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The Impact of Family History on Ovarian Cancer Risk: The Utah Population Database

The Impact of Family History on Ovarian Cancer Risk: The Utah Population Database Abstract Objective: To estimate the relative risks and population attributable risks of ovarian cancer associated with family histories of cancer at several sites. Methods: A matched case-control analytic study (662 cases, 2647 controls), employing the Utah Population Database, a genealogy of approximately 1 million individuals linked to cancer incidence data from the Utah Cancer Registry. Family history was assessed using kinship order and a kinship-weighted familial standardized incidence ratio statistic. Results: Family histories of ovarian, uterine, breast, and pancreatic cancer were significantly associated with increased risk of ovarian cancer. The relative risk of ovarian cancer was 4.31 (95% confidence interval [CI], 2.35 to 7.90) for women with a first-degree relative with ovarian cancer, 2.12 (95% CI, 1.19 to 3.78) for women with an affected second-degree relative, and 1.48 (95% CI, 0.98 to 2.24) for women with an affected third-degree relative. The odds ratio (OR) was 2.06 (95% CI, 1.44 to 2.93) for those with the highest familial standardized incidence ratio. No age differences were observed between cases with and without a family history of ovarian cancer. There was substantial heterogeneity of family history effects by cell type. Increased parity was not protective among women with a strong family history of cancer at the sites studied (OR, 1.11; 95% CI, 0.38 to 3.26), although it was protective among women without a family history of these cancers (OR, 0.29; 95% CI, 0.11 to 0.62). Conclusions: The risk of ovarian cancer was substantially increased among women with family histories of ovarian, uterine, pancreatic, and, to a lesser degree, breast cancer. Among women with family histories of any of these cancers, the risk of ovarian cancer is not diminished by high parity.(Arch Intern Med. 1995;155:905-912) References 1. Berek JS, Dembo A, Ozols RF. Ovarian cancer. In: Holland JF, Frei E III, Bast RC Jr, Kufe DW, Morton DL, Weichselbaum RR, eds. Cancer Medicine . 3rd ed. Philadelphia, Pa: Lea & Febiger; 1993:1659-1690. 2. Utah Cancer Registry. Cancer in Utah 1966-1990 . Salt Lake City, Utah: Utah Cancer Registry; 1992. 3. Cramer DW, Hutchison GB, Welch WR, Scully RE, Ryan KJ. Determinants of ovarian cancer risk, I: reproductive experiences and family history. J Natl Cancer Inst . 1983;71:711-716. 4. Polychronopoulou A, Tzonou A, Hsieh CC, et al. Reproductive variables, tobacco, ethanol, coffee and somatometry as risk factors for ovarian cancer. Int J Cancer . 1993;55:402-407.Crossref 5. Wu ML, Whittemore AS, Paffenbarger RS Jr, et al. Personal and environmental characteristics related to epithelial ovarian cancer, I: reproductive and menstrual events and oral contraceptive use. Am J Epidemiol . 1988;128:1216-1227. 6. Whittemore AS, Harris R, Itnyre J, and the Collaborative Ovarian Cancer Group. Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies, II: invasive epithelial ovarian cancers in white women [see comments]. Am J Epidemiol . 1992;136:1184-1203. 7. Hartge P, Schiffman MH, Hoover R, McGowan L, Lesher L, Norris HJ. A case-control study of epithelial ovarian cancer. Am J Obstet Gynecol . 1989;161:10-16.Crossref 8. Mori M, Harabuchi I, Miyake H, Casagrande JT, Henderson BE, Ross RK. Reproductive, genetic, and dietary risk factors for ovarian cancer. Am J Epidemiol . 1988;128:771-777.Crossref 9. Oral contraceptive use and the risk of ovarian cancer: the Centers for Disease Control Cancer and Steroid Hormone Study. JAMA . 