Skip to main content
The Yale Journal of Biology and Medicine logoLink to The Yale Journal of Biology and Medicine
. 1986 Sep-Oct;59(5):533–545.

Multiple primary cancers in Connecticut, 1935-82.

J D Boice Jr, R E Curtis, R A Kleinerman, J T Flannery, J F Fraumeni Jr
PMCID: PMC2590194  PMID: 3541409

Abstract

Recently, the National Cancer Institute published a comprehensive monograph on multiple primary cancers in Connecticut and Denmark. This paper summarizes some of the observations made on the Connecticut population. Data compiled by the Connecticut Tumor Registry have extended our knowledge about the patterns of multiple primary cancers, especially among long-term survivors of cancer and among patients with relatively rare tumors about which little information currently exists. When compared with the general Connecticut population, cancer patients had a 31 percent (RR = 1.31) increased risk of developing a second cancer and a 23 percent (RR = 1.23) elevated risk of second cancer at a different site from the first. Common environmental exposures seemed responsible for the excess occurrence of many second cancers, particularly those related to cigarette smoking, alcohol consumption, or both. For example, persons with epithelial cancers of the lung, larynx, esophagus, buccal cavity, and pharynx were particularly prone to develop new cancers in the same or contiguous tissue throughout their lifetimes. Cancers of the colon, uterine corpus, breast, and ovary frequently occurred together, suggesting underlying hormonal or dietary influences. Only patients with prostate cancer were at significantly low risk for second cancer development; this might be an artifact of case finding, since advanced age at initial diagnosis was generally associated with an underascertainment of second cancers. Radiotherapy may have caused rectal and other cancer among patients with cancers of the female genital tract, and leukemia among patients with uterine corpus cancer. Chemotherapy with alkylating agents probably contributed to the excess of acute nonlymphocytic leukemia following multiple myeloma or cancers of the breast and ovary. Genetic susceptibility seemed to explain some tumor complexes, such as the multiple occurrences of cutaneous melanoma and the excess of bone cancer following retinoblastoma. Research into multiple cancer syndromes should enhance our understanding of carcinogenic factors and mechanisms and the development of strategies for cancer prevention and control.

