Fertility and Sterility
Volume 92, Issue 2 , Pages 417-427 , August 2009

Effects of cancer treatment on ovarian function

  • Jaymeson S. Stroud, M.D.

      Affiliations

    • Department of Radiation Oncology, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • David Mutch, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Washington University School of Medicine, St. Louis, Missouri
    • Alvin J. Siteman Cancer Center, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Janet Rader, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Washington University School of Medicine, St. Louis, Missouri
    • Alvin J. Siteman Cancer Center, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Matt Powell, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Washington University School of Medicine, St. Louis, Missouri
    • Alvin J. Siteman Cancer Center, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Premal H. Thaker, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Washington University School of Medicine, St. Louis, Missouri
    • Alvin J. Siteman Cancer Center, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Perry W. Grigsby, M.D.

      Affiliations

    • Department of Radiation Oncology, Washington University School of Medicine, St. Louis, Missouri
    • Department of Radiology, Division of Nuclear Medicine, Washington University School of Medicine, St. Louis, Missouri
    • Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Washington University School of Medicine, St. Louis, Missouri
    • Alvin J. Siteman Cancer Center, Washington University School of Medicine, St. Louis, Missouri
    • Corresponding Author InformationReprint requests: Perry W. Grigsby, M.D., Department of Radiation Oncology, Box 8224, Mallinckrodt Institute of Radiology, Washington University School of Medicine, 4921 Parkview Place, Lower Level, St. Louis, MO 63110 (FAX: 314-747-9557).

Received 7 March 2008 ,Revised 23 June 2008 ,Accepted 9 July 2008.

