Citation: | Ruidong Ma, Ziyuan Wang, Ren Shen, Zhiquan Shu, Chen Ming, Dayong Gao. Rewarming strategies for cryopreservation: Technological challenges and opportunities in energy conversion[J]. Frigid Zone Medicine, 2025, 5(2): 91-107. doi: 10.1515/fzm-2025-0010 |
[1] |
Polge C, Smith A U, Parkes A S. Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature, 1949; 164(4172): 666. doi: 10.1038/164666a0
|
[2] |
Yánez-Ortiz I, Catalán J, Rodríguez-Gil J E, et al. Advances in sperm cryopreservation in farm animals: Cattle, horse, pig and sheep. Anim Reprod Sci, 2022, 246: 106904 doi: 10.1016/j.anireprosci.2021.106904
|
[3] |
Bedaiwy M A, El-Nashar S A, El Saman A M, et al. Reproductive outcome after transplantation of ovarian tissue: a systematic review. Hum Reprod, 2008; 23(12): 2709-2717. doi: 10.1093/humrep/den301
|
[4] |
Comizzoli P. Biobanking efforts and new advances in male fertility preservation for rare and endangered species. Asian J Androl, 2015; 17(4): 640-645. doi: 10.4103/1008-682X.153849
|
[5] |
Sharafi M, Borghei-Rad S M, Hezavehei M, et al. Cryopreservation of semen in domestic animals: a review of current challenges, applications, and prospective strategies. Animals-Basel, 2022; 12(23): 3271. doi: 10.3390/ani12233271
|
[6] |
Pence V C, Bruns E B. The tip of the iceberg: cryopreservation needs for meeting the challenge of exceptional plant conservation. Plants-Basel, 2022; 11(12): 1528. doi: 10.3390/plants11121528
|
[7] |
Rudick B, Opper N, Paulson R, et al. The status of oocyte cryopreservation in the united states. Fertil Steril, 2010; 94(7): 26422646. doi: 10.1016/j.fertnstert.2010.04.079
|
[8] |
Kim S S, Battaglia D E, Soules M R. The future of human ovarian cryopreservation and transplantation: fertility and beyond. Fertil Steril, 2001; 75(6): 1049-1056. doi: 10.1016/S0015-0282(01)01790-3
|
[9] |
Pomeroy K O, Comizzoli P, Rushing J S, et al. The art of cryopreservation and its changing landscape. Fertil Steril, 2022; 117(3): 469-476. doi: 10.1016/j.fertnstert.2022.01.018
|
[10] |
Wowk B. Thermodynamic aspects of vitrification. Cryobiology, 2010; 60(1): 11-22. doi: 10.1016/j.cryobiol.2009.05.007
|
[11] |
Huang Y, Dong Y, Gao B, et al. Transmembrane water transport and intracellular ice formation of human umbilical vein endothelial cells during freezing. Biopreserv Biobank, 2022; 20(4): 311-316. doi: 10.1089/bio.2022.0111
|
[12] |
Ma R, Peng J, Ren S, et al. Development of a 3-in-1 multifunctional cell processing system and optimization of cell type-dependent protocols for CPA addition/removal. Int Commun Heat Mass Transfer, 2025; 161: 108511. doi: 10.1016/j.icheatmasstransfer.2024.108511
|
[13] |
Hoffman D I, Zellman G L, Fair C C, et al. Cryopreserved embryos in the united states and their availability for research. Fertil Steril, 2003; 79(5): 1063-1069. doi: 10.1016/S0015-0282(03)00172-9
|
[14] |
Massip A, Vanderzwalmen P, Ectors F. Recent progress in cryopreservation of cattle embryos. Theriogenology, 1987; 27(1): 69-79. doi: 10.1016/0093-691X(87)90071-9
|
[15] |
Gao F, Ma R, Ren S, et al. Cryopreservation and biobanking of gametes, embryos, and reproductive tissues. Biopreserv Biobank, 2024; 22(1): 1-3. doi: 10.1089/bio.2024.29132.editorial
|
[16] |
