Towards Improving the Outcomes of Multiple Ovulation and Embryo Transfer in Sheep, with Particular Focus on Donor Superovulation
Abstract
:1. Introduction
2. Animal Management and Selection
3. Hormones for Superovulation
3.1. FSH and Superovulatory Response
3.2. eCG and Superovulation Response
3.3. Other Rarely Used Hormones
Breed | Superovulation Protocol | OR 1 | ER 2 | FR 3 (%) | TRR 4 | References |
---|---|---|---|---|---|---|
Awassi breed | FSH decreasing doses | 8.75 ± 0.4 ac | 4.83 ±0.6 | - | - | [68] |
eCG 1200 IU, single dose | 5.66 ± 0.4 bd | 4.66 ± 0.6 a | - | - | ||
Corriedale and Bond | In simplified protocol, FSH 180 mg | 10.2 ± 3.4 | 9.9 ± 3.6 | 52.5 | 5.1 ± 4.9 | [36] |
6 FSH administered twice daily | 10.8 ± 4.7 | 10.5 ± 5.2 | 37.1 | 2.9 ± 2.9 | ||
Corriedale | oFSH + eCG, single injection | 13.8 ± 1.9 a | 8.4 ± 1.4 a | 64.2 b | - | [29] |
oFSH dissolved in saline, divided into 4 equal doses | 6.2 ± 1.1 b | 3.1 ± 1.1 b | 45.9 b | - | ||
oFSH dissolved in 30% polyvinylpyrrolidone, single dose | 4.7 ± 1.0 b | 3.2 ± 1.1 b | 89.7 a | - | ||
oFSH 72 h before and 12 h after sponge removal, 8 decreasing doses | 10.7 ± 0.9 a | 5.5 ± 0.8 | 93.9 | - | ||
Fine wool Merino | FSH,7 decreasing doses 48 h before sponge removal during breeding and non-breeding season | 13.9 ±0.8 a 11.3 ±1.8 a | 6.0 ± 0.5 a 3.5 ± 1.0 b | - | - | [69] |
FSH 70 mg + eCG, single dose 48 h before sponge removal during breeding and non-breeding season | 3.2 ± 1.2 b 6.0 ± 1.1 b | 1.2 ± 0.6 b 1.6 ± 0.5 b | - | - | ||
Merino breed | eCG + 11.5 mg pFSH, 6 decreasing doses | 14.2±1.2 a | 5.2± 1.9 a | 58.3 a | - | [53] |
eCG, 1200 IU | 6.2 ± 0.8 b | 1.0 ± 0.5 b | 26.3 | - | ||
eCG, 1600 IU | 11.0 ± 3.0 ab | 1.2± 0.6 b | 19.2 | - | ||
Ojalada | 280 IU pFSH, 6 decreasing doses | 15.9 ± 2.0 a | 10.7± 1.7 a | 86 a | - | [35] |
210IU pFSH + 500 IU eCG, single dose | 14.5 ± 2.1 a | 11.3 ± 1.8 | 76 a | - | ||
Sarda | 250 IU pFSH, 4 decreasing doses | 11.8 ± 4.0 a | 8.80 c | 81.7 | - | [19] |
125 IU pFSH + 600 IU eCG | 8.05 ± 3.8 b | 4.82 d | 82 | |||
Suffolk | eCG, 750–1000 IU, single injection | 7.7 ± 1.4 | 3.5 ± 1.6 | - | - | [70] |
FSH, 20–24 mg, multiple injections | 8.4 ± 0.4 | 5.3 ± 0.5 | - | - | ||
Xinji fine wool | FSH at the rate of 60, 50, and 30 IU per injection on days 1, 2, and 3 | 9.67 ± 1.93 | 7.85 ± 2.4 | - | 4.52 ± 2.5 b | [71] |
150 mg Folltropin-V, twice daily at 35, 25, and 15 mg per injection on days 1, 2, and 3 | 12.47 ± 1.5 | 9.27 ± 1.8 | - | 7.86 ± 1.75 a |
4. Factors Affecting Outcomes of Superovulation
4.1. Ovarian Follicular Dynamics and Estrus Synchronization
4.2. Gonadotrophins and Superovulation
4.3. Dose–Response Relationship
Dose 1 | Hormone | Breed | OR 2 | ER 3 | FR 4 (%) | TRR 5 | References |
---|---|---|---|---|---|---|---|
500 | eCG | Chios | 2.6 ± 0.4 c | 2.2 ± 0.3 b | 59.1 | - | [85] |
750 | 3.9 ± 0.5 b | 3.4 ± 0.5 c | 72.4 | - | |||
1000 | 5.9 ± 0.8 a | 2.6 ± 0.4 b | 68.2 | - | |||
1500 | 5.0± 0.9 a | 1.6 ± 0.5 a | 64.8 | - | |||
250 | pFSH | Altamurana | 8.0 ± 1.5 b | 6.7 ± 1.4 | - | 4.1 ± 0.8 a | [54] |
500 | 10.2 ± 1.6 ab | 6.7 ± 1.5 | - | 2.8 ± 0.8 ab | |||
750 | 13.7 ± 1.6 a | 8.5 ± 1.4 | - | 1.3 ± 0.8 b | |||
1000 | 12.6 ± 1.6 ab | 9.4 ± 1.4 | - | 2.0 ± 0.9 b | |||
12 | pFSH | Chios | 5.5 ± 0.7 eu | 4.4 ± 0.7 cu | 65.4 w | - | [86] |
16 | 12.4 ± 0.9 fy | 8.7 ± 1.0 dw | 67.8 au | - | |||
12 | Fresian | 3.6 ± 0.4 ev | 2.4 ± 0.4 av | 95.6 x | - | ||
16 | 7.0 ± 0.6 fz | 4.3 ± 0.8 bx | 90.8 bv | - | |||
90 | Xinji Fine wool | 6.25 ± 2.73 b | 5.12 ± 2.47 b | [71] | |||
120 | 10.65 ± 2.21 a | 8.46 ± 2.25 a | |||||
150 | 9.55 ± 2.47 a | 7.82 ± 1.88 a | |||||
80 | pFSH | Katahdin hair | 1.4 ± 1.1 | 1.0 ± 0.6 b | - | 1.0 ± 0.5 b | [84] |
120 | 4.5 ± 1.2 | 3.0 ± 0.7 | - | 2.0 ± 0.6 | |||
140 | 4.6 ± 1.1 | 3.0 ± 0.6 | - | 2.3 ± 0.5 | |||
128 | pFSH | Dorper ewes | 11.3 ± 0.3 b | 5.9 ± 0.8 | 83.6 b | 5.1 ± 0.7 | [83] |
200 | 16.3 ± 0.3 a | 5.3 ± 0.8 | 62.4 a | 4.4 ± 0.7 | |||
140 | FSH | Romanov | 6.3 ± 4 | 6.6 ± 0.5 | [87] | ||
175 | 7.6 ± 6 | 5.6 ± 0.5 | |||||
100 | Santa Inês | 13.5 ± 5.7 | 2.63 ± 2.9 ab | [88] | |||
133 | 9.00 ± 3.6 | 1.5 ± 2.5 b | |||||
200 | 14.88 ± 6.9 | 3.9 ± 3.5 a | |||||
100 | pFSH | Lacaune | 2.6 ± 0.7 a | 1.0 ± 0.5 a | [28] | ||
200 | 11.6 ± 1.2 b | 6.9 ± 1.1 b |
4.4. Breed and Age
4.5. Season and Location
4.6. Nutritional Status
5. Strategies for Improving Superovulation Response in Sheep
5.1. Inhibin Immunization along with Conventional Superovulation Protocols
5.2. Melatonin Implants and Superovulation
5.3. Recombinant Hormones and Superovulation
6. Artificial Insemination (AI)
7. Donor Embryo Recovery and Transfer to the Recipient
No. of Donor Animals | Fluid Recovery (%) | Duration of Uterine Flushing (min) | NSER Performed (%) | Structures/Embryos Recovered | References |
---|---|---|---|---|---|
17 | 95.6 | - | 59.8 | 6.5 | [153] |
58 | 95.7 | - | 94.8 | 6.0 | [154] |
23 | 90.1 | - | 80–91 | 1.1 | [156] |
16 | 96.2 | - | 78–86 | 6.4–7.4 | [157] |
23 | 91–94.8 | 24.7–26.2 | 80–81.5 | 0.5–0.8 | [158] |
36 | 97–99 | 21.4–25.4 | 83.3–100 | 0.7–1.0 | [159] |
16 | 95.5–97.2 | 27.8–29.1 | 81.2–87.6 | 2.9–4.1 | [160] |
36 | 32.6 | 2.5–4.8 | [161] |
8. Successive Embryo Production through Repeated Superovulation
9. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kalds, P.; Zhou, S.; Cai, B.; Liu, J.; Wang, Y.; Petersen, B.; Sonstegard, T.; Wang, X.; Chen, Y. Sheep and goat genome engineering: From random transgenesis to the CRISPR era. Front. Genet. 2019, 10, 750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akinmoladun, O.F.; Muchenje, V.; Fon, F.N. Small ruminants: Farmers’ hope in a world threatened by water scarcity. Animals 2019, 9, 456. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wodajo, H.D.; Gemeda, B.A.; Kinati, W.; Mulem, A.A.; van Eerdewijk, A.; Wieland, B. Contribution of small ruminants to food security for Ethiopian smallholder farmers. Small Rumin. Res. 2020, 184, 106064. [Google Scholar] [CrossRef]
- Thornton, P.K. Livestock production: Recent trends, future prospects. Philos. Trans. R. Soc. B Biol. Sci. 2010, 365, 2853–2867. [Google Scholar] [CrossRef] [Green Version]
