IVF in Nonhuman Primates: Current Status and Future Directions

  • Barry D. Bavister
  • Dorothy E. Boatman
Conference paper
Part of the Serono Symposia, USA book series (SERONOSYMP)


A number of laboratories during the past two decades have contributed to the current technical status of nonhuman primate IVF. A major rationale for interest in nonhuman primate IVF was, and still is, to provide data on early development that could be directly applicable to humans. However, it is ironic that progress in production of human embryos by IVF has always been somewhat more advanced than that in nonhuman primates. Thus, although the feasibility of IVF in monkeys was demonstrated by the early 1970s, the first documented human IVF took place several years earlier (Table 2.1). In the early years of IVF research in humans and in monkeys, it was difficult to demonstrate much progress beyond fertilization itself or cleavage to 2 cells. Yet the birth of the first human IVF baby (1) preceded by several years the first demonstrations of live births in nonhuman primates derived from IVF eggs (2, 3). Nevertheless, the chronology of these events does not mean that nonhuman primate IVF cannot point the way to significant improvements in human IVF technology nor increase understanding of key areas in human reproduction. Rather, the indication is that IVF technology in nonhuman primates may be best employed to examine specific events, such as oocyte maturation, sperm capacitation, or development of new culture media, that are more difficult to study in the context of human clinical IVF.


