Gynecological Surgery

, Volume 13, Issue 4, pp 429–433 | Cite as

Laparoscopic autologous and heterologous ovarian transplantation in orthotopic and heterotopic location without vascular anastomosis in rabbits: morphologic and endocrinologic assessment

  • George Pados
  • Andreas Sortsis
  • Basil C. Tarlatzis
  • Petros Skepastianos
  • Katerina Saratsi
  • John Savas
  • Valentini Tzioufa
  • George Kazakos
Original Article


The purpose of this study was to assess the viability of the ovarian function and compare the success rate of autologous and heterologous ovarian transplantation in orthotopic and heterotopic location in rabbits. Eighty-nine virgin adult white New Zealand female rabbits weighing 3350–4550 g and 4–5 months old were used. The animals were randomly allocated into five groups: group Α (control group) with bilateral ovariectomy (n = 10); group Β, which underwent ovariectomy and intraperitoneal autologous heterotopic transplantation of the ovaries without vascular pedicle (n = 22); group C, in which ovariectomy was performed and autologous orthotopic transplantation in the same location without vascular anastomosis was performed, (n = 20); group D, included animals with ovariectomy and intraperitoneal heterologous heterotopic transplantation of the ovaries without vascular pedicle (n = 19); and group E, included rabbits which underwent ovariectomy and heterologous orthotopic transplantation in the same location without vascular anastomosis (n = 18). The animals were anesthetized by subcutaneous injection of xylazine (10 mg/kg) and ketamine (40 mg/kg). Once the ovaries were exposed, they were removed laparoscopically and the intact ovarian tissue was transplanted in a peritoneal pocket created in the lateral abdominal wall, or in the same location without anastomosis. In groups D and C, cyclosporine 5 mg/kg/day was administered postoperatively. Biopsies from the ovaries were taken 360 days postoperatively for histological evaluation. Blood samples for serum concentrations of FSH, LH E2, and progesterone (PROG) were measured, on day 0 (day of surgery), day 7, day 30, day 180, and day 360 postoperatively. The histological examination showed that the percentage of functional ovaries in group B was 68.18 %, in group C was 45 %, in group D was 63.16 %, and in group E was 38.89 %. No significant difference was found between groups B and C (p = 0.129), as well as between D and E (p = 0.14). The concentration of FSH and LH in group A was significantly higher than in the other groups (p < 0.05). There was no significant difference in the level of FSH between groups B and E (p = 0.053), while comparison between groups C and E revealed statistically significant difference (p < 0.05). On the contrary, there was no significant statistical difference in the LH level between B, C, D, and E groups (p > 0.05). In group A, the concentrations of E2 and PROG were significantly lower than the other groups (p < 0.05), while statistically significant difference was observed between B, C, D, and E groups (p < 0.05). In conclusion, autologous and heterologous ovarian transplantation of intact ovaries without vascular anastomosis was performed successfully and the animal tolerance was excellent. Orthotopic and heterotopic grafts proved to be functional by means of ovarian function and histological examination.


Ovarian transplantation Ovary Laparoscopy Autologous Heterologous Transplantation 


Compliance with ethical standards

This study was not funded at all.

Conflict of interest

George Pados declares that he has no conflict of interest.

Andreas Sortsis declares that he has no conflict of interest.

Basil Tarlatzis has an unrestricted research grant from Merck Serono and, also, an unrestricted research grant from Merck Sharp & Dohme.

Petros Skepastianos declares that he has no conflict of interest.

Katerina Saratsi declares that she has no conflict of interest.

John Savas declares that he has no conflict of interest.

Valentini Tzioufa declares that she has no conflict of interest.

George Kazakos declares that he has no conflict of interest.

Ethical approval

All the national and institutional guidelines for the care and use of animals were followed, and this experimental study was approved by the Directory of Veterinary Service of the Prefecture of Thessaloniki by the decisions with the following protocol numbers: 13/8980/22.7.2011, 13/9194/22.7.2013, and 13/7908/2014.