- Cannas, A.; Tedeschi, L.O.; Atzori, A.S.; Lunesu, M.F. How can nutrition models increase the production efficiency of sheep and goat operations? Anim. Front. 2019, 9, 33–44. [Google Scholar] [CrossRef]
- Maciel, G.S.; Rodriguez, M.G.K.; da Silva, P.D.A.; Nociti, R.P.; Uscategui, R.A.R.; Santos, V.J.C.; Feliciano, M.A.R.; Vicente, W.R.R.; Oliveira, M.E.F. Ovarian superstimulation treatment for multiple ovulation and embryo transfer programs in sheep. Investigação 2017, 16, 8. [Google Scholar] [CrossRef] [Green Version]
- Ramos, A.F.; Silva, B.D.M. Hormonal protocols in small ruminants. Embrapa Recur. Genéticos Biotecnol.-Capítulo Livro Cient. (ALICE) 2018, 74, 618–626. [Google Scholar]
- Batt, P.; Killeen, I.; Cameron, A. Use of single or multiple injections of FSH in embryo collection programmes in goats. Reprod. Fertil. Dev. 1993, 5, 49–56. [Google Scholar] [CrossRef]
- Brasil, O.; Moreira, N.; Júnior, G.S.; Silva, B.; Mariante, A.; Ramos, A. Superovulatory and embryo yielding in sheep using increased exposure time to progesterone associated with a GnRH agonist. Small Rumin. Res. 2016, 136, 54–58. [Google Scholar] [CrossRef] [Green Version]
- Ishwar, A.; Memon, M. Embryo transfer in sheep and goats: A review. Small Rumin. Res. 1996, 19, 35–43. [Google Scholar] [CrossRef]
- González-Bulnes, A.; Baird, D.T.; Campbell, B.K.; Cocero, M.J.; García-García, R.M.; Inskeep, E.K.; López-Sebastián, A.; McNeilly, A.S.; Santiago-Moreno, J.; Souza, C.J. Multiple factors affecting the efficiency of multiple ovulation and embryo transfer in sheep and goats. Reprod. Fertil. Dev. 2004, 16, 421–435. [Google Scholar] [CrossRef]
- Bettencourt, E.M.; Bettencourt, C.M.; e Silva, J.C.; Ferreira, P.; Manito, C.I.; Matos, C.M.; Romão, R.J.; Rocha, A. Effect of season and gonadotrophin preparation on superovulatory response and embryo quality in Portuguese Black Merinos. Small Rumin. Res. 2008, 74, 134–139. [Google Scholar] [CrossRef]
- Greyling, J.; Van der Nest, M.; Schwalbach, L.; Muller, T. Superovulation and embryo transfer in South African Boer and indigenous feral goats. Small Rumin. Res. 2002, 43, 45–51. [Google Scholar] [CrossRef]
- Gonzalez, F.; Calero, P.; Beckers, J.-F. Induction of superovulation in domestic ruminants. In Biotechnology in Animal Husbandry; Springer: Berlin/Heidelberg, Germany, 2001; pp. 209–223. [Google Scholar]
- Quan, F.; Zhang, Z.; An, Z.; Hua, S.; Zhao, X.; Zhang, Y. Multiple factors affecting superovulation in Poll Dorset in China. Reprod. Domest. Anim. 2011, 46, 39–44. [Google Scholar] [CrossRef]
- Cognie, Y.; Baril, G.; Poulin, N.; Mermillod, P. Current status of embryo technologies in sheep and goat. Theriogenology 2003, 59, 171–188. [Google Scholar] [CrossRef]
- Hameed, N.; Khan, M.I.-u.-R.; Zubair, M.; Andrabi, S.M.H. Approaches of estrous synchronization in sheep: Developments during the last two decades: A review. Trop. Anim. Health Prod. 2021, 53, 485. [Google Scholar] [CrossRef]
- Rahman, M.; Rahman, M.w.; Khadijah, W.W.; Abdullah, R. Follicle stimulating hormone (FSH) dosage based on body weight enhances ovulatory responses and subsequent embryo production in goats. Asian-Australas. J. Anim. Sci. 2014, 27, 1270. [Google Scholar] [CrossRef] [Green Version]
- Leoni, G.; Bogliolo, L.; Pintus, P.; Ledda, S.; Naitana, S. Sheep embryos derived from FSH/eCG treatment have a lower in vitro viability after vitrification than those derived from FSH treatment. Reprod. Nutr. Dev. 2001, 41, 239–246. [Google Scholar] [CrossRef] [Green Version]
- Daly, J.; Smith, H.; McGrice, H.A.; Kind, K.L.; van Wettere, W.H. Towards improving the outcomes of assisted reproductive technologies of cattle and sheep, with particular focus on recipient management. Animals 2020, 10, 293. [Google Scholar] [CrossRef] [Green Version]
- Júnior, E.L.; Maia, E.; Paula, N.; Teixeira, D.; Villarroel, A.; Rondina, D.; Freitas, V. Effect of age of donor on embryo production in Morada Nova (white variety) ewes participating in a conservation programme in Brazil. Trop. Anim. Health Prod. 2006, 38, 555–561. [Google Scholar] [CrossRef]
- Kolling, A.; Brilhante, G.; Drechmer, J.; Santos, L.; Silva, B.; Ramos, A. Relationship between superovulation and embryo production with ovarian follicular population before superovulatory treatment in Brazilian Bergamasca sheep. Arq. Bras. Med. Vet. Zootec. 2021, 73, 115–122. [Google Scholar] [CrossRef]
- De Albuquerque Lagares, M.; Varago, F.C.; Moustacas, V.S.; Gheller, V.A.; Nicolino, R.R.; Borges, I.; Henry, M. Effect of season and frequency of embryo collections on superovulatory response and embryo recovery in Santa Inês hair sheep. Small Rumin. Res. 2021, 201, 106441. [Google Scholar] [CrossRef]
- Abecia, J.; Forcada, F.; Palacín, I.; Sánchez-Prieto, L.; Sosa, C.; Fernández-Foren, A.; Meikle, A. Undernutrition affects embryo quality of superovulated ewes. Zygote 2015, 23, 116–124. [Google Scholar] [CrossRef]
- O’callaghan, D.; Yaakub, H.; Hyttel, P.; Spicer, L.; Boland, M. Effect of nutrition and superovulation on oocyte morphology, follicular fluid composition and systemic hormone concentrations in ewes. J. Reprod. Fertil. 2000, 118, 303–314. [Google Scholar] [CrossRef] [Green Version]
- Bari, F.; Khalid, M.; Haresign, W.; Murray, A.; Merrell, B. Factors affecting the survival of sheep embryos after transfer within a MOET program. Theriogenology 2003, 59, 1265–1275. [Google Scholar] [CrossRef]
- Suiter, J. Body condition scoring of sheep and goats. Farmnote 1994, 69, 1994. [Google Scholar]
- Figueira, L.M.; Alves, N.G.; Souza-Fabjan, J.M.G.; Batista, R.I.T.P.; Arrais, A.M.; Lima, R.R.; Oliveira, M.E.F.; Fonseca, J.F. In vivo embryo production and recovery in lacaune ewes after imposing a superovulation treatment regimen is related to pFSH dose. Anim. Reprod. Sci. 2020, 223, 106625. [Google Scholar] [CrossRef] [PubMed]
- Simonetti, L.; Forcada, F.; Rivera, O.; Carou, N.; Alberio, R.; Abecia, J.; Palacin, I. Simplified superovulatory treatments in Corriedale ewes. Anim. Reprod. Sci. 2008, 104, 227–237. [Google Scholar] [CrossRef] [PubMed]
