Theriogenology
Volume 77, Issue 3 , Pages 467-482 , February 2012

A review of the risk of contamination of semen and embryos during cryopreservation and measures to limit cross-contamination during banking to prevent disease transmission in ET practices

  • A. Bielanski

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +1 613 228 6698; fax: +1 613 228 6669

Received 14 March 2011 ,Revised 12 July 2011 ,Accepted 29 July 2011.

References 

  1. Karrow AM , Critser JK . Reproductive Tissue Banking (Scientific Principles) . Acad. Press; 1997;
  2. Vajta G , Nagy ZP . Are programmable freezers still needed in the embryo laboratory? (Review on vitrification) . Reprod Biomed Online . 2006;12:779–796
  3. Yavin S , Arav A . Measurement of essential physical properties of vitrification solutions . Theriogenology . 2007;67:81–89
  4. Kuwayama M . Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method . Theriogenology . 2007;67:73–80
  5. Mazur P , Leibo SP , Seidel GE . Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status, and future directions . Biol Reprod . 2008;78:2–12
  6. Mazur P , Seki S . Survival of mouse oocytes after being cooled in a vitrification solution to −196°C at 95° to 70,000°C/min and warmed at 610° to 118,000°C/min: a new paradigm for cryopreservation by vitrification . Cryobiology . 2011;62:1–7
  7. Rall WF . Avoidance of microbial cross-contamination of cryopreserved gametes, embryos, cells and tissues during storage in liquid nitrogen . Embryologists' Newsletter . 2003;6:2–15
  8. Tomlinson M . Risk management in cryopreservation associated with assisted reproduction . Cryo Letters . 2008;29:165–174
  9. Benson EE . Cryopreservation of phytodiversity: a critical appraisal of theory and practice . Critical Reviews in Plant Sciences . 2008;27:141–219
  10. Bielanski A , Vajta G . Risk of contamination of germplasm during cryopreservation and cryobanking in IVF units . Hum Reprod . 2009;24:2457–2468
  11. Pomeroy KO , Harris S , Conaghan J , Papadakis M , Centola G , Basuray R , et al.  Storage of cryopreserved reproductive tissues: evidence that cross-contamination of infectious agents is a negligible risk . Fertil Steril . 2010;94:1181–1188
  12. Mortimer D . Current and future concepts and practices in human sperm cryobanking . Reprod Biomed Online . 2004;9:134–151
  13. Thibier MD , Wagner HG . World statistics for artificial insemination in cattle . Livest Prod Sci . 2002;74:203–212
  14. Stroud B . IETS statistics and data retrieval committee report . In: Embryo Transfer Newsletter . IETS; 2010;p. 11–20
  15. Kuwayama M , Vajta G , Ieda S , Kato O . Comparison of open and closed methods for vitrification of human embryos and the elimination of potential contamination . Reprod Biomed Online . 2005;11:608–614
  16. Lindberg A, Ortman K, Alenius S. Seroconversion of bovine viral diarrhea virus (BVDV) in dairy heifers after embryo transfer. Proceedings of the 1th International Congress on Animal Reproduction, Stockholm, Sweden, 2000;250 [Abstract].
