In vitro oocyte maturation

Mikhailova N.D., Mishieva N.G., Kirillova A.O., Martazanova B.A., Dzhincharade L.G.

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow, Russia
In vitro maturation (IVM) is an assisted reproductive technology (ART) that implies aspiration of immature oocytes and their subsequent in vitro maturation. This technology is of particular importance for patients with polycystic ovary syndrome, as it prevents a formidable complication, such as ovarian hyperstimulation syndrome, as well as for those with resistant syndrome of the ovaries that are unresponsive to gonadotropin stimulation, and for those with cancers due to the possibility to completely abandon any stimulation. Nevertheless, IVM ranks below classical in vitro fertilization (IVF) in efficiency. To enhance the latter of classical IVM, an innovative embryological procedure, a two-stage capacitation in vitro maturation (CAPA-IVM) system that includes a preparatory (pre-IVM) step, has been developed, which contributes to the acquisition of competence by oocytes, and their further cultivation and maturation in the IVM media. This technology has shown to be effective, but it has a rather limited application and at this stage requires further investigation.
Conclusion: This literature review describes the experience and efficiency of IVM and CAPA-IVM procedures including those in comparison with classical IVF in different categories of patients on the basis of Russian and international publications on this topic from the Pubmed system. The choice of the optimal treatment policy for such patients also requires further investigation.

Keywords

infertility
polycystic ovary syndrome
in vitro maturation
capacitation in vitro maturation
gynecology
assisted reproductive technology
in vitro fertilization