- Mei, C.; Li, M.; Zhong, S.; Lei, Y.; Shi, Z. Enhancing embryo yield by immunization against inhibin in superovulated Holstein heifers. Reprod. Domest. Anim. 2009, 44, 735–739. [Google Scholar] [CrossRef] [PubMed]
- Schiewe, M.; Howard, J.; Goodrowe, K.; Stuart, L.; Wildt, D. Human menopausal gonadotropin induces ovulation in sheep, but embryo recovery after prostaglandin F2α synchronization is compromised by premature luteal regression. Theriogenology 1990, 34, 469–486. [Google Scholar] [CrossRef]
- Kaya, S.; Kaçar, C.; Kaya, D.; Aslan, S. The effectiveness of supplemental administration of progesterone with GnRH, hCG and PGF2α on the fertility of Tuj sheep during the non-breeding season. Small Rumin. Res. 2013, 113, 365–370. [Google Scholar] [CrossRef]
- Wang, X.; El-Gayar, M.; Knight, P.; Holtz, W. The long-term effect of active immunization against inhibin in goats. Theriogenology 2009, 71, 318–322. [Google Scholar] [CrossRef]
- Shi, J.-M.; Yi, J.-Y.; Tian, X.-Z.; Wang, F.; Lian, Z.-X.; Han, H.-B.; Fu, J.-C.; Lv, W.-F.; Liu, G.-S. Effects of seasonal changes on the ovulation rate and embryo quality in superovulated Black Suffolk ewes. Neuroendocrinol. Lett. 2015, 36, 330–336. [Google Scholar]
- Forcada, F.; Amer-Meziane, M.A.; Abecia, J.; Maurel, M.-C.; Cebrián-Pérez, J.; Muiño-Blanco, T.; Asenjo, B.; Vázquez, M.; Casao, A. Repeated superovulation using a simplified FSH/eCG treatment for in vivo embryo production in sheep. Theriogenology 2011, 75, 769–776. [Google Scholar] [CrossRef]
- Panyaboriban, S.; Suwimonteerabutr, J.; Swangchan-Uthai, T.; Tharasanit, T.; Suthikrai, W.; Suadsong, S.; Techakumphu, M. A simplified superovulation protocol using split-single administration of Folltropin®-V in hyaluronan: Application to purebred sheep. Vet. Med. 2018, 63, 321–328. [Google Scholar] [CrossRef] [Green Version]
- Chumchai, R.; Ratsiri, T.; Ratchamak, R.; Vongpralub, T.; Boonkum, W.; Chankitisakul, V. Ovarian responses and FSH profiles at superovulation with a single epidural administration of gonadotropin in the Thai-Holstein crossbreed. Anim. Reprod. 2021, 18, e20210053. [Google Scholar] [CrossRef]
- Lunenfeld, B.; Bilger, W.; Longobardi, S.; Alam, V.; D’Hooghe, T.; Sunkara, S.K. The development of gonadotropins for clinical use in the treatment of infertility. Front. Endocrinol. 2019, 10, 429. [Google Scholar] [CrossRef] [Green Version]
- Holtz, W. Embryo transfer in the goat—A review. DTW. Dtsch. Tierarztl. Wochenschr. 1996, 103, 293–297. [Google Scholar]
- Sebastian, A.L.; Cognie, Y.; Cocero, M.; De La Fuente, J.; Poulin, N. Effect of season and duration of FSH treatment on embryo production in sheep. Theriogenology 1990, 34, 175–180. [Google Scholar] [CrossRef]
- Dattena, M.; Vespignani, S.; Branca, A.; Gallus, M.; Ledda, S.; Naitana, S.; Cappai, P. Superovulatory response and quality of embryos recovered from anestrus ewes after a single injection of porcine FSH dissolved in polyvinylpyrrolidone. Theriogenology 1994, 42, 235–239. [Google Scholar] [CrossRef]
- Meinecke-Tillman, S.; Lewalski, H.; Meinecke, B. Induction of superovulation in Merinolandshaf ewes after single or multiple FSH injectons. Reprod. Domest. Anim. 1993, 28, 433–442. [Google Scholar]
- Peebles, I.; Kidd, J. Single treatment superovulation in the cashmere goat using porcine follicle stimulating hormone. Theriogenology 1994, 41, 271. [Google Scholar] [CrossRef]
- Maxwell, W.; Wilson, H. Superovulation and embryo recovery in adult and maiden ewes treated with single and multiple injections of pituitary extract. Proc. Aust. Soc. Reprod. Biol. 1990, 22, 15. [Google Scholar]
- Watanabe, H.; Miyamoto, A.; Okada, M.; Ishida, N.; Kimura, H.; Fukui, Y. A simple superovulation method of a single injection of follicle-stimulating hormone combined with equine chorionic gonadotropin for superovulation of Suffolk ewes during the breeding season: I. Effects of different treatments on the endocrine profiles. J. Reprod. Dev. 1998, 44, 169–176. [Google Scholar] [CrossRef] [Green Version]
- Yamada, A.; Kawana, M.; Tamura, Y.; Miyamoto, A.; Fukui, Y. Effect of single or multiple injection of follicle stimulating hormone combined with pregnant mare serum gonadotropin on superovulatory response, and normal and freezable embryos in ewes. J. Reprod. Dev. 1996, 42, 81–87. [Google Scholar] [CrossRef] [Green Version]
- Evans, G. Superovulation and embryo recovery in Merino ewes. Theriogenology 1994, 41, 192. [Google Scholar] [CrossRef]
- Chasombat, J.; Sakhong, D.; Nagai, T.; Parnpai, R.; Vongpralub, T. Superstimulation of follicular growth in Thai native heifers by a single administration of follicle stimulating hormone dissolved in polyvinylpyrrolidone. J. Reprod. Dev. 2012, 59, 214. [Google Scholar] [CrossRef] [Green Version]
- Tríbulo, A.; Rogan, D.; Tribulo, H.; Tribulo, R.; Alasino, R.V.; Beltramo, D.; Bianco, I.; Mapletoft, R.J.; Bó, G.A. Superstimulation of ovarian follicular development in beef cattle with a single intramuscular injection of Folltropin-V. Anim. Reprod. Sci. 2011, 129, 7–13. [Google Scholar] [CrossRef] [PubMed]
- Kimura, K.; Hirako, M.; Iwata, H.; Aoki, M.; Kawaguchi, M.; Seki, M. Successful superovulation of cattle by a single administration of FSH in aluminum hydroxide gel. Theriogenology 2007, 68, 633–639. [Google Scholar] [CrossRef] [PubMed]
- Bo, G.; Hockley, D.; Nasser, L.; Mapletoft, R. Superovulatory response to a single subcutaneous injection of Folltropin-V in beef cattle. Theriogenology 1994, 42, 963–975. [Google Scholar] [CrossRef]
- Yamamoto, M.; Ooe, M.; Kawaguchi, M.; Suzuki, T. Superovulation in the cow with a single intramuscular injection of FSH dissolved in polyvinylpyrrolidone. Theriogenology 1994, 41, 747–755. [Google Scholar] [CrossRef]
- Blanco, M.; Simonetti, L.; Rivera, O. Embryo production and progesterone profiles in ewes superovulated with different hormonal treatments. Small Rumin. Res. 2003, 47, 183–191. [Google Scholar] [CrossRef]
- D’Alessandro, A.; Martemucci, G.; Toteda, F.; Gambacorta, M.; Manchisi, A. Superovulation and embryo production in ewes using a commercial p-FSH. Small Rumin. Res. 1996, 19, 255–261. [Google Scholar] [CrossRef]
- Senthilkumar, P.; Rajasundaram, R.; Selvaraju, M.; Kathiresan, D. Effect of inclusion of norgestomet ear implants in the goat superovulationregimen. Indian Vet. J. 1998, 75, 595–597. [Google Scholar]
