{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T01:14:07Z","timestamp":1790298847186,"version":"4.1.0"},"reference-count":141,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,11,19]],"date-time":"2024-11-19T00:00:00Z","timestamp":1731974400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100010038","name":"Earmarked Fund for China Agriculture Research System","doi-asserted-by":"publisher","award":["CARS-39-08"],"award-info":[{"award-number":["CARS-39-08"]}],"id":[{"id":"10.13039\/501100010038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>Sperm cryopreservation is an approach to preserve sperm cells in liquid nitrogen or other cryogenic media for future use in assisted reproductive technologies, such as <jats:italic>in vitro<\/jats:italic> fertilization or artificial insemination. Sperm cryopreservation has been extensively used in the dairy industry and has attained excellent results after artificial insemination. However, for small ruminants the application of sperm cryopreservation is limited, due to the poor quality of frozen semen and special characteristics of the reproductive female tract. In order to improve post-thaw semen quality various cryoprotectants are used. Currently, many types of cryoprotectants, such as permeable organic solvents, sugars, antioxidants, and natural or synthetic ice blockers, have been tested on small ruminants\u2019 sperm cryopreservation. Among them, trehalose; has shown potential acting as an excellent cryoprotectant for semen freezing. While, the exact roles and action mechanisms of trehalose during cryopreservation remain unclear. In this review, we systematically summarized the present usage status, potential action mechanisms, and future application prospects of trehalose in small-ruminant sperm cryopreservation.<\/jats:p>","DOI":"10.3389\/fvets.2024.1467242","type":"journal-article","created":{"date-parts":[[2024,11,19]],"date-time":"2024-11-19T06:18:11Z","timestamp":1731997091000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["A review on the functional roles of trehalose during cryopreservation of small ruminant semen"],"prefix":"10.3389","volume":"11","author":[{"given":"Baoyu","family":"Jia","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Larbi","family":"Allai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunyan","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiachong","family":"Liang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunrong","family":"Lv","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guoquan","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guobo","family":"Quan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,11,19]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/j.anireprosci.2013.02.006","article-title":"Cryobanking of farm animal gametes and embryos as a means of conserving livestock genetics","volume":"138","author":"Mara","year":"2013","journal-title":"Anim Reprod Sci"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/j.1939-4640.2000.tb03268.x","article-title":"Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon","volume":"21","author":"Bailey","year":"2000","journal-title":"J Androl"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1089\/bio.2018.0113","article-title":"Spermatozoa cryopreservation: state of art and future in small ruminants","volume":"17","author":"Lv","year":"2019","journal-title":"Biopreserv Biobank"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1038\/s41420-024-02013-3","article-title":"Sperm freezing damage: the role of regulated cell death","volume":"10","author":"Hai","year":"2024","journal-title":"Cell Death Discov"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"609180","DOI":"10.3389\/fvets.2021.609180","article-title":"Impact of cryopreservation on spermatozoa freeze-thawed traits and relevance OMICS to assess sperm Cryo-tolerance in farm animals","volume":"8","author":"Khan","year":"2021","journal-title":"Front Vet Sci"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.rbmo.2018.05.012","article-title":"Sperm cryopreservation: A review on current molecular cryobiology and advanced approaches","volume":"37","author":"Hezavehei","year":"2018","journal-title":"Reprod Biomed Online"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1016\/j.theriogenology.2007.06.009","article-title":"Rapidly cooled horse spermatozoa: loss of viability is due to osmotic imbalance during thawing, not intracellular ice formation","volume":"68","author":"Morris","year":"2007","journal-title":"Theriogenology"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"4716","DOI":"10.3390\/cimb45060300","article-title":"Sperm cryopreservation today: approaches, efficiency, and pitfalls","volume":"45","author":"Ozimic","year":"2023","journal-title":"Curr Issues Mol Biol"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/s0093-691x(99)00239-3","article-title":"Fundamental aspects of sperm cryobiology: the importance of species and individual differences","volume":"53","author":"Holt","year":"2000","journal-title":"Theriogenology"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"871","DOI":"10.1071\/rd9950871","article-title":"Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function","volume":"7","author":"Watson","year":"1995","journal-title":"Reprod Fertil Dev"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"3271","DOI":"10.3390\/ani12233271","article-title":"Cryopreservation