Fertility and Sterility
Volume 94, Issue 4 , Pages 1181-1188 , September 2010

Storage of cryopreserved reproductive tissues: evidence that cross-contamination of infectious agents is a negligible risk

  • Kimball O. Pomeroy, Ph.D.

      Affiliations

    • Arizona Reproductive Medicine Specialists, Phoenix, Arizona
  • ,
  • Stanley Harris, B.S.

      Affiliations

    • Methodist Hospital, Omaha, Nebraska
  • ,
  • Joe Conaghan, Ph.D.

      Affiliations

    • Pacific Fertility Center, San Francisco, California
  • ,
  • Margaret Papadakis, Ph.D.

      Affiliations

    • Carolinas Medical Center, Charlotte, North Carolina
  • ,
  • Grace Centola, Ph.D.

      Affiliations

    • Macedon, New York
  • ,
  • Rita Basuray, Ph.D.

      Affiliations

    • University of Kentucky, Lexington, Kentucky
  • ,
  • David Battaglia, Ph.D.

      Affiliations

    • Oregon Health and Science University, Portland, Oregon
    • Corresponding Author InformationReprint requests: David Battaglia, Ph.D., Oregon Health and Science University Fertility Consultants 3303 SW Bond Ave., Portland, OR 97239 (FAX: 503-418-3757).

Received 12 January 2009 ,Revised 24 March 2009 ,Accepted 15 April 2009.