- Cseh, S.; Solti, L. Studies on factors affecting superovulation and embryo transfer in Hungarian Merino ewes. Acta Vet. Hung. 2001, 49, 431–441. [Google Scholar] [CrossRef]
- Ryan, J.; Hunton, J.; Maxwell, W. Increased production of sheep embryos following superovulation of Merino ewes with a combination of pregnant mare serum gonadotrophin and follicle stimulating hormone. Reprod. Fertil. Dev. 1991, 3, 551–560. [Google Scholar] [CrossRef]
- Moore, N.; Shelton, J. Egg transfer in sheep. Effect of degree of synchronization between donor and recipient, age of egg, and site of transfer on the survival of transferred eggs. J. Reprod. Fertil. 1964, 7, 145–152. [Google Scholar] [CrossRef] [Green Version]
- Moore, N. Fertilization in ewes treated with progesterone and equine anterior pituitary extract. J. Endocrinol. 1970, 46, 121–122. [Google Scholar] [CrossRef]
- Boland, M.; Crosby, T.; Gordon, I. Ovarian response in ewes following horse anterior pituitary extract and progestagen treatment. Anim. Reprod. Sci. 1983, 6, 119–127. [Google Scholar] [CrossRef]
- Baldassarre, A.; Aste, F.; Argerich, M.; de Matos, D. Comparative study between human menopausic gonadotrophin (HMG) and hipofisisary follicle stimulating hormone (FSH-P) for superovulation in sheep. In Proceedings of the 12th International Congress on Animal Reproduction, The Hague, The Netherlands, 23–27 August 1992; pp. 182–183. [Google Scholar]
- Bó, G.A.; Mapletoft, R.J. Superstimulation of ovarian follicles in cattle: Gonadotropin treatment protocols and FSH profiles. Theriogenology 2020, 150, 353–359. [Google Scholar] [CrossRef]
- Azawi, O. A new technique for nonsurgical embryo recovery in superovulated ewes treated with estradiol and oxytocin. Al-Qadisiyah J. Vet. Med. Sci. 2011, 10, 36–44. [Google Scholar] [CrossRef] [Green Version]
- Menchaca, A.; Vilariño, M.; Pinczak, A.; Kmaid, S.; Saldaña, J. Progesterone treatment, FSH plus eCG, GnRH administration, and Day 0 Protocol for MOET programs in sheep. Theriogenology 2009, 72, 477–483. [Google Scholar] [CrossRef]
- Balaro, M.; Fonseca, J.; Barbosa, T.; Souza-Fabjan, J.; Figueira, L.; Teixeira, T.; Carvalheira, L.; Brandão, F. Potential role for GnRH in the synchronization of follicular emergence before the superovulatory Day 0 protocol. Domest. Anim. Endocrinol. 2016, 54, 10–14. [Google Scholar] [CrossRef]
- Schmitt, E.-P.; Diaz, T.; Barros, C.; De la Sota, R.; Drost, M.; Fredriksson, E.; Staples, C.; Thorner, R.; Thatcher, W. Differential response of the luteal phase and fertility in cattle following ovulation of the first-wave follicle with human chorionic gonadotropin or an agonist of gonadotropin-releasing hormone. J. Anim. Sci. 1996, 74, 1074–1083. [Google Scholar] [CrossRef]
- Rajamahendran, R.; Sianangama, P. Effect of human chorionic gonadotrophin on dominant follicles in cows: Formation of accessory corpora lutea, progesterone production and pregnancy rates. Reproduction 1992, 95, 577–584. [Google Scholar] [CrossRef]
- Azawi, O.I.; Al-Mola, M. A study on superovulation using FSH and eCG in Awassi ewes. Trop. Anim. Health Prod. 2010, 42, 799–801. [Google Scholar] [CrossRef]
- Cueto, M.; Gibbons, A.; Pereyra-Bonnet, F.; Silvestre, P.; González-Bulnes, A. Effects of Season and Superovulatory Treatment on Embryo Yields in Fine-Wool Merinos Maintained Under Field Conditions. Reprod. Domest. Anim. 2011, 46, 770–775. [Google Scholar] [CrossRef]
- Armstrong, D.; Evans, G. Factors influencing success of embryo transfer in sheep and goats. Theriogenology 1983, 19, 31–42. [Google Scholar] [CrossRef]
- Wu, W.; Yang, M.; Gong, P.; Wang, F.; Tian, Y.; Xu, X.; Fu, X.; Tian, K.; Guo, Z. Effect of two follicle stimulating hormone (FSH) preparations and simplified superovulatory treatments on superovulatory response in Xinji fine-wool sheep. Afr. J. Biotechnol. 2011, 10, 15834–15837. [Google Scholar] [CrossRef]
- Oliveira, M.; Ayres, H.; Oliveira, L.; Oba, E.; Kridli, R.; Bartlewski, P.; Fonseca, J.; Bicudo, S.; Vicente, W. Follicular wave emergence in Santa Inês ewes subjected to long-term, progesterone-based estrous synchronization protocols at different times of the year. Anim. Reprod. Sci. 2016, 174, 80–86. [Google Scholar] [CrossRef] [Green Version]
- Souza-Fabjan, J.M.G.; da Rosa, R.M.; Balaro, M.F.A.; Pinto, P.H.N.; dos Santos, G.B.; Arashiro, E.K.N.; da Fonseca, J.F.; Ungerfeld, R.; Brandão, F.Z. Effect of different hormonal combinations on follicular wave emergence and superovulatory response in sheep. Theriogenology 2017, 103, 24–29. [Google Scholar] [CrossRef]
- Menchaca, A.; Vilariño, M.; Crispo, M.; De Castro, T.; Rubianes, E. New approaches to superovulation and embryo transfer in small ruminants. Reprod. Fertil. Dev. 2009, 22, 113–118. [Google Scholar] [CrossRef]
- Amiridis, G.; Cseh, S. Assisted reproductive technologies in the reproductive management of small ruminants. Anim. Reprod. Sci. 2012, 130, 152–161. [Google Scholar] [CrossRef]
- Toosi, B.M.; Davies, K.L.; Seekallu, S.V.; Ziegler, A.C.; Barrett, D.M.; Duggavathi, R.; Rawlings, N.C. Ovarian Follicular Dominance and the Induction of Daily Follicular Waves in the Ewe. Biol. Reprod. 2010, 83, 122–129. [Google Scholar] [CrossRef] [Green Version]
- Abecia, J.; Forcada, F.; González-Bulnes, A. Hormonal control of reproduction in small ruminants. Anim. Reprod. Sci. 2012, 130, 173–179. [Google Scholar] [CrossRef]
- Wildeus, S. Current concepts in synchronization of estrus: Sheep and goats. J. Anim. Sci 2000, 77, 47–53. [Google Scholar] [CrossRef]
- Mossa, F.; Duffy, P.; Naitana, S.; Lonergan, P.; Evans, A. Association between numbers of ovarian follicles in the first follicle wave and superovulatory response in ewes. Anim. Reprod. Sci. 2007, 100, 391–396. [Google Scholar] [CrossRef]
- Gonzalez-Bulnes, A.; Garcia-Garcia, R.; Santiago-Moreno, J.; Lopez-Sebastian, A.; Cocero, M. Effect of follicular status on superovulatory response in ewes is influenced by presence of corpus luteum at first FSH dose. Theriogenology 2002, 58, 1607–1614. [Google Scholar] [CrossRef]