of semen in domestic animals: A review of current challenges, applications, and prospective strategies","volume":"12","author":"Sharafi","year":"2022","journal-title":"Animals (Basel)"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/j.theriogenology.2022.03.015","article-title":"Identification and validation of ram sperm proteins associated with cryoinjuries caused by the cryopreservation process","volume":"184","author":"Jia","year":"2022","journal-title":"Theriogenology"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1016\/s0378-4320(00)00099-3","article-title":"The causes of reduced fertility with cryopreserved semen","author":"Watson","year":"2000","journal-title":"Anim Reprod Sci"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/s10561-008-9081-4","article-title":"Cryopreservation of domestic animal sperm cells","volume":"10","author":"Barbas","year":"2009","journal-title":"Cell Tissue Bank"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/S0749-0739(17)30476-5","article-title":"Artificial insemination and preservation of semen","volume":"8","author":"Brinsko","year":"1992","journal-title":"Vet Clin N Am Equine Pract"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1071\/RD04034","article-title":"Preservation and evaluation of semen for artificial insemination","volume":"16","author":"Gillan","year":"2004","journal-title":"Reprod Fertil Dev"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1876","DOI":"10.1016\/j.theriogenology.2006.04.039","article-title":"Influence of breed and age on morphometry and depth of inseminating catheter penetration in the ewe cervix: a postmortem study","volume":"66","author":"Kaabi","year":"2006","journal-title":"Theriogenology"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1071\/RD04037","article-title":"New treatments associated with timed artificial insemination in small ruminants","volume":"16","author":"Menchaca","year":"2004","journal-title":"Reprod Fertil Dev"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.theriogenology.2018.11.019","article-title":"Surgery on cervical folds for transcervical intrauterine artificial insemination with frozen-thawed semen enhances pregnancy rates in the sheep","volume":"126","author":"Pau","year":"2019","journal-title":"Theriogenology"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1111\/rda.12038","article-title":"Comparative fertility of freshly collected vs frozen-thawed semen with laparoscopic Oviductal artificial insemination in domestic cats","volume":"47","author":"Lambo","year":"2012","journal-title":"Reprod Domest Anim"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1111\/rda.14304","article-title":"Fertility results after exocervical insemination using goat semen cryopreserved with extenders based on egg yolk, skim milk, or soybean lecithin","volume":"58","author":"Liang","year":"2023","journal-title":"Reprod Domest Anim"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"106579","DOI":"10.1016\/j.anireprosci.2020.106579","article-title":"Treatment of rams with melatonin implants in the non-breeding season improves post-thaw sperm progressive motility and DNA integrity","volume":"221","author":"Pool","year":"2020","journal-title":"Anim Reprod Sci"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"802","DOI":"10.1002\/mrd.22840","article-title":"Artificial insemination with frozen-thawed boar sperm","volume":"84","author":"Yeste","year":"2017","journal-title":"Mol Reprod Dev"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"106904","DOI":"10.1016\/j.anireprosci.2021.106904","article-title":"Advances in sperm cryopreservation in farm animals: cattle, horse, pig and sheep","volume":"246","author":"Y\u00e1nez-Ortiz","year":"2022","journal-title":"Anim Reprod Sci"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"896","DOI":"10.1071\/BI9630896","article-title":"The use of various diluents for deep-freezing bull spermatozoa","volume":"16","author":"Choong","year":"1963","journal-title":"Aust J Bio Sci"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10561-019-09797-0","article-title":"Influence of cryopreservation on structure and function of mammalian spermatozoa: an overview","volume":"21","author":"Ezzati","year":"2020","journal-title":"Cell Tissue Bank"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"E4596","DOI":"10.3390\/ijms20184596","article-title":"Freezing-thawing procedures remodel the proteome of ram sperm before and after in vitro capacitation","volume":"20","author":"Peris-Frau","year":"2019","journal-title":"Int J Mol Sci"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/j.smallrumres.2005.02.015","article-title":"A review on goat sperm cryopreservation","volume":"63","author":"Purdy","year":"2006","journal-title":"Small Rumin Res"},{"key":"ref29","doi-asserted-by":"crossref","DOI":"10.5772\/intechopen.80477","article-title":"Cryoprotectants and their usage in cryopreservation process","volume-title":"Cryopreservation biotechnology in biomedical and biological sciences","author":"Bhattacharya","year":"2018"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"001","DOI":"10.19080\/AIBM.2024.17.555978","article-title":"A brief review of current strategies and advances in cryopreservation techniques","volume":"17","author":"Rittschof","year":"2023","journal-title":"AIBM"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1071\/AN13431","article-title":"Effect