Taylor M J, Weegman B P, Baicu S C, et al. New approaches to cryopreservation of cells, tissues, and organs. Transfus Med Hemother, 2019; 46(3): 197-215. doi: 10.1159/000499453
|
[17] |
Ruiz-Delgado G J, Mancias-Guerra C, Tamez-Gomez E L, et al. Dimethyl sulfoxide-induced toxicity in cord blood stem cell transplantation: report of three cases and review of the literature. Acta Haematol, 2009; 122(1): 1-5. doi: 10.1159/000227267
|
[18] |
Triana E, Ortega S, Azqueta C, et al. Thawing of cryopreserved hematopoietic progenitor cells from apheresis with a new dry-warming device. Transfusion, 2013; 53(1): 85-90. doi: 10.1111/j.1537-2995.2012.03669.x
|
[19] |
Shu Z Q, Hughes S M, Fang C F, et al. A study of the osmotic characteristics, water permeability, and cryoprotectant permeability of human vaginal immune cells. Cryobiology, 2016; 72(2): 93-99. doi: 10.1016/j.cryobiol.2016.03.003
|
[20] |
Wang L, Fu R, Xu C, et al. Methods and applications of full-field optical coherence tomography: a review. J Biomed Opt, 2022; 27(5): 050901. doi: 10.1117/1.JBO.27.5.050901
|
[21] |
Mazur P, Leibo S P, Chu E H. A two-factor hypothesis of freezing injury. Evidence from chinese hamster tissue-culture cells. Exp Cell Res, 1972; 71(2): 345-355. doi: 10.1016/0014-4827(72)90303-5
|
[22] |
Gao D, Critser J K. Mechanisms of cryoinjury in living cells. ILAR J, 2000; 41(4): 187-196. doi: 10.1093/ilar.41.4.187
|
[23] |
Mazur P. Freezing of living cells: mechanisms and implications. Am J Physiol, 1984; 247(3 Pt 1): C125-142. doi: 10.1152/ajpcell.1984.247.3.C125
|
[24] |
Karlsson J O M, Toner M. Long-term storage of tissues by cryopreservation: critical issues. Biomaterials, 1996; 17(3): 243-256. doi: 10.1016/0142-9612(96)85562-1
|
[25] |
Hocki S, Semple E, Leibo S P. Effect of cooling and warming rates during cryopreservation on survival of in vitro-produced bovine embryos. Theriogenology, 1996; 46(5): 837-847. doi: 10.1016/S0093-691X(96)00241-5
|
[26] |
Bank H. Visualization of freezing damage. 2. Structural alterations during warming. Cryobiology, 1973; 10(2): 157-170. doi: 10.1016/0011-2240(73)90023-0
|
[27] |
Fahy G M M D R, Angell C A, et al. Vitrification as an approach to cryopreservation. Cryobiology, 1984; 21(4): 407-426. doi: 10.1016/0011-2240(84)90079-8
|
[28] |
Amorim C A, Curaba M, Van Langendonckt A, et al. Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod Biomed Online, 2011; 23(2): 160-186. doi: 10.1016/j.rbmo.2011.04.005
|
[29] |
Shi Q, Xie Y, Wang Y, et al. Vitrification versus slow freezing for human ovarian tissue cryopreservation: a systematic review and meta-analysis. Sci Rep, 2017; 7(1): 8538. doi: 10.1038/s41598-017-09005-7
|
[30] |
Sharma A, Lee C Y, Namsrai B E, et al. Cryopreservation of whole rat livers by vitrification and nanowarming. Ann Biomed Eng, 2023; 51(3): 566-577. doi: 10.1007/s10439-022-03064-2
|
[31] |
Solanki P K, Rabin Y. Thermomechanical stress analysis of rabbit kidney and human kidney during cryopreservation by vitrification with the application of radiofrequency heating. Cryobiology, 2021; 100: 180-192. doi: 10.1016/j.cryobiol.2021.01.002
|
[32] |
Zhao G, Liu Z F, Zhang A L, et al. Theoretical analyses of thermal stress of blood vessel during cryopreservation. Cryo Letters, 2005; 26(4): 239-250.