- Menchaca, A.; Neto, C.; Cuadro, F. Estrous synchronization treatments in sheep: Brief update. Rev. Bras. Reprod. Anim. 2017, 41, 340–344. [Google Scholar]
- E Silva, J.C.; da Costa, L.L.; Cidadao, R.; Silva, J.R. Plasma progesterone profiles, ovulation rate, donor embryo yield and recipient embryo survival in native Saloia sheep in the fall and spring breeding seasons. Theriogenology 2003, 60, 521–532. [Google Scholar] [CrossRef]
- Loiola Filho, J.B.; Pains Oliveira do Monte, A.; dos Santos Souza, T.T.; de Souza Miranda, M.; Correia Magalhães, L.; Souza Costa Barros, C.H.; de Amorim Silva, A.A.; Oliveira Santos, A.; de Souza Leite Guimarães, A.; Maia da Silva Costa, J. Effect of pFSH dose reduction on in vivo embryo production in Dorper ewes. Semin. Ciênc. Agrár. 2015, 36, 4215–4224. [Google Scholar] [CrossRef] [Green Version]
- Sánchez, F.; Bernal, H.; del Bosque, A.S.; González, A.; Olivares, E.; Padilla, G.; Ledezma, R.A. Superovulation and embryo quality with porcine follicle stimulation hormone (pFSH) in Katahdin hair sheep during breeding season. Afr. J. Agric. 2013, 8, 2977–2982. [Google Scholar]
- Samartzi, F.; Boscos, C.; Vainas, E.; Tsakalof, P. Superovulatory response of Chios sheep to PMSG during spring and autumn. Anim. Reprod. Sci. 1995, 39, 215–222. [Google Scholar] [CrossRef]
- Boscos, C.; Vainas, E.; Kouskoura, T.; Samartzi, F.; Vafiadis, D.; Dellis, S. Superovulatory Response of Chios and Friesian Ewes to Two FSH-P Dose Levels. Reprod. Domest. Anim. 1997, 32, 195–198. [Google Scholar] [CrossRef]
- Carwell, B.; Carwell, D.; Hubbard, J.; Stuerman, D. 191 The effect of high and low doses of follicle-stimulating hormone on embryo collection in Romanov sheep. Reprod. Fertil. Dev. 2019, 31, 220. [Google Scholar] [CrossRef]
- Maciel, G.S.; Rodriguez, M.G.K.; Santos, V.J.C.; Uscategui, R.A.R.; Nociti, R.P.; Maronezi, M.C.; Oliveira, C.S.; Feliciano, M.A.R.; Vicente, W.R.R.; da Fonseca, J.F. Follicular dynamics and in vivo embryo production in Santa Ines ewes treated with smaller doses of pFSH. Anim. Reprod. Sci. 2019, 209, 106137. [Google Scholar] [CrossRef]
- Lehloenya, K.; Greyling, J. The ovarian response and embryo recovery rate in Boer goat does following different superovulation protocols, during the breeding season. Small Rumin. Res. 2010, 88, 38–43. [Google Scholar] [CrossRef]
- Vivanco, H. Evaluation of hormonal treatments applied to recipient ewes for the improvement of embryo survival. In Proceedings of the 13th International Congress on Animal Reproduction, Sydney, Australia, 30 June–4 July 1996. [Google Scholar]
- Xiao, Z.C. Production of Goat Offspring from In Vivo-Derived Embryos through Embryo Transfer Technique/Xiao Zhi Chao. Master’s Thesis, University of Malaya, Kuala Lumpur, Malaysia, 2013. [Google Scholar]
- Ammoun, I.; Encinas, T.; Veiga-Lopez, A.; Ros, J.; Contreras, I.; Gonzalez-Anover, P.; Cocero, M.; McNeilly, A.; Gonzalez-Bulnes, A. Effects of breed on kinetics of ovine FSH and ovarian response in superovulated sheep. Theriogenology 2006, 66, 896–905. [Google Scholar] [CrossRef]
- Bartlewski, P.M.; Seaton, P.; Oliveira, M.E.F.; Kridli, R.T.; Murawski, M.; Schwarz, T. Intrinsic determinants and predictors of superovulatory yields in sheep: Circulating concentrations of reproductive hormones, ovarian status, and antral follicular blood flow. Theriogenology 2016, 86, 130–143. [Google Scholar] [CrossRef] [Green Version]
- Chang, Z.; Fan, X.; Luo, M.; Wu, Z.; Tan, J. Factors affecting superovulation and embryo transfer in Boer goats. Asian Australas. J. Anim. Sci. 2006, 19, 341. [Google Scholar] [CrossRef]
- Wolf, B.; Mylne, M. Influence of age of donor ewe on MOET in Texel sheep. Proc. Br. Soc. Anim. Prod. (1972) 1994, 1994, 86. [Google Scholar] [CrossRef]
- Rosa, H.; Bryant, M. Seasonality of reproduction in sheep. Small Rumin. Res. 2003, 48, 155–171. [Google Scholar] [CrossRef]
- Torres, S.; Cognie, Y.; Colas, G. Transfer of superovulated sheep embryos obtained with different FSH-P. Theriogenology 1987, 27, 407–419. [Google Scholar] [CrossRef]
- Fukui, Y.; Tashiro, Y.; Kimura, H.; Miyamoto, A. Effects of progestogen treatment and season on superovulatory responses of ewes and developmental capacity of early embryos recovered. J. Reprod. Dev. 1994, 40, 251–257. [Google Scholar] [CrossRef] [Green Version]
- Greaney, K.; Mcdonald, M.; Vivanco, H.; Tervit, H. Out of season embryo transfer in five breeds of imported sheep. Proc. N. Z. Soc. Anim. Prod. 1991, 51, 121–129. [Google Scholar]
- Mitchell, L.; Dingwall, W.; Mylne, M.; Hunton, J.; Matthews, K.; Gebbie, F.; McCallum, G.; McEvoy, T. Season affects characteristics of the pre-ovulatory LH surge and embryo viability in superovulated ewes. Anim. Reprod. Sci. 2002, 74, 163–174. [Google Scholar] [CrossRef]
- Boland, M.; Lonergan, P.; O’callaghan, D. Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 2001, 55, 1323–1340. [Google Scholar] [CrossRef]
- Borowczyk, E.; Caton, J.; Redmer, D.; Bilski, J.; Weigl, R.; Vonnahme, K.; Borowicz, P.; Kirsch, J.; Kraft, K.; Reynolds, L. Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J. Anim. Sci. 2006, 84, 1593–1599. [Google Scholar] [CrossRef]
- Lozano, J.; Lonergan, P.; Boland, M.; O Callaghan, D. Influence of nutrition on the effectiveness of superovulation programmes in ewes: Effect on oocyte quality and post-fertilization development. Reproduction 2003, 125, 543–553. [Google Scholar] [CrossRef]
- Kraisoon, A.; Redmer, D.; Bass, C.; Navanukraw, C.; Dorsam, S.; Valkov, V.; Reyaz, A.; Grazul-Bilska, A. Corpora lutea in superovulated ewes fed different planes of nutrition. Domest. Anim. Endocrinol. 2018, 62, 16–23. [Google Scholar] [CrossRef]
- Grazul-Bilska, A.; Borowczyk, E.; Arndt, W.; Evoniuk, J.; O’neil, M.; Bilski, J.; Weigl, R.; Kirsch, J.D.; Kraft, K.C.; Vonnahme, K. Effects of overnutrition and undernutrition on in vitro fertilization (IVF) and early embryonic development in sheep. Sheep Beef Day 2006, 47, 56–66. [Google Scholar]
