Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-84b7d79bbc-4hvwz Total loading time: 0 Render date: 2024-07-25T14:18:27.707Z Has data issue: false hasContentIssue false

Chapter 6 - Principles of Vitrification as a Method of Cryopreservation in Reproductive Biology and Medicine

from Section 2 - Reproductive Biology and Cryobiology

Published online by Cambridge University Press:  27 March 2021

By
Gregory M Fahy
Edited by
Jacques Donnez  and
S. Samuel Kim
Jacques Donnez
Affiliation:
Catholic University of Louvain, Brussels
S. Samuel Kim
Affiliation:
University of Kansas School of Medicine
Get access

Summary

The popularity of vitrification (literally, glass formation) as a method of cryopreservation for reproductive cells, tissues, and even organs is evident from the rising number of citations of these applications in PubMed (Figure 6.1). The success of vitrification is based on the remarkable fact that it has been possible in many cases to reconcile the extreme physical and chemical requirements of vitrification with the biological requirements for sustaining life. Essentially, the same basic physical process that produces obsidian, window panes, porcelain vases, amber, and lollipops can be applied to living cells and tissues to preserve them in a viable state for very long periods.

The basic biological feasibility of vitrification was first discovered by nature. It now appears that many “poikilohydric” animals (whose water content depends on the ambient humidity) seem to survive the winter at deep subzero temperatures in the vitreous or partially vitreous state, and this strategy of survival may be even more prevalent than freeze tolerance [1, 2]. In addition, there are complex organisms that can dry to a vitreous state and survive even at temperatures well above zero [3, 4]. Therefore, cryopreservation by vitrification is supported by a broad base of biological evidence and evolutionary experience.

Type
Chapter
Information
Fertility Preservation
Principles and Practice
 , pp. 49 - 66
Publisher: Cambridge University Press
Print publication year: 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Fahy, GM, Wowk, B. Principles of ice-free cryopreservation by vitrification. Methods Mol Biol, 2020;2180:(in press).Google Scholar
Fahy, GM. Overview of biological vitrification. In Liebermann, J, Tucker, M (eds.) Vitrification in Assisted Reproduction: From Basic Science to Clinical Application. New York: Taylor & Francis Books, Ltd. 2015, 1–22.Google Scholar
Sakurai, M, Furuki T, Akao K et al. Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci U S A, 2008;105:5093–5098.CrossRefGoogle Scholar
Hengherr, S, Worland, MR, Reuner, A, Brummer, F, Schill, RO. High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool, 2009;82:749–755.CrossRefGoogle ScholarPubMed
Gehenio, PM, Luyet, BJ. A study of the mechanism of death by cold in the plasmodium of the myxomycetes. Biodynamica, 1939;2:1–22.Google Scholar
Luyet, BJ, Gehenio, PM. The mechanism of injury and death by low temperature. Biodynamica, 1940;3:33–60.Google Scholar
Goetz, A, Goetz, SS. Vitrification and crystallization of organic cells at low temperatures. J Applied Physics, 1938;9:718–729.CrossRefGoogle Scholar
Luyet, B. The vitrification of organic colloids and of protoplasm. Biodynamica, 1937;1:1–14.Google Scholar
Fahy, GM, Hirsh, A. Prospects for organ preservation by vitrification. In Pegg, DE, Jacobsen, IA, Halasz, NA (eds.) Organ Preservation, Basic and Applied Aspects. Lancaster: MTP Press. 1982, 399–404.CrossRefGoogle Scholar
Mazur, P. Cryobiology: the freezing of biological systems. Science, 1970;168:939–949.CrossRefGoogle ScholarPubMed
Mullen, SF, Fahy, GM. Fundamental aspects of vitrification as a method of reproductive cell, tissue, and organ cryopreservation. In Donnez, J, Kim, S (eds) Principles & Practice of Fertility Preservation. Cambridge: Cambridge University Press. 2011, 145–163.Google Scholar
Mazur, P, Schneider, U, Mahowald, AP. Characteristics and kinetics of subzero chilling injury in Drosophila embryos. Cryobiology, 1992;29:39–68.CrossRefGoogle ScholarPubMed
