Issues of preparation for implementing uterine transplantation in clinical practice
https://doi.org/10.23873/2074-0506-2023-15-1-79-88
Abstract
The absolute uterine factor infertility is a non-treatable cause of female infertility. Surrogacy has become the only option that allows this group of patients to achieve genetic, although biological motherhood. According to statistics there are more than 30 thousand women of fertile age in Russia who cannot get pregnant due to the absolute uterine factor infertility. The recently emerged possibility of uterine transplantation has become the only treatment for this kind of female infertility.
Prior to the very first clinical study of human uterine transplantation which was carried out in 2013 in Sweden, scientists had conducted systematic studies in animals (rodents, pigs, cattle and primates). The first clinical trial with the uterine transplantation performed resulted in a live birth in September 2014. Currently, cases of successful uterine transplantation in humans have been reported in Sweden, Brazil, USA and Italy. Experience and practice in animal research played a key role in the success of the first clinical study on uterine transplantation. The application of this method is fundamental in the introduction of the scientifically grounded technology of uterine transplantation in Russia.
Aim. Analysis of the problems of the clinical application of the uterine transplantation based on a literature review.
About the Authors
A. M. PolstianoyRussian Federation
Aleksey M. Polstianoy - Cand. Sci. (Med.), Head of the Married Couple Health Center
26 Kolomenskaya St., Krasnoyarsk 660037 Russia
K. K. Gubarev
Russian Federation
Konstantin K. Gubarev - Cand. Sci. (Med.), Head of the Surgical Department for the Coordination of Human Organ and Tissue Donation
23 Marshal Novikov St., Moscow 123098 Russia
O. Yu. Polstianaya
Russian Federation
Oksana Yu. Polstianaya - Deputy Chief Physician for Surgery
26 Kolomenskaya St., Krasnoyarsk 660037 Russia
I. V. Rendashkin
Russian Federation
Ivan V. Rendashkin - Urologist of the Gynecological Department
26 Kolomenskaya St., Krasnoyarsk 660037 Russia
References
1. Brännström M, Johannesson L, Bokström H, Kvarnström N, Mölne J,Dahm-Kähler P, et al. Livebirth after uterus transplantation. Lancet. 2015;385(9968):607–616. PMID: 25301505 https://doi.org/10.1016/S0140-6736(14)61728-1
2. Chan YY, Jayaprakasan K, Tan A, Thornton JG, Coomarasamy A, RaineFenning NJ. Reproductive outcomes in women with congenital uterine anomalies: a systematic review. Ultrasound Obstet Gynecol. 2011;38(4):371–382. PMID: 21830244 https://doi.org/10.1002/uog.10056
3. Sieunarine K, Zakaria FB, Boyle DC, Corlesset DJ, Noakes DE, Lindsay I, et al. Possibilities for fertility restoration: a new surgical technique. Int Surg. 2005;90(5):249–256. PMID: 16625941 https://doi.org/10.1016/j.fertn-stert.2005.07.1229
4. Brinsden PR. Gestational surrogacy. Hum Reprod Update. 2003;9(5):483–491. PMID: 14640380 https://doi.org/10.1093/humupd/dmg033
5. Brännström M, Diaz-Garcia C, Hanafy A, Olausson M, Tzakis A. Uterus transplantation: animal research and human possibilities. Fertil Steril. 2012;97(6):1269–1276. PMID: 22542990 https://doi.org/10.1016/j.fertn-stert.2012.04.001
6. McCulloch P, Altman DG, Campbell WB, Flum DR, Glasziou P, Marshall JC, et al. No surgical innovation without evaluation: the IDEAL recommendations. Lancet. 2009;374(9695):1105–1112. PMID: 19782876 https://doi.org/10.1016/S0140-6736(09)61116-8
7. El-Akouri RR, Kurlberg G, Dindelegan G, Mölne J, Wallin A, Brännström M. Heterotopic uterine transplantation by vascular anastomosis in the mouse. J Endocrinol. 2002;174(2):157–166. PMID: 12176655 https://doi.org/10.1677/joe.0.1740157
8. Racho El-Akouri R, Kurlberg G, Brännström M. Successful uterine transplantation in the mouse: pregnancy and postnatal development of offspring. Hum Reprod. 2003;18(10):2018–2023. PMID: 14507815 https://doi.org/10.1093/humrep/deg396
9. Wranning CA, Akhi SN, Kurlberg G, Brännström M. Uterus transplantation in the rat: model development, surgical learning and morphological evaluation of healing. Acta Obstet Gynecol Scand. 2008;87(11):1239–1247. PMID: 18951268 https://doi.org/10.1080/00016340802484966