1983;249:1596-1599.Crossref 10. The reduction in risk of ovarian cancer associated with oral-contraceptive use: The Cancer and Steroid Hormone Study of the Centers for Disease Control and the National Institute of Child Health and Human Development. N Engl J Med . 1987;316:650-655.Crossref 11. Cramer DW, Hutchison GB, Welch WR, Scully RE, Knapp RC. Factors affecting the association of oral contraceptives and ovarian cancer. N Engl J Med . 1982; 307:1047-1051.Crossref 12. Tzonou A, Day NE, Trichopoulos D, et al. The epidemiology of ovarian cancer in Greece: a case-control study. Eur J Cancer Clin Oncol . 1984;20:1045-1052.Crossref 13. Koch M, Gaedke H, Jenkins H. Family history of ovarian cancer patients: a case-control study. Int J Epidemiol . 1989;18:782-785.Crossref 14. McGowan L, Norris HJ, Hartge P, Hoover R, Lesher L. Risk factors in ovarian cancer. Eur J Gynaecol Oncol . 1988;9:195-199. 15. Schildkraut JM, Thompson WD. Familial ovarian cancer: a population-based case-control study [see comments]. Am J Epidemiol . 1988;128:456-466. 16. Hildreth NG, Kelsey JL, Livolsi VA, et al. An epidemiologic study of epithelial carcinoma of the ovary. Am J Epidemiol . 1981;114:398-405. 17. Casagrande JT, Pike MC, Ross RK, et al. 'Incessant ovulation' and ovarian cancer. Lancet . 1979;2:170-173.Crossref 18. Cramer DW. Lactase persistence and milk consumption as determinants of ovarian cancer risk. Am J Epidemiol . 1989;130:904-910. 19. Slattery ML, Schuman KL, West DW, French TK, Robison LM. Nutrient intake and ovarian cancer. Am J Epidemiol . 1989;130:497-502. 20. Engle A, Muscat JE, Harris RE. Nutritional risk factors and ovarian cancer. Nutr Cancer . 1991;15:239-247.Crossref 21. La-Vecchia C, Decarli A, Negri E, et al. Dietary factors and the risk of epithelial ovarian cancer. J Natl Cancer Inst . 1987;79:663-669. 22. Parazzini F, Negri E, La-Vecchia C, Restelli C, Franceschi S. Family history of reproductive cancers and ovarian cancer risk: an Italian case-control study. Am J Epidemiol . 1992;135:35-40. 23. Cramer DW, Harlow BL, Willett WC, et al. Galactose consumption and metabolism in relation to the risk of ovarian cancer [see comments]. Lancet . 1989; 2:66-71.Crossref 24. La Vecchia C, Negri E, Franceschi S, Parazzini F, Gentile A, Fasoli M. Alcohol and epithelial ovarian cancer. J Clin Epidemiol . 1992;45:1025-1030.Crossref 25. Byers T, Marshall J, Graham S, Mettlin C, Swanson M. A case-control study of dietary and nondietary factors in ovarian cancer. J Natl Cancer Inst . 1983;71: 681-686. 26. Miller DR, Rosenberg L, Kaufman DW, et al. Epithelial ovarian cancer and coffee drinking. Int J Epidemiol . 1987;16:13-17.Crossref 27. Whittemore AS, Wu ML, Paffenbarger RS Jr, et al. Personal and environmental characteristics related to epithelial ovarian cancer, II: exposures to talcum powder, tobacco, alcohol, and coffee. Am J Epidemiol . 1988;128:1228-1240. 28. Skolnick M. The Utah Population Database: a resource for genetic epidemiology. In: Cairns J, Lyon JL, Skolnick M, eds. Banbury Report Number Four: Cancer Incidence in Defined Populations . Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1980:285-297. 29. International Classification of Diseases of Oncology . Geneva, Switzerland: World Health Organization; 1976. 30. Malecot G. Les mathematiques de l'heredite . New York, NY: Masson Publishing USA Inc; 1948. 31. Breslow NE, Day NE. Statistical Methods in Cancer Research: The Design and Analysis of Cohort Studies . Lyon, France: International Agency for Research on Cancer; 1987;2. 32. Preston DL, Lubin JH, Pierce DA. EPICURE: Generalized Regression Models for Epidemiologic Data . Seattle, Wash: Hirosoft International; 1992. 33. Bruzzi P, Green SB, Byar DP, Brinton LA, Schairer C. Estimating the population attributable risk for multiple risk factors using case-control data. Am J Epidemiol . 1985;122:904-914. 34. Knudson AG Jr. The genetic predisposition to cancer. Birth Defects . 1989;25: 15-27. 