Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T08:21:27.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Factors affecting rabbit sperm cryopreservation: a mini-review

Published online by Cambridge University Press:  03 June 2021

Elena Kubovicova Open the ORCID record for Elena Kubovicova [Opens in a new window] ,
Alexander V. Makarevich ,
Andrej Balazi ,
Jaromir Vasicek  and
Peter Chrenek
Elena Kubovicova
Affiliation:
National Agricultural and Food Centre (NPPC), Research Institute for Animal Production, Nitra, Slovak Republic
Alexander V. Makarevich
Affiliation:
National Agricultural and Food Centre (NPPC), Research Institute for Animal Production, Nitra, Slovak Republic
Andrej Balazi
Affiliation:
National Agricultural and Food Centre (NPPC), Research Institute for Animal Production, Nitra, Slovak Republic
Jaromir Vasicek
Affiliation:
National Agricultural and Food Centre (NPPC), Research Institute for Animal Production, Nitra, Slovak Republic Slovak University of Agriculture, Faculty of Biotechnology and Food Sciences, Nitra, Slovak Republic
Peter Chrenek*
Affiliation:
National Agricultural and Food Centre (NPPC), Research Institute for Animal Production, Nitra, Slovak Republic Slovak University of Agriculture, Faculty of Biotechnology and Food Sciences, Nitra, Slovak Republic
*
Author for correspondence: Peter Chrenek. Research Institute for Animal Production, NAFC, Hlohovecká 2, 95141Lužianky, Slovak Republic. E-mail: peter.chrenek@nppc.sk; peter.chrenek@uniag.sk
Get access Rights & Permissions [Opens in a new window]

Summary

Rabbits are an important animal species for meeting the nutritional requirements of the world’s growing population due to the high conversion rate of feed. In most countries, the rabbit industry currently relies on artificial insemination with fresh or chilled and frozen–thawed spermatozoa. Various factors during the freezing process, including diluents, sperm preparation and freezing techniques, antioxidants, sudden temperature changes, ice formation and osmotic stress, have been proposed as reasons for the poor sperm quality post thaw. Despite the extensive progress reached in the field of rabbit sperm cryopreservation, new methodological approaches that could overcome problems in sperm cryopreservation are necessary. The aim of this review was to describe the factors that affect the cryopreservation of rabbit sperm.

Keywords

AntioxidantsBreedCryopreservationCryoprotective agentsRabbit sperm
Type
Review Article
Information
Zygote , Volume 30 , Issue 1 , February 2022 , pp. 1 - 8
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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

Aires, VA, Hinsch, KD, Muller-Schlosser, F, Bonger, K, Muller-Schlosser, S and Hinsch, E (2003). In vitro and in vivo comparison of egg-yolk-based and soya bean-based extenders for cryopreservation of bovine semen. Theriogenology 60, 269–79.CrossRefGoogle Scholar
Agarwal, A, Saleh, R and Bedaiwy, M (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79, 829–43.CrossRefGoogle ScholarPubMed
Ansari, MS, Rakha, BA, Andrabi, SM and Akhter, S (2010). Usefulness of powdered and fresh egg yolk for cryopreservation of Zebu bull spermatozoa. Reprod Biol 10, 235–40.CrossRefGoogle ScholarPubMed
Castellini, C (1996). Recent advances in rabbit artificial insemination. In Proceedings of the 6th World Rabbit Congress, Toulouse, France, 9 December 1996, pp. 13–28.Google Scholar
Curry, MR, Redding, BJ and Watson, PF (1995). Determination of water permeability coefficient and its activation energy for rabbit spermatozoa. Cryobiology 32, 175–81.CrossRefGoogle ScholarPubMed