Rhesus Monkey Embryo Transfer Oocyte Maturation Zona Pellucida Acrosome Reaction 
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  1. 1.
    Steptoe PC, Edwards RG. Birth after the reimplantation of a human embryo (letter). Lancet 1978;2:366.PubMedCrossRefGoogle Scholar
  2. 2.
    Bavister BD, Boatman DE, Collins K, Dierschke DJ, Eisele SG. Birth of rhesus monkey infant following in vitro fertilization and non-surgical embryo transfer. Proc Natl Acad Sci USA 1984;81:2218–2222.PubMedCrossRefGoogle Scholar
  3. 3.
    Clayton O, Kuehl TJ. The first successful in vitro fertilization and embryo transfer in a nonhuman primate. Theriogenology 1984;21:228.CrossRefGoogle Scholar
  4. 4.
    Bavister BD, Boatman DE, Leibfried ML, Loose M, Vernon MW. Fertilization and cleavage of rhesus monkey oocytes in vitro. Biol Reprod 1983;28:983–999.PubMedCrossRefGoogle Scholar
  5. 5.
    Boatman DE, Bavister BD. Stimulation of rhesus monkey sperm capacitation by cyclic nucleotide mediators. J Reprod Fertil 1984;77:357–366.Google Scholar
  6. 6.
    Cranfield MR, Schaffer N, Bavister BD, et al. Assessment of oocytes retrieved from stimulated and unstimulated ovaries of pig-tailed macaques (Macaca nemestrina) as a model to enhance the genetic diversity of the captive lion-tailed macaque (Macaca silenus). Zoo Biol 1989;suppl 1:33–46.CrossRefGoogle Scholar
  7. 7.
    Balmaceda JP, Pool TB, Arana JB, Heitman TS, Asch RH. Successful in vitro fertilization and embryo transfer in cynomolgus monkeys. Fertil Steril 1984;42:791–795.PubMedGoogle Scholar
  8. 8.
    Menezo YJR, Guerin JF, Czyba JC. Improvement of human early embryo development in vitro by coculture on monolayers of Vero cells. Biol Reprod 1990;42:301–306.PubMedCrossRefGoogle Scholar
  9. 9.
    Winston NJ, Braude PR, Pickering SJ, et al. The incidence of abnormal morphology and nucleocytoplasmic ratios in 2-, 3- and 5-day human preembryos. Hum Reprod 1991;6:17–24.PubMedGoogle Scholar
  10. 10.
    Austin CR. Dilemmas in human IVF practice. In: Bavister BD, Cummins J, Roldan ERS, eds. Fertilization in mammals. Norwell, MA: Serono, Symposia, USA, 1990:373–379.Google Scholar
  11. 11.
    Boatman DE, Morgan PM, Bavister BD. Variables affecting the yield and developmental potential of embryos following superstimulation and in vitro fertilization in rhesus monkeys. Gamete Res 1986;13:327–338.CrossRefGoogle Scholar
  12. 12.
    Bavister BD, Dees HC, Schultz RD. Refractoriness of rhesus monkeys to repeated gonadotropin stimulation is due to formation of non-precipitating antibodies. Am J Reprod Immunol Microbiol 1986;11:11–16.PubMedGoogle Scholar
  13. 13.
    VandeVoort CA, Baughman WL, Stouffer RL. Comparison of different regimens of human gonadotropins for superovulation of rhesus monkeys: ovulatory response and subsequent luteal function. J In Vitro Fertil Embryo Transfer 1989;6:85–91.CrossRefGoogle Scholar
  14. 14.
    Morgan PM, Warikoo PK, Bavister BD. In vitro maturation of ovarian oocytes from unstimulated rhesus monkeys: assessment of cytoplasmic maturity by embryonic development after in vitro fertilization. Biol Reprod 1991;45:89–93.PubMedCrossRefGoogle Scholar
  15. 15.
    Schramm RD, Tennier MT, Boatman DE, Bavister BD. Chromatin configurations and meiotic competence of oocytes are related to follicular maturation in non gonadotropin-stimulated rhesus monkeys. Biol Reprod (in press).Google Scholar
  16. 16.
    Mastroianni L, Manson WA. Collection of monkey semen by electro-ejaculation. Proc Soc Exp Biol Med 1963;112:1025–1027.PubMedGoogle Scholar
  17. 17.
    Bavister BD, Leibfried ML, Lieberman G. Development of preimplantation embryos of the golden hamster in a defined culture medium. Biol Reprod 1983;28:235–247.PubMedCrossRefGoogle Scholar
  18. 18.
    Boatman DE. In vitro growth of nonhuman primate pre- and peri-implantation embryos. In: Bavister BD, ed. The mammalian preimplantation embryo. New York: Plenum Press, 1987:273–308.Google Scholar
  19. 19.
    Bavister BD. Oocyte maturation and in vitro fertilization in the rhesus monkey. In: Stouffer RL, ed. The primate ovary. New York: Plenum Press, 1987:119–137.Google Scholar
  20. 20.
    Chan PJ, Hutz RJ, Dukelow WR. Nonhuman primate in vitro fertilization: seasonality, cumulus cells, cyclic nucleotides, ribonucleic acid, and viability assays. Fertil Steril 1982;38:609–615.PubMedGoogle Scholar
  21. 21.
    Burkman LJ. Characterization of hyperactivated motility by human spermatozoa during capacitation: comparison of fertile and Oligozoospermie sperm populations. Arch Androl 1984;13:153–165.PubMedCrossRefGoogle Scholar
  22. 22.
    Burkman LJ. Temporal pattern of hyperactivation-like motility in human spermatozoa [Abstract]. Biol Reprod 1986;34(suppl 1):226.Google Scholar
  23. 23.
    Robertson L, Wolf DP, Tash JS. Temporal changes in motility parameters related to acrosomal status: identification and characterization of populations of hyperactivated human sperm. Biol Reprod 1988;39:797–805.PubMedCrossRefGoogle Scholar
  24. 24.
    Wolf DP, Thomson JA, Zelinski-Wooten MB, Stouffer RL. In vitro fertilization-embryo transfer in nonhuman primates: the technique and its applications. Mol Reprod Dev 1990;27:261–280.PubMedCrossRefGoogle Scholar
  25. 25.
    Boatman DE, Andrews JC, Bavister BD. A quantitative assay for capacitation: evaluation of multiple sperm penetration through the zona pellucida of salt-stored hamster eggs. Gamete Res 1988;19:19–29.PubMedCrossRefGoogle Scholar
  26. 26.
    Burkman LJ, Coddington CC, Franken DR, Kruger TF, Rosenwaks Z, Hodgen GD. The hemizona assay (HZA): development of a diagnostic test for the binding of human spermatozoa to the human hemizona pellucida to predict fertilization potential. Fertil Steril 1988;49:688–697.PubMedGoogle Scholar
  27. 27.