References 

  1. Human cells, tissues, and cellular and tissue-based products; establishment registration and listing. Federal Register Vol. 66, No. 13, January 19, 2001. Available at: www.gpoaccess.gov/fr/. Last accessed August 4, 2010.
  2. Tedder RS, Zuckerman MA, Goldstone AH, Hawkins AE, Fielding A, Briggs EM, et al. Hepatitis B transmission from contaminated cryopreservation tank. Lancet. 1995;346:137–140
  3. Letur-Könirsch H, Collin G, Sifer C, Devaux A, Kuttenn F, Madelenat P, et al. Safety of cryopreservation straws for human gametes or embryos: a study with human immunodeficiency virus-1 under cryopreservation conditions. Hum Reprod. 2003;18:140–144
  4. Piasecka-Serafin M. The effect of the sediment accumulated in containers under experimental conditions on the infection of semen stored directly in liquid nitrogen (-196 degrees C). Bull Acad Pol Sci Biol. 1972;20:263–267
  5. Proposed approach to the regulation of cellular and tissue-based products: availability and public meeting. www.gpoaccess.gov/fr/ Federal Register Vol. 62, No. 42, March 4, 1997.
  6. Steyaert SR, Leroux-Roels GG, Dhont M. Infections in IVF: review and guidelines. Hum Reprod Update. 2000;6:432–441
  7. Speit G, Merk O. Evaluation of mutagenic effects of formaldehyde in vitro: detection of crosslinks and mutations in mouse lymphoma cells. Mutagenesis. 2002;17:183–187
  8. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000;62:1526–1535
  9. Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod. 1998;3:155–163
  10. Farin PW, Piedrahita JA, Farin CE. Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology. 2006;65:178–191
  11. Lindberg A, Ortman K, Alenius S. Seroconversion of bovine viral diarrhea virus (BVDV) in dairy heifers after embryo transfer. In: Proceedings of the 14th International Congress on Animal Reproduction, Stockholm, Sweden. 2000;1:250.
  12. Drew TW, Sandvik T, Wakeley P, Jones T, Howard P. BVD virus genotype 2 detected in British cattle. Vet Rec. 2002;151:551
  13. Wortley PM, Hammett TA, Fleming PL. Donor insemination and human immunodeficiency virus transmission. Obstet Gynecol. 1998;91:515–518
  14. Stringfellow DA, Givens MD. Infectious agents in bovine embryo production: hazards and solutions. Theriogenology. 2000;53:85–94
  15. Hare WCD, Mitchell D, Singh EL, Bouillant AMP, Eaglesome MD, Ruckerbauer FM, et al. Embryo transfer in relation to bovine leukemia virus (BLV) control and eradication. Can Vet J. 1985;26:231–234
  16. Wrathall AE, Mengeling WL. Effect of transferring parvovirus-infected fertilized pig eggs into seronegative gilts. Br Vet J. 1979;135:255–261
  17. Singh EL, Hare WCD, Thomas FC, Bielanski A. Embryo transfer as a means of controlling the transmission of viral infections. IV. Non-transmission of infectious bovine rhinotracheitis/infectious pustular vulvovaginitis virus from donors shedding virus. Theriogenology. 1983;20:169–176
  18. Gilbert RO, Coubrough RI, Weiss KE. The transmission of bluetongue virus by embryo transfer in sheep. Theriogenology. 1987;27:527–540
  19. Thibier M. Data retrieval committee statistics of embryo transfer—2007. IETS Embryo Transfer Newsletter. 2008;26:4–9
  20. Thibier M, Nibart M. Disease control and embryo imports. Theriogenology. 1987;27:37–47
  21. Wrathall AE, Sutmöller P. Potential of embryo transfer to control transmission of disease. In:  Stringfellow DA,  Seidel SM editor. Manual of the international embryo transfer society. 3rd ed. Savoy, IL: IETS; 1998;p. 17–44
  22. Singh EL, Eaglesome MD, Thomas FC, Papp-Vid G, Hare WCD. Embryo transfer as a means of controlling the transmission of viral infections. I. The in vitro exposure of preimplantation bovine embryos to akabane, bluetongue and bovine viral diarrhea viruses. Theriogenology. 1982;17:437–444
  23. Singh EL, McVicar JW, Hare WCD, Mebus CA. Embryo transfer as a means of controlling the transmission of viral infections. VII. The in vitro exposure of bovine and porcine embryos to foot-and-mouth disease virus. Theriogenology. 1986;26:587–593
  24. Bielanski A. Non-transmission of bacterial and viral microbes to embryos and semen stored in the vapour phase of liquid nitrogen in dry shippers. Cryobiology. 2005;50:206–210
  25. Tomlinson M, Sakkas D. Is a review of standard procedures for cryopreservation needed? Safe and effective cryopreservation—should sperm banks and fertility centres move toward storage in nitrogen vapour?. Hum Reprod. 2000;15:2460–2463
  26. Sherman JK. Synopsis of the use of frozen semen since 1964: state of the art of human semen banking. Fertil Steril. 1973;24:397–412
  27. American Association of Tissue Banks Committee. Frozen and cryopreserved tissue. In:  Pearson KA,  Brubaker SA editor. Standards for tissue banking. 11th ed. McLean; 2006;p. 54
  28. Fountain D, Ralston M, Higgins JB, Gorlin JB, Uhl LB, Wheeler C, et al. Liquid nitrogen freezers: a potential source of microbial contamination of hematopoietic stem cell components. Transfusion. 1997;37:585–591