Full text

PDF
533

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbey L. M., Schwab B. H., Landau G. C., Perkins E. R. Incidence of second primary breast cancer among patients with a first primary salivary gland tumor. Cancer. 1984 Oct 1;54(7):1439–1442. doi: 10.1002/1097-0142(19841001)54:7<1439::aid-cncr2820540735>3.0.co;2-9. [DOI] [PubMed] [Google Scholar]
  2. Abramson D. H., Ellsworth R. M., Kitchin F. D., Tung G. Second nonocular tumors in retinoblastoma survivors. Are they radiation-induced? Ophthalmology. 1984 Nov;91(11):1351–1355. doi: 10.1016/s0161-6420(84)34127-6. [DOI] [PubMed] [Google Scholar]
  3. Anderson T. C., Jones S. E., Soehnlen B. J., Moon T. E., Griffith K., Stanley P. Immunocompetence and malignant lymphoma: immunologic status before therapy. Cancer. 1981 Dec 15;48(12):2702–2709. doi: 10.1002/1097-0142(19811215)48:12<2702::aid-cncr2820481224>3.0.co;2-l. [DOI] [PubMed] [Google Scholar]
  4. Berg J. W., Hutter R. V., Foote F. W., Jr The unique association between salivary gland cancer and breast cancer. JAMA. 1968 May 27;204(9):771–774. [PubMed] [Google Scholar]
  5. Berg J. W., Schottenfeld D., Ritter F. Incidence of multiple primary cancers. III. Cancers of the respiratory and upper digestive system as multiple primary cancers. J Natl Cancer Inst. 1970 Feb;44(2):263–274. [PubMed] [Google Scholar]
  6. Bergsagel D. E., Bailey A. J., Langley G. R., MacDonald R. N., White D. F., Miller A. B. The chemotherapy on plasma-cell myeloma and the incidence of acute leukemia. N Engl J Med. 1979 Oct 4;301(14):743–748. doi: 10.1056/NEJM197910043011402. [DOI] [PubMed] [Google Scholar]
  7. Biggar R. J., Curtis R. E., Hoffman D. A., Flannery J. T. Second primary malignancies following salivary gland cancers. Br J Cancer. 1983 Mar;47(3):383–386. doi: 10.1038/bjc.1983.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boice J. D., Jr, Day N. E., Andersen A., Brinton L. A., Brown R., Choi N. W., Clarke E. A., Coleman M. P., Curtis R. E., Flannery J. T. Second cancers following radiation treatment for cervical cancer. An international collaboration among cancer registries. J Natl Cancer Inst. 1985 May;74(5):955–975. [PubMed] [Google Scholar]
  9. Boice J. D., Jr, Fraumeni J. F., Jr Second cancer following cancer of the respiratory system in Connecticut, 1935-1982. Natl Cancer Inst Monogr. 1985 Dec;68:83–98. [PubMed] [Google Scholar]
  10. Boice J. D., Jr, Greene M. H., Killen J. Y., Jr, Ellenberg S. S., Keehn R. J., McFadden E., Chen T. T., Fraumeni J. F., Jr Leukemia and preleukemia after adjuvant treatment of gastrointestinal cancer with semustine (methyl-CCNU). N Engl J Med. 1983 Nov 3;309(18):1079–1084. doi: 10.1056/NEJM198311033091802. [DOI] [PubMed] [Google Scholar]
  11. Boice J. D., Jr, Storm H. H., Curtis R. E., Jensen O. M., Kleinerman R. A., Jensen H. S., Flannery J. T., Fraumeni J. F., Jr Introduction to the study of multiple primary cancers. Natl Cancer Inst Monogr. 1985 Dec;68:3–9. [PubMed] [Google Scholar]
  12. Chak L. Y., Sikic B. I., Tucker M. A., Horns R. C., Jr, Cox R. S. Increased incidence of acute nonlymphocytic leukemia following therapy in patients with small cell carcinoma of the lung. J Clin Oncol. 1984 May;2(5):385–390. doi: 10.1200/JCO.1984.2.5.385. [DOI] [PubMed] [Google Scholar]
  13. Coleman C. N. Secondary neoplasms in patients treated for cancer: etiology and perspective. Radiat Res. 1982 Oct;92(1):188–200. [PubMed] [Google Scholar]
  14. Curtis R. E., Boice J. D., Jr, Kleinerman R. A., Flannery J. T., Fraumeni J. F., Jr Summary: multiple primary cancers in Connecticut, 1935-82. Natl Cancer Inst Monogr. 1985 Dec;68:219–242. [PubMed] [Google Scholar]
