laxmi, Y. Kanno, M. Suzuki, T. I. Apak, J. J. Sheng, and M. W. Duffel Mechanism of Lower Genotoxicity of Toremifene Compared with Tamoxifen Cancer Res., May 1, 2001; 61(10): 3925 - 3931. [Abstract] [Full Text]
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I. N.H. White, P. Carthew, R. Davies, J. Styles, K. Brown, J. E. Brown, L. L. Smith, and E. A. Martin Short-term dosing of {{alpha}}-hydroxytamoxifen results in DNA damage but does not lead to liver tumours in female Wistar/Han rats Carcinogenesis, April 1, 2001; 22(4): 553 - 557. [Abstract] [Full Text] [PDF]
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 M. Zhong, Z. Lu, T. Abbas, A. Hornia, K. Chatakondu, N. Barile, P. Kaplan, and D. A. Foster Novel Tumor-promoting Property of Tamoxifen Cell Growth Differ., April 1, 2001; 12(4): 187 - 192. [Abstract] [Full Text]
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 R. A. Smith, A. C. von Eschenbach, R. Wender, B. Levin, T. Byers, D. Rothenberger, D. Brooks, W. Creasman, C. Cohen, C. Runowicz, et al. American Cancer Society Guidelines for the Early Detection of Cancer: Update of Early Detection Guidelines for Prostate, Colorectal, and Endometrial Cancers: ALSO: Update 2001--Testing for Early Lung Cancer Detection CA Cancer J Clin, January 1, 2001; 51(1): 38 - 75. [Abstract] [Full Text] [PDF]
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R. R. Barakat, T. A. Gilewski, L. Almadrones, P. E. Saigo, E. Venkatraman, C. Hudis, and W. J. Hoskins Effect of Adjuvant Tamoxifen on the Endometrium in Women With Breast Cancer: A Prospective Study Using Office Endometrial Biopsy J. Clin. Oncol., October 20, 2000; 18(20): 3459 - 3463. [Abstract] [Full Text] [PDF]
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B. Gerber, A. Krause, H. Muller, T. Reimer, T. Kulz, J. Makovitzky, G. Kundt, and K. Friese Effects of Adjuvant Tamoxifen on the Endometrium in Postmenopausal Women With Breast Cancer: A Prospective Long-Term Study Using Transvaginal Ultrasound J. Clin. Oncol., October 20, 2000; 18(20): 3464 - 3470. [Abstract] [Full Text] [PDF]
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K. Holli, R. Valavaara, G. Blanco, V. Kataja, P. Hietanen, M. Flander, E. Pukkala, and H. Joensuu Safety and Efficacy Results of a Randomized Trial Comparing Adjuvant Toremifene and Tamoxifen in Postmenopausal Patients With Node-Positive Breast Cancer J. Clin. Oncol., October 20, 2000; 18(20): 3487 - 3494. [Abstract] [Full Text] [PDF]
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H. J. Burstein and E. P. Winer Primary Care for Survivors of Breast Cancer N. Engl. J. Med., October 12, 2000; 343(15): 1086 - 1094. [Full Text] [PDF]
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C. K. Osborne and S. A. W. Fuqua Selective Estrogen Receptor Modulators: Structure, Function, and Clinical Use J. Clin. Oncol., September 17, 2000; 18(17): 3172 - 3186. [Abstract] [Full Text] [PDF]
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 A. U. Buzdar Tamoxifen's Clinical Applications: Old and New Arch Fam Med, September 1, 2000; 9(9): 906 - 912. [Abstract] [Full Text] [PDF]
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A. Umemoto, Y. Monden, M. Suwa, Y. Kanno, M. Suzuki, C.-X. Lin, Y. Ueyama, Md.A. Momen, A. Ravindernath, S. Shibutani, et al. Identification of hepatic tamoxifen-DNA adducts in mice: {alpha}-(N2-deoxyguanosinyl)tamoxifen and {alpha}-(N2-deoxyguanosinyl)tamoxifen N-oxide Carcinogenesis, September 1, 2000; 21(9): 1737 - 1744. [Abstract] [Full Text] [PDF]
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S. Shibutani, A. Ravindernath, N. Suzuki, I. Terashima, S. M. Sugarman, A. P. Grollman, and M. L. Pearl Identification of tamoxifen-DNA adducts in the endometrium of women treated with tamoxifen Carcinogenesis, August 1, 2000; 21(8): 1461 - 1467. [Abstract] [Full Text] [PDF]
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 C. L. Walker, K. D. Burroughs, B. Davis, K. Sowell, J. I. Everitt, and R. Fuchs-Young Preclinical Evidence for Therapeutic Efficacy of Selective Estrogen receptor Modulators for Uterine Leiomyoma Reproductive Sciences, July 1, 2000; 7(4): 249 - 256. [Abstract] [PDF]
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M. Extermann, L. Balducci, and G. H. Lyman What Threshold for Adjuvant Therapy in Older Breast Cancer Patients? J. Clin. Oncol., April 1, 2000; 18(8): 1709 - 1717. [Abstract] [Full Text] [PDF]
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S. M. Ascher, I. Imaoka, and J. M. Lage Tamoxifen-induced Uterine Abnormalities: The Role of Imaging1 Radiology, January 1, 2000; 214(1): 29 - 38. [Abstract] [Full Text]
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L. louffe Jr. Selective Estrogen Receptor Modulators (SERMs) in Clinical Practice Reproductive Sciences, January 1, 2000; 7(1_suppl): S38 - S46. [Abstract] [PDF]
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L. Bernstein, D. Deapen, J. R. Cerhan, S. M. Schwartz, J. Liff, E. McGann-Maloney, J. A. Perlman, and L. Ford Tamoxifen Therapy for Breast Cancer and Endometrial Cancer Risk J Natl Cancer Inst, October 6, 1999; 91(19): 1654 - 1662. [Abstract] [Full Text] [PDF]
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