Curry, M, Kleinhans, F and Watson, PF (2000). Measurement of the water permeability of the membranes of boar, ram, and rabbit spermatozoa using concentration-dependent self-quenching of an entrapped fluorophore. Cryobiology 41, 167–73.CrossRefGoogle ScholarPubMed
Daader, AH and Seleem, TST (1997). Recent trends in rabbit production. Proceedings of the 1st International Conference. on Indigenous Versus Acclimatized Rabbits, El-Arish, Egypt, 7–9 September 2009, pp. 23–50.Google Scholar
Dessouki, SHM, Mehaisen, GMK, Abbas, AO and Ashour, G (2016). Sperm motility traits of cooled rabbit semen with different levels of melatonin. Proceedings of the 11th World Rabbit Congress, World Rabbit Science Association. June 15–18. 2016, pp. 185–8.Google Scholar
Di Iorio, M (2014). Cryopreservation of rabbit semen: effectiveness of different permeable and non-permeable cryoprotectants on post-thaw sperm quality and reproductive performances. Doctorate thesis, University of Molise, Italy, 132 pp.Google Scholar
Di Iorio, M, Rocco, M, Chrenek, P and Iaffaldano, N (2014). Comparison of different extenders on the preservability of rabbit semen stored at 5°C for 72 hours. Ital. J Anim Sci 13, 3444 CrossRefGoogle Scholar
Di Iorio, M, Rusco, G, Colonna, MA, Schiavitto, M, Dándrea, MS and Iaffaldano, N (2020). Improving the rabbit semen cryopreservation protocol: comparison between two extenders and inseminating doses. Annal Anim Sci 20, 887–98.CrossRefGoogle Scholar
Domingo, P, Olaciregui, M, Gonzáles, N, De Blas, I and Gil, L (2019). Comparison of different semen extenders and cryoprotectant agents to enhance cryopreservation of rabbit spermatozoa. Czech J Anim Sci 64, 59–66.CrossRefGoogle Scholar
El-Gaafary, MN (1994). Quality and fertility of cooled rabbit semen supplemented with cyclic-AMP stimulators. Anim Reprod Sci 34, 307–13.CrossRefGoogle Scholar
El-Kelawy, HM, Tawfeek, MI, El-Gaafary, MN and Ibrahim, H (2012). Viability and fertilizing ability of extended rabbit semen stored at 5°C. World Rabbit Science Association. Proceedings of the 10th World Rabbit Congress September 3–6 2012, Sharm El-Sheikh, Egypt, pp. 285–9.Google Scholar
El-Sherbieny, MA, Kalaba, ZM, El-Siefy, EME and Ayat, RA (2012). Freezing and fertilizing capacity of frozen rabbit semen extended with gelatin addition. Asian J Anim Sci 6, 291–9.CrossRefGoogle Scholar
Fadl, AM, Ghallab, AM and Abou-Ahmed, MM (2019). Quality assessment of cryopreserved New Zealand rabbit spermatozoa in INRA-82 extender containing different cryoprotectants. World Rabbit Sci 27, 77–83.CrossRefGoogle Scholar
Fukui, Y, Kohno, H, Togari, T, Hiwasa, M and Okabe, K (2008). Fertility after artificial insemination using a soybean-based semen extender in sheep. J Reprod Dev 54, 286–9.CrossRefGoogle ScholarPubMed
Hall, SE, Negus, C, Johinke, D and Bathgate, R (2017). Adjusting cryodiluent composition for improved post-thaw quality of rabbit spermatozoa. PLoS One 12, e0175965.CrossRefGoogle ScholarPubMed
Holt, WV (2000). Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 53, 47–58.CrossRefGoogle ScholarPubMed
Iaffaldano, N, Romagnoli, L, Manchisi, A and Rosato, MP (2011). Cryopreservation of turkey semen by the pellet method: effects of variables such as the extender, cryoprotectant concentration, cooling time and warming temperature on sperm quality determined through principal components analysis. Theriogenology 76, 794–801.CrossRefGoogle ScholarPubMed