Mazur, P, Cole, KW, Hall, JW, Schreuders, PD, Mahowald, AP. Cryobiological preservation of Drosophila embryos. Science, 1992;258:1896–1897.Google Scholar
Steponkus, PL, Myers SP, Lynch DV et al. Cryopreservation of Drosophila melanogaster embryos. Nature, 1990;345:170–172.Google Scholar
Martino, A, Songsasen, N, Leibo, SP. Development into blastocysts of bovine oocytes cryopreserved by ultra-rapid cooling. Biol Reprod, 1996;54:1059–1069.Google Scholar
Rall, WF, Meyer, TK. Zona fracture damage and its avoidance during the cryopreservation of mammalian embryos. Theriogenology, 1989;31:683–692.Google Scholar
Williams, RJ, Carnahan, DL. Fracture faces and other interfaces as ice nucleation sites. Cryobiology, 1990;27:479–482.CrossRefGoogle ScholarPubMed
Rall, WF, Fahy, GM. Ice-free cryopreservation of mouse embryos at −196°C by vitrification. Nature, 1985;313:573–575.CrossRefGoogle Scholar
Seki, S, Jin, B, Mazur, P. Extreme rapid warming yields high functional survivals of vitrified 8-cell mouse embryos even when suspended in a half-strength vitrification solution and cooled at moderate rates to −196°C. Cryobiology, 2014;68:71–78.Google Scholar
Vajta, G, Kuwayama, M, Vanderzwalmen, P. Disadvantages and benefits of vitrification. In Tucker, MJ, Liebermann, J (eds.) Vitrification in Assisted Reproduction, A User’s Manual and Trouble-Shooting Guide. London: Informa UK. 2007, 33–44.Google Scholar
Vajta, G. Are programmable freezers still needed in the embryo laboratory? Review on vitrification. Reprod Biomed Online, 2006;12:779–796.Google Scholar
Taylor, MJ, Song, YC, Brockbank, KG. Vitrification in tissue preservation: new developments. In Fuller, BJ, Lane, N, Benson, EE (eds.) Life in the Frozen State. Boca Raton: CRC Press. 2004, 603–641.CrossRefGoogle Scholar
Fahy, GM. Vitrification. In McGrath, JJ, Diller, KR (eds.) Low Temperature Biotechnology: Emerging Applications and Engineering Contributions. New York: American Society of Mechanical Engineers. 1988, 113–146.Google Scholar
Fahy, GM, MacFarlane, DR, Angell, CA, Meryman, HT. Vitrification as an approach to cryopreservation. Cryobiology, 1984;21:407–426.Google Scholar
Wowk, B. Thermodynamic aspects of vitrification. Cryobiology, 2010;60:11–22.Google Scholar
Angell, CA. Liquid fragility and the glass transition in water and aqueous solutions. Chemical Reviews, 2002;102:2627–2650.Google Scholar
Fahy, GM, Rall, WF. Vitrification: An overview. In Liebermann, J, Tucker, MJ (eds.) Vitrification in Assisted Reproduction: A User’s Manual and Troubleshooting Guide. London: Informa Healthcare. 2007, 1–20.Google Scholar
Bruggeller, P, Mayer, E. Complete vitrification in pure liquid water and dilute aqueous solutions. Nature, 1980;288:569–571.Google Scholar
Fahy, GM, Levy, DI, Ali, SE. Some emerging principles underlying the physical properties, biological actions, and utility of vitrification solutions. Cryobiology, 1987;24:196–213.Google Scholar
MacFarlane, DR. Devitrification in glass-forming aqueous solutions. Cryobiology, 1986;23:230–244.Google Scholar
MacFarlane, DR, Forsyth, M. Devitrification and recrystallization of glass forming aqueous solutions. In Pegg, DE, Karow, AM, Jr (eds.) The Biophysics of Organ Cryopreservation. New York: Plenum Press. 1987, 237–257.Google Scholar
Takahashi, T, Hirsh, A, Erbe, EF et al. Vitrification of human monocytes. Cryobiology, 1986;23:103–115.Google Scholar
Fahy, GM. Understanding and controlling ice nucleation and growth in the renal inner medulla. Cryobiology, 2015;71:540.CrossRefGoogle Scholar
Forsyth, M, MacFarlane, DR. Recrystallization revisited. Cryo-Letters, 1986;7:367–378.Google Scholar
Goetz, A, Goetz, SS. Death by devitrification in yeast cells. Biodynamica, 1938;2:1–8.Google Scholar
Bank, H. Visualization of freezing damage. II. Structural alterations during warming. Cryobiology, 1973;10:157–170.CrossRefGoogle ScholarPubMed
Boutron, P. Comparison with the theory of the kinetics and extent of ice crystallization and of the glass-forming tendency in aqueous cryoprotective solutions. Cryobiology, 1986;23:88–102.Google Scholar