35. Peltomaki P, Lothe RA, Aaltonen LA, et al. Microsatellite instability is associated with tumors that characterize the hereditary non-polyposis colorectal carcinoma syndrome. Cancer Res . 1993;53:5853-5855. 36. Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci US A . 1993;90:7915-7922.Crossref 37. Lynch HT, Watson P, Lynch JF, Conway TA, Fili M. Hereditary ovarian cancer: heterogeneity in age at onset. Cancer . 1993;71( (suppl) ):573-581.Crossref 38. Piver MS, Baker TR, Jishi MF, et al. Familial ovarian cancer: a report of 658 families from the Gilda Radner Familial Ovarian Cancer Registry 1981-1991. Cancer . 1993;71( (suppl) ):582-588.Crossref 39. Amos CI, Shaw GL, Tucker MA, Hartge P. Age at onset for familial epithelial ovarian cancer. JAMA . 1992;268:1896-1899.Crossref 40. Amos CI, Struewing JP. Genetic epidemiology of epithelial ovarian cancer. Cancer . 1993;71( (suppl) ):566-572.Crossref 41. Feunteun J, Narod SA, Lynch HT, et al. A breast-ovarian cancer susceptibility gene maps to chromosome 17q21. Am J Hum Genet . 1993;52:736-742. 42. Easton DF, Bishop DT, Ford D, Crockford GP, and the Breast Cancer Linkage Consortium. Genetic linkage analysis in familial breast and ovarian cancer: results from 214 families. Am J Hum Genet . 1993;52:678-701. 43. Goldgar DE, Cannon-Albright LA, Oliphant A, et al. Chromosome 17q linkage studies of 18 Utah breast cancer kindreds. Am J Hum Genet . 1993;52:743-748. 44. Risinger JI, Berchuck A, Kohler MF, Watson P, Lynch HT, Boyd J. Genetic instability of microsatellites in endometrial carcinoma. Cancer Res . 1993;53: 5100-5103. 45. Potter JD, Slattery ML, Bostick RM, Gapstur SM. Colon cancer: a review of the epidemiology. Epidemiol Rev . 1993;15:499-545. 46. Malkin D, Li FP, Strong LC, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms [see comments]. Science . 1990;250:1233-1238.Crossref 47. Borresen AL. Oncogenesis in ovarian cancer. Acta Obstet Gynecol Scand . 1992; 71( (suppl 155) ):25-30. 48. Jolly KW, Malkin D, Douglass EC, Brown TF, Sinclair AE, Look AT. Splice-site mutation of the p53 gene in a family with hereditary breast-ovarian cancer. Oncogene . 1994;9:97-102. 49. Narod S, Tonin P, Lynch H, Watson P, Feunteun J, Lenoir G. Histology of BRCA1-associated ovarian tumours. Lancet . 1994;343:236.Crossref 50. Saito S, Saito H, Koi S, et al. Fine-scale deletion mapping of the distal long arm of chromosome 6 in 70 human ovarian cancers. Cancer Res . 1992;52: 5815-5817. 51. Gardner WU. Hormonal imbalances in tumorigenesis. Cancer Res . 1948;8: 397. 52. Cramer DW, Welch WR. Determinants of ovarian cancer risk, II: inferences regarding pathogenesis. J Natl Cancer Inst . 1983;71:717-721. 53. Fathalla MF. Incessant ovulation: a factor in ovarian neoplasia? Lancet . 1971; 2:163.Crossref 54. Preston-Martin S, Pike MC, Ross RK, Henderson BE. Epidemiologic evidence for the increased cell proliferation model of carcinogenesis. Prog Clin Biol Res . 1991;369:21-34. 55. Whittemore AS, Wu ML, Paffenbarger RS Jr, et al. Epithelial ovarian cancer and the ability to conceive. Cancer Res . 1989;49:4047-4052. 56. Whittemore AS, Harris R, Itnyre J, and the Collaborative Ovarian Cancer Group. Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies, IV: the pathogenesis of epithelial ovarian cancer. Am J Epidemiol . 1992;136:1212-1220. 57. Greggi S, Genuardi M, Benedetti-Panici P, et al. Analysis of 138 consecutive ovarian cancer patients: incidence and characteristics of familial cases. Gynecol Oncol . 1990;39:300-304.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Internal Medicine American Medical Association

The Impact of Family History on Ovarian Cancer Risk: The Utah Population Database

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Publisher
American Medical Association
Copyright
Copyright © 1995 American Medical Association. All Rights Reserved.