|
[33] |
Solanki P K, Bischof J C, Rabin Y. Thermo-mechanical stress analysis of cryopreservation in cryobags and the potential benefit of nanowarming. Cryobiology, 2017; 76: 129-139. doi: 10.1016/j.cryobiol.2017.02.001
|
[34] |
Hua Z Z, Xu H Y, Zhou G Y, et al. Analyses of thermal stress and fracture during cryopreservation of blood vessel. Sci China Ser E-Technol Sci, 2000; 44: 158-163. doi: 10.1007/BF03014626
|
[35] |
Peng J, Ma R, Ren S, et al. A study of thermal stress generation during the rewarming process of cryopreserved large biomaterials. Cryobiology, 2021; 103: 167-168. doi: 10.1016/j.cryobiol.2021.11.042
|
[36] |
Yong K W, Laouar L, Elliott J A W, et al. Review of non-permeating cryoprotectants as supplements for vitrification of mammalian tissues. Cryobiology, 2020; 96: 1-11. doi: 10.1016/j.cryobiol.2020.08.012
|
[37] |
Bunnik E M. Ethics of allocation of donor organs. Curr Opin Organ Tran, 2023; 28(3): 192-196. doi: 10.1097/MOT.0000000000001058
|
[38] |
Panda K, Mazumder A, Krishnamurthy A. Kidneychain: leveraging blockchain & artificial intelligence for a streamlined organ donation solution. medRxiv, 2024. doi: 10.1101/2024.06.08.24308145
|
[39] |
Baust J G, Gao D, Baust J M. Cryopreservation: an emerging paradigm change. Organogenesis, 2009; 5(3): 90-96. doi: 10.4161/org.5.3.10021
|
[40] |
Giwa S, Lewis J K, Alvarez L, et al. The promise of organ and tissue preservation to transform medicine. Nat Biotechnol, 2017; 35(6): 530542. doi: 10.1038/nbt.3889
|
[41] |
Olmo A, Barroso P, Barroso F, et al. The use of high-intensity focused ultrasound for the rewarming of cryopreserved biological material. IEEE Trans Ultrason Ferroelectr Freq Control, 2021; 68(3): 599607. doi: 10.1109/TUFFC.2020.3016950
|
[42] |
Xu R, Bradley E T, Eleanor M. Experiments and simulations demonstrating the rapid ultrasonic rewarming of frozen beef cryovials. arXiv preprint arXiv, 2022; 153(1): 517. doi: 10.1121/10.0016886
|
[43] |
Liu Y, Kangas J, Wang Y, et al. Photothermal conversion of gold nanoparticles for uniform pulsed laser warming of vitrified biomaterials. Nanoscale, 2020; 12(23): 12346-12356. doi: 10.1039/D0NR01614D
|
[44] |
Zhan L, Guo S Z, Kangas J, et al. Conduction cooling and plasmonic heating dramatically increase droplet vitrification volumes for cell cryopreservation. Adv Sci(Weinh), 2021; 8(11): 2004605. doi: 10.1002/advs.202004605
|
[45] |
Alvarez C, Berrospe-Rodriguez C, Wu C, et al. Photothermal heating of titanium nitride nanomaterials for fast and uniform laser warming of cryopreserved biomaterials. Front Bioeng Biotechnol, 2022; 10: 957481. doi: 10.3389/fbioe.2022.957481
|
[46] |
Luo D, Yu C, He L, et al. Development of a single mode electromagnetic resonant cavity for rewarming of cryopreserved biomaterials. Cryobiology, 2006; 53(2): 288-293. doi: 10.1016/j.cryobiol.2006.07.001
|
[47] |
Pan J, Ren S, Sekar P K, et al. Investigation of electromagnetic resonance rewarming enhanced by magnetic nanoparticles for cryopreservation. Langmuir, 2019; 35(23): 7560-7570. doi: 10.1021/acs.langmuir.8b03060
|
[48] |
Ren S, Shu Z, Pan J, et al. Single-mode electromagnetic resonance rewarming for the cryopreservation of samples with large volumes: a numerical and experimental study. Biopreserv Biobank, 2022; 20(4): 317322. doi: 10.1089/bio.2022.0107