References 

  1. Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER∗Stat Database: Incidence—SEER 9 Regs Public-Use, Nov 2005 Sub (1973–2003), National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2006, based on the November 2005 submission.
  2. Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER ∗ Stat Database: Mortality—All COD, Public-Use With State, Total U.S. (1969–2003), National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2006. Underlying mortality data provided by NCHS (http://www.cdc.gov/nchs).
  3. Bleyer WA. The impact of childhood cancer on the United States and the world. CA Cancer J Clin. 1990;40:355–367
  4. Wallace WH, Kelsey TW. Ovarian reserve and reproductive age may be determined from measurement of ovarian volume by transvaginal sonography. Hum Reprod. 2004;19:1612–1617
  5. Wallace WH, Shalet SM, Hendry JH, Morris-Jones PH, Gattamaneni HR. Ovarian failure following abdominal irradiation in childhood: the radiosensitivity of the human oocyte. Br J Radiol. 1989;62:995–998
  6. Wallace WH, Thomson AB, Kelsey TW. The radiosensitivity of the human oocyte. Hum Reprod. 2003;18:117–121
  7. Wallace WH, Thomson AB, Saran F, Kelsey TW. Predicting age of ovarian failure after radiation to a field that includes the ovaries. Int J Radiat Oncol Biol Phys. 2005;62:738–744
  8. Sanders JE, Hawley J, Levy W, Gooley T, Buckner CD, Deeg HJ, et al. Pregnancies following high-dose cyclophosphamide with or without high-dose busulfan or total-body irradiation and bone marrow transplantation. Blood. 1996;87:3045–3052
  9. Blumenfeld Z, Avivi I, Linn S, Epelbaum R, Ben-Shahar M, Haim N. Prevention of irreversible chemotherapy-induced ovarian damage in young women with lymphoma by a gonadotrophin-releasing hormone agonist in parallel to chemotherapy. Hum Reprod. 1996;11:1620–1626
  10. Marchesoni D, Driul L, Fruscalzo A, Santuz M, Calcagno A, Ianni A, et al. Premature ovarian failure in patients affected by oncohematological disease. Minerva Ginecol. 2005;57:545–550
  11. Blumenfeld Z. Preservation of fertility and ovarian function and minimalization of chemotherapy associated gonadotoxicity and premature ovarian failure: the role of inhibin-A and -B as markers. Mol Cell Endocrinol. 2002;187:93–105
  12. Blumenfeld Z, Ritter M, Shen-Orr Z, Shariki K, Ben-Shahar M, Haim N. Inhibin A concentrations in the sera of young women during and after chemotherapy for lymphoma: correlation with ovarian toxicity. Am J Reprod Immunol. 1998;39:33–40
  13. Rubin P, Casarett GW. The female genital tract. In:  Rubin P,  Casarett GW editor. Clinical radiation pathology. Philadelphia: W.B. Saunders; 1986;p. 396–422
  14. Fajardo LF. Female reproductive organs. In:  Fajardo LF editors. Pathology of radiation injury. New York: Mason Publishing USA; 1982;p. 108–128
  15. Chemaitilly W, Mertens AC, Mitby P, Whitton J, Stovall M, Yasui Y, et al. Acute ovarian failure in the childhood cancer survivor study. J Clin Endocrinol Metab. 2006;91:1723–1728
  16. Sklar CA, Mertens AC, Mitby P, Whitton J, Stovall M, Kasper C, et al. Premature menopause in survivors of childhood cancer: a report from the childhood cancer survivor study. J Natl Cancer Inst. 2006;98:890–896
  17. Larsen EC, Muller J, Schmiegelow K, Rechnitzer C, Andersen AN. Reduced ovarian function in long-term survivors of radiation- and chemotherapy-treated childhood cancer. J Clin Endocrinol Metab. 2003;88:5307–5314
  18. Livesey EA, Brook CG. Gonadal dysfunction after treatment of intracranial tumours. Arch Dis Childhood. 1988;63:495–500
  19. Hamre MR, Robison LL, Nesbit ME, Sather HN, Meadows AT, Ortega JA, et al. Effects of radiation on ovarian function in long-term survivors of childhood acute lymphoblastic leukemia: a report from the Children's Cancer Study Group. J Clin Oncol. 1987;5:1759–1765
  20. Grigsby P, Russell A, Bruner D, Eifel P, Koh W, Spanos W, et al. Late injury of cancer therapy on the female reproductive tract. Intern J Rad Oncol Biol Phys. 1995;31:1281–1299
  21. Peck WS, McGreer JT, Kretzschmar NR, Brown WE. Castration of the female by irradiation: the results in 334 patients. Radiology. 1940;34:176–186
  22. Nathanson IT, Rice C, Meigs JV. Hormonal studies in artificial menopause produced by roentgen rays. Am J Obstet Gynecol. 1940;40:936–5
  23. Diczfalusy E, Notter G, Edsymr F, Westman A. Estrogen excretion in breast cancer patients before and after ovarian irradiation and oophorectomy. J Clin Oncol. 1959;19:1230–1244
  24. Leung SF, Tsao SY, Teo PML, Choi PHK, Shiu WCT. Ovarian ablation failures by radiation. Br J Radiol. 1991;64:537–538
  25. Meakin JW. Review of Canadian trials of adjuvant endocrine therapy for breast cancer. NCI Monogr. 1986;111–113
  26. Payne S. The treatment of female infertility by x-ray therapy. W J Surg Obstet Gyn. 1954;62:173–176
  27. Kaplan I. The treatment of female sterility with x-ray therapy directed to the pituitary and ovaries. Am J Obstet Gynecol. 1958;76:447–453