Iaffaldano, N, Di Iorio, M and Rosato, MP (2012). The cryoprotectant used, its concentration, and the equilibration time are critical for the successful cryopreservation of rabbit sperm: dimethylacetamide versus dimethyl sulfoxide. Theriogenology 78, 1381–9.CrossRefGoogle Scholar
Iaffaldano, NH, DiOrio, M, Rosato, MP and Manchisi, A (2014). Cryopreservation of rabbit semen using non-permeable cryoprotectants: effectiveness of different concentrations of low-density lipoproteins (LDL) from egg yolk versus egg yolk or sucrose. Anim Reprod Sci 151(3-4), 220–8.CrossRefGoogle ScholarPubMed
Isachenko, E, Isachenko, V, Katkov, II, Dessole, S and Nawroth, F (2003). Vitrification of mammalian spermatozoa in the absence of cryoprotectants: from past practical difficulties to present success. Reprod BioMed Online 6, 191–200.CrossRefGoogle ScholarPubMed
Kaneko, T and Serikawa, T (2012a). Successful long-term preservation of rat sperm by freeze-drying. PLoS One 7, e35043.CrossRefGoogle ScholarPubMed
Kaneko, T and Serikawa, T (2012b). Long-term preservation of freeze-dried mouse spermatozoa. Cryobiology 64, 211–4.CrossRefGoogle ScholarPubMed
Kaneko, T, Ito, H, Sakamoto, H, Onuma, M and Inoue-Murayama, M (2014). Sperm preservation by freeze-drying for the conservation of wild animals. PLoS One 9, e113381.CrossRefGoogle ScholarPubMed
Kashiwazaki, N, Okuda, Y, Seita, Y, Hisamatsu, S, Sonoki, S, Shino, M, Masaoka, T and Inomata, T (2006). Comparison of glycerol, lactamide, acetamide and dimethyl sulfoxide as cryoprotectants of Japanese white rabbit spermatozoa. Reprod Dev 52, 511–6.CrossRefGoogle ScholarPubMed
Keskintepe, L and Eroglu, A (2015). Freeze-drying of mammalian sperm. Methods Mol Biol 1257, 489–97.CrossRefGoogle ScholarPubMed
Keskintepe, L, Pacholczyk, G, Machnicka, A, Norris, K, Curuk, MA, Khan, I and Brackett, BG (2002). Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biol Reprod 67, 409–15.CrossRefGoogle ScholarPubMed
Kopeika, J, Thornhill, A and Khalaf, Y (2015). The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence. Hum Reprod Update 21, 209–27.CrossRefGoogle Scholar
Kulíková, B, Di Iorio, M, Kubovičová, E, Kuželová, L, Iaffaldano, N and Chrenek, P (2015). The cryoprotective effect of Ficoll on the rabbit spermatozoa quality. Zygote 23, 785–94.CrossRefGoogle ScholarPubMed
Kulíková, B, Oravcová, M, Baláži, A, Supuka, P and Chrenek, P (2017). Factors affecting storage of Slovak native rabbit semen in the gene bank. Zygote 25, 592–600.CrossRefGoogle ScholarPubMed
Kusakabe, H, Yanagimachi, R and Kamiguchi, Y (2008). Mouse and human spermatozoa can be freeze-dried without damaging their chromosomes. Hum Reprod 23, 233–9.CrossRefGoogle ScholarPubMed
Leibo, S and Songsasen, N (2002). Cryopreservation of gametes and embryos of non-domestic species. Theriogenology 57, 303–26.CrossRefGoogle ScholarPubMed
Liu, Z, Foote, RH and Brockett, CC (1998). Survival of bull sperm frozen at different rates in media varying in osmolarity. Cryobiology 37, 219–30.CrossRefGoogle ScholarPubMed
Liu, JL, Kusakabe, H, Chang, CC, Suzuki, H, Schmidt, DW, Julian, M, Pfeffer, R, Bormann, CL, Tian, XC, Yanagimachi, R and Yang, X (2004). Freeze-dried sperm fertilization leads to full-term development in rabbits. Biol Reprod 70, 1776–81.CrossRefGoogle ScholarPubMed
Long, JA (2006). Avian semen cryopreservation: what are the biological challenges? Poult Sci 85, 232–6.CrossRefGoogle ScholarPubMed
López, FJ and Alvariño, JMR (2000). Effects of added caffeine on results following artificial insemination with fresh and refrigerated rabbit semen. Anim Reprod Sci 8(1–2), 147–54.CrossRefGoogle Scholar