References

  1. Pincus G., Enzmann E.V. The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J. Exp. Med. 1935; 62(5): 665-75. https://dx.doi.org/10.1084/jem.62.5.665.
  2. De Vos M., Smitz J., Thompson J.G., Gilchrist R.B. The definition of IVM is clear-variations need defining. Hum. Reprod. 2016; 31(11): 2411-5. https://dx.doi.org/10.1093/humrep/dew208.
  3. Cha K.Y., Chian R.C. Maturation in vitro of immature human oocytes for clinical use. Hum. Reprod. Update. 1998; 4(2): 103-20. https://dx.doi.org/10.1093/humupd/4.2.103.
  4. Yang Z.Y., Chian R.C. Development of in vitro maturation techniques for clinical applications. Fertil. Steril. 2017; 108(4): 577-84. https://dx.doi.org/10.1016/j.fertnstert.2017.08.020.
  5. Edwards R.G. Maturation in vitro of human ovarian oocytes. Lancet. 1965; 2(7419): 926-9. https://dx.doi.org/10.1016/s0140-6736(65)92903-x.
  6. Cha K.Y., Koo J.J., Ko J.J., Choi D.H., Han S.Y., Yoon T.K. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil. Steril. 1991; 55(1): 109-13. https://dx.doi.org/10.1016/s0015-0282(16)54068-0.
  7. Trounson A., Wood C., Kausche A. In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients. Fertil. Steril. 1994; 62(2): 353-62. https://dx.doi.org/10.1016/s0015-0282(16)56891-5.
  8. Child T.J., Phillips S.J., Abdul-Jalil A.K., Gulekli B., Tan S.L. A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovaries. Obstet. Gynecol. 2002; 100(4): 665-70. https://dx.doi.org/10.1016/s0029-7844(02)02193-2.
  9. Ho V.N.A., Braam S.C., Pham T.D., Mol B.W., Vuong L.N. The effectiveness and safety of in vitro maturation of oocytes versus in vitro fertilization in women with a high antral follicle count. Hum. Reprod. 2019; 34(6): 1055-64. https://dx.doi.org/10.1093/humrep/dez060.
  10. Patel S.S., Carr B.R. Oocyte quality in adult polycystic ovary syndrome. Semin. Reprod. Med. 2008; 26(2): 196-203. https://dx.doi.org/10.1055/s-2008-1042958.
  11. Siristatidis C., Sergentanis T.N., Vogiatzi P., Kanavidis P., Chrelias C., Papantoniou N. et al. In vitro maturation in women with vs. without polycystic ovarian syndrome: a systematic review and meta-analysis. PLoS One. 2015; 10(8): e0134696. https://dx.doi.org/10.1371/journal.pone.0134696.
  12. Vuong L.N., Ho V.N.A., Ho T.M., Dang V.Q., Phung T.H., Giang N.H. et al. In-vitro maturation of oocytes versus conventional IVF in women with infertility and a high antral follicle count: a randomized non-inferiority controlled trial. Hum. Reprod. 2020; 35(11): 2537-47. https://dx.doi.org/10.1093/humrep/deaa240.
  13. Wang P., Zhao J., Jin C., Yu R., Lin J., Zhu R. et al. Comparision of in vitro maturation applied in PCOS and non-PCOS patients undergo stimulated and unstimulated protocols. Zhonghua Fu Chan Ke Za Zhi. 2014; 49(12): 903-8.
  14. Practice Committees of the American Society for Reproductive Medicine, the Society of Reproductive Biologists and Technologists, and the Society for Assisted Reproductive Technology. In vitro maturation: a committee opinion. Fertil. Steril. 2021; 115(2): 298-304. https://dx.doi.org/10.1016/j.fertnstert.2020.11.018.
  15. Fadini R., Dal Canto M.B., Mignini Renzini M., Brambillasca F., Comi R., Fumagalli D. et al. Effect of different gonadotrophin priming on IVM of oocytes from women with normal ovaries: a prospective randomized study. Reprod. Biomed. Online. 2009; 19(3): 343-51. https://dx.doi.org/10.1016/s1472-6483(10)60168-x.
  16. Tannus S., Hatirnaz S., Tan J., Ata B., Tan S., Hatırnaz E. et al. Predictive factors for live birth after in vitro maturation of oocytes in women with polycystic ovary syndrome. Arch. Gynecol. Obstet. 2018; 297: 199-204. https://dx.doi.org/10.1007/s00404-017-4561-z.
  17. Ho V.N.A., Pham T.D., Le A.H., Ho T.M., Vuong L.N. Live birth rate after human chorionic gonadotropin priming in vitro maturation in women with polycystic ovary syndrome. J. Ovarian Res. 2018; 11(1): 70. https://dx.doi.org/10.1186/s13048-018-0445-5.
  18. Lin Y., Zheng X., Ma C., Li X., Zhang X., Yang P. et al. Human chorionic gonadotropin priming does not improve pregnancy outcomes of PCOS-IVM cycles. Front. Endocrinol. (Lausanne). 2020; 11: 279. https://dx.doi.org/10.3389/fendo.2020.00279.
  19. Klement A.H., Navve D., Ghetler Y., Wiser A., Shavit T., Weitzner O. et al. Gonadotropin releasing hormone agonist triggering for in vitro maturation cycles. Hum. Fertil. (Camb). 2020; 1-11. https://dx.doi.org/10.1080/14647273.2020.1858511.
  20. Walls M.L., Hunter T., Ryan J.P., Keelan J.A., Nathan E., Hart R.J. In vitro maturation as an alternative to standard in vitro fertilization for patients diagnosed with polycystic ovaries: a comparative analysis of fresh, frozen and cumulative cycle outcomes. Hum. Reprod. 2015; 30(1): 88-96. https://dx.doi.org/10.1093/humrep/deu248.
  21. Mostinckx L., Segers I., Belva F., Buyl R., Santos-Ribeiro S., Blockeel C. et al. Obstetric and neonatal outcome of ART in patients with polycystic ovary syndrome: IVM of oocytes versus controlled ovarian stimulation. Hum. Reprod. 2019; 34(8): 1595-607. https://dx.doi.org/10.1093/humrep/dez086.
  22. Mackens S., Mostinckx L., Drakopoulos P., Segers., Santos-Ribeiro S., Popovic-Todorovic B. et al. Early pregnancy loss in patients with polycystic ovary syndrome after IVM versus standard ovarian stimulation for IVF/ICSI. Hum. Reprod. 2020; 35(12): 2763-73. https://dx.doi.org/10.1093/humrep/deaa200.
  23. Яковлев П.П., Корнилов Р.Н., Павлова М.Н., Корнилов Н.В. Синдром резистентных яичников и дозревание ооцитов в пробирке. Акушерство и гинекология. 2020; 11: 226-31. [Yakovlev P.P., Kornilov R.N., Pavlova M.N., Kornilov N.V. Resistant ovary syndrome and in vitro maturation of oocytes. Obstetrics and gynecology. 2020; 11: 226-31. (in Russian)]. https://dx.doi.org/10.18565/aig.2020.11.226-231.
  24. Grynberg M., Peltoketo H., Christin-Maître S., Poulain M., Bouchard P., Fanchin R. First birth achieved after in vitro maturation of oocytes from a woman endowed with multiple antral follicles unresponsive to follicle-stimulating hormone. J. Clin. Endocrinol. Metab. 2013; 98(11): 4493-8. https://dx.doi.org/10.1210/jc.2013-1967.
