Fertility Preservation in 2016: Where Are We?

Anu David; Lisa Jeannette Green; Ariella Shikanov

doi:10.1055/s-0037-1599087

Seminars in Reproductive Medicine, Table of Contents

Semin Reprod Med 2017; 35(02): 160-166
DOI: 10.1055/s-0037-1599087

Review Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Fertility Preservation in 2016: Where Are We?

Anu David

¹Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan

,

Lisa Jeannette Green

²Department of Obstetrics and Gynecology, University of Michigan Health System, Ann Arbor, Michigan

,

Ariella Shikanov

¹Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan

› Author Affiliations

Abstract

This review focuses on advances in the field of fertility preservation achieved over the past few decades. The main purpose of fertility preservation is to help young cancer survivors retain their fertility by restoring either their ability to procreate or simply their reproductive endocrine function. Although different options are available in this regard, successful fertility preservation is yet to reach its full potential. Herein, we review the most significant work conducted over the past five decades and present new methodologies.

Keywords

fertility preservation - oocyte and embryo cryopreservation - ovarian tissue cryopreservation - whole ovary cryopreservation - artificial ovary - immunoisolation

Full Text

References

References
1 Blatt J. Pregnancy outcome in long-term survivors of childhood cancer. Med Pediatr Oncol 1999; 33 (1) 29-33
2 Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM. Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update 2006; 12 (5) 519-535
3 Meirow D, Nugent D. The effects of radiotherapy and chemotherapy on female reproduction. Hum Reprod Update 2001; 7 (6) 535-543
4 Donnez J, Bassil S. Indications for cryopreservation of ovarian tissue. Hum Reprod Update 1998; 4 (3) 248-259
5 Torrents E, Boiso I, Barri PN, Veiga A. Applications of ovarian tissue transplantation in experimental biology and medicine. Hum Reprod Update 2003; 9 (5) 471-481
6 Lee SJ ; ASCO Fertility Preservation Guidelines Committee. Preservation of fertility in patients with cancer. N Engl J Med 2009; 360 (25) 2680 , author reply 2682–2683
7 Ethics Committee of American Society for Reproductive Medicine. Fertility preservation and reproduction in patients facing gonadotoxic therapies: a committee opinion. Fertil Steril 2013; 100 (5) 1224-1231
8 Anand Kumar TC. Architect of India's first test tube baby: Dr Subhas Mukerji (16 January 1931 to 19 July 1981). Curr Sci 1997; 72 (7) 5
9 Trounson A, Leeton J, Besanko M, Wood C, Conti A. Pregnancy established in an infertile patient after transfer of a donated embryo fertilised in vitro. Br Med J (Clin Res Ed) 1983; 286 (6368): 835-838
10 Hoffman DI, Zellman GL, Fair CC , et al; Society for Assisted Reproduction Technology (SART) and RAND. Cryopreserved embryos in the United States and their availability for research. Fertil Steril 2003; 79 (5) 1063-1069
11 Brown JR, Modell E, Obasaju M, King YK. Natural cycle in-vitro fertilization with embryo cryopreservation prior to chemotherapy for carcinoma of the breast. Hum Reprod 1996; 11 (1) 197-199
12 Lomax GP, Trounson AO. Correcting misperceptions about cryopreserved embryos and stem cell research. Nat Biotechnol 2013; 31 (4) 288-290
13 Toftager M, Bogstad J, Bryndorf T , et al. Risk of severe ovarian hyperstimulation syndrome in GnRH antagonist versus GnRH agonist protocol: RCT including 1050 first IVF/ICSI cycles. Hum Reprod 2016; 31 (6) 1253-1264
14 Oktay K, Türkçüoğlu I, Rodriguez-Wallberg KA. GnRH agonist trigger for women with breast cancer undergoing fertility preservation by aromatase inhibitor/FSH stimulation. Reprod Biomed Online 2010; 20 (6) 783-788
15 Youssef MA, Van der Veen F, Al-Inany HG , et al. Gonadotropin-releasing hormone agonist versus HCG for oocyte triggering in antagonist-assisted reproductive technology. Cochrane Database Syst Rev 2014; (10) CD008046