  29. Appelbaum FR, Herzig GP, Graw RG, Bull MI, Bowles C, Gorin NC, et al. Study of cell dose and storage time on engraftment of cryopreserved autologous bone marrow in a canine model. Transplantation. 1978;26:245–248
  30. Leibo SP, Picton HM, Gosden RG. Cryopreservation of human spermatozoa. In:  Vayena E,  Rowe PJ,  Griffin PD editor. Current practices and controversies in assisted reproduction. Geneva: World Health Organization; 2001;p. 152–165
  31. Human cells, tissues, and cellular and tissue-based products: establishment registration and listing. Federal Register Vol. 72, No. 117, June 19, 2007.
  32. Bielanski A, Bergeron H, Lau PCK, Devenish J. Microbial contamination of embryos and semen during long term banking in liquid nitrogen. Cryobiology. 2003;46:146–152
  33. Vanroose G, Naumyaek H, Vansoom A, Ysebaert MT, Charlier G, Van Oostueldt P, et al. Structural aspects of the zona pellucida of in vitro-produced bovine embryos: a scanning electron and confocal laser scanning microscopic study. Biol Reprod. 2000;62:463–469
  34. Bielanski A, Dubuc C. In vitro fertilization of ova from cows experimentally infected with a non-cytopathic strain of bovine viral diarrhea virus. Anim Reprod Sci. 1995;38:215–221
  35. Hare WCD, Mitchell D, Singh EL, Bouillant AMP, Eaglesome MD, Ruckerbauer GM, et al. Embryo transfer in relation to bovine leukemia virus (BLV) control and eradication. Can Vet J. 1985;26:231–234
  36. Bowen RA, Howard TH, Pickett BW. Interaction of bluetongue virus with preimplantation embryos from mice and cattle. Am J Vet Res. 1982;43:1907–1911
  37. Potter ML, Corstvet RE, Looney CR, Fulton RW, Archbald LF, Godke RA. Evaluation of bovine viral diarrhea virus uptake by preimplantation embryos. Am J Vet Res. 1984;45:1778–1780
  38. Schlafer DH, Gillespie JH, Foote RH, Quick S, Pennow NW, Dougherty EP, et al. Experimental transmission of bovine viral diseases by insemination with contaminated semen or during embryo transfer. Dtsch tierarzth Wschr. 1990;97:68–72
  39. Van Soom A, Vanopdenbosch E, Mahmoudzadeh AR, de Kruif A. In vitro production of Belgian Blue cattle embryos: some data on the risk of viral infections. Vlaams Diergeneeskd Tijdschr. 1994;63:139–145
  40. Lopez-Teiijon M, Serra O, Olivares R, Moragas M, Castello C, Alvarez JG. Delivery of a healthy baby following the transfer of embryos cryopreserved for 13 years. RBM Online. 2006;13:821–822
  41. Fogarty NM, Maxwell WM, Eppleston J, Evans G. The viability of transferred sheep embryos after long-term cryopreservation. Reprod Fertil Dev. 2000;12:31–37
  42. Niskanen R, Alenius S, Belák K, Baule C, Belák S, Voges H, et al. Insemination of susceptible heifers with semen from a non-viraemic bull with persistent bovine virus diarrhoea virus infection localized in the testes. Reprod Domest Anim. 2002;37:171–175
  43. Bielanski A, Nadin-Davis S, Sapp T, Lutze-Wallace C. Viral contamination of embryos cryopreserved in liquid nitrogen. Cryobiology. 2000;40:110–116
  44. Baccetti B, Benedetto A, Collodel G, di Caro A, Garbuglia AR, Piomboni P. The debate on the presence of HIV-1 in human gametes. J Reprod Immunol. 1998;41:41–67
  45. Devaux A, Soula V, Sifer C, Branger M, Naouri M, Porcher R, et al. Hepatitis C virus detection in follicular fluid and culture media from HCV+ women, and viral risk during IVF procedures. Human Reprod. 2003;18:2342–2349
  46. Papaxanthos-Roche A, Trimoulet P, Commenges-Ducos M, Hocke C, Fleury HJA, Mayer G. PCR-detected hepatitis C virus RNA associated with human zona-intact oocytes collected from infected women for ART. Hum Reprod. 2004;19:1170–1175
  47. Lesourd F, Izopet J, Mervan C, Payen JL, Sandres K, Monrozies X, et al. Transmissions of hepatitis C virus during the ancillary procedures for assisted conception. Hum Reprod. 2000;15:1083–1085
  48. Schwartz P, Magerkurth C, Michelman HW. Scanning electron microscopy of the zona pellucida of human oocytes during intracytoplasmic sperm injection (ICSI). Hum Reprod. 1996;11:2693–2696
  49. Kuleshova LL, Shaw JM. A strategy for rapid cooling of mouse embryos within a double straw to eliminate the risk of contamination during storage in liquid nitrogen. Hum Reprod. 2000;15:2604–2609
  50. Stringfellow DA, Givens MD, Waldrop JG. Biosecurity issues associated with current and emerging embryo technologies. Reprod Fertil Devel. 2004;16:93–102
  51. Wrathall AE, Simmons HA, Bowles DJ, Jones S. Biosecurity strategies for conserving valuable livestock genetic resources. Reprod Fertil Devel. 2004;16:103–112

 K.O.P. has nothing to disclose. S.H. has nothing to disclose. J.C. is a member of the scientific advisory boards for Irvine Scientific and Serono. M.P. has nothing to disclose. G.C. has nothing to disclose. R.B. has nothing to disclose. D.B. has nothing to disclose.

PII: S0015-0282(09)00897-8

doi: 10.1016/j.fertnstert.2009.04.031

Fertility and Sterility
Volume 94, Issue 4 , Pages 1181-1188 , September 2010