  17. Drew TW , Sandvik P , Wakeley P , Jones T , Howard P . BVD virus genotype 2 detected in British cattle . Vet Rec . 2002;151:551–552
  18. In:  Stringfellow D ,  Givens D editor. Manual of the International Embryo Transfer Society. 4th edition. IETS; 2010;
  19. Anon  . In: The Terrestrial Animal Health Code. Vol. 1: The World Animal Health Organization (OIE); 2010;
  20. Polge C , Smith AU , Parkes AS . Revital of spermatozoa after vitrification and dehydration at low temperature . Nature . 1949;164:666
  21. Whittingham DG . Survival of mouse embryos after freezing and thawing . Nature . 1971;233:125–126
  22. Wilmut I . The effect of cooling rate, warming rate, cryoprotective agent, and stage of development on survival of mouse embryos . Life Sci . 1972;11:1071–1079
  23. Trounson AO , Mohr L . Human pregnancy following cryopreservation thawing and transfer of an eight-cell embryo . Nature . 1983;305:707–709
  24. Rall WF , Fahy GM . Ice-free cryopreservation of mouse embryos at −196 oC by vitrification . Nature . 1985;313:573–575
  25. Arav A . Vitrification of oocytes and embryos . In:  Lauria A ,  Gandolfi F editor. New Trends in Embryo Transfer. Portland Press; 1992;p. 255–264
  26. Tedeschi R , De Paoli P . Collection and preservation of frozen microorganisms . Methods Mol Biol . 2011;675:313–326
  27. Hubalek Z . Protectants used in the cryopreservation of microorganisms . Cryobiology . 2003;46:205–229
  28. Wallis C , Melnik JL . Stabilization of enveloped viruses by dimethyl sulfoxide . J Virol . 1968;2:953–954
  29. Van der Maaten MJ . Determining the health status of embryos for international movement . In:  Hare WCD ,  Seidel SM editor. International Embryo Movement. IETS; 1987;p. 147–161
  30. Mazurowa J , Rysanek M , Forejtek M . Effect of long-term freezing preservation on the level of bacterial contamination of the sperm . Vet Med (Praha) . 1975;20:147–152
  31. Wierzbowski S . Bull semen opportunistic pathogen and ubiquitary microflora . In: Disease Control in Semen and Embryos (FAO Animal Production and Health Paper). 1985;p. 21–28 23
  32. Stringfellow DA , Wolfe DF , McGuire JA , Lauerman LH , Gray BW , Sparling PH . Effects of embryo-freezing and thawing techniques on the survivability of Brucella abortus . Theriogenology . 1986;26:553–559
  33. Glander HJ , Rytter M , Baumann L , Schonborn C . Risk of transmission of sexually transmitted diseases by cryopreserved semen . Andrologia . 1986;18:323–325
  34. Jones SK , Darville JM . Transmission of virus particles by cryotherapy and multi-use caustic pencils: a problem to dermatologists? . Br J Dermatol . 1989;121:481–486
  35. Schaffer TW , Everett J , Silver GH , Came PE . Biohazard potential: recovery of infectious virus from the liquid nitrogen of a virus repository . Health Lab Sci . 1976;13:23–24
  36. Tedder RS , Zuckerman MA , Goldstone AH , Hawkins AE , Fielding A , Briggs EM , et al.  Hepatitis B transmission from contaminated cryopreservation tank . Lancet . 1995;346:137–139
  37. 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 oC) . Bull Acad Pol Sci Biol . 1972;20:263–267
  38. Bielanski A , Nadin Davis S , Sapp T , Lutze-Wallace C . Viral contamination of embryos cryopreserved in liquid nitrogen . Cryobiology . 2000;40:110–116
  39. Bielanski A , Bergeron H , Lau PC , Devenish J . Microbial contamination of embryos and semen during long term banking in liquid nitrogen . Cryobiology . 2003;46:46–52
  40. Stringfellow JS , Hathcock TL , Riddel KP , Stringfellow DA , Galik PK , Riddel MGJ , et al.  Introduction of Stenotrophomonas maltophilia through semen used for in vitro production of bovine embryos . Theriogenology . 1997;47:382; [Abstract]