ISSN
0003-9926
eISSN
1538-3679
DOI
10.1001/archinte.1995.00430090034005
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Abstract

Abstract Objective: To estimate the relative risks and population attributable risks of ovarian cancer associated with family histories of cancer at several sites. Methods: A matched case-control analytic study (662 cases, 2647 controls), employing the Utah Population Database, a genealogy of approximately 1 million individuals linked to cancer incidence data from the Utah Cancer Registry. Family history was assessed using kinship order and a kinship-weighted familial standardized incidence ratio statistic. Results: Family histories of ovarian, uterine, breast, and pancreatic cancer were significantly associated with increased risk of ovarian cancer. The relative risk of ovarian cancer was 4.31 (95% confidence interval [CI], 2.35 to 7.90) for women with a first-degree relative with ovarian cancer, 2.12 (95% CI, 1.19 to 3.78) for women with an affected second-degree relative, and 1.48 (95% CI, 0.98 to 2.24) for women with an affected third-degree relative. The odds ratio (OR) was 2.06 (95% CI, 1.44 to 2.93) for those with the highest familial standardized incidence ratio. No age differences were observed between cases with and without a family history of ovarian cancer. There was substantial heterogeneity of family history effects by cell type. Increased parity was not protective among women with a strong family history of cancer at the sites studied (OR, 1.11; 95% CI, 0.38 to 3.26), although it was protective among women without a family history of these cancers (OR, 0.29; 95% CI, 0.11 to 0.62). Conclusions: The risk of ovarian cancer was substantially increased among women with family histories of ovarian, uterine, pancreatic, and, to a lesser degree, breast cancer. Among women with family histories of any of these cancers, the risk of ovarian cancer is not diminished by high parity.(Arch Intern Med. 1995;155:905-912) References 1. Berek JS, Dembo A, Ozols RF. Ovarian cancer. In: Holland JF, Frei E III, Bast RC Jr, Kufe DW, Morton DL, Weichselbaum RR, eds. Cancer Medicine . 3rd ed. Philadelphia, Pa: Lea & Febiger; 1993:1659-1690. 2. Utah Cancer Registry. Cancer in Utah 1966-1990 . Salt Lake City, Utah: Utah Cancer Registry; 1992. 3. Cramer DW, Hutchison GB, Welch WR, Scully RE, Ryan KJ. Determinants of ovarian cancer risk, I: reproductive experiences and family history. J Natl Cancer Inst . 1983;71:711-716. 4. Polychronopoulou A, Tzonou A, Hsieh CC, et al. Reproductive variables, tobacco, ethanol, coffee and somatometry as risk factors for ovarian cancer. Int J Cancer . 1993;55:402-407.Crossref 5. Wu ML, Whittemore AS, Paffenbarger RS Jr, et al. Personal and environmental characteristics related to epithelial ovarian cancer, I: reproductive and menstrual events and oral contraceptive use. Am J Epidemiol . 1988;128:1216-1227. 6. Whittemore AS, Harris R, Itnyre J, and the Collaborative Ovarian Cancer Group. Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies, II: invasive epithelial ovarian cancers in white women [see comments]. Am J Epidemiol . 1992;136:1184-1203. 7. Hartge P, Schiffman MH, Hoover R, McGowan L, Lesher L, Norris HJ. A case-control study of epithelial ovarian cancer. Am J Obstet Gynecol . 1989;161:10-16.Crossref 8. Mori M, Harabuchi I, Miyake H, Casagrande JT, Henderson BE, Ross RK. Reproductive, genetic, and dietary risk factors for ovarian cancer. Am J Epidemiol . 1988;128:771-777.Crossref 9. Oral contraceptive use and the risk of ovarian cancer: the Centers for Disease Control Cancer and Steroid Hormone Study. JAMA . 