16 Fauser BC, de Jong D, Olivennes F , et al. Endocrine profiles after triggering of final oocyte maturation with GnRH agonist after cotreatment with the GnRH antagonist ganirelix during ovarian hyperstimulation for in vitro fertilization. J Clin Endocrinol Metab 2002; 87 (2) 709-715
17 Cakmak H, Rosen MP. Ovarian stimulation in cancer patients. Fertil Steril 2013; 99 (6) 1476-1484
18 Simi G, Obino ME, Casarosa E, Litta P, Artini PG, Cela V. Different stimulation protocols for oocyte cryopreservation in oncological patients: a retrospective analysis of single university centre. Gynecol Endocrinol 2015; 31 (12) 966-970
19 Cakmak H, Katz A, Cedars MI, Rosen MP. Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril 2013; 100 (6) 1673-1680
20 Sönmezer M, Türkçüoğlu I, Coşkun U, Oktay K. Random-start controlled ovarian hyperstimulation for emergency fertility preservation in letrozole cycles. Fertil Steril 2011; 95 (6) 2125.e9-2125.e11
21 Quintero RB, Helmer A, Huang JQ, Westphal LM. Ovarian stimulation for fertility preservation in patients with cancer. Fertil Steril 2010; 93 (3) 865-868
22 Madrigrano A, Westphal L, Wapnir I. Egg retrieval with cryopreservation does not delay breast cancer treatment. Am J Surg 2007; 194 (4) 477-481
23 Baynosa J, Westphal LM, Madrigrano A, Wapnir I. Timing of breast cancer treatments with oocyte retrieval and embryo cryopreservation. J Am Coll Surg 2009; 209 (5) 603-607
24 Turan V, Bedoschi G, Moy F, Oktay K. Safety and feasibility of performing two consecutive ovarian stimulation cycles with the use of letrozole-gonadotropin protocol for fertility preservation in breast cancer patients. Fertil Steril 2013; 100 (6) 1681-5.e1
25 Whittingham DG. Survival of mouse embryos after freezing and thawing. Nature 1971; 233 (5315): 125-126
26 Wilmut I. The effect of cooling rate, warming rate, cryoprotective agent and stage of development on survival of mouse embryos during freezing and thawing. Life Sci II 1972; 11 (22) 1071-1079
27 Whittingham DG, Leibo SP, Mazur P. Survival of mouse embryos frozen to -196 degrees and -269 degrees C. Science 1972; 178 (4059): 411-414
28 Cha KY, Chung HM, Lim JM , et al. Freezing immature oocytes. Mol Cell Endocrinol 2000; 169 (01/02) 43-47
29 Levi-Setti PE, Patrizio P, Scaravelli G. Evolution of human oocyte cryopreservation: slow freezing versus vitrification. Curr Opin Endocrinol Diabetes Obes 2016; 23 (6) 445-450
30 Debrock S, Peeraer K, Fernandez Gallardo E, De Neubourg D, Spiessens C, D'Hooghe TM. Vitrification of cleavage stage day 3 embryos results in higher live birth rates than conventional slow freezing: a RCT. Hum Reprod 2015; 30 (8) 1820-1830
31 Glujovsky D, Riestra B, Sueldo C , et al. Vitrification versus slow freezing for women undergoing oocyte cryopreservation. Cochrane Database Syst Rev 2014; (9) CD010047
32 AbdelHafez FF, Desai N, Abou-Setta AM, Falcone T, Goldfarb J. Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. Reprod Biomed Online 2010; 20 (2) 209-222
33 Oktay K, Cil AP, Bang H. Efficiency of oocyte cryopreservation: a meta-analysis. Fertil Steril 2006; 86 (1) 70-80
34 Smith GD, Serafini PC, Fioravanti J , et al. Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril 2010; 94 (6) 2088-2095
35 Cao YX, Xing Q, Li L , et al. Comparison of survival and embryonic development in human oocytes cryopreserved by slow-freezing and vitrification. Fertil Steril 2009; 92 (4) 1306-1311
36 Balaban B, Urman B, Ata B , et al. A randomized controlled study of human Day 3 embryo cryopreservation by slow freezing or vitrification: vitrification is associated with higher survival, metabolism and blastocyst formation. Hum Reprod 2008; 23 (9) 1976-1982
37 Baldwin K, Culley L, Hudson N, Mitchell H, Lavery S. Oocyte cryopreservation for social reasons: demographic profile and disposal intentions of UK users. Reprod Biomed Online 2015; 31 (2) 239-245
38 Cil AP, Bang H, Oktay K. Age-specific probability of live birth with oocyte cryopreservation: an individual patient data meta-analysis. Fertil Steril 2013; 100 (2) 492-9.e3