  41. Van Soom A , Nauwynck H , Wrathall A . Scientific foundations for the epidemiologigal safety of embryo transfer . In:  Stringfellow DA ,  Givens D editor. Manual of the International Embryo Transfer Society. fourth ed.. IETS; 2010;p. 13–41
  42. Bielanski A . Disinfection procedures for controlling microorganisms in the semen and embryos of human and farm animals . Theriogenology . 2007;68:1–22
  43. Stringfellow D . Recommendations for the sanitary handling of in vivo-derived embryos . In:  Stringfellow DA ,  Givens D editor. Manual of the International Embryo Transfer Society. fourth ed.. IETS; 2010;p. 65–69
  44. Dejucq-Rainsford N , Jegou B . Viruses in semen and male genital tissues consequences for the reproductive system and therapeutic perspectives . Curr Pharm Des . 2004;10:557–575
  45. Hare WCD . Diseases transmissible by semen and embryo transfer technigues . OIE Tech Bull . 1985;4:1–117
  46. Guerin B , Pozzi N . Viruses in boar semen: detection and clinical as well as epidemiological consequences regarding disease transmission by artificial insemination . Theriogenology . 2005;63:556–572
  47. Garcia A , Sierra MF , Friberg J . Survival of bacteria after freezing of human semen in liquid nitrogen . Fertil Steril . 1981;35:549–551
  48. Mazzilli F , Delfino M , Imbrogno N , Elia J , Dondero F . Survival of micro-organisms in cryostorage of human sperm . Cell Tissue Bank . 2006;7:75–79
  49. Wrathall AE , Simmons HA , Van Soom A . Evaluation of risks of viral transmission to recipients of bovine embryos arising from fertilisation with virus-infected semen . Theriogenology . 2006;65:247–274
  50. Bielanski A , Lalonde J , Algire J . Transmission of noncytopathic bovine diarrhea virus by infected semen to embryo donors and by embryos to embryo transfer recipients and offspring . Reprod Fert Develop . 2009;22:251; [Abstract]
  51. Bielanski A , Lalonde A , Algire J . Risk of transmission of bovine herpes virus (BHV-1) by infected semen to recipients and embryos . Reprod Fertil Develop . 2008;21:173; [Abstract]
  52. Maertens A , Bourlet T , Plotton N , Pozzetto B , Levy R . Validation of safety procedures for the cryopreservation of semen contaminated with hepatitis C virus in assisted reproductive technology . Hum Reprod . 2004;19:1554–1557
  53. Morfeld KA , White B , Mills G , Krisher R , Mellencamp MA , Loskutoff NM . A novel sperm processing method for eliminating porcine reproductive and respiratory syndrome virus (PRRSv) from boar semen and its effects on embryo development in vitro and in vivo . Reprod Fert Devel . 2005;17:186; [Abstract]
  54. Loskutoff NM , Huyser C , Singh R , Morfeld KA , Walker DL , Thornhill AR , et al.  Removing HIV-1 and hepatitis C virus from semen: an improved method for washing sperm using a trypsinized silica particle suspension and a novel tube insert . Fertil Steril . 2005;84:1001–1010
  55. Herlong JL , Reubish K , Higdon HL , Boone WR . Quantitative and qualitative analysis of microorganisms in an assisted reproductive technology facility . Fertil Steril . 2008;89:847–853
  56. Cobo F , Concha A . Environmental microbial contamination in a stem cell bank . Lett Appl Microbiol . 2007;44:379–386
  57. Schiewe M , Hasler J . General hygiene and quality control practices in an embryo-production laboratory . In:  Stringfellow D ,  Givens D editor. Manual of the International Embryo Transfer Society. fourth ed.. IETS; 2010;p. 73–86
