Journal of Assisted Reproduction and Genetics

, Volume 30, Issue 1, pp 11–24

The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature

  • Mikkel Rosendahl
  • Tine Greve
  • Claus Yding Andersen
Fertility Preservation

Abstract

Background

Transplantation of frozen/thawed ovarian tissue from patients with a malignant condition is associated with a risk of re-introduction of the disease as the tissue usually is removed before anti-cancer therapy and may thus contain malignant cells. We review studies investigating the presence of malignant cells in cryopreserved ovarian tissue from patients with malignant disease and based on the strength of the evidence, recommendations for transplantations are proposed.

Materials and methods

A systematic review of the literature. All peer reviewed studies evaluating the presence of malignant cells in cryopreserved human ovarian tissue were included. Data were searched in Pubmed and Embase with no language restrictions.

Results

The majority of the reviewed papers were casuistic reports and few of the included papers were specifically designed to search for malignant cells. Ovarian tissue from 422 patients has been subject to testing for malignant cells by imaging, histology, immunohistochemistry, molecular biology, animal- or clinical transplantation. In 31 (7 %) of the cases the applied test raised suspicion of malignant cell infiltration. No transplantation-related relapse of cancer has been reported after 33 transplantations of frozen/thawed ovarian cortex.

Conclusion

The quality and strength of the evidence is generally low and prospective studies are needed. The risk of re-introducing a malignant condition when transplanting ovarian tissue depends on the particular disease. Based on the available data, the risk was estimated: Leukaemia: HIGH. Gastrointestinal cancers: MODERATE. Breast cancer, sarcomas of the bone and connective tissue, gynaecological cancers, Hodgkin’s and Non-Hodgkin’s Lymphoma: LOW.

Keywords

Fertility preservation Ovarian tissue cryopreservation Minimal residual disease Safety Cancer Cryobiology Ovarian reserve Lymphoma Breast cancer Leukaemia 