of different concentrations of trehalose and glycerol on the freezability of ram semen using soybean lecithin-based diluents","volume":"55","author":"Bohlool","year":"2014","journal-title":"Anim Prod Sci"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.anireprosci.2016.12.004","article-title":"Ethylene glycol, but not DMSO, could replace glycerol inclusion in soybean lecithin-based extenders in ram sperm cryopreservation","volume":"177","author":"Najafi","year":"2017","journal-title":"Anim Reprod Sci"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.anireprosci.2012.05.014","article-title":"In vitro evaluation of ram sperm frozen with glycerol, ethylene glycol or acetamide","volume":"132","author":"Silva","year":"2012","journal-title":"Anim Reprod Sci"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.anireprosci.2010.06.006","article-title":"Effect of sugars on characteristics of Boer goat semen after cryopreservation","volume":"122","author":"Naing","year":"2010","journal-title":"Anim Reprod Sci"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1089\/bio.2012.0013","article-title":"Comparison of the effect of various disaccharides on frozen goat spermatozoa","volume":"10","author":"Quan","year":"2012","journal-title":"Biopreserv Biobank"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1016\/S0093-691X(00)00373-3","article-title":"Influence of sugar supplementation of the extender on motility, viability and acrosomal integrity of dog spermatozoa during freezing","volume":"54","author":"Yildiz","year":"2000","journal-title":"Theriogenology"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"101226","DOI":"10.1016\/j.jksus.2020.10.023","article-title":"Use of antioxidants to augment semen efficiency during liquid storage and cryopreservation in livestock animals: A review","volume":"33","author":"Al-Mutary","year":"2021","journal-title":"J King Saud Univ"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"106127","DOI":"10.1016\/j.anireprosci.2019.106127","article-title":"Improving the quality of cryopreserved goat semen with a commercial bull extender supplemented with resveratrol","volume":"208","author":"Lv","year":"2019","journal-title":"Anim Reprod Sci"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"771440","DOI":"10.3389\/fvets.2021.771440","article-title":"Effect of glutathione on sperm quality in Guanzhong dairy goat sperm during cryopreservation","volume":"8","author":"Zou","year":"2021","journal-title":"Front Vet Sci"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1089\/bio.2020.0140","article-title":"The effects of antifreeze protein III supplementation on the Cryosurvival of goat spermatozoa during cryopreservation","volume":"19","author":"Lv","year":"2021","journal-title":"Biopreserv Biobank"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"107232","DOI":"10.1016\/j.anireprosci.2023.107232","article-title":"Antifreeze protein type III addition to freezing extender comprehensively improves post-thaw sperm properties in Okinawan native Agu pig","volume":"252","author":"Masuda","year":"2023","journal-title":"Anim Reprod Sci"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1016\/j.rvsc.2022.12.006","article-title":"Effect of antifreeze protein type III on frozen\/thawed of spermatozoa recover from goat epididymis","volume":"154","author":"Monteiro","year":"2023","journal-title":"Res Vet Sci"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.smallrumres.2014.11.007","article-title":"Cryopreservation of ram spermatozoa in the presence of cyclohexanhexol-derived synthetic ice blocker","volume":"123","author":"Quan","year":"2015","journal-title":"Small Rumin Res"},{"key":"ref44","first-page":"217","article-title":"The effects of 1,4-cyclohexanediol on frozen ram spermatozoa","volume":"34","author":"Quan","year":"2013","journal-title":"Cryo Letters"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1016\/j.cryobiol.2005.02.002","article-title":"Ultramicroscopic and biochemical changes in ram spermatozoa cryopreserved with trehalose-based hypertonic extenders","volume":"50","author":"Aisen","year":"2005","journal-title":"Cryobiology"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1016\/j.jevs.2016.08.020","article-title":"The effect of Trehalose supplementation of INRA-82 extender on quality and fertility of cooled and frozen-thawed stallion spermatozoa","volume":"48","author":"El-Badry","year":"2017","journal-title":"J Equine Vet"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.cryobiol.2020.03.008","article-title":"The synergistic effect of trehalose and low concentrations of cryoprotectants can improve post-thaw ram sperm parameters","volume":"95","author":"\u00d6zt\u00fcrk","year":"2020","journal-title":"Cryobiology"},{"key":"ref48","first-page":"307","article-title":"The effects of trehalose and sucrose on frozen spermatozoa of Yunnan semi-fine wool sheep during a non-mating season","volume":"33","author":"Quan","year":"2012","journal-title":"Cryo Letters"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1501\/Vetfak_0000002176","article-title":"The role of different trehalose concentrations and cooling rates in freezing of ram semen","volume":"56","author":"Uysal","year":"2009","journal-title":"Ankara Univ Vet Fak Derg"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"749735","DOI":"10.3389\/fphys.2021.749735","article-title":"Effect