Boutron, P, Mehl, P. Theoretical prediction of devitrification tendency: determination of critical warming rates without using finite expansions. Cryobiology, 1990;27:359–377.Google Scholar
Boutron, P. Glass-forming tendency and stability of the amorphous state in solutions of a 2,3-butanediol containing mainly the levo and dextro isomers in water, buffer, and Euro-Collins. Cryobiology, 1993;30:86–97.Google Scholar
Stiles, W. On the cause of cold death of plants. Protoplasma, 1930;9:459–468.Google Scholar
Anonymous. Curriculum vitae and list of publications of B. J. Luyet. Cryobiology, 1975;12:440–453.Google Scholar
Luyet, BJ, Thoennes, G. The survival of plant cells immersed in liquid air. Science, 1938;88:284–285.Google Scholar
Luyet, BJ, Gehenio, PM. The survival of moss vitrified in liquid air and its relation to water content. Biodynamica, 1938;2:1–7.Google Scholar
Keith, SC, Jr. Factors influencing the survival of bacteria at temperatures in the vicinity of the freezing point of water. Science, 1913;37:877–879.Google Scholar
Smith, AU. Effects of low temperatures on living cells and tissues. In Harris, RJC (ed.) Biological Applications of Freezing and Drying. New York: Academic Press. 1954, 1–53.Google Scholar
Polge, C, Smith, AU, Parkes, AS. Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature, 1949;164:666.Google Scholar
Lovelock, JE. The protective action of neutral solutes against haemolysis by freezing and thawing. Biochem J, 1954;56:265–270.CrossRefGoogle ScholarPubMed
Luyet, BJ, Gehenio, PM. Effect of the rewarming velocity on the survival of embryonic tissues frozen after treatment with ethylene glycol. Biodynamica, 1954;7:213–223.Google ScholarPubMed
Meryman, HT. X-ray analysis of rapidly frozen gelatin gels. Biodynamica, 1958;8:69–72.Google Scholar
Luyet, B, Rapatz, G. Patterns of ice formation in some aqueous solutions. Biodynamica, 1958;8:1–68.Google Scholar
Luyet, B. On the amount of water remaining amorphous in frozen aqueous solutions. Biodynamica, 1969;10:277–291.Google Scholar
Dubochet, J, McDowall, AW. Vitrification of pure water for electron microscopy. J Microsc, 1981;124:RP3–RP4.Google Scholar
Farrant, J. Mechanism of cell damage during freezing and thawing and its prevention. Nature, 1965;205:1284–1287.Google Scholar
Luyet, B, Kroener, C. The temperature of the “glass transition” in aqueous solutions of glycerol and ethylene glycol. Biodynamica, 1966;10:33–40.Google ScholarPubMed
Luyet, B, Rasmussen, D. Study by differential thermal analysis of the temperatures of instability of rapidly cooled solutions of glycerol, ethylene glycol, sucrose, and glucose. Biodynamica, 1968;10:167–191.Google Scholar
Rasmussen, D, Luyet, B. Complementary study of some non-equilibrium phase transitions in frozen solutions of glycerol, ethylene glycol, glucose, and sucrose. Biodynamica, 1969;10:319–331.Google Scholar
Rasmussen, D, Luyet, B. Contribution to the establishment of the temperature-concentration curves of homogeneous nucleation in solutions of some cryoprotective agents. Biodynamica, 1970;11:33–44.Google Scholar
Luyet, B, Rasmussen, DH. On some inconspicuous changes occurring in aqueous systems subjected to below zero C temperatures. Biodynamica, 1973;11:209–215.Google Scholar
Rapatz, G, Luyet, B. Electron microscope study of erythrocytes in rapidly cooled suspensions containing various concentrations of glycerol. Biodynamica, 1968;10:193–210.Google Scholar
Rapatz, G. Resumption of activity in frog hearts after freezing to low temperatures. Biodynamica, 1970;11:1–12.Google Scholar
Rapatz, G, Keener, R. Effect of concentration of ethylene glycol on the recovery of frog hearts after freezing to low temperatures. Cryobiology, 1974;11:571–572.Google Scholar
Boutron, P, Kaufmann, A. Stability of the amorphous state in the system water-glycerol-dimethylsulfoxide. Cryobiology, 1978;15:93–108.Google Scholar
Boutron, P, Kaufmann, A. Stability of the amorphous state in the system water-glycerol-ethylene glycol. Cryobiology, 1979;16:83–89.Google Scholar