References

  1. 1.
    Abir R, Feinmesser M, Yaniv I, Fisch B, Cohen IJ, Ben-Haroush A, et al. Occasional involvement of the ovary in Ewing sarcoma. Hum Reprod. 2010;25:1708–12.PubMedCrossRefGoogle Scholar
  2. 2.
    Akar ME, Carrillo AJ, Jennell JL, Yalcinkaya TM. Robotic-assisted laparoscopic ovarian tissue transplantation. Fertil Steril. 2011;95:1120–8.PubMedCrossRefGoogle Scholar
  3. 3.
    Amorim CA, Dolmans MM, David A, Jaeger J, Vanacker J, Camboni A, et al. Vitrification and xenografting of human ovarian tissue. Fertil Steril. 2012;98:1291–8.PubMedCrossRefGoogle Scholar
  4. 4.
    Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M, et al. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod. 2008;23:2266–72.PubMedCrossRefGoogle Scholar
  5. 5.
    Andersen CY, Silber S, Berghold SH, Stener Jørgensen J, Ernst E. Long-term duration of function of ovarian tissue transplants: case reports. Reprod Biomed Online. 2012;25:128–32.Google Scholar
  6. 6.
    Azem F, Hasson J, Ben-Yosef D, Kossoy N, Cohen T, Almog B, et al. Histologic evaluation of fresh human ovarian tissue before cryopreservation. Int J Gynecol Pathol. 2010;29:19–23.PubMedCrossRefGoogle Scholar
  7. 7.
    Bigorie V, Morice P, Duvillard P, Antoine M, Cortez A, Flejou JF, et al. Ovarian metastases from breast cancer: report of 29 cases. Cancer. 2010;116:799–804.PubMedCrossRefGoogle Scholar
  8. 8.
    Bittinger SE, Nazaretian SP, Gook DA, Parmar C, Harrup RA, Stern CJ. Detection of Hodgkin lymphoma within ovarian tissue. Fertil Steril. 2011;95:803–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Dath C, Van Eyck AS, Dolmans MM, Romeu L, Delle VL, Donnez J, et al. Xenotransplantation of human ovarian tissue to nude mice: comparison between four grafting sites. Hum Reprod. 2010;25:1734–43.PubMedCrossRefGoogle Scholar
  10. 10.
    de Waal YR, Thomas CM, Oei AL, Sweep FC, Massuger LF. Secondary ovarian malignancies: frequency, origin, and characteristics. Int J Gynecol Cancer. 2009;19:1160–5.PubMedCrossRefGoogle Scholar
  11. 11.
    Demeestere I, Simon P, Buxant F, Robin V, Fernandez SA, Centner J, et al. Ovarian function and spontaneous pregnancy after combined heterotopic and orthotopic cryopreserved ovarian tissue transplantation in a patient previously treated with bone marrow transplantation: case report. Hum Reprod. 2006;21:2010–4.PubMedCrossRefGoogle Scholar
  12. 12.
    Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin’s disease. Oncologist. 2007;12:1437–42.PubMedCrossRefGoogle Scholar
  13. 13.
    Demeestere I, Simon P, Moffa F, Delbaere A, Englert Y. Birth of a second healthy girl more than 3 years after cryopreserved ovarian graft. Hum Reprod. 2010;25:1590–1.PubMedCrossRefGoogle Scholar
  14. 14.
    Dittrich R, Lotz L, Keck G, Hoffmann I, Mueller A, Beckmann MW, et al. Live birth after ovarian tissue autotransplantation following overnight transportation before cryopreservation. Fertil Steril. 2012;97:387–90.PubMedCrossRefGoogle Scholar
  15. 15.
    Dittrich R, Mueller A, Binder H, Oppelt PG, Renner SP, Goecke T, et al. First retransplantation of cryopreserved ovarian tissue following cancer therapy in Germany. Dtsch Arztebl Int. 2008;105:274–8.PubMedGoogle Scholar
  16. 16.
    Dolmans MM, Donnez J, Camboni A, Demylle D, Amorim C, Van LA, et al. IVF outcome in patients with orthotopically transplanted ovarian tissue. Hum Reprod. 2009;24:2778–87.PubMedCrossRefGoogle Scholar
  17. 17.
    Dolmans MM, Marinescu C, Saussoy P, Van LA, Amorim C, Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood. 2010;116:2908–14.PubMedCrossRefGoogle Scholar
  18. 18.
    Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet. 2004;364:1405–10.PubMedCrossRefGoogle Scholar
  19. 19.
    Donnez J, Silber S, Andersen CY, Demeestere I, Piver P, Meirow D, et al. Children born after autotransplantation of cryopreserved ovarian tissue. a review of 13 live births. Ann Med. 2011;43:437–50.PubMedCrossRefGoogle Scholar
  20. 20.
    Donnez J, Squifflet J, Jadoul P, Demylle D, Cheron AC, Van LA, et al. Pregnancy and live birth after autotransplantation of frozen-thawed ovarian tissue in a patient with metastatic disease undergoing chemotherapy and hematopoietic stem cell transplantation. Fertil Steril. 2011;95:1787.e1–4.CrossRefGoogle Scholar
  21. 21.
    Donnez J, Squifflet J, Van Eyck AS, Demylle D, Jadoul P, Van LA, et al. Restoration of ovarian function in orthotopically transplanted cryopreserved ovarian tissue: a pilot experience. Reprod Biomed Online. 2008;16:694–704.PubMedCrossRefGoogle Scholar
  22. 22.
    Ernst E, Bergholdt S, Jorgensen JS, Andersen CY. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reprod. 2010;25:1280–1.PubMedCrossRefGoogle Scholar
  23. 23.
    Ernst E, Kjærsgaard M, Birkebæk NH, Clausen N, Andersen CY. Stimulation of puberty in a girl with chemo - and radiation therapy induced ovarian failure by transplantation of a small part of her frozen/thawed ovarian tissue. Eur J Cancer. 2012. doi:10.1016/j.ejca.2012.09.028.
  24. 24.
    Evens AM, Hutchings M, Diehl V. Treatment of Hodgkin lymphoma: the past, present, and future. Nat Clin Pract Oncol. 2008;5:543–56.PubMedCrossRefGoogle Scholar
  25. 25.
    Fogh J, Tiso J, Orfeo T, Sharkey FE, Daniels WP, Fogh JM. Thirty-four lines of six human tumor categories established in nude mice. J Natl Cancer Inst. 1980;64:745–51.PubMedGoogle Scholar
  26. 26.
    Friedman O, Orvieto R, Fisch B, Felz C, Freud E, Ben-Haroush A, et al. Possible improvements in human ovarian grafting by various host and graft treatments. Hum Reprod. 2012;27:474–82.PubMedCrossRefGoogle Scholar
  27. 27.
    Giovanella BC, Stehlin Jr JS, Williams Jr LJ, Lee SS, Shepard RC. Heterotransplantation of human cancers into nude mice: a model system for human cancer chemotherapy. Cancer. 1978;42:2269–81.PubMedCrossRefGoogle Scholar
  28. 28.
    Gook DA, Edgar DH, Borg J, Archer J, Lutjen PJ, McBain JC. Oocyte maturation, follicle rupture and luteinization in human cryopreserved ovarian tissue following xenografting. Hum Reprod. 2003;18:1772–81.PubMedCrossRefGoogle Scholar
  29. 29.
    Gook DA, McCully BA, Edgar DH, McBain JC. Development of antral follicles in human cryopreserved ovarian tissue following xenografting. Hum Reprod. 2001;16:417–22.PubMedCrossRefGoogle Scholar
  30. 30.
    Greve T, Clasen-Linde E, Andersen MT, Andersen MK, Sørensen SD, Rosendahl M, et al. Cryopreserved ovarian cortex from patients with leukemia in complete remission contains no apparent viable malignant cells. Blood. 2012;120:4311–6.Google Scholar
  31. 31.
    Guyatt GH, Oxman AD, Kunz R, Falck-Ytter Y, Vist GE, Liberati A, et al. Going from evidence to recommendations. BMJ. 2008;336:1049–51.PubMedCrossRefGoogle Scholar
  32. 32.
    Guyatt GH, Oxman AD, Kunz R, Vist GE, Falck-Ytter Y, Schunemann HJ. What is “quality of evidence” and why is it important to clinicians? BMJ. 2008;336:995–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924–6.PubMedCrossRefGoogle Scholar
  34. 34.
    Horvath TJ, Schindler AE. Ovarian metastases in breast carcinoma. Fortschr Med. 1977;95:358–60.PubMedGoogle Scholar
  35. 35.
    Imamura T, Huang CC, Minowada J, Moore GE. Heterologous transplantation of human hematopoietic cell lines. Cancer. 1970;25:1320–31.PubMedCrossRefGoogle Scholar
  36. 36.