|
[49] |
Wang Z, Shu Z, Ren S, et al. Development of electromagnetic warming technology for cryopreservation. Annual Review of Heat Transfer, 2024; 27: 319-356. doi: 10.1615/AnnualRevHeatTransfer.2024055368
|
[50] |
Wang Z, Ren S, Shu Z, et al. An efficient and effective electromagnetic rewarming platform for cryopreservation. Cryobiology, 2024; 117: 104987. doi: 10.1016/j.cryobiol.2024.104987
|
[51] |
Etheridge M L, Xu Y, Rott L, et al. RF heating of magnetic nanoparticles improves the thawing of cryopreserved biomaterials. Technology, 2014; 2(3): 229-242. doi: 10.1142/S2339547814500204
|
[52] |
Manuchehrabi N, Gao Z, Zhang J, et al. Improved tissue cryopreservation using inductive heating of magnetic nanoparticles. Sci Transl Med, 2017; 9(379): 4586. doi: 10.1126/scitranslmed.aah4586
|
[53] |
Sharma A, Rao J S, Han Z, et al. Vitrification and nanowarming of kidneys. Adv Sci(Weinh), 2021; 8(19): e2101691. doi: 10.1002/advs.202101691
|
[54] |
Rollig C, Babatz J, Wagner I, et al. Thawing of cryopreserved mobilized peripheral blood: comparison between waterbath and dry warming device. Cytotherapy, 2002; 4(6): 551-555. doi: 10.1080/146532402761624719
|
[55] |
Kilbride P, Meneghel J, Creasey G, et al. Automated dry thawing of cryopreserved haematopoietic cells is not adversely influenced by cryostorage time, patient age or gender. Plos One, 2020; 15(10): e0240310. doi: 10.1371/journal.pone.0240310
|
[56] |
Petrenko V, Whitworth R. Thermal properties of ice. Physics of ice. Oxford: Oxford University Press, 1999.
|
[57] |
Marquet P. On the computation of moist-air specific thermal enthalpy. Q J Roy Meteor Soc, 2015; 141(686): 67-84. doi: 10.1002/qj.2335
|
[58] |
Melinder A. Thermophysical properties of aqueous solutions used as secondary working fluids. Stockholm: Royal Institute of Technology KTH, 2007.
|
[59] |
Han H X, Zhan T J, Cui M D, et al. Investigation of rapid rewarming chips for cryopreservation by Joule heating. Langmuir, 2023; 39(31): 11048-11062. doi: 10.1021/acs.langmuir.3c01364
|
[60] |
Pegg D E. The history and principles of cryopreservation. Seminars in Reproductive Medicine, 2002; 20(3): 247-256. doi: 10.1055/s-2002-23515
|
[61] |
Bank H L, Davis R F, Emerson D. Cryogenic preservation of isolated rat islets of langerhans - effect of cooling and warming rates. Diabetologia, 1979; 16(3): 195-199. doi: 10.1007/BF01219798
|
[62] |
Gurina T M, Pakhomov A V, Polyakova A L, et al. The development of the cell cryopreservation protocol with controlled rate thawing. Cell Tissue Bank, 2016; 17(2): 303-316. doi: 10.1007/s10561-015-9533-6
|
[63] |
Song Y C, Pegg D E, Hunt C J. Cryopreservation of the common carotid artery of the rabbit: optimization of dimethyl sulfoxide concentration and cooling rate. Cryobiology, 2020; 93: 18-26. doi: 10.1016/j.cryobiol.2020.02.009
|
[64] |
Siu J Y, Liu C, Zhou Y. High-intensity focused ultrasound ablation around the tubing. PLoS One, 2017; 12(11): e0188206. doi: 10.1371/journal.pone.0188206
|
[65] |
Prakash P, Salgaonkar V A, Diederich C J. Modelling of endoluminal and interstitial ultrasound hyperthermia and thermal ablation: applications for device design, feedback control and treatment planning. Int J Hyperther, 2013; 29(4): 296-307. doi: 10.3109/02656736.2013.800998