Boutron, P. Stability of the amorphous state in the system water-1,2-propanediol. Cryobiology, 1979;16:557–568.Google Scholar
Boutron, P. levo- and dextro-2,3-butanediol and their racemic mixture: very efficient solutes for vitrification. Cryobiology, 1990;27:55–69.Google Scholar
Boutron, P, Arnaud, F. Comparison of the cryoprotection of red blood cells by 1,2-propanediol and glycerol. Cryobiology, 1984;21:348–358.Google Scholar
Mehl, P, Boutron, P. Cryoprotection of red blood cells by 1,3-butanediol and 2,3-butanediol. Cryobiology, 1988;25:44–54.Google Scholar
James, ER. Cryopreservation of Schistosoma mansoni schistosomula using 40% v/v (10 M) methanol and rapid cooling. Cryo-Letters, 1980;1:535–544.Google Scholar
James, ER, Farrant, J. Recovery of infective Schistosoma mansoni schistosomula from liquid nitrogen: a step towards storage of a live schistosomiasis vaccine. Trans Roy Soc Trop Med Hyg, 1977;71:498–500.CrossRefGoogle ScholarPubMed
Fahy, GM. Vitrification as an approach to organ cryopreservation: past, present, and future. In Smit Sibinga, CT, Das, PC, Meryman, HT (eds.) Cryopreservation and Low Temperature Biology in Blood Transfusion. Boston: Kluwer. 1990, 255–268.Google Scholar
Fahy, GM. Prospects for vitrification of whole organs. Cryobiology, 1981;18:617.Google Scholar
MacFarlane, DR, Angell, CA, Fahy, GM. Homogeneous nucleation and glass formation in cryoprotective systems at high pressures. Cryo-Letters, 1981;2:353–358.Google Scholar
Fahy, GM, MacFarlane, DR, Angell, CA. Recent progress toward vitrification of kidneys. Cryobiology, 1982;19:668–669.Google Scholar
Fahy, GM, MacFarlane, DR, Angell, CA, Meryman, HT. Vitrification as an approach to cryopreservation. Cryobiology, 1983;20:699.Google Scholar
Rall, WF, Reid, DS, Farrant, J. Innocuous biological freezing during warming. Nature, 1980;286:511–514.Google Scholar
Rall, WF. The role of intracellular ice in the slow warming injury of mouse embryos. In Zeilmaker, GH (ed.) Frozen Storage of Laboratory Animals. New York: Gustav Fischer Verlag. 1981, 33–44.Google Scholar
Lehn-Jensen, H, Rall, WF. Cryomicroscopic observations of cattle embryos during freezing and thawing. Theriogenology, 1983;19:263–277.Google Scholar
Ashburner, M. Frosted flies. Science, 1992;258:1896–1897.Google Scholar
Mazur, P, Seki, S. Survival of mouse ooctyes 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.Google Scholar
Fahy, GM, Wowk B, Wu J et al. Cryopreservation of organs by vitrification: perspectives and recent advances. Cryobiology, 2004;48:157–178.CrossRefGoogle ScholarPubMed
Baudot, A, Alger, L, Boutron, P. Glass-forming tendency in the system water-dimethyl sulfoxide. Cryobiology, 2000;40:151–158.Google Scholar
Baudot, A, Odagescu, V. Thermal properties of ethylene glycol and aqueous solutions. Cryobiology, 2004;48:283–294.Google Scholar
Toner, M, Cravalho, EG, Chiang, YM. Vitrification of biological cell suspensions: the importance of ultrarapid cooling and warming. Cryobiology, 1988;25:551.CrossRefGoogle Scholar
Kuleshova, LL, MacFarlane, DR, Trounson, AO, Shaw, JM. Sugars exert a major influence on the vitrification properties of ethylene glycol-based solutions and have low toxicity to embryos and oocytes. Cryobiology, 1999;38:119–130.Google Scholar
Fahy, GM. Process for preparing novel ice-controlling molecules. US Patent 6,303,388 B1 (October 16, 2001).Google Scholar
Wowk, B, Leitl, E, Rasch, CM et al. Vitrification enhancement by synthetic ice blocking agents. Cryobiology, 2000;40:228–236.Google Scholar
Wowk, B, Fahy, GM. Inhibition of bacterial ice nucleation by polyglycerol polymers. Cryobiology, 2002;44:14–23.Google Scholar
Kami, D, Kasuga, J, Arakawa, K, Fujikawa, S. Improved cryopreservation by diluted vitrification solution with supercooling-facilitating flavonol glycoside. Cryobiology, 2008;57:242–245.Google Scholar
Shibao, Y, Fujiwara, K, Kawasaki, Y et al. The effect of a novel cryoprotective agent, carboxylated epsilon-poly-l-lysine, on the developmental ability of re-vitrified mouse embryos at the pronuclear stage. Cryobiology, 2014;68:200–204.Google Scholar