    Insabato L, De RG, Franco R, D’Onofrio V, Di VD. Ovarian metastasis from renal cell carcinoma: a report of three cases. Int J Surg Pathol. 2003;11:309–12.PubMedCrossRefGoogle Scholar
  37. 37.
    Jaffrey BJ, Lair SV, Hudson JW, Lozzio BB, Machado EA, Chase DC. Heterotransplantation of human neoplasms. J Oral Surg. 1979;37:16–20.PubMedGoogle Scholar
  38. 38.
    Jemal A, Ward E, Thun M. Declining death rates reflect progress against cancer. PLoS One. 2010;5:e9584.PubMedCrossRefGoogle Scholar
  39. 39.
    Khan MA, Dahill SW, Stewart KS. Primary Hodgkin’s disease of the ovary. Case report. Br J Obstet Gynaecol. 1986;93:1300–1.PubMedCrossRefGoogle Scholar
  40. 40.
    Kim SS, Lee WS, Chung MK, Lee HC, Lee HH, Hill D. Long-term ovarian function and fertility after heterotopic autotransplantation of cryobanked human ovarian tissue: 8-year experience in cancer patients. Fertil Steril. 2009;91:2349–54.PubMedCrossRefGoogle Scholar
  41. 41.
    Kim SS, Radford J, Harris M, Varley J, Rutherford AJ, Lieberman B, et al. Ovarian tissue harvested from lymphoma patients to preserve fertility may be safe for autotransplantation. Hum Reprod. 2001;16:2056–60.PubMedCrossRefGoogle Scholar
  42. 42.
    Kristensen SG, Rasmussen A, Byskov AG, Andersen CY. Isolation of pre-antral follicles from human ovarian medulla tissue. Hum Reprod. 2011;26:157–66.PubMedCrossRefGoogle Scholar
  43. 43.
    Kyono K, Doshida M, Toya M, Sato Y, Akahira J, Sasano H. Potential indications for ovarian autotransplantation based on the analysis of 5,571 autopsy findings of females under the age of 40 in Japan. Fertil Steril. 2010;93:2429–30.PubMedCrossRefGoogle Scholar
  44. 44.
    Liu LY. Metastatic cancer in the ovary—report of 57 cases. Zhonghua Zhong Liu Za Zhi. 1989;11:464–7.PubMedGoogle Scholar
  45. 45.
    Lock RB, Liem N, Farnsworth ML, Milross CG, Xue C, Tajbakhsh M, et al. The nonobese diabetic/severe combined immunodeficient (NOD/SCID) mouse model of childhood acute lymphoblastic leukemia reveals intrinsic differences in biologic characteristics at diagnosis and relapse. Blood. 2002;99:4100–8.PubMedCrossRefGoogle Scholar
  46. 46.
    Lotz L, Montag M, Van der Ven H, von Wolff M, Mueller A, Hoffmann I, et al. Xenotransplantation of cryopreserved ovarian tissue from patients with ovarian tumors into SCID mice—no evidence of malignant cell contamination. Fertil Steril. 2011;95:2612–4.PubMedCrossRefGoogle Scholar
  47. 47.
    Meirow D, Baum M, Yaron R, Levron J, Hardan I, Schiff E, et al. Ovarian tissue cryopreservation in hematologic malignancy: ten years’ experience. Leuk Lymphoma. 2007;48:1569–76.PubMedCrossRefGoogle Scholar
  48. 48.
    Meirow D, Ben YD, Prus D, Poliack A, Schenker JG, Rachmilewitz EA, et al. Ovarian tissue banking in patients with Hodgkin’s disease: is it safe? Fertil Steril. 1998;69:996–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Meirow D, Biederman H, Anderson RA, Wallace WH. Toxicity of chemotherapy and radiation on female reproduction. Clin Obstet Gynecol. 2010;53:727–39.PubMedCrossRefGoogle Scholar
  50. 50.
    Meirow D, Hardan I, Dor J, Fridman E, Elizur S, Ra’anani H, et al. Searching for evidence of disease and malignant cell contamination in ovarian tissue stored from hematologic cancer patients. Hum Reprod. 2008;23:1007–13.PubMedCrossRefGoogle Scholar
  51. 51.
    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;353:318–21.PubMedCrossRefGoogle Scholar
  52. 52.
    Meyer LH, Debatin KM. Diversity of human leukemia xenograft mouse models: implications for disease biology. Cancer Res. 2011;71:7141–4.PubMedCrossRefGoogle Scholar
  53. 53.