  25. Galvão A., Segers I., Smitz J., Tournaye H., De Vos M. In vitro maturation (IVM) of oocytes in patients with resistant ovary syndrome and in patients with repeated deficient oocyte maturation. J. Assist. Reprod. Genet. 2018; 35(12): 2161-71. https://dx.doi.org/10.1007/s10815-018-1317-z.
  26. Flageole C., Toufaily C., Bernard D.J., Ates S., Blais V., Chénier S. et al. Successful in vitro maturation of oocytes in a woman with gonadotropin-resistant ovary syndrome associated with a novel combination of FSH receptor gene variants: a case report. J. Assist. Reprod. Genet. 2019; 36(3): 425-32. https://dx.doi.org/10.1007/s10815-018-1394-z.
  27. Kornilov N.V., Pavlova M.N., Yakovlev P.P. The live birth in a woman with resistant ovary syndrome after in vitro oocyte maturation and preimplantation genetic testing for aneuploidy. J. Assist. Reprod. Genet. 2021; 38(6): 1303-9. https://dx.doi.org/10.1007/s10815-021-02085-5.
  28. De Vos M., Smitz J., Woodruff T.K. Fertility preservation in women with cancer. Lancet. 2014; 384(9950): 1302-10. https://dx.doi.org/10.1016/S0140-6736(14)60834-5.
  29. Park C.W., Lee S.H., Yang K.M., Lee I.H., Lim K.T., Lee K.H. et al. Cryopreservation of in vitro matured oocytes after ex vivo oocyte retrieval from gynecologic cancer patients undergoing radical surgery. Clin. Exp. Reprod. Med. 2016; 43(2): 119-25. https://dx.doi.org/10.5653/cerm.2016.43.2.119.
  30. Ковальская Е.В., Кириллова А.О., Буняева Е.С., Хабас Г.Н., Камалетдинов Н.С., Назаренко Т.А., Абубакиров А.Н. Эффективность дозревания ооцитов, полученных в ходе овариэктомии, у онкологических пациенток. Акушерство и гинекология. 2019; 9: 87-91. [Kovalskaya E.V., Kirillova A.O., Bunyaeva E.S., Khabas G.N., Kamaletdinov N.S., Nazarenko T.A., Abubakirov A.N. Efficiency of maturation of oocytes obtained from cancer patients during ovariectomy. Obstetrics and gynecology. 2019; 9: 87-91. (in Russian)]. https://dx.doi.org/10.18565/aig.2019.9.87-91.
  31. Prasath E.B., Chan M.L., Wong W.H., Lim C.J., Tharmalingam M.D., Hendricks M. et al. First pregnancy and live birth resulting from cryopreserved embryos obtained from in vitro matured oocytes after oophorectomy in an ovarian cancer patient. Hum. Reprod. 2014; 29(2): 276-8. https://dx.doi.org/10.1093/humrep/det420.
  32. Segers I., Mateizel I., Van Moer E., Smitz J., Tournaye H., Verheyen G. et al. In vitro maturation (IVM) of oocytes recovered from ovariectomy specimens in the laboratory: a promising "ex vivo" method of oocyte cryopreservation resulting in the first report of an ongoing pregnancy in Europe. J. Assist. Reprod. Genet. 2015; 32(8): 1221-31. https://dx.doi.org/10.1007/s10815-015-0528-9.
  33. Uzelac P.S., Delaney A.A., Christensen G.L., Bohler H.C., Nakajima S.T. Live birth following in vitro maturation of oocytes retrieved from extracorporeal ovarian tissue aspiration and embryo cryopreservation for 5 years. Fertil. Steril. 2015; 104(5): 1258-60. https://dx.doi.org/10.1016/j.fertnstert.2015.07.1148.
  34. Кириллова А.О., Буняева Е.С., Ковальская Е.В., Камалетдинов Н.С., Хабас Г.Н., Фармаковская М.Д., Сироткина Е.А., Мишиева Н.Г., Назаренко Т.А., Абубакиров А.Н. Сохранение фертильности у пациенток с диагностированным во время беременности онкологическим заболеванием. Акушерство и гинекология. 2020; 4: 59-64. [Kirillova A.O., Bunyaeva E.S., Koval’skaya E.V., Kamaletdinov N.S., Khabas G.N., Farmakovskaya M.D, Sirotkina E.A., Mishieva N.G., Nazarenko T.A., Abubakirov A.N. Fertility preservation in patients diagnosed with cancer during pregnancy. Obstetrics and gynecology. 2020; 4: 59-64. (in Russian)]. https://dx.doi.org/10.18565/aig.2020.4.59-64.
  35. Segers I., Bardhi E., Mateizel I., Van Moer E., Schots R., Verheyen G. et al. Live births following fertility preservation using in-vitro maturation of ovarian tissue oocytes. Hum. Reprod. 2020; 35(9): 2026-36. https://dx.doi.org/10.1093/humrep/deaa175.
  36. Delattre S., Segers I., Van Moer E., Drakopoulos P., Mateizel I., Enghels L. et al. Combining fertility preservation procedures to spread the eggs across different baskets: a feasibility study. Hum. Reprod. 2020; 35(11): 2524-36. https://dx.doi.org/10.1093/humrep/deaa193.
  37. Kirillova A., Kovalskaya E., Brovkina O., Ekimov A., Bunyaeva E., Gordiev M. et al. Cryopreservation of euploid blastocysts obtained after fertilization of in vitro matured ovarian tissue oocytes: a case report. J. Assist. Reprod. Genet. 2020; 37(4): 905-11. https://dx.doi.org/10.1007/s10815-020-01729-2.
  38. Zhao Y., Liao X., Krysta A.E., Bertoldo M.J., Richani D., Gilchrist R.B. Capacitation IVM improves cumulus function and oocyte quality in minimally stimulated mice. J. Assist. Reprod. Genet. 2020; 37(1): 77-88. https://dx.doi.org/10.1007/s10815-019-01610-x.
  39. Sánchez F., Lolicato F., Romero S., De Vos M., Van Ranst H., Verheyen G. et al. An improved IVM method for cumulus-oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield. Hum. Reprod. 2017; 32(10): 2056-68. https://dx.doi.org/10.1093/humrep/dex262.
  40. Sanchez F., Le A.H., Ho V.N.A., Romero S., Van Ranst H., De Vos M. et al. Biphasic in vitro maturation (CAPA-IVM) specifically improves the developmental capacity of oocytes from small antral follicles. J. Assist. Reprod. Genet. 2019; 36(10): 2135-44. https://dx.doi.org/10.1007/s10815-019-01551-5.
  41. Vuong L.N., Le A.H., Ho V.N.A., Pham T.D., Sanchez F., Romero S. et al. Live births after oocyte in vitro maturation with a prematuration step in women with polycystic ovary syndrome. J. Assist. Reprod. Genet. 2020; 37(2): 347-57. https://dx.doi.org/10.1007/s10815-019-01677-6.
  42. Kirillova A., Bunyaeva E., Van Ranst H., Khabas G., Farmakovskaya M., Kamaletdinov N. et al. Improved maturation competence of ovarian tissue oocytes using a biphasic in vitro maturation system for patients with gynecological malignancy: a study on sibling oocytes. J. Assist. Reprod. Genet. 2021; 38(6): 1331-40. https://dx.doi.org/10.1007/s10815-021-02118-z.