  15. Curtis R. E., Hankey B. F., Myers M. H., Young J. L., Jr Risk of leukemia associated with the first course of cancer treatment: an analysis of the Surveillance, Epidemiology, and End Results Program experience. J Natl Cancer Inst. 1984 Mar;72(3):531–544. [PubMed] [Google Scholar]
  16. Curtis R. E., Hoover R. N., Kleinerman R. A., Harvey E. B. Second cancer following cancer of the female genital system in Connecticut, 1935-82. Natl Cancer Inst Monogr. 1985 Dec;68:113–137. [PubMed] [Google Scholar]
  17. Ewertz M., Machado S. G., Boice J. D., Jr, Jensen O. M. Endometrial cancer following treatment for breast cancer: a case-control study in Denmark. Br J Cancer. 1984 Nov;50(5):687–692. doi: 10.1038/bjc.1984.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fisher B., Rockette H., Fisher E. R., Wickerham D. L., Redmond C., Brown A. Leukemia in breast cancer patients following adjuvant chemotherapy or postoperative radiation: the NSABP experience. J Clin Oncol. 1985 Dec;3(12):1640–1658. doi: 10.1200/JCO.1985.3.12.1640. [DOI] [PubMed] [Google Scholar]
  19. Fraumeni J. F., Jr, Hoover R. Immunosurveillance and cancer: epidemiologic observations. Natl Cancer Inst Monogr. 1977 Dec;47:121–126. [PubMed] [Google Scholar]
  20. Fuchs E. F., Kay R., Poole R., Barry J. M., Pearse H. D. Uroepithelial carcinoma in association with cyclophosphamide ingestion. J Urol. 1981 Oct;126(4):544–545. doi: 10.1016/s0022-5347(17)54619-4. [DOI] [PubMed] [Google Scholar]
  21. Greene M. H., Boice J. D., Jr, Greer B. E., Blessing J. A., Dembo A. J. Acute nonlymphocytic leukemia after therapy with alkylating agents for ovarian cancer: a study of five randomized clinical trials. N Engl J Med. 1982 Dec 2;307(23):1416–1421. doi: 10.1056/NEJM198212023072302. [DOI] [PubMed] [Google Scholar]
  22. Greene M. H., Glaubiger D. L., Mead G. D., Fraumeni J. F., Jr Subsequent cancer in patients with Ewing's sarcoma. Cancer Treat Rep. 1979 Nov-Dec;63(11-12):2043–2046. [PubMed] [Google Scholar]
  23. Greene M. H., Hoover R. N., Fraumeni J. F., Jr Subsequent cancer in patients with chronic lymphocytic leukemia--a possible immunologic mechanism. J Natl Cancer Inst. 1978 Aug;61(2):337–340. [PubMed] [Google Scholar]
  24. Greene M. H., Wilson J. Second cancer following lymphatic and hematopoietic cancers in Connecticut, 1935-82. Natl Cancer Inst Monogr. 1985 Dec;68:191–217. [PubMed] [Google Scholar]
  25. Greene M. H., Young R. C., Merrill J. M., DeVita V. T. Evidence of a treatment dose response in acute nonlymphocytic leukemias which occur after therapy of non-Hodgkin's lymphoma. Cancer Res. 1983 Apr;43(4):1891–1898. [PubMed] [Google Scholar]
  26. Harvey E. B., Brinton L. A. Second cancer following cancer of the breast in Connecticut, 1935-82. Natl Cancer Inst Monogr. 1985 Dec;68:99–112. [PubMed] [Google Scholar]
  27. Hoar S. K., Wilson J., Blot W. J., McLaughlin J. K., Winn D. M., Kantor A. F. Second cancer following cancer of the digestive system in Connecticut, 1935-82. Natl Cancer Inst Monogr. 1985 Dec;68:49–82. [PubMed] [Google Scholar]
  28. Hoover R., Fraumeni J. F., Everson R., Myers M. H. Cancer of the uterine corpus after hormonal treatment for breast cancer. Lancet. 1976 Apr 24;1(7965):885–887. doi: 10.1016/s0140-6736(76)92099-7. [DOI] [PubMed] [Google Scholar]
  29. Kim J. H., Chu F. C., Woodard H. Q., Melamed M. R., Huvos A., Cantin J. Radiation-induced soft-tissue and bone sarcoma. Radiology. 1978 Nov;129(2):501–508. doi: 10.1148/129.2.501. [DOI] [PubMed] [Google Scholar]
  30. Krikorian J. G., Burke J. S., Rosenberg S. A., Kaplan H. S. Occurrence of non-Hodgkin's lymphoma after therapy for Hodgkin's disease. N Engl J Med. 1979 Mar 1;300(9):452–458. doi: 10.1056/NEJM197903013000902. [DOI] [PubMed] [Google Scholar]