López-Gatius, F, Sances, G, Sancho, M, Yániz, J, Santolaria, P, Gutiérrez, R, Núñez, M, Núñez, J and Soler, C (2005). Effect of solid storage at 15°C on the subsequent motility and fertility of rabbit semen. Theriogenology 64, 252–60.CrossRefGoogle Scholar
Maertens, L and Luzi, L (1995). Effect of diluent and storage time of rabbit semen on the fertility of does reared under two different lighting schedules. World Rabbit Sci 1, 27–34.Google Scholar
Makarevich, AV, Parkányi, V, Ondruška, Ľ, Kubovičová, E, Fľak, P, Slezáková, M, Pivko, J and Rafay, J (2008). Evaluation of fertilizing capacity of rabbit sperm on the basis of annexin V-labelled membrane changes. Slovak J Anim Sci 41, 1–5.Google Scholar
Martínez-Páramo, S, Pérez-Cerezales, S, Gómez-Romano, F, Blanco, G, Sánchez, JA and Herráez, MP (2009). Cryobanking as tool for conservation of biodiversity: effect of brown trout sperm cryopreservation on the male genetic potential. Theriogenology 71, 594–604.CrossRefGoogle ScholarPubMed
Masoudi, R, Sharafi, M, Zareh Shahneh, A, Towhidi, A, Kohram, H, Esmaeili, V, Shahverdi, A and Davachi, ND (2016). Fertility and flow cytometry study of frozen–thawed sperm in cryopreservation medium supplemented with soybean. Cryobiology 73, 69–72.CrossRefGoogle ScholarPubMed
Maya-Soriano, MJ, Taberner, E, Sabés-Alsina, M, Piles, M and Lopez-Bejar, M (2015). Absence of beneficial effects on rabbit sperm cell cryopreservation by several antioxidant agents. Zygote 23, 1–10.CrossRefGoogle ScholarPubMed
Mocé, E and Vicente, JS (2009). Rabbit sperm cryopreservation: a review. Anim Reprod Sci 110, 1–24.CrossRefGoogle ScholarPubMed
Mocé, E, Vicente, JS and Lavara, R (2003). Effect of freezing–thawing protocols on the performance of semen from three rabbit lines after artificial insemination. Theriogenology 60, 115–23.CrossRefGoogle ScholarPubMed
Mocé, E, Blanch, A, Talaván, M and Viudes-de-Castro, M (2015). Effect of different freezing velocities on the quality and fertilising ability of cryopreserved rabbit spermatozoa. Reprod Fert Dev 27, 846–51.CrossRefGoogle ScholarPubMed
Nishijima, K, Kitajima, S, Koshimoto, C, Morimoto, M, Watanabe, T, Fan, J and Matsuda, Y (2015). Motility and fertility of rabbit sperm cryopreserved using soybean lecithin as an alternative to egg yolk. Theriogenology 84, 1172–5.CrossRefGoogle ScholarPubMed
Okuda, Y, Seita, Y, Hisamatsu, S, Sonoki, S, Shino, M, Masaoka, T, Inomata, T, Kamijo, S and Kashiwazaki, N (2007). Fertility of spermatozoa cryopreserved with 2% acetamide or glycerol through artificial insemination in the Japanese white rabbit. Exp Anim 56, 29–34.CrossRefGoogle ScholarPubMed
Ollero, M, Perez-Pe, R, Muiño-Blanco, T and Cebrian-Perez, JA (1998). Improvement of ram sperm cryopreservation protocols assessed by sperm quality parameters and heterogeneity analysis. Cryobiology 37, 1–12.CrossRefGoogle ScholarPubMed
Pace, MM and Graham, EF (1974). Components in egg yolk which protect bovine spermatozoa during freezing. J Anim Sci 39, 1144–9.CrossRefGoogle ScholarPubMed
Paál, D, Strejček, F, Tvrdá, E, Vašíček, J, Baláži, A, Chrenek, P and Massányi, P (2017). Taurine does not improve the quality of short-term stored rabbit spermatozoa in vitro . Reprod Domest Anim 52, 1046–51.CrossRefGoogle Scholar
Polge, C, Smith, AU and Parkes, AS (1949). Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature 164, 666.CrossRefGoogle ScholarPubMed
Puente, M, Covelo, I and Tartaglione, CM (2018). Effect of the addition of antioxidants in the rabbit semen extender on the fertility and prolificacy. Modern Agric Sci Technol 4(1–2), 44–7.Google Scholar