  1. 1.
    Morris R (1895) The ovarian graft. New York Medical Journal 62:496–500Google Scholar
  2. 2.
    Einige KE (1896) Versuche uber Ovarientransplantation bei Kaninchen. Zentralblatt Gynakolfur 20:524–528Google Scholar
  3. 3.
    Foa C (1900) La greffe des ovaries en relation avec quelques questions de biologie generale. Archieves Italiennes de Biologie 34:43–73Google Scholar
  4. 4.
    Currel A, Cuthrie C (1906) Technique de la transplantation homoplastique de l’ovaire. Comptes Rendus Hebdomaidaires des Seanses de la Societe de Biologie 1:466–468Google Scholar
  5. 5.
    Baird DT, Campbell B, de Souza C, Telfer E (2004) Long-term ovarian functioning sheep after ovariectomy and auto transplantation of cryopreserved cortical strips. Eur J Obst Gynecol Reprod Biol 113:55–59CrossRefGoogle Scholar
  6. 6.
    Torrents E, Boiso I, Barri PN, Veiga A (2003) Applications of ovarian tissue transplantation in experimental biology and medicine. Hum Reprod Update 9:471–481CrossRefPubMedGoogle Scholar
  7. 7.
    Green C, Simpkin S, Grimaldi P (1982) Pregnancy after autografting and allografting vascularized ovaries and en bloc vascularized ovaries with adnexa in rabbits. Br J Obstet Gynaecol 89:645–650CrossRefPubMedGoogle Scholar
  8. 8.
    Wang X, Bilolo K, Qi S, Xu D, Jiang W, Vu M, Chen H (2002) Restoration of fertility in oophorectomized rats after tubo-ovarian transplantation. Microsurgery 22:30–33CrossRefPubMedGoogle Scholar
  9. 9.
    Alberti L, Vasconcellos L, Petroianu A, Nunes M (2002) Availiacao morfofuncional do auto-implante ovariano no retroperitoneo. Medicina 35:30–35Google Scholar
  10. 10.
    Oktay K, Karilkaya G (2000) Ovarian function after transplantation of frozen, banked autologous ovarian tissue. N Engl J Med 342:219–225CrossRefGoogle Scholar
  11. 11.
    Donnez J, Dolmans M, Demylle D, Jadoul P, Pirard C, Squifflet J, Martinez-Madrid B, Van Langendonckt A (2004) Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 364:1405–1410CrossRefPubMedGoogle Scholar
  12. 12.
    Turnbull KE, Braden AWH, Mattner PE (1977) The pattern of follicular growth and atresia in the ovine ovary. Aust J Biol Sci 30:229–241CrossRefPubMedGoogle Scholar
  13. 13.
    Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y (2009) Orthotopic and heterotopic ovarian tissue transplantation. Hum Reprod Update 15:649–665CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Ronaldo AL, Vasconellos L d S, Andy P (2013) Autologous and allogenic ovarian orthotopic transplantation: morphologic, endocrinologic and natural pregnancy assessment. Acta Bras 28:56–65Google Scholar
  15. 15.
    Almondin CG, Minguetti-Camara VC, Meister H (2004) Recovery of fertility grafting of cryopreserved germinative tissue in female rabbits following radiotherapy. Hum Reprod 19:1287–1293CrossRefGoogle Scholar
  16. 16.
    Bedaiwy MA, Falcone T (2004) Ovarian tissue banking for cancer patients. Reduction of post transplantation ischemic injury: intact ovary freezing and transplantation. Hum Reprod 19:1242–1244CrossRefPubMedGoogle Scholar
  17. 17.
    Martinez-Madrid Β, Donnez J (2005) Freeze-thawing of human ovary. Fertil Steril 83:1069–1070CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • George Pados
    • 1
    • 2
  • Andreas Sortsis
    • 1
  • Basil C. Tarlatzis
    • 1
  • Petros Skepastianos
    • 3
  • Katerina Saratsi
    • 4
  • John Savas
    • 4
  • Valentini Tzioufa
    • 5
  • George Kazakos
    • 4
  1. 1.1st Department of Obstetrics & GynecologyAristotle University of ThessalonikiThessalonikiGreece
  2. 2.Department of PathologyAristotle University of ThessalonikiThessalonikiGreece
  3. 3.Centre for Endoscopic Surgery“Diavalkaniko” HospitalThessalonikiGreece
  4. 4.Department of MicrobiologyTechnological Institute of ThessalonikiThessalonikiGreece
  5. 5.Hospital for small animals, School of Veterinary MedicineAristotle University of ThessalonikiThessalonikiGreece

Personalised recommendations