Received 28.07.2021

Accepted 07.10.2021

About the Authors

Nina D. Mikhaylova, graduate student of 1st Gynecology Department, V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology,
Ministry of Health of Russia, +7(915)456-81-51, mihailnina@mail.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.
Nona G. Mishieva, PhD, Senior Researcher of 1st Gynecology Department, V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, +7(495)438-26-22, nondoc555@mail.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.
Anastasia O. Kirillova, PhD, Senior Researcher of 1st Gynecology Department, V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, +7(495)531-44-44, a_kozyreva@oparina4.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.
Bella A. Martazanova, PhD, Junior Researcher of 1st Gynecology Department, V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, +7(967)123-88-24, bellamart88@mail.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.
Lana G. Dzhincharadze, graduate student of 1st Gynecology Department, V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, +7(926)073-77-73, lanachka@list.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.

Authors’ contributions: Mishieva N.G., Kirillova A.O. – development and design of the investigation; Mikhailova N.D. – review of publications on the topic of the article; analysis of the findings; writing the text of the manuscript; Kirillova A.O.,
Martazanova B.A., Dzhincharade L.G. – editing.
Conflicts of interest: The authors declare that there are no possible conflicts of interest.
Funding: The investigation has been conducted without sponsorship within the framework of N.L. Mikhailova’s thesis research.
For citation: Mikhailova N.D., Mishieva N.G., Kirillova A.O., Martazanova B.A.,
Dzhincharade L.G. In vitro oocyte maturation.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2021; 11: 64-70 (in Russian)
https://dx.doi.org/10.18565/aig.2021.11.64-70

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.