  28. Belohorsky B, Siracky J, Sandor L, Klauber E. Comments on the development of amenorrhea caused by myleran in cases of chronic myelosis. Neoplasma. 1960;7:397–403
  29. Chapman RM. Cytotoxic therapy on sexuality and gonadal function. Semin Oncol. 1982;9:84–94
  30. Fisher B, Sherman B, Rockett H, Redmond C, Margolese R, Fisher E. L-phenylalanine mustard (L-PAM) in the management of premenopausal patients with primary breast cancer: lack of association of disease-free survival with depression of ovarian function. National Surgical Adjuvant Project for Breast and Bowel Cancers. Cancer. 1979;44:847–857
  31. Fosdick WM, Parsons JL, Hill DF. Preliminary report: long-term cyclophosphamide therapy in rheumatoid arthritis. Arthritis Rheum. 1968;11:151–161
  32. Koyama H, Wada T, Nishizawa J, Iwanaga T, Aoki Y. Cyclophosphamide-induced ovarian failure and its therapeutic significance in patients with breast cancer. Cancer. 1977;39:1403–1409
  33. Miller JJ, Williams GF, Leissring JC. Multiple late complications of therapy with cyclophosphamide, including ovarian destruction. Am J Med. 1971;50:530–535
  34. Rose DP, Davis TE. Ovarian function in patients receiving adjuvant chemotherapy for breast cancer. Lancet. 1977;1:1174–1176
  35. Shalet SM. Disorders of the endocrine system due to radiation and cytotoxic chemotherapy. Clin Endocrinol. 1983;18:637–659
  36. Shalet SM. Effects of cancer chemotherapy on gonadal function of patients. Cancer Treat Res. 1980;7:141–152
  37. Warne GL, Fairley KF, Hobbs JB, Martin FL. Cyclophosphamide-induced ovarian failure. N Engl J Med. 1973;289:1159–1162
  38. Thomson AB, Critchley HO, Wallace WH. Fertility and progeny. Eur J Cancer. 2002;38:1634–1644[discussion 45–6]
  39. Andrieu JM, Ochoa-Molina ME. Menstrual cycle, pregnancies and offspring before and after MOPP therapy for Hodgkin's disease. Cancer. 1983;52:435–438
  40. Chapman RM, Sutcliffe SB, Malpas JS. Cytotoxic-induced ovarian failure in women with Hodgkin's disease. I. Hormone function. JAMA. 1979;242:1877–1881
  41. Morganfeld MC, Goldberg V, Parisier H, Bugnard SC, Bur GE. Ovarian lesions due to cytostatic agents during the treatment of Hodgkin's disease. Surg Gynecol Obstet. 1972;1134:826–828
  42. Schilsky RL, Sherins RJ, Hubbard SM, Wesley MN, Young RC, DeVita VT. Long-term follow-up of ovarian function in women treated with MOPP chemotherapy for Hodgkin's disease. Am J Med. 1981;71:552–556
  43. Sobrinho LG, Levine RA, DeConti RC. Amenorrhea in patients with Hodgkin's disease treated with antineoplastic agents. Am J Obstet Gynecol. 1971;109:135–139
  44. Howell S, Shalet S. Gonadal damage from chemotherapy and radiotherapy. Endocrinol Metab Clin North Am. 1998;27:927–943
  45. Bokemeyer C, Schmoll HJ, van Rhee J, Kuczyk M, Schuppert F, Poliwoda H. Long-term gonadal toxicity after therapy for Hodgkin's and non-Hodgkin's lymphoma. Ann Hematol. 1994;68:105–110
  46. Counsell R, Bain G, Williams MV, Dixon AK. Artificial radiation menopause: where are the ovaries?. Clin Oncol (R Coll Radiol). 1996;8:250–253
  47. Rigsby CK, Siegel MJ. CT appearance of pediatric ovaries and uterus. J Comput Assist Tomogr. 1994;18:72–76
  48. Nicholson R, Coucher J, Thornton A, Connor F. Effect of a full and empty bladder on radiation dose to the uterus, ovaries and bladder from lumbar spine CT and X-ray examinations. Br J Radiol. 2000;73:1290–1296
  49. Harden SV, Twyman N, Lomas DJ, Williams D, Burnet NG, Williams MV. A method for reducing ovarian doses in whole neuro-axis irradiation for medulloblastoma. Radiother Oncol. 2003;69:183–188
  50. Yuh GE, Loredo LN, Yonemoto LT, Bush DA, Shahnazi K, Preston W, et al. Reducing toxicity from craniospinal irradiation: using proton beams to treat medulloblastoma in young children. Cancer J. 2004;10:386–390
  51. Miralbell R, Lomax A, Russo M. Potential role of proton therapy in the treatment of pediatric medulloblastoma/primitive neuro-ectodermal tumors: spinal theca irradiation. Int J Radiat Oncol Biol Phys. 1997;38:805–811
  52. Lee CT, Bilton SD, Famiglietti RM, Riley BA, Mahajan A, Chang EL, et al. Treatment planning with protons for pediatric retinoblastoma, medulloblastoma, and pelvic sarcoma: how do protons compare with other conformal techniques?. Int J Radiat Oncol Biol Phys. 2005;63:362–372
  53. Belinson JL, Doherty M, McDay JB. A new technique for ovarian transposition. Surg Gynecol Obstet. 1984;159:157–160
  54. Hodel K, Rich WM, Austin P, DiSaia PJ. The role of ovarian transposition in conservation of ovarian function in radical hysterectomy followed by pelvic radiation. Gynecol Oncol. 1982;13:195–202
  55. Husseinzadeh N, Nahhas WA, Velkly DE, Whitney CW, Mortel R. The preservation of ovarian function in young women undergoing pelvic radiation therapy. Gynecol Oncol. 1984;18:373–379
  56. Husseinzadeh N, van Aken ML, Aron B. Ovarian transposition in young patients with invasive cervical cancer receiving radiation therapy. Int J Gynecol Cancer. 1994;4:61–65
