Long-Term Cryopreservation Does Not Affect Quality of Peripheral Blood Stem Cell Grafts: A Comparative Study of Native, Short-Term and Long-Term Cryopreserved Haematopoietic Stem Cells
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34328022
PubMed Central
PMC8327011
DOI
10.1177/09636897211036004
Knihovny.cz E-zdroje
- Klíčová slova
- ALDH, cryopreservation, haematopoietic stem cell, mitochondrial activity, pH, potency, storage, viability,
- MeSH
- hematopoetické kmenové buňky metabolismus MeSH
- kmenové buňky z periferní krve metabolismus MeSH
- kryoprezervace metody MeSH
- lidé MeSH
- transplantace periferních kmenových buněk metody MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Cryopreserved haematopoietic progenitor cells are used to restore autologous haematopoiesis after high dose chemotherapy. Although the cells are routinely stored for a long period, concerns remain about the maximum storage time and the possible negative effect of storage on their potency. We evaluated the effect of cryopreservation on the quality of peripheral stem cell grafts stored for a short (3 months) and a long (10 years) period and we compared it to native products.The viability of CD34+ cells remained unaffected during storage, the apoptotic cells were represented up to 10% and did not differ between groups. The clonogenic activity measured by ATP production has decreased with the length of storage (ATP/cell 1.28 nM in native vs. 0.63 in long term stored products, P < 0.05). Only borderline changes without statistical significance were detected when examining mitochondrial and aldehyde dehydrogenase metabolic activity and intracellular pH, showing their good preservation during cell storage. Our experience demonstrates that cryostorage has no major negative effect on stem cell quality and potency, and therefore autologous stem cells can be stored safely for an extended period of at least 10 years. On the other hand, long term storage for 10 years and longer may lead to mild reduction of clonogenic capacity. When a sufficient dose of stem cells is infused, these changes will not have a clinical impact. However, in products stored beyond 10 years, especially when a low number of CD34+ cells is available, the quality of stem cell graft should be verified before infusion using the appropriate potency assays.
Biomedical Center Faculty of Medicine in Pilsen Charles University Prague Pilsen Czech Republic
Department of Haematology and Oncology University Hospital Pilsen Pilsen Czech Republic
Institute of Immunology and Allergology University Hospital Pilsen Pilsen Czech Republic
Zobrazit více v PubMed
Martino M, Recchia AG, Fedele R, Neri S, Vincelli ID, Moscato T, Gentile M, Morabito F. The role of tandem stem cell transplantation for multiple myeloma patients. Expert Opin Biol Ther. 2016;16(4):515–534. PubMed
Lewalle P, Wittnebel S. Risk-adapted transplant strategies for high-risk Hodgkin lymphoma: are we there? Curr Opin Oncol. 2016;28(5):390–397. PubMed
Windrum P, Morris TCM, Drake MB, Niederwieser D, Ruutu T, EBMT Chronic Leukaemia Working Party Complications Subcommittee. Variation in dimethyl sulfoxide use in stem cell transplantation: a survey of EBMT centres. Bone Marrow Transplant. 2005;36(7):601–603. PubMed
Sutherland DR, Anderson L, Keeney M, Nayar R, Chin-Yee I. The ISHAGE guidelines for CD34+ cell determination by flow cytometry. International Society of Hematotherapy and Graft Engineering. J Hematother. 1996;5(3):213–226. PubMed
Morgenstern DA, Ahsan G, Brocklesby M, Ings S, Balsa C, Veys P, Brock P, Anderson J, Amrolia P, Goulden N, Cale CM, et al. Post-thaw viability of cryopreserved peripheral blood stem cells (PBSC) does not guarantee functional activity: important implications for quality assurance of stem cell transplant programmes. Br J Haematol. 2016;174(6):942–951. PubMed
Abrahamsen JF, Wentzel-Larsen T, Bruserud O. Autologous transplantation: the viable transplanted CD34+ cell dose measured post-thaw does not predict engraftment kinetics better than the total CD34+ cell dose measured pre-freeze in patients that receive more than 2 × 10(6) CD34+ cells/kg. Cytotherapy. 2004;6(4):356–362. PubMed
Lanza F, Mangianti S, Accorsi P, Lombardini L, Martino M, Saccardi R, Vassanelli A, Ostuni A, Ciceri F. Manipulation, and cryopreservation of autologous peripheral blood stem cell products in Italy: A survey by GITMO, SIDEM and GIIMA societies. Transfus. Apher Sci. 2020;59(2):102753. PubMed