39 Polge C, Smith AU, Parkes AS. Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature 1949; 164 (4172): 666
40 Parkes AS, Smith AU. Regeneration of rat ovarian tissue grafted after exposure to low temperatures. Proc R Soc Lond B Biol Sci 1953; 140 (901) 455-470
41 Green SH, Smith AU, Zuckerman S. The number of oocytes in ovarian autografts after freezing and thawing. J Endocrinol 1956; 13 (3) 330-334
42 Deanesly R. Egg survival in immature rat ovaries grafted after freezing and thawing. Proc R Soc Lond B Biol Sci 1957; 147 (928) 412-421
43 Amorim CA, Gonçalves PB, Figueiredo JR. Cryopreservation of oocytes from pre-antral follicles. Hum Reprod Update 2003; 9 (2) 119-129
44 Hovatta O, Silye R, Krausz T , et al. Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol-sucrose as cryoprotectants. Hum Reprod 1996; 11 (6) 1268-1272
45 Donnez J, Dolmans MM, Demylle D , et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 2004; 364 (9443): 1405-1410
46 Silber SJ, Lenahan KM, Levine DJ , et al. Ovarian transplantation between monozygotic twins discordant for premature ovarian failure. N Engl J Med 2005; 353 (1) 58-63
47 Silber SJ, DeRosa M, Pineda J , et al. A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Hum Reprod 2008; 23 (7) 1531-1537
48 Silber SJ, Grudzinskas G, Gosden RG. Successful pregnancy after microsurgical transplantation of an intact ovary. N Engl J Med 2008; 359 (24) 2617-2618
49 Silber S, Kagawa N, Kuwayama M, Gosden R. Duration of fertility after fresh and frozen ovary transplantation. Fertil Steril 2010; 94 (6) 2191-2196
50 Silber S. Ovarian tissue cryopreservation and transplantation: scientific implications. J Assist Reprod Genet 2016; 33 (12) 1595-1603
51 Donnez J, Dolmans MM, Pellicer A , et al. Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil Steril 2013; 99 (6) 1503-1513
52 Donnez J, Dolmans MM. Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. J Assist Reprod Genet 2015; 32 (8) 1167-1170
53 Takamatsu H, Rubinsky B. Viability of deformed cells. Cryobiology 1999; 39 (3) 243-251
54 Mazur P, Leibo SP, Chu EH. A two-factor hypothesis of freezing injury. Evidence from Chinese hamster tissue-culture cells. Exp Cell Res 1972; 71 (2) 345-355
55 Mazur P. The role of intracellular freezing in the death of cells cooled at supraoptimal rates. Cryobiology 1977; 14 (3) 251-272
56 Pegg DE. The role of vitrification techniques of cryopreservation in reproductive medicine. Hum Fertil (Camb) 2005; 8 (4) 231-239
57 Hani T, Tachibe T, Shingai S, Kamada N, Ueda O, Jishage K. Fertility of mice receiving vitrified adult mouse ovaries. Reproduction 2006; 131 (4) 681-687
58 Bordes A, Lornage J, Demirci B , et al. Normal gestations and live births after orthotopic autograft of vitrified-warmed hemi-ovaries into ewes. Hum Reprod 2005; 20 (10) 2745-2748
59 Sheikhi M, Hultenby K, Niklasson B, Lundqvist M, Hovatta O. Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue. Hum Reprod 2011; 26 (3) 594-603
60 Keros V, Xella S, Hultenby K , et al. Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum Reprod 2009; 24 (7) 1670-1683
61 Isachenko V, Lapidus I, Isachenko E , et al. Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation. Reproduction 2009; 138 (2) 319-327
62 Amorim CA, David A, Van Langendonckt A, Dolmans MM, Donnez J. Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil Steril 2011; 95 (3) 1094-1097
63 Zhou XH, Wu YJ, Shi J, Xia YX, Zheng SS. Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification. Cryobiology 2010; 60 (2) 101-105
64 Donnez J, Dolmans MM, Diaz C, Pellicer A. Ovarian cortex transplantation: time to move on from experimental studies to open clinical application. Fertil Steril 2015; 104 (5) 1097-1098
65 Wang X, Chen H, Yin H, Kim SS, Lin Tan S, Gosden RG. Fertility after intact ovary transplantation. Nature 2002; 415 (6870): 385
66 Imhof M, Bergmeister H, Lipovac M, Rudas M, Hofstetter G, Huber J. Orthotopic microvascular reanastomosis of whole cryopreserved ovine ovaries resulting in pregnancy and live birth. Fertil Steril 2006; 85 (Suppl. 01) 1208-1215