1983;249:1596-1599.Crossref 10. The reduction in risk of ovarian cancer associated with oral-contraceptive use: The Cancer and Steroid Hormone Study of the Centers for Disease Control and the National Institute of Child Health and Human Development. N Engl J Med . 1987;316:650-655.Crossref 11. Cramer DW, Hutchison GB, Welch WR, Scully RE, Knapp RC. Factors affecting the association of oral contraceptives and ovarian cancer. N Engl J Med . 1982; 307:1047-1051.Crossref 12. Tzonou A, Day NE, Trichopoulos D, et al. The epidemiology of ovarian cancer in Greece: a case-control study. Eur J Cancer Clin Oncol . 1984;20:1045-1052.Crossref 13. Koch M, Gaedke H, Jenkins H. Family history of ovarian cancer patients: a case-control study. Int J Epidemiol . 1989;18:782-785.Crossref 14. McGowan L, Norris HJ, Hartge P, Hoover R, Lesher L. Risk factors in ovarian cancer. Eur J Gynaecol Oncol . 1988;9:195-199. 15. Schildkraut JM, Thompson WD. Familial ovarian cancer: a population-based case-control study [see comments]. Am J Epidemiol . 1988;128:456-466. 16. Hildreth NG, Kelsey JL, Livolsi VA, et al. An epidemiologic study of epithelial carcinoma of the ovary. Am J Epidemiol . 1981;114:398-405. 17. Casagrande JT, Pike MC, Ross RK, et al. 'Incessant ovulation' and ovarian cancer. Lancet . 1979;2:170-173.Crossref 18. Cramer DW. Lactase persistence and milk consumption as determinants of ovarian cancer risk. Am J Epidemiol . 1989;130:904-910. 19. Slattery ML, Schuman KL, West DW, French TK, Robison LM. Nutrient intake and ovarian cancer. Am J Epidemiol . 1989;130:497-502. 20. Engle A, Muscat JE, Harris RE. Nutritional risk factors and ovarian cancer. Nutr Cancer . 1991;15:239-247.Crossref 21. La-Vecchia C, Decarli A, Negri E, et al. Dietary factors and the risk of epithelial ovarian cancer. J Natl Cancer Inst . 1987;79:663-669. 22. Parazzini F, Negri E, La-Vecchia C, Restelli C, Franceschi S. Family history of reproductive cancers and ovarian cancer risk: an Italian case-control study. Am J Epidemiol . 1992;135:35-40. 23. Cramer DW, Harlow BL, Willett WC, et al. Galactose consumption and metabolism in relation to the risk of ovarian cancer [see comments]. Lancet . 1989; 2:66-71.Crossref 24. La Vecchia C, Negri E, Franceschi S, Parazzini F, Gentile A, Fasoli M. Alcohol and epithelial ovarian cancer. J Clin Epidemiol . 1992;45:1025-1030.Crossref 25. Byers T, Marshall J, Graham S, Mettlin C, Swanson M. A case-control study of dietary and nondietary factors in ovarian cancer. J Natl Cancer Inst . 1983;71: 681-686. 26. Miller DR, Rosenberg L, Kaufman DW, et al. Epithelial ovarian cancer and coffee drinking. Int J Epidemiol . 1987;16:13-17.Crossref 27. Whittemore AS, Wu ML, Paffenbarger RS Jr, et al. Personal and environmental characteristics related to epithelial ovarian cancer, II: exposures to talcum powder, tobacco, alcohol, and coffee. Am J Epidemiol . 1988;128:1228-1240. 28. Skolnick M. The Utah Population Database: a resource for genetic epidemiology. In: Cairns J, Lyon JL, Skolnick M, eds. Banbury Report Number Four: Cancer Incidence in Defined Populations . Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1980:285-297. 29. International Classification of Diseases of Oncology . Geneva, Switzerland: World Health Organization; 1976. 30. Malecot G. Les mathematiques de l'heredite . New York, NY: Masson Publishing USA Inc; 1948. 31. Breslow NE, Day NE. Statistical Methods in Cancer Research: The Design and Analysis of Cohort Studies . Lyon, France: International Agency for Research on Cancer; 1987;2. 32. Preston DL, Lubin JH, Pierce DA. EPICURE: Generalized Regression Models for Epidemiologic Data . Seattle, Wash: Hirosoft International; 1992. 33. Bruzzi P, Green SB, Byar DP, Brinton LA, Schairer C. Estimating the population attributable risk for multiple risk factors using case-control data. Am J Epidemiol . 