  58. Marquant-Le Guienne B , Guyader-Joly C , Ponsart C , Guerin B . General sanitary procedures associated with in vitro production of embryos . In:  Stringfellow D ,  Givens D editor. Manual of the International Embryo Transfer Society. fourth ed.. IETS; 2010;p. 57–65
  59. Morris CB . Cryopreservation of animal and human cell lines . Meth Mol Biol . 2007;386:227–237
  60. Nickolai DJ , Lammel CJ , Byford BA , Morris JH , Kaplan EB , Hadley WK , et al.  Effects of storage temperature and pH on the stability of eleven beta-lactam antibiotics in MIC trays . J Clin Microbiol . 1985;21:366–370
  61. Morris J . Contamination issues . In:  McLaughlin E ,  Pacey A ,  Elliot T editor. Safe Cryopreservation of Gametes and Embryos. Ladybrook Publishing; 1999;p. 26
  62. Radnot D , Farkas E . Sterility and cryosurgery . Arch Ophthalmol . 1966;75:302–303
  63. McBurnie LD , Bardo B . Validation of sterile filtration of liquid nitrogen . Pharmaceutical Technology North America . 2002;26:74–82
  64. Vajta G , Lewis IM , Kuwayama M , Greve T , Callesen H . Sterile application of the open pulled straw (OPS) vitrification method . Cryo Lett . 1998;19:389–392
  65. Wang Y . Reply: human ovarian tissue: vitrification versus conventional freezing . Hum Reprod . 2009;24:1768–1769
  66. Isachenko V . Response: efficacy of ultraviolet sterilization of liquid nitrogen . Reprod Biomed Online . 2011;22:501
  67. Parmegiani L , Accorsi A , Cognigni GE , Bernardi S , Troilo E , Filicori M . Sterilization of liquid nitrogen with ultraviolet irradiation for safe vitrification of human oocytes or embryos . Fertil Steril . 2010;94:1525–1528
  68. Linden KG , Thurston J , Schaefer R , Malley JP . Enhanced UV inactivation of adenoviruses under polychromatic UV lamps . Appl Environ Microbiol . 2007;73:7571–7574
  69. Van Soom A , Wrathall AE , Herrler A , Nauwynck HJ . Is the zona pellucida an efficient barrier to viral infection? . Reprod Fertil Dev . 2010;22:21–31
  70. Bielanski A , Schneider U , Pawlyshyn VP , Mapletoft RJ . Factors affecting survival of deep frozen bovine embryos in vitro: the effect of freezing container and method of removing cryoprotectant . Theriogenology . 1986;25:429–437
  71. Rall WF , Meyer TK . Zona fracture damage and its avoidance during the cryopreservation of mammalian embryos . Theriogenology . 1989;31:683–692
  72. Schiewe MC , Rall WF , Stuart LD , Wild DE . Analysis of cryoprotectant, cooling rate and in situ dilution using conventional or vitrification for cryopreserving sheep embryos . Theriogenology . 1991;36:270–293
  73. Van den Abbeel E , Van Steirteghem A . Zona pellucida damage to human embryos after cryopreservation and the consequences for their blastomere survival and in-vitro viability . Hum Reprod . 2000;15:373–378
  74. Moreira da Silva F , Metelo R . Relation between physical properties of the zona pellucida and viability of bovine embryos after slow-freezing and vitrification . Reprod Domest Anim . 2005;40:205–209
  75. Bielanski A , Sapp T , Lutze-Wallace C , Palasz A . The effect of high concentrations of cryoprotectants on the passage of bovine viral diarrhea virus through the zona pellucida of in vitro fertilized embryos . Anim Reprod Sci . 1999;55:83–90
  76. Vincent C , Pickering SJ , Johnson MH . The hardening effect of dimethylsulphoxide on the mouse zona pellucida requires the presence of an oocyte and is associated with a reduction in the number of cortical granules present . J Reprod Fertil . 1990;89:253–259
  77. Chen HI , Tsai CD , Wang HT , Hwang SM . Cryovial with partial membrane sealing can prevent liquid nitrogen penetration in submerged storage . Cryobiology . 2006;53:283–287
  78. Clarke GN . Sperm cryopreservation: is there a significant risk of cross-contamination? . Hum Reprod . 1999;14:2941–2943