67 Martinez-Madrid B, Dolmans MM, Van Langendonckt A, Defrère S, Donnez J. Freeze-thawing intact human ovary with its vascular pedicle with a passive cooling device. Fertil Steril 2004; 82 (5) 1390-1394
68 Martinez-Madrid B, Camboni A, Dolmans MM, Nottola S, Van Langendonckt A, Donnez J. Apoptosis and ultrastructural assessment after cryopreservation of whole human ovaries with their vascular pedicle. Fertil Steril 2007; 87 (5) 1153-1165
69 Jadoul P, Donnez J, Dolmans MM, Squifflet J, Lengele B, Martinez-Madrid B. Laparoscopic ovariectomy for whole human ovary cryopreservation: technical aspects. Fertil Steril 2007; 87 (4) 971-975
70 Campbell BK, Hernandez-Medrano J, Onions V , et al. Restoration of ovarian function and natural fertility following the cryopreservation and autotransplantation of whole adult sheep ovaries. Hum Reprod 2014; 29 (8) 1749-1763
71 Dolmans MM, Martinez-Madrid B, Gadisseux E , et al. Short-term transplantation of isolated human ovarian follicles and cortical tissue into nude mice. Reproduction 2007; 134 (2) 253-262
72 Kreeger PK, Deck JW, Woodruff TK, Shea LD. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials 2006; 27 (5) 714-723
73 Amorim CA, Van Langendonckt A, David A, Dolmans MM, Donnez J. Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Hum Reprod 2009; 24 (1) 92-99
74 Telfer E, Torrance C, Gosden RG. Morphological study of cultured preantral ovarian follicles of mice after transplantation under the kidney capsule. J Reprod Fertil 1990; 89 (2) 565-571
75 Kniazeva E, Hardy AN, Boukaidi SA, Woodruff TK, Jeruss JS, Shea LD. Primordial follicle transplantation within designer biomaterial grafts produce live births in a mouse infertility model. Sci Rep 2015; 5: 17709
76 Vanacker J, Dolmans MM, Luyckx V, Donnez J, Amorim CA. First transplantation of isolated murine follicles in alginate. Regen Med 2014; 9 (5) 609-619
77 Amorim CA, Shikanov A. The artificial ovary: current status and future perspectives. Future Oncol 2016; 12 (20) 2323-2332
78 Tibbitt MW, Anseth KS. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 2009; 103 (4) 655-663
79 Kim J, Kong YP, Niedzielski SM, Singh RK, Putnam AJ, Shikanov A. Characterization of the crosslinking kinetics of multi-arm poly(ethylene glycol) hydrogels formed via Michael-type addition. Soft Matter 2016; 12 (7) 2076-2085
80 Kim J, Perez AS, Claflin J, David A, Zhou H, Shikanov A. Synthetic hydrogel supports the function and regeneration of artificial ovarian tissue in mice. NPJ Regenerative Med 2016; 16010;
81 Donnez J, Squifflet J, Pirard C, Jadoul P, Dolmans MM. Restoration of ovarian function after allografting of ovarian cortex between genetically non-identical sisters. Hum Reprod 2010; 25 (10) 2489-2495
82 David A, Day J, Shikanov A. Immunoisolation to prevent tissue graft rejection: Current knowledge and future use. Exp Biol Med (Maywood) 2016; 241 (9) 955-961
83 Bisceglie V. Ueber die antineoplastische Immunitat; Ueber die Wachstumsfaehigkeit der heterologen Geschwuelste in erwachsenen Tieren nach Einpflanzung in Kollodiumsaeckchen. Ztschr Krebsforsch 1933; 40: 141
84 Chick WL, Perna JJ, Lauris V , et al. Artificial pancreas using living beta cells. effects on glucose homeostasis in diabetic rats. Science 1977; 197 (4305): 780-782
85 Veiseh O, Doloff JC, Ma M , et al. Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates. Nat Mater 2015; 14 (6) 643-651
86 Boettler T, Schneider D, Cheng Y , et al. Pancreatic tissue transplanted in TheraCyte encapsulation devices is protected and prevents hyperglycemia in a mouse model of immune-mediated diabetes. Cell Transplant 2016; 25 (3) 609-614
87 Headen DM, Aubry G, Lu H, García AJ. Microfluidic-based generation of size-controlled, biofunctionalized synthetic polymer microgels for cell encapsulation. Adv Mater 2014; 26 (19) 3003-3008
88 David A, Day JR, Cichon AL, Lefferts A, Cascalho M, Shikanov A. Restoring ovarian endocrine function with encapsulated ovarian allograft in immune competent mice. Ann Biomed Eng