of Trehalose and sucrose in post-thaw quality of Crassostrea angulata sperm","volume":"12","author":"Anjos","year":"2021","journal-title":"Front Physiol"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.cryobiol.2017.02.006","article-title":"Trehalose improves rabbit sperm quality during cryopreservation","volume":"75","author":"Zhu","year":"2017","journal-title":"Cryobiology"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"1267","DOI":"10.1016\/j.theriogenology.2009.12.007","article-title":"Effects of different cryoprotective agents on ram sperm morphology and DNAintegrity","volume":"73","author":"Nur","year":"2010","journal-title":"Theriogenology"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"e12757","DOI":"10.1111\/and.12757","article-title":"Trehalose sustains a higher post-thaw sperm motility than sucrose in vitrified human sperm","volume":"49","author":"Schulz","year":"2017","journal-title":"Andrologia"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/0378-4320(94)90058-2","article-title":"Effect of monosaccharides and disaccharides in Tris-based diluents on motility, acrosome integrity and fertility of pellet frozen ram spermatozoa","volume":"36","author":"Molinia","year":"1994","journal-title":"Anim Reprod Sci"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.cryobiol.2017.12.002","article-title":"Effect of trehalose- and sucrose-based extenders on equine sperm quality after vitrification: preliminary results","volume":"80","author":"P\u00e9rez-Mar\u00edn","year":"2018","journal-title":"Cryobiology"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.theriogenology.2021.05.004","article-title":"Trehalose modifies the protein profile of ram spermatozoa during cryopreservation","volume":"171","author":"Jia","year":"2021","journal-title":"Theriogenology"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1038\/72580","article-title":"Preservation of mammalian cells\u2014learning nature\u2019s tricks","volume":"18","author":"Crowe","year":"2000","journal-title":"Nat Biotechnol"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1006\/cryo.2001.2353","article-title":"The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state","volume":"43","author":"Crowe","year":"2001","journal-title":"Cryobiology"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"101397","DOI":"10.1016\/j.fochx.2024.101397","article-title":"Evaluation of digestibility, solubility, and surface properties of trehalose-conjugated quinoa proteins prepared via pH shifting technique","volume":"22","author":"Alrosan","year":"2024","journal-title":"Food Chem X"},{"key":"ref60","doi-asserted-by":"publisher","first-page":"1393","DOI":"10.3390\/nu15061393","article-title":"Dietary Trehalose as a bioactive nutrient","volume":"15","author":"Chen","year":"2023","journal-title":"Nutrients"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"1223","DOI":"10.1515\/pac-2016-1025","article-title":"Tailoring trehalose for biomedical and biotechnological applications","volume":"89","author":"O\u2019Neill","year":"2017","journal-title":"Pure Appl Chem"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1002\/pro.3","article-title":"Effect of trehalose on protein structure","volume":"18","author":"Jain","year":"2009","journal-title":"Protein Sci"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"1561","DOI":"10.1021\/jacsau.2c00309","article-title":"Synthesis and application of Trehalose materials","volume":"2","author":"Vinciguerra","year":"2022","journal-title":"JACS Au"},{"key":"ref64","doi-asserted-by":"publisher","first-page":"106625","DOI":"10.1016\/j.ejps.2023.106625","article-title":"Stabilization effects of saccharides in protein formulations: A review of sucrose, trehalose, cyclodextrins and dextrans","volume":"192","author":"Li","year":"2024","journal-title":"Eur J Pharm Sci"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"65","DOI":"10.3390\/vaccines12010065","article-title":"Screening and stability evaluation of freeze-dried protective agents for a live recombinant pseudorabies virus vaccine","volume":"12","author":"Liu","year":"2024","journal-title":"Vaccines (Basel)"},{"key":"ref66","doi-asserted-by":"publisher","first-page":"5004","DOI":"10.1111\/1541-4337.13048","article-title":"Trehalose and its applications in the food industry","volume":"21","author":"Chen","year":"2022","journal-title":"Compr Rev Food Sci Food Saf"},{"key":"ref67","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1080\/08820139.2021.1891095","article-title":"Trehalose and N-acetyl cysteine alleviate inflammatory cytokine production and oxidative stress in LPS-stimulated human peripheral blood mononuclear cells","volume":"51","author":"Bastin","year":"2022","journal-title":"Immunol Investig"},{"key":"ref68","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.3390\/antiox12061166","article-title":"Trehalose inhibits inflammatory responses through mitochondrial reprogramming in RAW 264.7 macrophages","volume":"12","author":"Yu","year":"2023","journal-title":"Antioxidants"},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1190","DOI":"10.1021\/acsbiomaterials.2c01225","article-title":"Trehalose in biomedical cryopreservation\u2013properties, mechanisms, delivery methods, applications, benefits, and problems","volume":"9","author":"Hu","year":"2023","journal-title":"ACS Biomater Sci