Riad Rowida, M, Amal, AM, Ghoniem, TS and Seleem, T (2004). Physical characteristics and microbial count of rabbit semen supplemented with Nigella sativa extraction. Asian Journal Vet Med 103, 199–211.Google Scholar
Roca, J, Martínez, S, Vázquez, JM, Lucas, X, Parrilla, I and Martínez, EA (2000). Viability and fertility of rabbit spermatozoa diluted in Tris-buffer extenders and stored at 15°C. Anim Reprod Sci 64(1–2), 103–12.CrossRefGoogle ScholarPubMed
Rodriguez-Martinez, H and Wallgren, M (2010). Advances in boar semen cryopreservation. Vet Med Int 2010, 396181.Google ScholarPubMed
Rossato, MP and Iaffaldano, N (2013). Cryopreservation of rabbit semen: comparing the effects of different cryoprotectants, cryoprotectant-free vitrification, and the use of albumin plus osmoprotectants on sperm survival and fertility after standard vapour freezing and vitrification. Theriogenology 79, 508–16.CrossRefGoogle Scholar
Safaa, HM, Lavara, R, Viudes-de-Castro, MP, Elsayed, DAA, Mehaisen, GMK, Marco-Jiménez, F and Vicente, JS (2012). Effect of different freezing extenders on semen quality, fertility and prolificacy in two selected lines of rabbit bucks. Proceedings of the 10th World Rabbit Congress, Sharm El-Sheikh, Egypt, 3–6 September 2012, pp. 325–9.Google Scholar
Salamon, S and Maxwell, WMC (1995). Frozen storage of ram semen. I. Processing, freezing, thawing and fertility after cervical insemination. Anim Reprod Sci 37, 185–249.CrossRefGoogle Scholar
Seleem, TST and Riad, RM (2005). Enzymatic activity and fertilizing ability of rabbit semen supplemented with Nigella sativa extraction. In Proceedings of the 4th International Conference on Rabbit Production in Hot Climates, Sharm El-Sheikh, Egypt, pp. 83–189.Google Scholar
Sztein, JM, Farley, JS and Mobraaten, LE (2000). In vitro fertilization with cryopreserved inbred mouse sperm. Biol Reprod 63, 1774–80.CrossRefGoogle ScholarPubMed
Thurston, L, Watson, PF and Holt, WV (2002). Cryopreservation? A genetic explanation for species and individual variation. Cryo Lett 23, 255–62.Google ScholarPubMed
Thuwanut, P, Srisuwatanasagul, S, Wongbandue, G, Tanpradit, N, Thongpakdee, A, Tongthainan, D, Manee-In, S and Chatdarong, K (2013). Sperm quality and the morphology of cryopreserved testicular tissues recovered post-mortem from diverse wild species. Cryobiology 67, 244–7.CrossRefGoogle ScholarPubMed
Viudes-de-Castro, MP, Lavara, R, Safaa, HM, Marco-Jiménez, F, Mehaisen, GM and Vicente, JS (2014). Effect of freezing extender composition and male line on semen traits and reproductive performance in rabbits. Animal 8, 765–70.CrossRefGoogle ScholarPubMed
Waterhouse, KE, Hofmo, PO, Tverdal, A and Miller, RR Jr (2006). Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 131, 887–94.CrossRefGoogle ScholarPubMed
Zaniboni, L, Cassinelli, C, Mangiagalli, MG, Gliozzi, TM and Cerolini, S (2014). Pellet cryopreservation for chicken semen: effects of sperm working concentration, cryoprotectant concentration, and equilibration time during in vitro processing. Theriogenology 82, 251−8.CrossRefGoogle ScholarPubMed
Zeidan, EB, El-Zaiat, EHR, Rowida, M and El-Aasar, R (2008). Viability, acrosomal status and sex ratio of the centrifuged rabbit spermatozoa. Am Eurasian J Agric Environ Sci 4, 318–25.Google Scholar
Zhu, Z, Fan, X, Lv, Y, Zhang, N, Fan, C, Zhang, P and Zheng, W (2015). Vitamin E analogue improves rabbit sperm quality during the process of cryopreservation through its antioxidative action. PLoS One 10, e0145383.CrossRefGoogle ScholarPubMed