  57. Scott SM, Schlaff W. Laparoscopic medial oophoropexy prior to radiation therapy in an adolescent with Hodgkin's disease. J Pediatr Adol Gynecol. 2005;18:355–357
  58. Williams RS, Littell RD, Mendenhall NP. Laparoscopic oophoropexy and ovarian function in the treatment of Hodgkin disease. Cancer. 1999;86:2138–2142
  59. Hadar H, Loven D, Herskovitz P, Bairey O, Yagoda A, Levavi H. An evaluation of lateral and medial transposition of the ovaries out of radiation fields. Cancer. 1994;74:774–779
  60. LeFloch O, Donaldson SS, Kaplan HS. Pregnancy following oophoropexy and total nodal irradiation in women with Hodgkin's disease. Cancer. 1976;38:2263–2268
  61. Thibaud E, Ramirez M, Brauner R, Flamant F, Zucker JM, Fekete C, et al. Preservation of ovarian function by ovarian transposition performed before pelvic irradiation during childhood. J Pediatr. 1992;121:880–884
  62. Franke HR, Smit WM, Vermes I. Gonadal protection by a gonadotropin-releasing hormone agonist depot in young women with Hodgkin's disease undergoing chemotherapy. Gynecol Endocrinol. 2005;20:274–278
  63. Monnier A. Clinical management of adverse events in adjuvant therapy for hormone-responsive early breast cancer. Ann Oncol. 2007;18(Suppl):viii36–viii44
  64. Gook DA, Edgar DH. Human oocyte cryopreservation. Human Reprod Update. 2007;13:591–605
  65. al-Shawaf T, Dave R, Harper J, Linehan D, Riley P, Craft I. Transfer of embryos into the uterus: how much do technical factors affect pregnancy rates?. J Assist Reprod Genet. 1993;10:31–36
  66. Frederick JL, Ord T, Kettel LM, Stone SC, Balmaceda JP, Asch RH. Successful pregnancy outcome after cryopreservation of all fresh embryos with subsequent transfer into an unstimulated cycle. Fertil Steril. 1995;64:987–990
  67. Selick CE, Hofmann GE, Albano C, Horowitz GM, Copperman AB, Garrisi GJ, et al. Embryo quality and pregnancy potential of fresh compared with frozen embryos—is freezing detrimental to high quality embryos?. Hum Reprod. 1995;10:392–395
  68. Senn A, Vozzi C, Chanson A, De Grandi P, Germond M. Prospective randomized study of two cryopreservation policies avoiding embryo selection: the pronucleate stage leads to a higher cumulative delivery rate than the early cleavage stage. Fertil Steril. 2000;74:946–952
  69. Wang JX, Yap YY, Matthews CD. Frozen-thawed embryo transfer: influence of clinical factors on implantation rate and risk of multiple conception. Hum Reprod. 2001;16:2316–2319
  70. Son WY, Yoon SH, Yoon HJ, Lee SM, Lim JH. Pregnancy outcome following transfer of human blastocysts vitrified on electron microscopy grids after induced collapse of the blastocoele. Hum Reprod. 2003;18:137–139
  71. Mandelbaum J, Junca AM, Plachot M, Alnot MO, Salat-Baroux J, Alvarez S, et al. Cryopreservation of human embryos and oocytes. Hum Reprod. 1988;3:117–119
  72. Imoedemhe DG, Sigue AB. Survival of human oocytes cryopreserved with or without the cumulus in 1,2-propanediol. J Assist Reprod Genet. 1992;9:323–327
  73. Oktay K, Kan MT, Rosenwaks Z. Recent progress in oocyte and ovarian tissue cryopreservation and transplantation. Curr Opin Obstet Gynecol. 2001;13:263–268
  74. Sonmezer M, Oktay K. Fertility preservation in female patients. Hum Reprod Update. 2004;10:251–266
  75. Katayama KP, Stehlik J, Kuwayama M, Kato O, Stehlik E. High survival rate of vitrified human oocytes results in clinical pregnancy. Fertil Steril. 2003;80:223–224
  76. Yoon TK, Kim TJ, Park SE, Hong SW, Ko JJ, Chung HM, et al. Live births after vitrification of oocytes in a stimulated in vitro fertilization–embryo transfer program. Fertil Steril. 2003;79:1323–1326
  77. Cobo A, Kuwayama M, Pérez S, Ruiz A, Pellicer A, Remohí J. Comparison of concomitant outcome achieved with fresh and cryopreserved donor oocytes vitrified by the Cryotop method. Fertil Steril. 2008;89:1657–1664
  78. Wallace WH, Pritchard J. Livebirth after cryopreserved ovarian tissue autotransplantation. Lancet. 2004;364:2093–2094
  79. Kim SS. Fertility preservation in female cancer patients: current developments and future directions. Fertil Steril. 2006;85:1–11
  80. Silber SJ, Lenahan KM, Levine DJ, Pineda JA, Gorman KS, Friez MJ, et al. Ovarian transplantation between monozygotic twins discordant for premature ovarian failure. N Engl J Med. 2005;353:58–63
  81. Meirow D, Levron J, Eldar-Geva T, Hardan I, Fridman E, Zalel Y, et al. Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. N Engl J Med. 2005;353:318–321

 J.S.S. has nothing to disclose. D.M. has nothing to disclose. J.R. has nothing to disclose. M.P. has nothing to disclose. P.H.T. has nothing to disclose. P.W.G. has nothing to disclose.

PII: S0015-0282(08)01489-1

doi: 10.1016/j.fertnstert.2008.07.1714

Fertility and Sterility
Volume 92, Issue 2 , Pages 417-427 , August 2009

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