Takahashi, T, Hirsh, A, Erbe, E, Williams, RJ. Mechanism of cryoprotection by extracellular polymeric solutes. Biophys J, 1988;54:509–518.Google Scholar
Fahy, GM, Saur, J, Williams, RJ. Physical problems with the vitrification of large biological systems. Cryobiology, 1990;27:492–510.Google Scholar
Fahy, GM, Wowk B, Pagotan R et al. Physical and biological aspects of renal vitrification. Organogenesis, 2009;5:167–175.Google Scholar
Pegg, DE, Wusteman, MC, Boylan, S. Fractures in cryopreserved elastic arteries. Cryobiology, 1997;34:183–192.Google Scholar
McIntyre, RL, Fahy, GM. Aldehyde-stabilized cryopreservation. Cryobiology, 2015;71:448–458.Google Scholar
Manuchehrabadi, N, Gao Z, Zhang J et al. Improved tissue cryopreservation using inductive heating of magnetic nanoparticles. Sci Transl Med, 2017;9:eaah4586.Google Scholar
Ali, J, Shelton, J. Development of vitrification solutions. In Tucker, MJ, Liebermann, J (eds.) Vitrification in Assisted Reproduction, A User’s Manual and Trouble-shooting Guide. London: Informa Healthcare. 2007, 45–63.Google Scholar
Fahy, GM, Wowk, B, Wu, J, Paynter, S. Improved vitrification solutions based on predictability of vitrification solution toxicity. Cryobiology, 2004;48:22–35.Google Scholar
McGrath, JJ. Cold shock: thermoelastic stress in chilled biological membranes. In Diller, KR (ed.) Network Thermodynamics, Heat and Mass Transfer in Biotechnology. New York: United Engineering Center. 1987, 57–66.Google Scholar
Ting, AY, Yeoman RR, Campos JR et al. Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Hum Reprod, 2013;28:1267–1279.Google Scholar
Briard, JG, Ferandez, M, de Luna, P, Woo, TK, Ben, RN. QSAR accelerated discovery of potent ice recrystallization inhibitors. Sci Rep, 2016;6 DOI:10.1038/srep26403.Google Scholar
Poisson, JS, Acker, JP, Briard, JG, Meyer, JE, Ben, RN. Modulating intracellular ice growth with cell permeable small molecule ice recrystallization inhibitors. Langmuir, 2019 June 11;35(23):7452–7458.Google Scholar
Fahy, GM, Guan, N, De Graaf, IAM et al. Cryopreservation of precision-cut tissue slices. Xenobiotica, 2013;43:113–132.Google Scholar
Fahy, GM. Cryoprotectant toxicity neutralization. Cryobiology, 2010;60:S45–S53.Google Scholar
Larman, MG, Katz-Jaffe, MG, Sheehan, CB, Gardner, DK. 1,2-propanediol and the type of cryopreservation procedure adversely affect mouse oocyte physiology. Hum Reprod, 2007;22:250–259.CrossRefGoogle ScholarPubMed
Elmoazzen, HY, Elliott, JA, McGann, LE. Osmotic transport across cell membranes in nondilute solutions: a new nondilute solute transport equation. Biophys J, 2009;96:2559–2571.Google Scholar
Benson, JD, Kearsley, AJ, Higgins, AZ. Mathematical optimization of procedures for cryoprotectant equilibration using a toxicity cost function. Cryobiology, 2012;64:144–151.Google Scholar
Zeron, Y, Tomczak, M, Crowe, J, Arav, A. The effect of liposomes on thermotropic membrane phase transitions of bovine spermatozoa and oocytes: implications for reducing chilling sensitivity. Cryobiology, 2002;45:143–152.CrossRefGoogle ScholarPubMed
Horvath, G, Seidel, GE, Jr. Vitrification of bovine oocytes after treatment with cholesterol-loaded methyl-beta-cyclodextrin. Theriogenology, 2006;66:1026–1033.Google Scholar
Burton, V, Mitchell, HK, Young, P, Petersen, NS. Heat shock protection against cold stress of Drosophila melanogaster. Mol Cell Biol, 1988;8:3550–3552.Google Scholar
Tomczak, MM, Hincha DK, Estrada SD et al. A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophy J, 2002;82:874–881.Google Scholar
Zhou, GB, Li, N. Cryopreservation of porcine oocytes: recent advances. Mol Hum Reprod, 2009;15:279–285.Google Scholar
Cameron, RD, Beebe, LF, Blackshaw, AW. Cryopreservation and transfer of pig embryos. Soc Reprod Fertil Suppl, 2006;62:277–291.Google Scholar
Song, YC et al. Stability of vitrified tissues in the vapor phase of liquid nitrogen. Cryobiology, 2002;45:243.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×