|
[66] |
Zhou Y F. High intensity focused ultrasound in clinical tumor ablation. World J Clin Oncol, 2011; 2(1): 8-27. doi: 10.5306/wjco.v2.i1.8
|
[67] |
Encabo L, Alcala E, Lopez-Soria J, et al. Hifu rewarming of organs after cold preservation: ex vivo assessment of heart performance in murine model. Transplantation, 2024; 108(1): E15-E7. doi: 10.1097/TP.0000000000004846
|
[68] |
Ziskin M C. Fundamental physics of ultrasound and its propagation in tissue. Radiographics, 1993; 13(3): 705-709. doi: 10.1148/radiographics.13.3.8316679
|
[69] |
Daly J, Zuchowicz N, Nunez Lendo C I, et al. Successful cryopreservation of coral larvae using vitrification and laser warming. Sci Rep, 2018; 8(1): 15714. doi: 10.1038/s41598-018-34035-0
|
[70] |
Khosla K, Zhan L, Bhati A, et al. Characterization of laser gold nanowarming: a platform for millimeter-scale cryopreservation. Langmuir, 2019; 35(23): 7364-7375. doi: 10.1021/acs.langmuir.8b03011
|
[71] |
Habibi M, Berger R D, Calkins H. Radiofrequency ablation: technological trends, challenges, and opportunities. EP Europace, 2021; 23(4): 511-519. doi: 10.1093/europace/euaa328
|
[72] |
Zheng H, Li P C, Ma R D, et al. Development of a three-dimensional multi-modal perfusion-thermal electrode system for complete tumor eradication. Cancers, 2022; 14(19): 4768. doi: 10.3390/cancers14194768
|
[73] |
Zhan L, Han Z H, Shao Q, et al. Rapid joule heating improves vitrification based cryopreservation. Nat Commun, 2022; 13(1): 6017. doi: 10.1038/s41467-022-33546-9
|
[74] |
Osepchuk J M. The history of the microwave oven: a critical review. IEEE, 2009. doi: 10.1109/MWSYM.2009.5165967
|
[75] |
Pegg D E, Green C J, Walter C A. Attempted canine renal cryopreservation using dimethyl sulphoxide helium perfusion and microwave thawing. Cryobiology, 1978; 15(6): 618-626. doi: 10.1016/0011-2240(78)90086-X
|
[76] |
Lehr H B, Berggren R B, Summers A L, et al. Freezing and thawing of large organs. Cryobiology, 1964; 1(2): 194-197. doi: 10.1016/0011-2240(64)90011-2
|
[77] |
Wowk B, Phan J, Pagotan R, et al. 27 mhz constant field dielectric warming of kidneys cryopreserved by vitrification. Cryobiology, 2024; 115: 104893. doi: 10.1016/j.cryobiol.2024.104893
|
[78] |
Burdette E C, Karow A M, Jeske A H. Design, development, and performance of an electromagnetic illumination system for thawing cryopreserved kidneys of rabbits and dogs. Cryobiology, 1978; 15(2): 152-167. doi: 10.1016/0011-2240(78)90020-2
|
[79] |
Ruan H L, Wang T, Gao C. Microwave-water bath hybrid warming for frozen cryoprotectant solution using a helical antenna. Cryoletters, 2020; 41(1): 26-30. http://pubmed.ncbi.nlm.nih.gov/33973981/
|
[80] |
Rachman M J, Evans S, Pegg D E. Experimental results on the rewarming of a cryopreserved organ phantom in a uhf field. J Biomed Eng, 1992; 14(5): 397-403. doi: 10.1016/0141-5425(92)90085-Y
|
[81] |
Ketterer F D, Holst H I, Lehr H B. Improved viability of kidneys with microwave thawing. Proc Cryobiol, 1971; 8(3): 309-315. doi: 10.1016/0011-2240(71)90197-0
|
[82] |