- Peura, T.T.; Kleemann, D.O.; Rudiger, S.R.; Nattrass, G.S.; McLaughlan, C.J.; Walker, S.K. Effect of nutrition of oocyte donor on the outcomes of somatic cell nuclear transfer in the sheep. Biol. Reprod. 2003, 68, 45–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Padilla, G.; Knight, P.; Holtz, W. Superovulation and embryo collection in nulliparous Boer goat does immunized against a recombinant ovine α-subunit inhibin. Small Rumin. Res. 2008, 74, 159–164. [Google Scholar] [CrossRef]
- Bhardwaj, A.; Nayan, V.; Parvati, M.; Gupta, A. Inhibin: A role for fecundity augmentation in farm animals. Asian J. Anim. Vet. Adv. 2012, 7, 771–789. [Google Scholar] [CrossRef]
- Liu, Q.; Han, L.; Rehman, Z.U.; Dan, X.; Liu, X.; Bhattarai, D.; Yang, L. The efficacy of an inhibin DNA vaccine delivered by attenuated Salmonella choleraesuis on follicular development and ovulation responses in crossbred buffaloes. Anim. Reprod. Sci. 2016, 172, 76–82. [Google Scholar] [CrossRef]
- Liu, Q.; Rehman, Z.; Liu, J.; Han, L.; Liu, X.; Yang, L. Nasal immunization with inhibin DNA vaccine delivered by attenuated Salmonella choleraesuis for improving ovarian responses and fertility in cross-bred buffaloes. Reprod. Domest. Anim. 2017, 52, 189–194. [Google Scholar] [CrossRef]
- Anderson, S.; Bindon, B.; Hillard, M.; O’Shea, T. Increased ovulation rate in Merino ewes immunized against small synthetic peptide fragments of the inhibin α subunit. Reprod. Fertil. Dev. 1998, 10, 421–432. [Google Scholar] [CrossRef]
- D’alessandro, A.; Martemucci, G.; Iaffaldano, N. Active immunization with a synthetic fragment of pig inhibin α-subunit increases ovulation rate and embryo production in superovulated ewes but season affects its efficiency. J. Reprod. Fertil. 1999, 115, 185–191. [Google Scholar] [CrossRef] [Green Version]
- Takeo, T.; Nakagata, N. Superovulation using the combined administration of inhibin antiserum and equine chorionic gonadotropin increases the number of ovulated oocytes in C57BL/6 female mice. PLoS ONE 2015, 10, e0128330. [Google Scholar] [CrossRef]
- Wang, L.; Zhuo, Z.-Y.; Shi, W.-Q.; Tan, D.-X.; Gao, C.; Tian, X.-Z.; Zhang, L.; Zhou, G.-B.; Zhu, S.-E.; Yun, P. Melatonin promotes superovulation in sika deer (Cervus nippon). Int. J. Mol. Sci. 2014, 15, 12107–12118. [Google Scholar] [CrossRef] [Green Version]
- Chen, H.Y.; Chen, T.Y.; Lee, M.Y.; Chen, S.T.; Hsu, Y.S.; Kuo, Y.L.; Chang, G.L.; Wu, T.S.; Lee, E.J. Melatonin decreases neurovascular oxidative/nitrosative damage and protects against early increases in the blood–brain barrier permeability after transient focal cerebral ischemia in mice. J. Pineal Res. 2006, 41, 175–182. [Google Scholar] [CrossRef]
- Nakamura, Y.; Tamura, H.; Takayama, H.; Kato, H. Increased endogenous level of melatonin in preovulatory human follicles does not directly influence progesterone production. Fertil. Steril. 2003, 80, 1012–1016. [Google Scholar] [CrossRef]
- Tamura, H.; Nakamura, Y.; Korkmaz, A.; Manchester, L.C.; Tan, D.-X.; Sugino, N.; Reiter, R.J. Melatonin and the ovary: Physiological and pathophysiological implications. Fertil. Steril. 2009, 92, 328–343. [Google Scholar] [CrossRef]
- Zhang, L.; Chai, M.; Tian, X.; Wang, F.; Fu, Y.; He, C.; Deng, S.; Lian, Z.; Feng, J.; Tan, D. Effects of melatonin on superovulation and transgenic embryo transplantation in small-tailed han sheep (Ovis aries). Neuroendocrinol. Lett. 2013, 34, 294–301. [Google Scholar]
- Song, Y.; Wu, H.; Wang, X.; Haire, A.; Zhang, X.; Zhang, J.; Wu, Y.; Lian, Z.; Fu, J.; Liu, G. Melatonin improves the efficiency of super-ovulation and timed artificial insemination in sheep. PeerJ 2019, 7, e6750. [Google Scholar] [CrossRef]
- Wang, T.; Gao, Y.-Y.; Chen, L.; Nie, Z.-W.; Cheng, W.; Liu, X.; Schatten, H.; Zhang, X.; Miao, Y.-L. Melatonin prevents postovulatory oocyte aging and promotes subsequent embryonic development in the pig. Aging 2017, 9, 1552. [Google Scholar] [CrossRef] [Green Version]
- Galano, A.; Tan, D.-X.; Reiter, R. Melatonin: A versatile protector against oxidative DNA damage. Molecules 2018, 23, 530. [Google Scholar] [CrossRef] [Green Version]
- McEvoy, T.; Robinson, J.; Aitken, R.; Robertson, I. Melatonin treatment of embryo donor and recipient ewes during anestrus affects their endocrine status, but not ovulation rate, embryo survival or pregnancy. Theriogenology 1998, 49, 943–955. [Google Scholar] [CrossRef]
- Forcada, F.; Abecia, J.; Cebrian-Perez, J.; Muino-Blanco, T.; Valares, J.; Palacin, I.; Casao, A. The effect of melatonin implants during the seasonal anestrus on embryo production after superovulation in aged high-prolificacy Rasa Aragonesa ewes. Theriogenology 2006, 65, 356–365. [Google Scholar] [CrossRef]
- He, C.; Ma, T.; Shi, J.; Zhang, Z.; Wang, J.; Zhu, K.; Li, Y.; Yang, M.; Song, Y.; Liu, G. Melatonin and its receptor MT1 are involved in the downstream reaction to luteinizing hormone and participate in the regulation of luteinization in different species. J. Pineal Res. 2016, 61, 279–290. [Google Scholar] [CrossRef]
- Mapletoft, R.J.; Bó, G.A. The evolution of improved and simplified superovulation protocols in cattle. Reprod. Fertil. Dev. 2011, 24, 278–283. [Google Scholar] [CrossRef]
- Sanderson, N.; Martinez, M. A single administration of a long-acting recombinant ovine FSH (roFSH) for cattle superovulation. Theriogenology 2020, 154, 66–72. [Google Scholar] [CrossRef]
- Pech-Cervantes, A.A.; Irfan, M.; Estrada-Reyes, Z.M.; Ogunade, I.M. Recombinant Technologies to Improve Ruminant Production Systems: The Past, Present and Future. Processes 2020, 8, 1633. [Google Scholar] [CrossRef]
- Gutiérrez-Reinoso, M.A.; Aguilera, C.J.; Navarrete, F.; Cabezas, J.; Castro, F.O.; Cabezas, I.; Sánchez, O.; García-Herreros, M.; Rodríguez-Alvarez, L. Effects of Extra-Long-Acting Recombinant Bovine FSH (bscrFSH) on Cattle Superovulation. Animals 2022, 12, 153. [Google Scholar] [CrossRef]
- Alexander, B.; Mastromonaco, G.; King, W.A. Recent advances in reproductive biotechnologies in sheep and goat. J. Vet. Sci. Technol. 2010, 1, 101. [Google Scholar] [CrossRef]
- Santolaria, P.; Yániz, J.; Fantova, E.; Vicente-Fiel, S.; Palacín, I. Climate factors affecting fertility after cervical insemination during the first months of the breeding season in Rasa Aragonesa ewes. Int. J. Biometeorol. 2014, 58, 1651–1655. [Google Scholar] [CrossRef]