Eng"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1089\/bio.2021.0120","article-title":"Ultrastructural modification of ram sperm frozen with Cyclohexanediol and Trehalose","volume":"20","author":"Liang","year":"2022","journal-title":"Biopreserv Biobank"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1186\/s13287-020-01969-0","article-title":"The combination of trehalose and glycerol: an effective and non-toxic recipe for cryopreservation of human adipose-derived stem cells","volume":"11","author":"Zhang","year":"2020","journal-title":"Stem Cell Res Ther"},{"key":"ref72","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/S2305-0500(14)60053-1","article-title":"Effects of different concentrations of sucrose or trehalose on the post-thawing quality of cattle bull semen","volume":"4","author":"El-Sheshtawy","year":"2015","journal-title":"Asian Pac J Reprod"},{"key":"ref73","doi-asserted-by":"publisher","first-page":"e0271210","DOI":"10.1371\/journal.pone.0271210","article-title":"Beneficial effects of trehalose and gentiobiose on human sperm cryopreservation","volume":"18","author":"Gholami","year":"2023","journal-title":"PLoS One"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"343","DOI":"10.54680\/fr23610110712","article-title":"Role of oleic acid and trehalose on frozen-thawed ram semen","volume":"44","author":"Soltani","year":"2023","journal-title":"Cryo Letters"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"e20200061","DOI":"10.37496\/rbz4920200061","article-title":"Trehalose addition to a Tris-fructose egg yolk extender on quality of ram sperm preserved at 0 \u00b0C","volume":"49","author":"Zhao","year":"2020","journal-title":"Rev Bras Zootec"},{"key":"ref76","doi-asserted-by":"publisher","first-page":"1801","DOI":"10.1016\/s0093-691x(02)00653-2","article-title":"Cryopreservation and post-thawed fertility of ram semen frozen in different trehalose concentrations","volume":"57","author":"Aisen","year":"2002","journal-title":"Theriogenology"},{"key":"ref77","doi-asserted-by":"publisher","first-page":"1000","DOI":"10.1111\/andr.12974","article-title":"Combination of fetuin and trehalose in presence of low glycerol has beneficial effects on freeze-thawed ram spermatozoa","volume":"9","author":"Bucak","year":"2021","journal-title":"Andrology"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.cryobiol.2022.12.019","article-title":"Protective effects of different doses of MitoQ separately and combined with trehalose on oxidative stress and sperm function of cryopreserved Markhoz goat semen","volume":"110","author":"Rezaei","year":"2023","journal-title":"Cryobiology"},{"key":"ref79","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.cryobiol.2020.09.001","article-title":"Decreasing glycerol content by co-supplementation of trehalose and taxifolin hydrate in ram semen extender: microscopic, oxidative stress, and gene expression analyses","volume":"96","author":"Bucak","year":"2020","journal-title":"Cryobiology"},{"key":"ref80","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/j.cryobiol.2013.03.002","article-title":"Trehalose and glycerol have a dose-dependent synergistic effect on the post-thawing quality of ram semen cryopreserved in a soybean lecithin-based extender","volume":"66","author":"Najafi","year":"2013","journal-title":"Cryobiology"},{"key":"ref81","doi-asserted-by":"publisher","first-page":"169","DOI":"10.5455\/javar.2023.j666","article-title":"Effects of glucose and trehalose on tris-citric acid-egg yolk-fructose diluents for semen cryopreservation in goat","volume":"10","author":"Kamal","year":"2023","journal-title":"J Adv Vet Anim Res"},{"key":"ref82","doi-asserted-by":"publisher","first-page":"1614","DOI":"10.5713\/ajas.2009.90286","article-title":"Effects of sucrose and Trehalose on the Freezability of Markhoz goat spermatozoa","volume":"22","author":"Khalili","year":"2009","journal-title":"Asian Australas J Anim Sci"},{"key":"ref83","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1089\/bio.2021.0081","article-title":"Protective effects of Trehalose and Pentoxifylline on goat sperm exposed to chilling-freezing process","volume":"20","author":"Nazari","year":"2022","journal-title":"Biopreserv Biobank"},{"key":"ref84","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/j.smallrumres.2013.04.012","article-title":"Effects of different doses of trehalose supplementation in egg yolk extender in frozen\u2013thawed angora buck semen","volume":"113","author":"Tuncer","year":"2013","journal-title":"Small Rumin Res"},{"key":"ref85","doi-asserted-by":"publisher","first-page":"938622","DOI":"10.3389\/fgene.2022.938622","article-title":"Metabolomics analysis of buck semen cryopreserved with trehalose","volume":"13","author":"Xu","year":"2022","journal-title":"Front Genet"},{"key":"ref86","doi-asserted-by":"publisher","first-page":"1060","DOI":"10.1016\/j.theriogenology.2006.12.004","article-title":"The influence of trehalose, taurine, cysteamine and hyaluronan on ram semen microscopic and oxidative stress parameters after freeze-thawing process","volume":"67","author":"Bucak","year":"2007","journal-title":"Theriogenology"},{"key":"ref87","doi-asserted-by":"publisher","first-page":"299","DOI":"10.54680\/fr23510110612","article-title":"Effect of membrane stabilizers on semen quality and sperm membrane protein expression during cryopreservation of goat semen","volume":"44","author":"Dutta","year":"2023","journal-title":"Cryo