Veeraputhiran M, Theus JW, Pesek G, Barlogie B, Cottler-Fox M. Viability and engraftment of hematopoietic progenitor cells after long-term cryopreservation: effect of diagnosis and percentage dimethyl sulfoxide concentration. Cytotherapy. 2010;12(6):764–766. PubMed
Humpe A, Riggert J, Vehmeyer K, Troff C, Hiddemann W, Köhler M, Wörmann B. Comparison of CD34+ cell numbers and colony growth before and after cryopreservation of peripheral blood progenitor and stem cell harvests: influence of prior chemotherapy. Transfusion (Paris). 1997;37(10):1050–1057. PubMed
Broxmeyer HE, Srour EF, Hangoc G, Cooper S, Anderson SA, Bodine DM. High-efficiency recovery of functional hematopoietic progenitor and stem cells from human cord blood cryopreserved for 15 years. Proc Natl Acad Sci U S A. 2003;100(2):645–650. PubMed PMC
Mugishima H, Harada K, Chin M, Suzuki T, Takagi K, Hayakawa S, Sato K, Klein JP, Gale RP. Effects of long-term cryopreservation on hematopoietic progenitor cells in umbilical cord blood. Bone Marrow Transplant. 1999;23(4):395–396. PubMed
Detry G, Calvet L, Straetmans N, Cabrespine A, Ravoet C, Bay JO, Petre H, Paillard C, Husson B, Merlin E, Boon-Falleur L, et al. Impact of uncontrolled freezing and long-term storage of peripheral blood stem cells at - 80 °C on haematopoietic recovery after autologous transplantation. Report from two centres. Bone Marrow Transplant. 2014;49(6):780–785. PubMed
Ayello J, Semidei-Pomales M, Preti R, Hesdorffer C, Reiss RF. Effects of long-term storage at -90 degrees C of bone marrow and PBPC on cell recovery, viability, and clonogenic potential. J Hematother. 1998;7(4):385–390. PubMed
Valeri CR, Pivacek LE. Effects of the temperature, the duration of frozen storage, and the freezing container on in vitro measurements in human peripheral blood mononuclear cells. Transfusion (Paris). 1996;36(4):303–308. PubMed
Fernyhough LJ, Buchan VA, McArthur LT, Hock BD. Relative recovery of haematopoietic stem cell products after cryogenic storage of up to 19 years. Bone Marrow Transplant. 2013;48(1):32–35. PubMed
Donnenberg AD, Koch EK, Griffin DL, Stanczak HM, Kiss JE, Carlos TM, Buchbarker DM, Yeager AM. Viability of cryopreserved BM progenitor cells stored for more than a decade. Cytotherapy. 2002;4(2):157–163. PubMed
Weaver CH, Hazelton B, Birch R, Palmer P, Allen C, Schwartzberg L, West W. An analysis of engraftment kinetics as a function of the CD34 content of peripheral blood progenitor cell collections in 692 patients after the administration of myeloablative chemotherapy. Blood. 1995;86(10):3961–3969. PubMed
Ergene U, Cağirgan S, Pehlivan M, Yilmaz M, Tombuloğlu M. Factors influencing engraftment in autologous peripheral hematopoetic stem cell transplantation (PBSCT). Transfus Apher Sci. 2007;36(1):23–29. PubMed
Levering WHBM, Preijers FWMB, van Wieringen WN, Kraan J, van Beers WAM, Sintnicolaas K, van Rhenen DJ, Gratama JW. Flow cytometric CD34+ stem cell enumeration: lessons from nine years’ external quality assessment within the Benelux countries. Cytometry B Clin Cytom. 2007;72(3):178–188. PubMed
Castelhano MV, Reis-Alves SC, Vigorito AC, Rocha FF, Pereira-Cunha FG, De Souza CA, Lorand-Metze I. Quantifying loss of CD34+ cells collected by apheresis after processing for freezing and post-thaw. Transfus Apher Sci. 2013;48(2):241–246. PubMed
D’Rozario J, Parisotto R, Stapleton J, Gidley A, Owen D. Pre infusion, post thaw CD34+ peripheral blood stem cell enumeration as a predictor of haematopoietic engraftment in autologous haematopoietic cell transplantation. Transfus Apher Sci. 2014;50(3):443–450. PubMed
Reich-Slotky R, Colovai AI, Semidei-Pomales M, Patel N, Cairo M, Jhang J, Schwartz J. Determining post-thaw CD34+ cell dose of cryopreserved haematopoietic progenitor cells demonstrates high recovery and confirms their integrity. Vox Sang. 2008;94(4):351–357. PubMed
Itoh T, Minegishi M, Fushimi J, Takahashi H, Kudo Y, Suzuki A, Narita A, Sato Y, Akagi K, Wada Y, Saito A, et al. A simple controlled-rate freezing method without a rate-controlled programmed freezer provides optimal conditions for both large-scale and small-scale cryopreservation of umbilical cord blood cells. Transfusion (Paris). 2003;43(9):1303–1308. PubMed