    Oktay K. Spontaneous conceptions and live birth after heterotopic ovarian transplantation: is there a germline stem cell connection? Hum Reprod. 2006;21:1345–8.PubMedCrossRefGoogle Scholar
  54. 54.
    Oktay K, Buyuk E, Veeck L, Zaninovic N, Xu K, Takeuchi T, et al. Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. Lancet. 2004;363:837–40.PubMedCrossRefGoogle Scholar
  55. 55.
    Oktay K, Newton H, Mullan J, Gosden RG. Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum Reprod. 1998;13:1133–8.PubMedCrossRefGoogle Scholar
  56. 56.
    Oktay K, Turkcuoglu I, Rodriguez-Wallberg KA. Four spontaneous pregnancies and three live births following subcutaneous transplantation of frozen banked ovarian tissue: what is the explanation? Fertil Steril. 2011;95:804–10.PubMedCrossRefGoogle Scholar
  57. 57.
    Perrotin F, Marret H, Bouquin R, Fischer-Perrotin N, Lansac J, Body G. Incidence, diagnosis and prognosis of ovarian metastasis in breast cancer. Gynecol Obstet Fertil. 2001;29:308–15.PubMedCrossRefGoogle Scholar
  58. 58.
    Povlsen C, Rygaard J. Growth of human tumors in the nude mouse. In: Bloom BR, David JR, editors. In vitro methods in cell-mediated and tumor immunity. New York: Academic; 1976. p. 701–11.Google Scholar
  59. 59.
    Radford JA, Lieberman BA, Brison DR, Smith AR, Critchlow JD, Russell SA, et al. Orthotopic reimplantation of cryopreserved ovarian cortical strips after high-dose chemotherapy for Hodgkin’s lymphoma. Lancet. 2001;357:1172–5.PubMedCrossRefGoogle Scholar
  60. 60.
    Revel A, Laufer N, Ben MA, Lebovich M, Mitrani E. Micro-organ ovarian transplantation enables pregnancy: a case report. Hum Reprod. 2011;26:1097–103.PubMedCrossRefGoogle Scholar
  61. 61.
    Rosendahl M, Andersen CY, Ernst E, Westergaard LG, Rasmussen PE, Loft A, et al. Ovarian function after removal of an entire ovary for cryopreservation of pieces of cortex prior to gonadotoxic treatment: a follow-up study. Hum Reprod. 2008;23:2475–83.PubMedCrossRefGoogle Scholar
  62. 62.
    Rosendahl M, Andersen MT, Ralfkiaer E, Kjeldsen L, Andersen MK, Andersen CY. Evidence of residual disease in cryopreserved ovarian cortex from female patients with leukemia. Fertil Steril. 2010;94:2186–90.PubMedCrossRefGoogle Scholar
  63. 63.
    Rosendahl M, Loft A, Byskov AG, Ziebe S, Schmidt KT, Andersen AN, et al. Biochemical pregnancy after fertilization of an oocyte aspirated from a heterotopic autotransplant of cryopreserved ovarian tissue: case report. Hum Reprod. 2006;21:2006–9.PubMedCrossRefGoogle Scholar
  64. 64.
    Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG, et al. Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod Biomed Online. 2011;22:162–71.PubMedCrossRefGoogle Scholar
  65. 65.
    Rosendahl M, Timmermans WV, Nedergaard L, Kristensen SG, Ernst E, Rasmussen PE, et al. Cryopreservation of ovarian tissue for fertility preservation: no evidence of malignant cell contamination in ovarian tissue from patients with breast cancer. Fertil Steril. 2011;95:2158–61.PubMedCrossRefGoogle Scholar
  66. 66.
    Roux C, Amiot C, Agnani G, Aubard Y, Rohrlich PS, Piver P. Live birth after ovarian tissue autograft in a patient with sickle cell disease treated by allogeneic bone marrow transplantation. Fertil Steril. 2010;93:2413–9.PubMedCrossRefGoogle Scholar
  67. 67.
    Sanchez M, Novella-Maestre E, Teruel J, Ortiz E, Pellicer A. The Valencia programme for fertility preservation. Clin Transl Oncol. 2008;10:433–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Sanchez-Serrano M, Crespo J, Mirabet V, Cobo AC, Escriba MJ, Simon C, et al. Twins born after transplantation of ovarian cortical tissue and oocyte vitrification. Fertil Steril. 2010;93:268–3.PubMedGoogle Scholar