Letters"},{"key":"ref88","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.cryobiol.2018.10.266","article-title":"Dimethylacetamide and trehalose for ram semen cryopreservation","volume":"85","author":"Bittencourt","year":"2018","journal-title":"Cryobiology"},{"key":"ref89","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.anireprosci.2013.03.010","article-title":"Comparison of cryoprotective effects of iodixanol, trehalose and cysteamine on ram semen","volume":"139","author":"Cirit","year":"2013","journal-title":"Anim Reprod Sci"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"e13656","DOI":"10.1111\/and.13656","article-title":"Evaluation of synergic effects of iodixanol and trehalose on cryosurvival of electroejaculated ram semen","volume":"52","author":"\u00d6zmen","year":"2020","journal-title":"Andrologia"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"1359","DOI":"10.1111\/rda.13253","article-title":"The protease inhibitor antipain has a beneficial synergistic effect with trehalose for ram semen cryopreservation","volume":"53","author":"Akhtarshenas","year":"2018","journal-title":"Reprod Domest Anim"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"809","DOI":"10.1016\/j.theriogenology.2003.12.003","article-title":"Effects of the supplementation of trehalose extender containing egg yolk with sodium dodecyl sulfate on the freezability of goat spermatozoa","volume":"62","author":"Aboagla","year":"2004","journal-title":"Theriogenology"},{"key":"ref93","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.cryobiol.2021.07.002","article-title":"The effects of varying concentrations of glutathione and trehalose in improving microscopic and oxidative stress parameters in Turkey semen during liquid storage at 5 \u00b0C","volume":"101","author":"Izanloo","year":"2021","journal-title":"Cryobiology"},{"key":"ref94","doi-asserted-by":"publisher","first-page":"1657","DOI":"10.2527\/jas.2009-2335","article-title":"Effects of trehalose supplementation on semen quality and oxidative stress variables in frozen-thawed bovine semen1","volume":"88","author":"Hu","year":"2010","journal-title":"J Anim Sci"},{"key":"ref95","doi-asserted-by":"publisher","first-page":"BSR20191601","DOI":"10.1042\/BSR20191601","article-title":"The roles of reactive oxygen species and antioxidants in cryopreservation","volume":"39","author":"Len","year":"2019","journal-title":"Biosci Rep"},{"key":"ref96","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1007\/978-3-030-32300-4_54","article-title":"Antioxidants in sperm cryopreservation","volume-title":"Male infertility: Contemporary clinical approaches, andrology, ART and Antioxidants","author":"Majzoub","year":"2020"},{"key":"ref97","doi-asserted-by":"publisher","first-page":"1245","DOI":"10.1095\/biolreprod.103.017889","article-title":"Trehalose-enhanced fluidity of the goat sperm membrane and its protection during freezing","volume":"69","author":"Aboagla","year":"2003","journal-title":"Biol Reprod"},{"key":"ref98","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.anireprosci.2012.06.010","article-title":"Effect of different monosaccharides and disaccharides on boar sperm quality after cryopreservation","volume":"133","author":"G\u00f3mez-Fern\u00e1ndez","year":"2012","journal-title":"Anim Reprod Sci"},{"key":"ref99","doi-asserted-by":"publisher","first-page":"5920","DOI":"10.3390\/molecules26195920","article-title":"Role of mono- and disaccharide combination in Cryoprotective medium for rooster semen to ensure Cryoresistance of spermatozoa","volume":"26","author":"Stanishevskaya","year":"2021","journal-title":"Molecules"},{"key":"ref100","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/0304-4157(88)90015-9","article-title":"Interactions of sugars with membranes. Biochimica et Biophysica Acta (BBA) \u2013 reviews on","volume":"947","author":"Crowe","year":"1988","journal-title":"Biomembranes"},{"key":"ref101","doi-asserted-by":"publisher","first-page":"e0130323","DOI":"10.1371\/journal.pone.0130323","article-title":"Engineered Trehalose permeable to mammalian cells","volume":"10","author":"Abazari","year":"2015","journal-title":"PLoS One"},{"key":"ref102","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1080\/19396368.2016.1274791","article-title":"Sperm epigenetics in the study of male fertility, offspring health, and potential clinical applications","volume":"63","author":"Jenkins","year":"2017","journal-title":"Syst Biol Reprod Med"},{"key":"ref103","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1002\/1097-0320(20011101)45:3<161::AID-CYTO1159>3.0.CO;2-7","article-title":"Trehalose improves survival of electrotransfected mammalian cells","volume":"45","author":"Mussauer","year":"2001","journal-title":"Cytometry"},{"key":"ref104","doi-asserted-by":"publisher","first-page":"7414","DOI":"10.1021\/acs.langmuir.8b02015","article-title":"Intracellular delivery of Trehalose for cell banking","volume":"35","author":"Stewart","year":"2019","journal-title":"Langmuir"},{"key":"ref105","doi-asserted-by":"publisher","first-page":"4464","DOI":"10.1016\/j.jnoncrysol.2006.02.182","article-title":"The liquid\u2013glass transition in sugars: relaxation dynamics in trehalose","volume":"352","author":"Cummins","year":"2006","journal-title":"J Non-Cryst Solids"},{"key":"ref106","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1007\/s10561-008-9075-2","article-title":"Animal