10. Saso S, Petts G, Chatterjee J, Thum MY, David AL, Corless D, et al. Uterine allotransplantation in a rabbit model using aorto-caval anastomosis: a long-term viability study. Eur J Obstet Gynecol Reprod Biol. 2014;182:185–193. PMID: 25306223 https://doi.org/10.1016/j.ejogrb.2014.09.029
11. Avison DL, DeFaria W, Tryphonopoulos P, Tekin A, Attia GR, Takahashi H, et al. Heterotopic uterus transplantation in a swine model. Transplantation. 2009;88(4):465–469. PMID: 19696628 https://doi.org/10.1097/TP.0b013e3181b07666
12. Wranning CA, Marcickiewicz J, Enskog A, Dahm-Kähler P, Hanafy A, Brännström M. Fertility after autologous ovine uterine-tubal-ovarian transplantation by vascular anastomosis to the external iliac vessels. Hum Reprod. 2010;25(8):1973–1979. PMID: 20519245 https://doi.org/10.1093/humrep/deq130
13. Ramirez ER, Ramirez DK, Pillari VT, Vasquez H, Ramirez HA. Modified uterine transplant procedure in the sheep model. J Minim Invasive Gynecol. 2008;15(3):311–314. PMID: 18439503 https://doi.org/10.1016/j.jmig.2008.01.014
14. Wei L, Xue T, Yang H, Zhao GY, Zhang G, Lu ZH, et al. Modified uterine allotransplantation and immunosuppression procedure in the sheep model. PLoS One. 2013;8(11):e81300. PMID: 24278415 https://doi.org/10.1371/journal.pone.0081300
15. Gauthier T, Bertin F, Fourcade L, Maubon A, Marcoux FS, Piver P, et al. Uterine allotransplantation in ewes using an aortocava patch. Hum Reprod. 2011;26(11):3028–3036. PMID: 21896546 https://doi.org/10.1093/humrep/der288
16. Gonzalez-Pinto IM, Tryphonopoulos P, Avison DL, Nishida S, Tekin A, Santiago S, et al. Uterus transplantation model in sheep with heterotopic whole graft and aorta and cava anastomoses. Transplant Proc. 2013;45(5):1802–1804. PMID: 23769047 https://doi.org/10.1016/j.transproceed.2012.08.024
17. Enskog A, Johannesson L, Chai DC, Dahm-Kähler P, Marcickiewicz J, Nyachieo A, et al. Uterus transplantation in the baboon: methodology and long-term function after auto-transplantation. Hum Reprod. 2010;25(8):1980–1987. PMID: 20519250 https://doi.org/10.1093/humrep/deq109
18. Johannesson L, Enskog A, DahmKähler P, Hanafy A, Chai DC, Mwenda JM, et al. Uterus transplantation in a non-human primate: long-term followup after autologous transplantation. Hum Reprod. 2012;27(6):1640–1648. PMID: 22454459 https://doi.org/10.1093/humrep/des093
19. Johannesson L, Enskog A, Mölne J, Diaz-Garcia C, Hanafy A, DahmKähler P, et al. Preclinical report on allogeneic uterus transplantation in non-human primates. Hum Reprod. 2013;28(1):189–198. PMID: 23108346 https://doi.org/10.1093/humrep/des381
20. Tryphonopoulos P, Tzakis AG, Tekin A, Johannesson L, Rivas K, Morales PR, et al. Allogeneic uterus transplantation in baboons: surgical technique and challenges to long-term graft survival. Transplantation. 2014;98(5):e51–e56. PMID: 25171537 https://doi.org/10.1097/TP.0000000000000322
21. Kisu I, Mihara M, Banno K, Hara H, Yamamoto T, Araki J, et al. A new surgical technique of uterine autotransplantation in cynomolgus monkey: preliminary report about two cases. Arch Gynecol Obstet. 2012;285(1):129–137. PMID: 21475964 https://doi.org/10.1007/s00404-011-1901-2
22. Mihara M, Kisu I, Hara H, Iida T, Yamamoto T, Araki J, et al. Uterus autotransplantation in cynomolgus macaques: intraoperative evaluation of uterine blood flow using indocyanine green. Hum Reprod. 2011;26(11):3019–3027. PMID: 21896548 https://doi.org/10.1093/humrep/der276
23. Kisu I, Mihara M, Banno K, Hara H, Masugi Y, Araki J, et al. Uterus allotransplantation in cynomolgus macaque: A preliminary experience with non-human primate models. J Obstet Gynaecol Res. 2014;40(4):907–918. PMID: 24612366 https://doi.org/10.1111/jog.12302
24. El-Akouri R, Wranning CA, Mölne J, Kurlberg G, Brännström M, et al. Pregnancy in transplanted mouse uterus after long-term cold ischaemic preservation. Hum Reprod. 2003;18(10):2024–2030. PMID: 14507816 https://doi.org/10.1093/humrep/deg395
25. Tricard J, Ponsonnard S, Tholance Y, Mesturoux L, Lachatre D, Couquet C, et al. Uterus tolerance to extended cold ischemic storage after auto-transplantation in ewes. Eur J Obstet Gynecol Reprod Biol. 2017;214:162–167. PMID: 28535402 https://doi.org/10.1016/j.ejogrb.2017.05.013