Guttman F M, Lizin J, Robitaille P, et al. Survival of canine kidneys after treatment with dimethyl-sulfoxide, freezing at --80 degrees c, and thawing by microwave illumination. Cryobiology, 1977; 14(5): 559-567. doi: 10.1016/0011-2240(77)90166-3
|
[83] |
Ma R, Ren S, Wang Z, et al. Electromagnetic rewarming for cryopreservation: a numerical comparison between multi-mode and single-mode electromagnetic cavity. Cryobiology, 2022; 109: 23. doi: 10.1016/j.cryobiol.2022.11.073
|
[84] |
Martin Paul Robinson D E P. Rapid electromagnetic warming of cells and tissues. IEEE Transactions on Biomedical Engineering, 1999; 46(10): 1175-1181. doi: 10.1109/10.804569
|
[85] |
Pan J, Shu Z, Ren S, et al. Determination of dielectric properties of cryoprotective agent solutions with a resonant cavity for the electromagnetic rewarming in cryopreservation. Biopreserv Biobank, 2017; 15(5): 404-409. doi: 10.1089/bio.2016.0096
|
[86] |
Ren S, Shu Z, Peng J, et al. Rapid and uniform rewarming by single-mode electromagnetic resonance cavity: effect of sample shape. Cryobiology, 2021; 103: 188. doi: 10.1016/j.cryobiol.2021.11.105
|
[87] |
Lewis J, Stoddart K, Reitinger V, et al. Molecular dynamics-informed optimization of cryoprotectant solutions for enhanced single-mode electromagnetic rewarming. Cryobiology, 2024; 117: 105091. doi: 10.1016/j.cryobiol.2024.105091
|
[88] |
Wang Z, Ren S, Shu Z, et al. Screening and optimization of cryoprotective agents(cpas) for electromagnetic heating of cryopreserved biomaterials. Cryobiology, 2022; 109: 16. doi: 10.1016/j.cryobiol.2022.11.052
|
[89] |
Ren S, Shu Z, Wang Z, et al. Successful vitreous cryopreservation of rabbit jugular vein using magnetic nanoparticles enhanced single-mode electromagnetic resonance rewarming system. Cryobiology, 2021; 103: 173-174. doi: 10.1016/j.cryobiol.2021.11.060
|
[90] |
Wang W. Design of low-noise low-power ecg amplifier circuit with high integration level. Journal of Physics Conference Series, 2023; 2649(1): 012062. doi: 10.1088/1742-6596/2649/1/012062
|
[91] |
Sun J, Wang W, Yue Q. Review on microwave-matter interaction fundamentals and efficient microwave-associated heating strategies. Materials(Basel), 2016; 9(4): 231. doi: 10.3390/ma9040231
|
[92] |
Han Z H, Rao J S, Gangwar L, et al. Vitrification and nanowarming enable long-term organ cryopreservation and life-sustaining kidney transplantation in a rat model. Nat Commun, 2023; 14(1): 3407. doi: 10.1038/s41467-023-38824-8
|
[93] |
Gangwar L, Han Z, Scheithauer C, et al. Physical vitrification and nanowarming at human organ scale to enable cryopreservation. bioRxiv, 2024. doi: 10.1101/2024.11.08.622572
|
[94] |
Bischof J C, Oziri O J, Rao J S, et al. Scalable purification of iron oxide nanoparticles by tangential flow filtration for organ cryopreservation and transplantation. SPIE, 2025. doi: 10.1117/12.3043417
|
[95] |
Ye Z, Tai Y, Han Z, et al. Engineering magnetic nanoclusters for highly efficient heating in radio-frequency nanowarming. Nano Lett, 2024; 24(15): 4588-4594. doi: 10.1021/acs.nanolett.4c00721
|
[96] |
Han Z, Gangwar L, Namsrai B-E, et al. Kidney tissue loading reduces the critical cooling and warming rates of vs55 and vmp cryoprotective solutions. Cryobiology, 2024; 117: 104977. doi: 10.1016/j.cryobiol.2024.104977
|