oocyte and embryo cryopreservation","volume":"9","author":"Pereira","year":"2008","journal-title":"Cell Tissue Bank"},{"key":"ref107","doi-asserted-by":"publisher","first-page":"1249","DOI":"10.1021\/acs.jctc.9b01071","article-title":"Properties of aqueous Trehalose mixtures: glass transition and hydrogen bonding","volume":"16","author":"Olgenblum","year":"2020","journal-title":"J Chem Theory Comput"},{"key":"ref108","doi-asserted-by":"publisher","first-page":"100645","DOI":"10.1016\/j.chphi.2024.100645","article-title":"Comparative study of molecular mechanisms of sucrose & trehalose mediated protection and stabilization of Escherichia coli lipid membrane during desiccation","volume":"8","author":"Rani","year":"2024","journal-title":"Chem Phys Impact"},{"key":"ref109","doi-asserted-by":"publisher","first-page":"1387","DOI":"10.3390\/agriculture13071387","article-title":"Trehalose as a stabilizer of the lipid composition of membranes and the composition of the cytosol of frozen\/thawed rooster spermatozoa","volume":"13","author":"Stanishevskaya","year":"2023","journal-title":"Agriculture"},{"key":"ref110","doi-asserted-by":"publisher","first-page":"2374","DOI":"10.1007\/s11095-010-0243-2","article-title":"Crystallization of Trehalose in frozen solutions and its phase behavior during drying","volume":"27","author":"Sundaramurthi","year":"2010","journal-title":"Pharm Res"},{"key":"ref111","doi-asserted-by":"publisher","first-page":"2452","DOI":"10.1016\/S0006-3495(00)76789-0","article-title":"Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers","volume":"78","author":"Luzardo","year":"2000","journal-title":"Biophys J"},{"key":"ref112","first-page":"123","volume-title":"Trehalose as a cryoprotective agent for the sperm cells: a mini review","author":"Ahmad","year":"2012"},{"key":"ref113","doi-asserted-by":"publisher","first-page":"104293","DOI":"10.1016\/j.jevs.2023.104293","article-title":"Freezability and fertility rates of stallion semen supplemented with Trehalose in lactose extender","volume":"126","author":"Jhamb","year":"2023","journal-title":"J Equine Vet"},{"key":"ref114","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/j.anireprosci.2012.01.014","article-title":"Semen processing and artificial insemination in health management of small ruminants","volume":"130","author":"Cseh","year":"2012","journal-title":"Anim Reprod Sci"},{"key":"ref115","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1111\/and.12329","article-title":"Trehalose enhances osmotic tolerance and suppresses lysophosphatidylcholine-induced acrosome reaction in ram spermatozoon","volume":"47","author":"Ahmad","year":"2015","journal-title":"Andrologia"},{"key":"ref116","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1016\/j.theriogenology.2014.10.015","article-title":"Comparative transcript profiling of gene expression of fresh and frozen-thawed bull sperm","volume":"83","author":"Chen","year":"2015","journal-title":"Theriogenology"},{"key":"ref117","doi-asserted-by":"publisher","first-page":"1025004","DOI":"10.3389\/fgene.2022.1025004","article-title":"Cryopreservation process alters the expression of genes involved in pathways associated with the fertility of bull spermatozoa","volume":"13","author":"Ebenezer Samuel King","year":"2022","journal-title":"Front Genet"},{"key":"ref118","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1093\/humupd\/dmu063","article-title":"The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence","volume":"21","author":"Kopeika","year":"2015","journal-title":"Hum Reprod Update"},{"key":"ref119","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1002\/vms3.355","article-title":"Cryopreservation and its effects on motility and gene expression patterns and fertilizing potential of bovine epididymal sperm","volume":"7","author":"Nazari","year":"2020","journal-title":"Vet Med Sci"},{"key":"ref120","first-page":"207","article-title":"Influence of freezing at different temperatures on the transcription activity of buffalo sperm chromatin","volume":"83","author":"Pironcheva","year":"1995","journal-title":"Cytobios"},{"key":"ref121","doi-asserted-by":"publisher","first-page":"e67614","DOI":"10.1371\/journal.pone.0067614","article-title":"Cryopreservation causes genetic and epigenetic changes in zebrafish genital ridges","volume":"8","author":"Riesco","year":"2013","journal-title":"PLoS One"},{"key":"ref122","doi-asserted-by":"publisher","first-page":"1162","DOI":"10.1016\/S0015-0282(98)00349-5","article-title":"Effect of storage temperature on sperm cryopreservation","volume":"70","author":"Trummer","year":"1998","journal-title":"Fertil Steril"},{"key":"ref123","doi-asserted-by":"publisher","first-page":"10983","DOI":"10.3390\/ijms241310983","article-title":"Cryopreservation induces acetylation of metabolism-related proteins in boar sperm","volume":"24","author":"Ali","year":"2023","journal-title":"Int J Mol Sci"},{"key":"ref124","doi-asserted-by":"publisher","first-page":"107441","DOI":"10.1016\/j.anireprosci.2024.107441","article-title":"An updated review on the application of proteomics to explore sperm cryoinjury mechanisms in livestock animals","volume":"263","author":"Larbi","year":"2024","journal-title":"Anim Reprod Sci"},{"key":"ref125","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1016\/j.theriogenology.2010.02.024","article-title":"Ice-age endurance: the effects of cryopreservation