  79. Benifla JL , Letur-Konirsch H , Collin G , Devaux A , Kuttenn F , Madelenat P , et al.  Safety of cryopreservation straws for human gametes or embryos: a preliminary study with human immunodeficiency virus-1 . Hum Reprod . 2000;15:2186–2189
  80. Letur-Konirsch 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
  81. Guerin B . CBS high security cryobanking systems (Product monograph) . In: Cryo Biosystem ITG . IMV Technologies Group; 2001;p. 25
  82. Russell PH , Lyaruu VH , Millar JD , Curry MR , Watson PF . The potential transmission of infectious agents by semen packaging during storage for artificial insemination . Anim Reprod Sci . 1997;4:337–342
  83. Bass LD , Denniston DJ , Maclellan LJ , Mccue PM , Seidel GE , Squires EL . Methanol as a cryoprotectant for equine embryos . Theriogenology . 2004;62:1153–1159
  84. Czlonkowska M , Pais K , Guszkiewicz A , Kossakowski M , Eysymont U . Freezing of sheep in 3.0 M methanol . Cryo Letters . 1991;2:11–16
  85. Rall WF , Czlonkowska M , Barton SC , Polge C . Cryoprotection of day-4 mouse embryos by methanol . J Reprod Fertil . 1984;70:293–300
  86. Willadsen SM . Factors affecting the survival of sheep embryos during deep-freezing and thawing . In:  Elliot K ,  Whelan J editor. The freezing of Mammalian Embryos. Elsevier-Exerpta Medica; 1977;p. 175–201
  87. Stachecki JJ , Garrisi J , Sabino S , Caetano JPJ , Wiemer KE , Cohen J . A new safe, simple and successful vitrification method for bovine and human blastocysts . Reprod Biomed Online . 2008;17:360–367
  88. Vajta G , Booth PJ , Holm P , Greve T , Callesen H . Successful vitrification of early stage bovine in vitro produced embryos with the open pulled straw (OPS) method . Cryo Lett . 1997;18:191–195
  89. Isachenko V , Katkov II , Yakovenko S , Lulat AG , Ulug M , Arvas A , et al.  Vitrification of human laser treated blastocysts within cut standard straws (CSS): novel aseptic packaging and reduced concentrations of cryoprotectants . Cryobiology . 2007;54:305–309
  90. Vanderzwalmen P , Bertin G , Debauche C , Standaert V , Bollen N , van Roosendaal E , et al.  Vitrification of human blastocysts with the Hemi-Straw carrier: application of assisted hatching after thawing . Hum Reprod . 2003;18:1504–1511
  91. Bielanski A , Hanniman A . Non-cross-contamination of bovine embryos with microbes using the OPS vitrification system . Reprod Fert Devel . 2007;19:232; [Abstract]
  92. Isachenko V , Montag M , Isachenko E , van der Ven H . Vitrification of mouse pronuclear embryos after polar body biopsy without direct contact with liquid nitrogen . Fertil Steril . 2005;84:1011–1016
  93. 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
  94. Larman MG , Gardner DK . Vitrification of mouse embryos with super-cooled air . Fertil Steril . 2011;95:1462–1466
  95. Schiewe MC . Microsecure vitrification (μS-VTF) procedure: optimum simplicity, security, cost-saving and effectiveness combining FDA-approved products . J Clin Embr . 2010;13:33–41
  96. Hirayama Y . Successful production of piglets derived from vitrified morulae and early blastocysts without direct exposure to liquid nitrogen . Reprod Fertil Develop . 2007;17:177; [Abstract]
  97. Yu XL , Deng W , Liu FJ , Li YH , Li XX , Zhang YL , et al.  Closed pulled straw vitrification of in vitro-produced and in vivo-produced bovine embryos . Theriogenology . 2010;73:474–479
  98. Isachenko V , Isachenko E , Montag M , Zaeva V , Krivokharchenko I , Nawroth F , et al.  Clean technique for cryoprotectant-free vitrification of human spermatozoa . Reprod Biomed Online . 2005;10:350–354