- Richardson, L.; Hanrahan, J.P.; Donovan, A.; Martí, J.I.; Fair, S.; Evans, A.C.; Lonergan, P. Effect of site of deposition on the fertility of sheep inseminated with frozen-thawed semen. Anim. Reprod. Sci. 2012, 131, 160–164. [Google Scholar] [CrossRef]
- Casali, R.; Pinczak, A.; Cuadro, F.; Guillen-Muñoz, J.; Mezzalira, A.; Menchaca, A. Semen deposition by cervical, transcervical and intrauterine route for fixed-time artificial insemination (FTAI) in the ewe. Theriogenology 2017, 103, 30–35. [Google Scholar] [CrossRef]
- Lima, J.; Fonseca, J.; Balaro, M.; Esteves, L.; Ascoli, F.; Leite, C.; Ribeiro, A.; Delgado, K.; Souza-Fabjan, J.; Torres Filho, R. Effect of natural mating or laparoscopic artificial insemination in superovulated Santa Inês ewes on superovulatory response, fertility and embryo viability. Anim. Prod. Sci. 2016, 56, 1463–1468. [Google Scholar] [CrossRef]
- Bari, F.; Khalid, M.; Haresign, W.; Murray, A.; Merrell, B. Effect of mating system, flushing procedure, progesterone dose and donor ewe age on the yield and quality of embryos within a MOET program in sheep. Theriogenology 2000, 53, 727–742. [Google Scholar] [CrossRef]
- Alvares, C.T.G.; Cruz, J.F.; Romano, C.C.; Brandão, F.Z. Reproductive performance and luteal function of Santa Ines ewes inseminated by cervical retraction with fresh or frozen semen. Rev. Bras. Saúde Prod. Anim. 2020, 21, e2121032020. [Google Scholar] [CrossRef]
- Najafi, G.; Cedden, F.; Kohram, H.; Akbari Sharif, A. The effects of using artificial insemination techniques on reproductive performance in Ghezel sheep. Int. J. Adv. Biol. Biomed. Res. 2014, 2, 2898–2904. [Google Scholar]
- Fair, S.; Hanrahan, J.; O’Meara, C.; Duffy, P.; Rizos, D.; Wade, M.; Donovan, A.; Boland, M.; Lonergan, P.; Evans, A. Differences between Belclare and Suffolk ewes in fertilization rate, embryo quality and accessory sperm number after cervical or laparoscopic artificial insemination. Theriogenology 2005, 63, 1995–2005. [Google Scholar] [CrossRef] [PubMed]
- Masoudi, R.; Shahneh, A.Z.; Towhidi, A.; Kohram, H.; Akbarisharif, A.; Sharafi, M. Fertility response of artificial insemination methods in sheep with fresh and frozen-thawed semen. Cryobiology 2017, 74, 77–80. [Google Scholar] [CrossRef] [Green Version]
- Moore, N.; Eppleston, J. Embryo transfer in the Angora goat. Aust. J. Agric. Res. 1979, 30, 973–981. [Google Scholar] [CrossRef]
- Robinson, J.; Wallace, J.M.; Aitken, R. Fertilization and ovum recovery rates in superovulated ewes following cervical insemination or laparoscopic intrauterine insemination at different times after progestagen withdrawal and in one or both uterine horns. Reproduction 1989, 87, 771–782. [Google Scholar] [CrossRef] [Green Version]
- Cognie, Y. State of the art in sheep-goat embryo transfer. Theriogenology 1999, 51, 105–116. [Google Scholar] [CrossRef]
- Fonseca, J.F.; Souza-Fabjan, J.M.G.; Oliveira, M.E.F.; Leite, C.R.; Nascimento-Penido, P.M.P.; Brandão, F.Z.; Lehloenya, K.C. Nonsurgical embryo recovery and transfer in sheep and goats. Theriogenology 2016, 86, 144–151. [Google Scholar] [CrossRef] [Green Version]
- Loi, P.; Ptak, G.; Dattena, M.; Ledda, S.; Naitana, S.; Cappai, P. Embryo transfer and related technologies in sheep reproduction. Reprod. Nutr. Dev. 1998, 38, 615–628. [Google Scholar] [CrossRef] [Green Version]
- Hunter, G.; Adams, C.; Rowson, L. Inter-breed ovum transfer in sheep. J. Agric. Sci. 1955, 46, 143–149. [Google Scholar] [CrossRef]
- Gibbons, A.; Gueto, M. Embryo Transfer in Sheep and Goats—A Training Manual; National Institute for Agricultural Technology: Buenos Aires, Argentina, 2011. [Google Scholar]
- Miyamoto, A.; Shirasuna, K.; Hayashi, K.-G.; Kamada, D.; Awashima, C.; Kaneko, E.; Acosta, T.J.; Matsui, M. A potential use of color ultrasound as a tool for reproductive management: New observations using color ultrasound scanning that were not possible with imaging only in black and white. J. Reprod. Dev. 2006, 52, 153–160. [Google Scholar] [CrossRef] [Green Version]
- Oliveira, M.E.; Feliciano, M.A.; D’Amato, C.C.; Oliveira, L.G.; Bicudo, S.D.; Fonseca, J.F.; Vicente, W.R.; Visco, E.; Bartlewski, P.M. Correlations between ovarian follicular blood flow and superovulatory responses in ewes. Anim. Reprod. Sci. 2014, 144, 30–37. [Google Scholar] [CrossRef] [Green Version]
- Bartlewski, P.M. Recent advances in superovulation in sheep. Rev. Bras. Reprod. Anim. 2019, 43, 126–128. [Google Scholar]
- Oliveira, M.; Ribeiro, I.; Rodriguez, M.; Maciel, G.; Fonseca, J.; Brandão, F.; Bartlewski, P. Assessing the usefulness of B-mode and colour Doppler sonography, and measurements of circulating progesterone concentrations for determining ovarian responses in superovulated ewes. Reprod. Domest. Anim. 2018, 53, 742–750. [Google Scholar] [CrossRef]
- Pinto, P.; Bragança, G.; Balaro, M.; Arashiro, E.; Dos Santos, G.; de Souza, G.; Souza-Fabjan, J.; Da Fonseca, J.; Brandão, F. Colour-Doppler ultrasound imaging as a laparoscopy substitute to count corpora lutea in superovulated sheep. Reprod. Domest. Anim. 2018, 53, 266–269. [Google Scholar] [CrossRef]
- Coonrod, S.; Coren, B.; McBride, B.; Bowen, M.; Kraemer, D. Successful non-surgical collection of ovine embryos. Theriogenology 1986, 25, 149. [Google Scholar] [CrossRef]
- Barry, D.; Van Niekerk, C.; Rust, J.; Van der Walt, T. Cervical embryo collection in sheep after ripening of the cervix with prostaglandin E2and estradiol. Theriogenology 1990, 33, 190. [Google Scholar] [CrossRef]
- Lopes Gusmão, A.; Campos da Silva, J.; Quintela, A.; Moura, J.C.d.A.; Resende, J.; Dultra Gordiano, H.; Chalhoub Coelho Lima, M.; Ribeiro Filho, A.d.L.; Bittencourt, T.C.B.d.S.C.; Barbosa, L.P. Colheita transcervical de embriões ovinos da raça Santa Inês no semi-árido nordestino. Rev. Bras. Saúde Prod. Anim. 2007, 8, 1–10. [Google Scholar]
- Gusmão, A.; Silva, J.; Bittencourt, T.; Martins, L.; Gordiano, H.; Barbosa, L. Coleta transcervical de embriões em ovinos da raça Dorper no semiárido do Nordeste Brasileiro. Arq. Bras. Med. Vet. Zootec. 2009, 61, 313–318. [Google Scholar] [CrossRef] [Green Version]