1985;122:904-914. 34. Knudson AG Jr. The genetic predisposition to cancer. Birth Defects . 1989;25: 15-27. 35. Peltomaki P, Lothe RA, Aaltonen LA, et al. Microsatellite instability is associated with tumors that characterize the hereditary non-polyposis colorectal carcinoma syndrome. Cancer Res . 1993;53:5853-5855. 36. Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci US A . 1993;90:7915-7922.Crossref 37. Lynch HT, Watson P, Lynch JF, Conway TA, Fili M. Hereditary ovarian cancer: heterogeneity in age at onset. Cancer . 1993;71( (suppl) ):573-581.Crossref 38. Piver MS, Baker TR, Jishi MF, et al. Familial ovarian cancer: a report of 658 families from the Gilda Radner Familial Ovarian Cancer Registry 1981-1991. Cancer . 1993;71( (suppl) ):582-588.Crossref 39. Amos CI, Shaw GL, Tucker MA, Hartge P. Age at onset for familial epithelial ovarian cancer. JAMA . 1992;268:1896-1899.Crossref 40. Amos CI, Struewing JP. Genetic epidemiology of epithelial ovarian cancer. Cancer . 1993;71( (suppl) ):566-572.Crossref 41. Feunteun J, Narod SA, Lynch HT, et al. A breast-ovarian cancer susceptibility gene maps to chromosome 17q21. Am J Hum Genet . 1993;52:736-742. 42. Easton DF, Bishop DT, Ford D, Crockford GP, and the Breast Cancer Linkage Consortium. Genetic linkage analysis in familial breast and ovarian cancer: results from 214 families. Am J Hum Genet . 1993;52:678-701. 43. Goldgar DE, Cannon-Albright LA, Oliphant A, et al. Chromosome 17q linkage studies of 18 Utah breast cancer kindreds. Am J Hum Genet . 1993;52:743-748. 44. Risinger JI, Berchuck A, Kohler MF, Watson P, Lynch HT, Boyd J. Genetic instability of microsatellites in endometrial carcinoma. Cancer Res . 1993;53: 5100-5103. 45. Potter JD, Slattery ML, Bostick RM, Gapstur SM. Colon cancer: a review of the epidemiology. Epidemiol Rev . 1993;15:499-545. 46. Malkin D, Li FP, Strong LC, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms [see comments]. Science . 1990;250:1233-1238.Crossref 47. Borresen AL. Oncogenesis in ovarian cancer. Acta Obstet Gynecol Scand . 1992; 71( (suppl 155) ):25-30. 48. Jolly KW, Malkin D, Douglass EC, Brown TF, Sinclair AE, Look AT. Splice-site mutation of the p53 gene in a family with hereditary breast-ovarian cancer. Oncogene . 1994;9:97-102. 49. Narod S, Tonin P, Lynch H, Watson P, Feunteun J, Lenoir G. Histology of BRCA1-associated ovarian tumours. Lancet . 1994;343:236.Crossref 50. Saito S, Saito H, Koi S, et al. Fine-scale deletion mapping of the distal long arm of chromosome 6 in 70 human ovarian cancers. Cancer Res . 1992;52: 5815-5817. 51. Gardner WU. Hormonal imbalances in tumorigenesis. Cancer Res . 1948;8: 397. 52. Cramer DW, Welch WR. Determinants of ovarian cancer risk, II: inferences regarding pathogenesis. J Natl Cancer Inst . 1983;71:717-721. 53. Fathalla MF. Incessant ovulation: a factor in ovarian neoplasia? Lancet . 1971; 2:163.Crossref 54. Preston-Martin S, Pike MC, Ross RK, Henderson BE. Epidemiologic evidence for the increased cell proliferation model of carcinogenesis. Prog Clin Biol Res . 1991;369:21-34. 55. Whittemore AS, Wu ML, Paffenbarger RS Jr, et al. Epithelial ovarian cancer and the ability to conceive. Cancer Res . 1989;49:4047-4052. 56. Whittemore AS, Harris R, Itnyre J, and the Collaborative Ovarian Cancer Group. Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies, IV: the pathogenesis of epithelial ovarian cancer. Am J Epidemiol . 1992;136:1212-1220. 57. Greggi S, Genuardi M, Benedetti-Panici P, et al. Analysis of 138 consecutive ovarian cancer patients: incidence and characteristics of familial cases. Gynecol Oncol . 1990;39:300-304.Crossref

Journal

Archives of Internal MedicineAmerican Medical Association

Published: May 8, 1995

References