  99. Isachenko V , Montag M , Isachenko E , Zaeva V , Krivokharchenko I , Shafei R , et al.  Aseptic technology of vitrification of human pronuclear oocytes using open-pulled straws . Hum Reprod . 2005;20:492–496
  100. Criado E , Moalli F , Polentarutti N , Albani E , Morreale G , Menduni F , et al.  Experimental contamination assessment of a novel closed ultravitrification device . Fertil Steril . 2011;95:1777–1779
  101. Dinnyes A , Dai YP , Jiang S , Yang XZ . High developmental rates of vitrified bovine oocytes following parthenogenetic activation, in vitro fertilization, and somatic cell nuclear transfer . Biol Reprod . 2000;63:2; 513–8
  102. Yavin S , Aroyo A , Roth Z , Arav A . Embryo cryopreservation in the presence of low concentration of vitrification solution with sealed pulled straws in liquid nitrogen slush . Hum Reprod . 2009;24:797–804
  103. Faszer K , Draper D , Green JE , Morris J , Grout BW . Cryopreservation of horse semen under laboratory and field conditions using a Stirling Cycle freezer . Cryo Letters . 2006;27:179–186
  104. Bielanski A , Lalonde A . Effect of cryopreservation by slow cooling and vitrification on viral contamination of IVF embryos experimentally exposed to bovine viral diarrhea virus and bovine herpesvirus-1 . Theriogenology . 2009;72:919–925
  105. Ashwood-Snith J , Grant E . Genetic stability in cellular systems stored in the frozen state . In:  Elliot K ,  Whelan J editor. The Freezing of Mammalian Embryos. Elsevier-Exerpta Medica; 1977;p. 251–272
  106. Glenister PH , Lyon MF . Long-term storage of eight-cell mouse embryos at −196 degrees C . J In Vitro Fert Embryo Transf . 1986;3:20–27
  107. Riggs R , Mayer J , Dowling-Lacey D , Chi TF , Jones E , Oehninger S . Does storage time influence posthaw survival and pregnancy outcome? (An analysis of 11,768 cryopreserved human embryos) . Fertil Steril . 2010;93:109–115
  108. Fogarty NM , Maxwell WM , Eppleston J , Evans G . The viability of transferred sheep embryos after long-term cryopreservation . Reprod Fertil Dev . 2000;2:31–37
  109. Tomlinson M , Morroll D . Risks associated with cryopreservation: a survey of assisted conception units in the UK and Ireland . Hum Fertil (Camb) . 2008;11:33–42
  110. Morris GJ . The origin, ultrastructure, and microbiology of the sediment accumulating in liquid nitrogen storage vessels . Cryobiology . 2005;50:231–238
  111. Morris J . Cryopreservation and contamination . ART and Science . 2003;2:1–3
  112. Cobo A , Romero JL , Perez S , Los Santos MJ , Meseguer M , Remohi J . Storage of human oocytes in the vapor phase of nitrogen . Fertil Steril . 2010;94:1903–1907
  113. Fountain D , Ralston M , Higgins N , Gorlin JB , Wheeler C , Antin JH , et al.  Liquid nitrogen freezers: a potential source of microbial contamination of hematopoietic stem cell components . Transfusion . 1997;37:585–591
  114. Bielanski A . Non-transmission of bacterial and viral microbes to embryos and semen stored in the vapor phase of liquid nitrogen in dry shippers . Cryobiology . 2005;50:206–210
  115. Grout BW , Morris GJ . Contaminated liquid nitrogen vapour as a risk factor in pathogen transfer . Theriogenology . 2009;71:1079–1082
  116. Bielanski A . Experimental microbial contamination and disinfection of dry (vapour) shipper dewars designed for short-term storage and transportation of cryopreserved germplasm and other biological specimens . Theriogenology . 2005;63:1946–1957

PII: S0093-691X(11)00392-X

doi: 10.1016/j.theriogenology.2011.07.043

Theriogenology
Volume 77, Issue 3 , Pages 467-482 , February 2012

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