on proteins of sperm of common carp, Cyprinus carpio L.","volume":"74","author":"Li","year":"2010","journal-title":"Theriogenology"},{"key":"ref126","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.cryobiol.2020.10.011","article-title":"The proteomic characterization of ram sperm during cryopreservation analyzed by the two-dimensional electrophoresis coupled with mass spectrometry","volume":"97","author":"Lv","year":"2020","journal-title":"Cryobiology"},{"key":"ref127","doi-asserted-by":"publisher","first-page":"2643","DOI":"10.1002\/pmic.201400525","article-title":"Cryopreservation-induced alterations in protein composition of rainbow trout semen","volume":"15","author":"Nynca","year":"2015","journal-title":"Proteomics"},{"key":"ref128","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.theriogenology.2023.03.023","article-title":"Ram sperm cryopreservation disrupts metabolism of unsaturated fatty acids","volume":"204","author":"Ofosu","year":"2023","journal-title":"Theriogenology"},{"key":"ref129","doi-asserted-by":"publisher","first-page":"1593","DOI":"10.1111\/rda.14236","article-title":"Changes in sperm metabolites of Dezhou donkey after cryopreservation","volume":"57","author":"Yu","year":"2022","journal-title":"Reprod Domest Anim"},{"key":"ref130","doi-asserted-by":"publisher","first-page":"1939","DOI":"10.3390\/ani11071939","article-title":"Metabolomic analysis and identification of sperm Freezability-related metabolites in boar seminal plasma","volume":"11","author":"Zhang","year":"2021","journal-title":"Animals (Basel)"},{"key":"ref131","doi-asserted-by":"publisher","first-page":"1004683","DOI":"10.3389\/fvets.2022.1004683","article-title":"Evaluation of lipidomic change in goat sperm after cryopreservation","volume":"9","author":"Xu","year":"2022","journal-title":"Front Vet Sci"},{"key":"ref132","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/j.anireprosci.2014.03.009","article-title":"Association between the presence of protein bands in ram seminal plasma and sperm tolerance to freezing","volume":"146","author":"Goularte","year":"2014","journal-title":"Anim Reprod Sci"},{"key":"ref133","doi-asserted-by":"publisher","first-page":"802","DOI":"10.3390\/ijms20040802","article-title":"Exploration of miRNA and mRNA profiles in fresh and frozen-thawed boar sperm by transcriptome and small RNA sequencing","volume":"20","author":"Dai","year":"2019","journal-title":"Int J Mol Sci"},{"key":"ref134","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1016\/j.theriogenology.2019.11.001","article-title":"Transcriptome analysis of boar spermatozoa with different freezability using RNA-Seq","volume":"142","author":"Fraser","year":"2020","journal-title":"Theriogenology"},{"key":"ref135","doi-asserted-by":"publisher","first-page":"588","DOI":"10.1186\/s12864-021-07904-8","article-title":"Transcriptome-wide m6A profiling reveals mRNA post-transcriptional modification of boar sperm during cryopreservation","volume":"22","author":"Qin","year":"2021","journal-title":"BMC Genomics"},{"key":"ref136","doi-asserted-by":"publisher","first-page":"300","DOI":"10.3390\/life10110300","article-title":"Regulatory potential of long non-coding RNAs (lncRNAs) in boar spermatozoa with good and poor Freezability","volume":"10","author":"Fraser","year":"2020","journal-title":"Life (Basel)"},{"key":"ref137","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1111\/rda.13615","article-title":"Effects of cryopreservation on stallion sperm protamine messenger RNAs","volume":"55","author":"Kadivar","year":"2020","journal-title":"Reprod Domest Anim"},{"key":"ref138","doi-asserted-by":"publisher","first-page":"E3066","DOI":"10.3390\/ijms19103066","article-title":"Transcriptome sequencing reveals the differentially expressed lncRNAs and mRNAs involved in cryoinjuries in frozen-thawed Giant panda (Ailuropoda melanoleuca) sperm","volume":"19","author":"Ran","year":"2018","journal-title":"Int J Mol Sci"},{"key":"ref139","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.cryobiol.2013.05.007","article-title":"Effect of cryopreservation on human sperm messenger RNAs crucial for fertilization and early embryo development","volume":"67","author":"Valcarce","year":"2013","journal-title":"Cryobiology"},{"key":"ref140","doi-asserted-by":"publisher","first-page":"1172","DOI":"10.1016\/S0140-6736(97)10514-1","article-title":"Relation between semen quality and fertility: a population-based study of 430 first-pregnancy planners","volume":"352","author":"Bonde","year":"1998","journal-title":"Lancet"},{"key":"ref141","doi-asserted-by":"publisher","first-page":"1815","DOI":"10.1007\/s10815-022-02545-6","article-title":"Sperm cryopreservation and DNA methylation: possible implications for ART success and the health of offspring","volume":"39","author":"Khosravizadeh","year":"2022","journal-title":"J Assist Reprod Genet"}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2024.1467242\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,11,19]],"date-time":"2024-11-19T06:18:19Z","timestamp":1731997099000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2024.1467242\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,19]]},"references-count":141,"alternative-id":["10.3389\/fvets.2024.1467242"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2024.1467242","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,19]]},"article-number":"1467242"}}