  69. 69.
    Sanchez-Serrano M, Novella-Maestre E, Rosello-Sastre E, Camarasa N, Teruel J, Pellicer A. Malignant cells are not found in ovarian cortex from breast cancer patients undergoing ovarian cortex cryopreservation. Hum Reprod. 2009;24:268.e11–3.CrossRefGoogle Scholar
  70. 70.
    Schmidt KL, Andersen CY, Loft A, Byskov AG, Ernst E, Andersen AN. Follow-up of ovarian function post-chemotherapy following ovarian cryopreservation and transplantation. Hum Reprod. 2005;20:3539–46.PubMedCrossRefGoogle Scholar
  71. 71.
    Schmidt KL, Ernst E, Byskov AG, Nyboe AA, Yding AC. Survival of primordial follicles following prolonged transportation of ovarian tissue prior to cryopreservation. Hum Reprod. 2003;18:2654–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Schmidt KT, Rosendahl M, Ernst E, Loft A, Andersen AN, Dueholm M, et al. Autotransplantation of cryopreserved ovarian tissue in 12 women with chemotherapy-induced premature ovarian failure: the Danish experience. Fertil Steril. 2011;95:695–701.PubMedCrossRefGoogle Scholar
  73. 73.
    Seshadri T, Gook D, Lade S, Spencer A, Grigg A, Tiedemann K, et al. Lack of evidence of disease contamination in ovarian tissue harvested for cryopreservation from patients with Hodgkin lymphoma and analysis of factors predictive of oocyte yield. Br J Cancer. 2006;94:1007–10.PubMedCrossRefGoogle Scholar
  74. 74.
    Shimada M, Kigawa J, Nishimura R, Yamaguchi S, Kuzuya K, Nakanishi T, et al. Ovarian metastasis in carcinoma of the uterine cervix. Gynecol Oncol. 2006;101:234–7.PubMedCrossRefGoogle Scholar
  75. 75.
    Silber S, Kagawa N, Kuwayama M, Gosden R. Duration of fertility after fresh and frozen ovary transplantation. Fertil Steril. 2010;94:2191–6.PubMedCrossRefGoogle Scholar
  76. 76.
    Silber SJ. Ovary cryopreservation and transplantation for fertility preservation. Mol Hum Reprod. 2012;18:59–67.PubMedCrossRefGoogle Scholar
  77. 77.
    Silber SJ, DeRosa M, Pineda J, Lenahan K, Grenia D, Gorman K, et al. A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Hum Reprod. 2008;23:1531–7.PubMedCrossRefGoogle Scholar
  78. 78.
    Stern CJ, Toledo MG, Hale LG, Gook DA, Edgar DH. The first Australian experience of heterotopic grafting of cryopreserved ovarian tissue: evidence of establishment of normal ovarian function. Aust N Z J Obstet Gynaecol. 2011;51:268–75.PubMedCrossRefGoogle Scholar
  79. 79.
    Telfer EE, McLaughlin M. Natural history of the mammalian oocyte. Reprod Biomed Online. 2007;15:288–95.PubMedCrossRefGoogle Scholar
  80. 80.
    Tryde Schmidt KL, Yding AC, Starup J, Loft A, Byskov AG, Nyboe AA. Orthotopic autotransplantation of cryopreserved ovarian tissue to a woman cured of cancer—follicular growth, steroid production and oocyte retrieval. Reprod Biomed Online. 2004;8:448–53.PubMedCrossRefGoogle Scholar
  81. 81.
    Van Eyck AS, Bouzin C, Feron O, Romeu L, Van LA, Donnez J, et al. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.PubMedCrossRefGoogle Scholar
  82. 82.
    Yada-Hashimoto N, Yamamoto T, Kamiura S, Seino H, Ohira H, Sawai K, et al. Metastatic ovarian tumors: a review of 64 cases. Gynecol Oncol. 2003;89:314–7.PubMedCrossRefGoogle Scholar
  83. 83.
    Young RH, Kozakewich HP, Scully RE. Metastatic ovarian tumors in children: a report of 14 cases and review of the literature. Int J Gynecol Pathol. 1993;12:8–19.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Mikkel Rosendahl
    • 1
  • Tine Greve
    • 1
  • Claus Yding Andersen
    • 1
  1. 1.Laboratory of Reproductive BiologyCopenhagen University Hospital—RigshospitaletCopenhagen ØDenmark

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