26. Díaz-García C, Akhi SN, MartínezVarea A, Brännström M. The effect of warm ischemia at uterus transplantation in a rat model. Acta Obstet Gynecol Scand. 2013;92(2):152–159. PMID: 23061896 https://doi.org/10.1111/aogs.12027
27. Adachi M, Kisu I, Nagai T, Emoto K, Banno K, Umene K, et al. Evaluation of allowable time and histopathological changes in warm ischemia of the uterus in cynomolgus monkey as a model for uterus transplantation. Acta Obstet Gynecol Scand. 2016;95(9):991–998. PMID: 27329637 https://doi.org/10.1111/aogs.12943
28. Akhi SN, Diaz-Garcia C, ElAkouri RR, Wranning CA, Mölne J, Brännström M, et al. Uterine rejection after allogeneic uterus transplantation in the rat is effectively suppressed by tacrolimus. Fertil Steril. 2013;99(3):862–870. PMID: 23218920 https://doi.org/10.1016/j.fertnstert.2012.11.002
29. Groth K, Akhi SN, Mölne J, Wranning CA, Brännström M. Effects of immunosuppression by cyclosporine A on allogenic uterine transplant in the rat. Eur J Obstet Gynecol Reprod Biol. 2012;163(1):97-103. PMID: 22502817 https://doi.org/10.1016/j.ejogrb.2012.03.026
30. El-Akouri RR, Mölne J, Groth K, Kurlberg G, Brännström M. Rejection patterns in allogeneic uterus transplantation in the mouse. Hum Reprod. 2006;21(2):436–442. PMID: 16253976 https://doi.org/10.1093/humrep/dei349
31. Groth K, Akouri R, Wranning CA, Molne J, Brannstrom M. Rejection of allogenic uterus transplant in the mouse: time-dependent and site-specific infiltration of leukocyte subtypes. Hum Reprod. 2009;24(11):2746–2754. PMID: 19617209 https://doi.org/10.1093/humrep/dep248
32. Wranning CA, Akhi SN, Diaz-Garcia C, Brannstrom M. Pregnancy after syngeneic uterus transplantation and spontaneous mating in the rat. Hum Reprod. 2011;26(3):553–558. PMID: 21159686 https://doi.org/10.1093/humrep/deq358
33. Mihara M, Kisu I, Hara H, Iida T, Araki J, Shim T, et al. Uterine autotransplantation in cynomolgus macaques: the first case of pregnancy and delivery. Hum Reprod. 2012;27(8):2332–2340. PMID: 22647448 https://doi.org/10.1093/humrep/des169
34. Díaz-García C, Akhi SN, Wallin A, Pellicer A, Brännström M. First report on fertility after allogeneic uterus transplantation. Acta Obstet Gynecol Scand. 2010;89(11):1491–1494. PMID: 20879912 https://doi.org/10.3109/00016349.2010.520688
35. Saso S, Petts G, David AL, Thum MY, Chatterjee J, Vicente JS, et al. Achieving an early pregnancy following allogeneic uterine transplantation in a rabbit model. Eur J Obstet Gynecol Reprod Biol. 2015;185:164–169. PMID: 25590500 https://doi.org/10.1016/j.ejogrb.2014.12.017
36. Ramirez ER, Ramirez Nessetti DK, Nessetti MB, Khatamee M, Wolfson MR, et al. Pregnancy and outcome of uterine allotransplantation and assisted reproduction in sheep. J Minim Invasive Gynecol. 2011;18(2):238–245. PMID: 21354071 https://doi.org/10.1016/j.jmig.2010.11.006
37. Díaz-García C, Johannesson L, Shao R, Bilig H, Brännström M. Pregnancy after allogeneic uterus transplantation in the rat: perinatal outcome and growth trajectory. Fertil Steril. 2014;102(6):1545–1552.e1. PMID: 25439799 https://doi.org/10.1016/j.fertnstert.2014.09.010
38. Wranning C, Mölne J, El-Akouri R, Kurlberg G, Brännström M. Shortterm ischaemic storage of human uterine myometrium-basic studies towards uterine transplantation. Hum Reprod. 2005;20(10):2736–2744. PMID: 15980004 https://doi.org/10.1093/humrep/dei125
39. Del Priore G, Stega J, Sieunarine K, Ungar L, Smith J. Human uterus retrieval from a multi-organ donor. Obstet Gynecol. 2007;109(1):101–104. PMID: 17197594 https://doi.org/10.1097/01.aog.0000248535.58004.2f
40. Gauthier T, Piver P, Pichon N, Bibes R, Guillaudeau A, Piccardo A, et al. Uterus retrieval process from brain dead donors. Fertil Steril. 2014;102(2):476–482. PMID: 24837613 https://doi.org/10.1016/j.fertnstert.2014.04.016
41. Johannesson L, Diaz-Garcia C, Leonhardt H, Dahm-Kähler P, Marcickiewicz J, Olausson M, et al. Vascular pedicle lengths after hysterectomy: toward future human uterus transplantation. Obstet Gynecol. 2012;119(6):1219–1225. PMID: 22617587 https://doi.org/10.1097/AOG.0b013e318255006f
Review
For citations:
Polstianoy A.M., Gubarev K.K., Polstianaya O.Yu., Rendashkin I.V. Issues of preparation for implementing uterine transplantation in clinical practice. Transplantologiya. The Russian Journal of Transplantation. 2023;15(1):79-88. https://doi.org/10.23873/2074-0506-2023-15-1-79-88