  31. Li F. P., Fraumen J. F., Jr Letter: Familial breast cancer, soft-tissue sarcomas, and other neoplasms. Ann Intern Med. 1975 Dec;83(6):833–834. doi: 10.7326/0003-4819-83-6-833_2. [DOI] [PubMed] [Google Scholar]
  32. Li F. P. Second malignant tumors after cancer in childhood. Cancer. 1977 Oct;40(4 Suppl):1899–1902. doi: 10.1002/1097-0142(197710)40:4+<1899::aid-cncr2820400821>3.0.co;2-u. [DOI] [PubMed] [Google Scholar]
  33. MacMahon B., Austin J. H. Association of carcinomas of the breast and corpus uteri. Cancer. 1969 Feb;23(2):275–280. doi: 10.1002/1097-0142(196902)23:2<275::aid-cncr2820230204>3.0.co;2-s. [DOI] [PubMed] [Google Scholar]
  34. McMichael A. J., Potter J. D. Reproduction, endogenous and exogenous sex hormones, and colon cancer: a review and hypothesis. J Natl Cancer Inst. 1980 Dec;65(6):1201–1207. [PubMed] [Google Scholar]
  35. Moertel C. G., Elveback L. R. The association between salivary gland cancer and breast cancer. JAMA. 1969 Oct 13;210(2):306–308. [PubMed] [Google Scholar]
  36. Prior P., Waterhouse J. A. Multiple primary cancers of the breast and ovary. Br J Cancer. 1981 Nov;44(5):628–636. doi: 10.1038/bjc.1981.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Prior P., Waterhouse J. A. Second primary cancers in patients with tumours of the salivary glands. Br J Cancer. 1977 Sep;36(3):362–368. doi: 10.1038/bjc.1977.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schoenberg B. S., Greenberg R. A., Eisenberg H. Occurrence of certain multiple primary cancers in females. J Natl Cancer Inst. 1969 Jul;43(1):15–32. doi: 10.1093/jnci/43.1.15. [DOI] [PubMed] [Google Scholar]
  39. Schottenfeld D., Berg J. Incidence of miltiple primary cancers. IV. Cancers of the female breast and genital organs. J Natl Cancer Inst. 1971 Jan;46(1):161–170. [PubMed] [Google Scholar]
  40. Schottenfeld D., Gantt R. C., Wyner E. L. The role of alcohol and tobacco in multiple primary cancers of the upper digestive system, larynx and lung: a prospective study. Prev Med. 1974 Jun;3(2):277–293. doi: 10.1016/0091-7435(74)90037-1. [DOI] [PubMed] [Google Scholar]
  41. Tester W. J., Kinsella T. J., Waller B., Makuch R. W., Kelley P. A., Glatstein E., DeVita V. T. Second malignant neoplasms complicating Hodgkin's disease: the National Cancer Institute experience. J Clin Oncol. 1984 Jul;2(7):762–769. doi: 10.1200/JCO.1984.2.7.762. [DOI] [PubMed] [Google Scholar]
  42. Tucker M. A., Boice J. D., Jr, Hoffman D. A. Second cancer following cutaneous melanoma and cancers of the brain, thyroid, connective tissue, bone, and eye in Connecticut, 1935-82. Natl Cancer Inst Monogr. 1985 Dec;68:161–189. [PubMed] [Google Scholar]
  43. Willett W. C., MacMahon B. Diet and cancer--an overview (second of two parts). N Engl J Med. 1984 Mar 15;310(11):697–703. doi: 10.1056/NEJM198403153101106. [DOI] [PubMed] [Google Scholar]
  44. Wynder E. L., Dodo H., Bloch D. A., Gantt R. C., Moore O. S. Epidemiologic investigation of multiple primary cancer of the upper alimentary and respiratory tracts. I. A retrospective study. Cancer. 1969 Oct;24(4):730–739. doi: 10.1002/1097-0142(196910)24:4<730::aid-cncr2820240411>3.0.co;2-l. [DOI] [PubMed] [Google Scholar]
  45. Wynder E. L., Mushinski M. H., Spivak J. C. Tobacco and alcohol consumption in relation to the development of multiple primary cancers. Cancer. 1977 Oct;40(4 Suppl):1872–1878. doi: 10.1002/1097-0142(197710)40:4+<1872::aid-cncr2820400817>3.0.co;2-#. [DOI] [PubMed] [Google Scholar]

Articles from The Yale Journal of Biology and Medicine are provided here courtesy of Yale Journal of Biology and Medicine

RESOURCES