Kurita N, Frassoni F, Chiba S, Podestà M. Impact of length of cryopreservation and origin of cord blood units on hematologic recovery following cord blood transplantation. Bone Marrow Transplant. 2015;50(6):818–821. PubMed
Kim G-H, Kwak J, Kim SH, Kim HJ, Hong HK, Jin HJ, Choi SJ, Oh W, Um S. High integrity and fidelity of long-term cryopreserved umbilical cord blood for transplantation. J Clin Med. 2021;10(2):293. Available from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7830419/ PubMed PMC
Mitchell R, Wagner JE, Brunstein CG, Cao Q, McKenna DH, Lund TC, Verneris MR. Impact of long-term cryopreservation on single umbilical cord blood transplantation outcomes. Biol Blood Marrow Transplant. 2015;21(1):50–54. PubMed PMC
Arutyunyan I, Fatkhudinov T, Sukhikh G. Umbilical cord tissue cryopreservation: a short review. Stem Cell Res Ther. 2018;9(1):236. PubMed PMC
Abbruzzese L, Agostini F, Durante C, Toffola RT, Rupolo M, Rossi FM, Lleshi A, Zanolin S, Michieli M, Mazzucato M. Long term cryopreservation in 5% DMSO maintains unchanged CD34(+) cells viability and allows satisfactory hematological engraftment after peripheral blood stem cell transplantation. Vox Sang. 2013;105(1):77–80. PubMed
Liseth K, Ersvær E, Abrahamsen JF, Nesthus I, Ryningen A, Bruserud Ø. Long-term cryopreservation of autologous stem cell grafts: a clinical and experimental study of hematopoietic and immunocompetent cells. Transfusion (Paris). 2009;49(8):1709–1719. PubMed
Lisenko K, Pavel P, Kriegsmann M, Bruckner T, Hillengass J, Goldschmidt H, Witzens-Harig M, Ho AD, Wuchter P. Storage duration of autologous stem cell preparations has no impact on hematopoietic recovery after transplantation. biol. blood marrow transplant. Blood Marrow Transplant. 2017;23(4):684–690. PubMed
de Boer F, Dräger AM, Pinedo HM, Kessler FL, van der Wall E, Jonkhoff AR, van der Lelie J, Huijgens PC, Ossenkoppele GJ, Schuurhuis GJ. Extensive early apoptosis in frozen-thawed CD34-positive stem cells decreases threshold doses for haematological recovery after autologous peripheral blood progenitor cell transplantation. Bone Marrow Transplant. 2002;29(3):249–255. PubMed
Wu L, Al-Hejazi A, Filion L, Ben R, Halpenny M, Yang L, Giulivi A, Allan DS. Increased apoptosis in cryopreserved autologous hematopoietic progenitor cells collected by apheresis and delayed neutrophil recovery after transplantation: a nested case-control study. Cytotherapy. 2012;14(2):205–214. PubMed
Duggleby RC, Querol S, Davy RC, Fry LJ, Gibson DA, Horton RBV, Mahmood SN, Gomez SG, Madrigal JA. Flow cytometry assessment of apoptotic CD34+ cells by annexin V labeling may improve prediction of cord blood potency for engraftment. Transfusion (Paris). 2012;52(3):549–559. PubMed
Bonora M, Pinton P, Ito K. Mitochondrial control of hematopoietic stem cell balance and hematopoiesis. Front Biol. 2015;10(2):117–124.
Vannini N, Girotra M, Naveiras O, Nikitin G, Campos V, Giger S, Roch A, Auwerx J, Lutolf MP. Specification of haematopoietic stem cell fate via modulation of mitochondrial activity. Nat Commun. 2016;7:13125. PubMed PMC
Stéphenne X, Najimi M, Ngoc DK, Smets F, Hue L, Guigas B, Sokal EM. Cryopreservation of human hepatocytes alters the mitochondrial respiratory chain complex 1. Cell Transplant. 2007;16(4):409–419. PubMed
Xu X, Liu Y, Cui Z, Wei Y, Zhang L. Effects of osmotic and cold shock on adherent human mesenchymal stem cells during cryopreservation. J Biotechnol. 2012;162(2–3):224–231. PubMed
Yamamoto S, Ikeda H, Toyama D, Hayashi M, Akiyama K, Suzuki M, Tanaka Y, Watanabe T, Fujimoto Y, Hosaki I, Nishihira H, et al. Quality of long-term cryopreserved umbilical cord blood units for hematopoietic cell transplantation. Int J Hematol. 2011;93(1):99–105. PubMed
Winter JM, Jacobson P, Bullough B, Christensen AP, Boyer M, Reems J-A. Long-term effects of cryopreservation on clinically prepared hematopoietic progenitor cell products. Cytotherapy. 2014;16(7):965–975. PubMed
Vosganian GS, Waalen J, Kim K, Jhatakia S, Schram E, Lee T, Riddell D, Mason JR. Effects of long-term cryopreservation on peripheral blood progenitor cells. Cytotherapy. 2012;14(10):1228–1234. PubMed
Xu X, Cui ZF, Wilkins RJ, Urban JPG. Intracellular pH changes in isolated bovine articular chondrocytes during the loading and removal of cryoprotective agents. Cryobiology. 2003;46(2):161–173. PubMed