    Schatten G, Simerly C, Schatten H. Maternal inheritance of centrosomes in mammals? Studies on parthenogenesis and polyspermy in mice. Proc Natl Acad Sci USA 1991;88:6785–6789.PubMedCrossRefGoogle Scholar
  28. 28.
    Florman HM, Tombes RM, First NL, Babcock DF. An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of internal Ca2+ and pH that mediate mammalian sperm acrosomal exocytosis. Dev Biol 1989;135:133–146.PubMedCrossRefGoogle Scholar
  29. 29.
    Boatman DE. Oviductal modulators of sperm fertilizing ability. In: Bavister BD, Cummins J, Roldan ERS, eds. Fertilization in mammals. Norwell, MA: Serono Symposia, USA, 1990:223–238.Google Scholar
  30. 30.
    Barnett DK, Bavister BD. Hypotaurine requirement for in vitro development of golden hamster one-cell embryos into morulae and blastocysts, and production of term offspring from in vitro fertilized ova. Biol Reprod 1992.Google Scholar
  31. 31.
    Stewart-Savage J, Bavister BD. A cell surface block to polyspermy occurs in golden hamster eggs. Dev Biol 1988;128:150–157.PubMedCrossRefGoogle Scholar
  32. 32.
    Gordon JW. Zona drilling: a new approach to male infertility. J In Vitro Fertil Embryo Transfer 1990;7:223–228.CrossRefGoogle Scholar
  33. 33.
    Enders AC, Schlafke S, Boatman DE, Morgan PM, Bavister BD. Differentiation of blastocysts derived from in vitro fertilized rhesus monkey oocytes. Biol Reprod 1989;41:715–727.PubMedCrossRefGoogle Scholar
  34. 34.
    Bolton VN, Hawes SM, Taylor CT, Parsons JH. Development of spare human preimplantation embryos in vitro: an analysis of the correlations among gross morphology, cleavage rates, and development to the blastocyst. J In Vitro Fertil Embryo Transfer 1989;6:30–35.CrossRefGoogle Scholar
  35. 35.
    Lopata A, Hay DL. The potential of early human embryos to form blastocysts, hatch from their zona and secrete HCG in culture. Hum Reprod 1989;4:87–94.PubMedGoogle Scholar
  36. 36.
    Bolton VN, Wren ME, Parsons JH. Pregnancies after in vitro fertilization and transfer of human blastocysts. Fertil Steril 1991;55:830–832.PubMedGoogle Scholar
  37. 37.
    Gott AL, Hardy K, Winston RML, Leese HJ. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum Reprod 1990;5:104–108.PubMedGoogle Scholar
  38. 38.
    Seshagiri PB, Hearn JP. Protein-free culture media that support in vitro development of rhesus monkey blastocysts. ARTA 1992.Google Scholar
  39. 39.
    Tollner TL, VandeVoort CA, Overstreet JW, Drobnis EZ. Cryopreservation of spermatozoa from cynomolgus monkeys (Macaca fascicularis). J Reprod Fertil 1990:90:347–352.PubMedCrossRefGoogle Scholar
  40. 40.
    Morgan PM, Warikoo PK, Bavister BD. In vitro maturation of ovarian oocytes from unstimulated rhesus monkeys: assessment of cytoplasmic maturity by embryonic development after in vitro fertilization. Biol Reprod 1991;45:89–93.PubMedCrossRefGoogle Scholar
  41. 41.
    Parrish JJ, First NL. Bovine in vitro fertilization. In: Dunbar BS, O’Rand MG, eds. A comparative overview of mammalian fertilization. New York: Plenum Press, 1991:351–362.Google Scholar
  42. 42.
    Eppig JJ, Schroeder AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod 1989;41:268–276.PubMedCrossRefGoogle Scholar
  43. 43.
    Lanzendorf SE, Zelinski-Wooten MB, Stouffer RL, Wolf DP. Maturity at collection and the developmental potential of rhesus monkey oocytes. Biol Reprod 1990;42:703–711.PubMedCrossRefGoogle Scholar
  44. 44.
    Edwards RG, Bavister BD, Steptoe PC. Early stages of fertilization in vitro of human oocytes matured in vitro. Nature (London) 1969;221:632–635.PubMedCrossRefGoogle Scholar
  45. 45.
    Cline EM, Gould KG, Foley CW. Regulation of ovulation, recovery of mature ova and fertilization in vitro of mature ova of the squirrel monkey (Saimiri sciureus) [Abstract]. Fed Am Soc Exp Biol 1972;31:360.Google Scholar
  46. 46.
    Gould KG, Cline EM, Williams WL. Observations on the induction of ovulation and fertilization in vitro in the squirrel monkey (Saimiri sciureus). Fertil Steril 1973;24:260–268.PubMedGoogle Scholar
  47. 47.
    Kuehl TJ, Dukelow WR. Maturation and in vitro fertilization of follicular oocytes of the squirrel monkey (Saimiri sciureus). Biol Reprod 1979;21:545–556.PubMedCrossRefGoogle Scholar
  48. 48.
    Kreitman O, Lynch A, Nixon WE, Hodgen GD. Ovum collection, induced luteal dysfunction, in vitro fertilization, embryo development and low tubal ovum transfer in primates. In: Hafez ESE, Semm K, eds. In vitro fertilization and embryo transfer. Lancaster, UK: MTP Press, 1982:303–324.Google Scholar
  49. 49.
    Gould KG. Ovum recovery and in vitro fertilization in the chimpanzee. Fertil Steril 1983;40:378–383.PubMedGoogle Scholar
  50. 50.
    Morgan PM, Boatman DE, Collins K, Bavister BD. Complete preimplantation development in culture of in vitro fertilized rhesus monkey oocytes [Abstract]. Biol Reprod 1984;30(suppl 1):96.Google Scholar
  51. 51.
    Lopata A, Summers PM, Hearn JP. Births following the transfer of cultured embryos obtained by in vitro and in vivo fertilization in the marmoset monkey (Callithrix jacchus). Fertil Steril 1988;50:503–509.PubMedGoogle Scholar
  52. 52.
    Cranfield MR, Berger NG, Kempske S, Bavister BD, Boatman DE, Ialeggio DM. Macaque monkey birth following transfer of in vitro fertilized, frozen-thawed embryos to a surrogate mother [Abstract]. Theriogenology 1992;37:197.CrossRefGoogle Scholar
  53. 53.
    Oehninger S, Scott RT, Coddington CC, Franken DR, Acosta AA, Hodgen GD. Validation of the hemizona assay in a monkey model: influence of oocyte maturational stages. Fertil Steril 1989;51:881–885.PubMedGoogle Scholar
  54. 54.
    Bavister BD, Boatman DE. “Test-tube” primates: the next generation. Hum Reprod 1992;7:1035.PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 1993

Authors and Affiliations

  • Barry D. Bavister
  • Dorothy E. Boatman

There are no affiliations available

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