- Candappa, I.B.; Bartlewski, P.M. Induction of cervical dilation for transcervical embryo transfer in ewes. Reprod. Biol. Endocrinol. 2014, 12, 8. [Google Scholar] [CrossRef] [Green Version]
- Fonseca, J.; Zambrini, F.; Guimarães, J.; Pereira, V.; Souza-Fabjan, J.; Ribeiro, C.; Brandão, F.; Garcia, A.; Esteves, S.; Machado, R. Successful transcervical uterine flushing in Morada Nova sheep. In Proceedings of the XXI Congresso Brasileiro de Reprodução Animal (CBRA), Belo Horizonte, Brasil, 27–29 May 2015. [Google Scholar]
- Zambrini, F.; Guimaraes, J.; Prates, J.; Esteves, L.; Souza-Fabjan, J.; Brandao, F.; Castro, A.; Fonseca, J. Superovulation and non-surgical embryo recovery in Santa Inês ewes. Anim. Reprod. 2015, 12, 720. [Google Scholar]
- Fonseca, J.F.d.; Zambrini, F.N.; Guimaraes, J.D.; Silva, M.R.; Franco Oliveira, M.E.; Brandao, F.Z.; Bartlewski, P.M.; Goncalves Souza-Fabjan, J.M. Combined treatment with oestradiol benzoate, d-cloprostenol and oxytocin permits cervical dilation and nonsurgical embryo recovery in ewes. Reprod. Domest. Anim. 2019, 54, 118–125. [Google Scholar] [CrossRef] [Green Version]
- Dias, J.H.; Pupin, M.A.; Duarte, G.S.; Brair, V.L.; de Paula, C.J.C.; de Sousa, M.A.P.; Batista, R.I.T.P.; Souza-Fabjan, J.M.G.; Oliveira, M.E.F.; Fonseca, J.F. Successful transcervical uterine flushing can be performed without or reduced dose of oestradiol benzoate in cervical relaxation protocol in Dorper ewes. Reprod. Domest. Anim. 2020, 55, 844–850. [Google Scholar] [CrossRef]
- Oliveira, M.; Zambrini, F.; Souza-Fabjan, J.; Bartlewski, P.; Guimarães, J.; Brandão, F.; Fonseca, J. Repeated trans-cervical embryo recoveries in Santa inês ewes subjected to short-or long-term superovulatory treatment regimens. Anim. Reprod. Sci. 2020, 217, 106469. [Google Scholar] [CrossRef]
- Arrais, A.M.; Mello, M.R.B.d.; Vergani, G.B.; Figueira, L.M.; Esteves, S.N.; Pereira, V.S.d.A.; Bartlewski, P.M.; Oliveira, M.E.F.; Souza-Fabjan, J.M.G.; Fonseca, J.F.d. NonSurgical Embryo Recovery from Estrus-Synchronized or Superovulated Morada Nova Ewes: A Feasible Strategy for Sheep Embryo Banking. Biopreserv. Biobank. 2021, 19, 360–368. [Google Scholar] [CrossRef]
- Xiao, P.; Nie, J.; Wang, X.; Lu, K.; Lu, S.; Liang, X. Melatonin alleviates the deterioration of oocytes from mice subjected to repeated superovulation. J. Cell. Physiol. 2019, 234, 13413–13422. [Google Scholar] [CrossRef]
- ÜSTÜNER, B.; Alcay, S.; Nak, Y.; Nur, Z.; Nak, D.; Tuna, B.; Şimşek, G.; Sağirkaya, H. Repeated superovulation treatments in Kivircik ewes during breeding and nonbreeding seasons. Turk. J. Vet. Anim. Sci. 2014, 38, 480–484. [Google Scholar] [CrossRef]
- Lehloenya, K.; Greyling, J.; Groble, S. Can repeated superovulation and embryo recovery in Boer goats limit donor participation in a MOET programme? South Afr. J. Anim. Sci. 2009, 39, 193–197. [Google Scholar] [CrossRef]
- Bruno-Galarraga, M.M.; Cueto, M.; Gibbons, A.E.; Pereyra-Bonnet, F.; Catalano, R.; Gonzalez-Bulnes, A. Repeatability of superovulatory response to successive FSH treatments in Merino sheep. Small Rumin. Res. 2014, 120, 84–89. [Google Scholar] [CrossRef]
- Forcada, F.; Abecia, J.; Lozano, J.; Zúñiga, O. Repeated superovulation of high-prolificacy Rasa Aragonesa ewes before culling as an inexpensive way to obtain high-quality embryos. Livest. Prod. Sci. 2000, 66, 263–269. [Google Scholar] [CrossRef]
- Pinto, P.H.N.; Balaro, M.F.A.; de Almeida Saraiva, H.F.R.; Brair, V.L.; Alfradique, V.A.P.; Côrtes, L.R.; Cosentino, I.O.; Souza-Fabjan, J.M.G.; da Fonseca, J.F.; Brandão, F.Z. Successive in vivo embryo production in Santa Inês sheep. Anim. Prod. Sci. 2020, 60, 497–502. [Google Scholar] [CrossRef]
Breeding vs. Non-Breeding (B vs. NB) | Reference | |||
---|---|---|---|---|
Ovulation Rate | Embryo Recovery Rate | Fertilization Rate | Transferrable Embryo | |
8.7 ± 5.2 a vs. 8.7 ± 6.9 | 6.9 ± 4.3 vs. 7.1 ± 5.7 | 4 ± 4.2 b vs. 4.4 ± 3.6 | - | [40] |
21.8 ± 2.9 a vs. 9.3 ± 1.6 b | 7.3 ± 2.4 a vs. 3.0 ± 1.5 b | - | - | [98] |
9.3 ± 1.1 vs. 8.3 ± 0.8 | 4.7 ± 0.8 vs. 5.0 ± 0.8 | - | 3.2 ± 0.6 vs. 3.7 ± 0.7 | [82] |
12.5 ± 1.8 vs. 12.9 ± 1.4 | 9.5 ± 1.5 vs. 6.8 ± 1.2 | 96.7 ± 2.9 vs. 94.8 ± 2.4 | - | [12] |
8.75 ± 0.45 a vs. 4.41 ± 0.52 ac | 4.83 ± 0.6 vs. 3.16 ± 0.4 c | - | - | [68] |
5.66 ± 0.39 bd vs. 2.41 ± 0.38 c | 4.66 ± 0.6 a vs. 0.83 ± 0.3 bd | - | - | |
13.9 ± 0.8 a vs. 11.3 ± 1.8 a | 6.0 ± 0.5 a vs. 3.5 ± 1.0 b | - | - | [69] |
- | 7.5 ± 4.9 a vs. 9.4 ± 6.5 a | - | 5.1 ± 4.13 a vs. 7.24 ± 5.6 a | [15] |
10.2 ± 2.94 a vs. 16.8 ± 3.23 b | 6.4 ± 1.70 a vs. 11.5 ± 1.7 b | - | 5.9 ± 1.16 a vs. 6.2 ± 1.57 a | [34] |
8.6 ± 6.5 b vs. 2.9 ± 4.5 a | - | - | 5.12 a vs. 0.29 b | [23] |
Breed | Ovarian Response | 1st Treatment | Second Treatment | Third Treatment | Superovulatory Protocol | References |
---|---|---|---|---|---|---|
Kivircik | Ovulation rate | 8.80 ± 1.3 | 8.75 ± 1.3 | 3.81 ± 0.8 | Eight pFSH injections +PGF 2α; 250 µg cloprostenol | [163] |
Embryo recovery | 68.7 | 58.8 | 19.6 | |||
Transferrable embryo | 4.55 | 3.4 | 0.5 | |||
Merino | Ovulation rate | 13.8 ± 2.2 a | 12.1 ± 2.2 a | 12.0 ± 2.2 a | FSH in decline dose for 3 days twice daily | [165] |
Embryo recovery | 8.3 ± 1.4 c | 6.3 ± 1.4 cd | 3.9 ± 1.4 d | |||
Ojalada | Ovulation rate | 15.9 ± 2.0 a | 13.2 ± 1.6 c | 8.8 ± 1.5 bd | Six injections of 6 mL (210 IU) of pFSH | [35] |
Embryo recovery | 10.7 ± 1.7 a | 9.0 ± 1.5 a | 5.0 ± 0.9 b | |||
Fertilization rate | 86 | 48 | 51 | |||
Transferrable embryo | 7.8 ± 1.7 c | 3.8 ± 1.4 d | 2.5 ± 0.9 b | |||
Ojalada | Ovulation rate | 14.5 ± 2.1 a | 10.6 ± 2.3 | 7.5 ± 1.5 b | Single injection of 6 mL (210 IU) of pFSH | |
Embryo recovery | 11.3 ± 1.8 ac | 6.5 ± 1.6 d | 4.7 ± 1.4 b | |||
Fertilization rate | 76 a | 53 b | 71 a | |||
Transferrable embryo | 7.7 ± 1.6 a | 3.1 ± 1.3 b | 2.9 ± 1.4 b | |||
Poll Dorset | Ovulation rate | 11.50 ± 6.9 | 9.00 ± 5.8 | 6.92 ± 4.0 | Folltropin-V in decreasing dose | [15] |
Transferrable embryo | 7.68 | 6.47 | 6.04 | |||
Rasa Aragonesa | Ovulation rate | 11.0 ± 0.8 c | 11.6 ± 0.9 c | 8.5 ± 1.5 d | FSH in 8 decreasing dose | [166] |
Embryo recovery | 7.3 ± 0.6 cd | 8.0 ± 0.7 c | 5.4 ± 1.2 d | |||
Fertilization rate | 79.5 | 77.5 | 63.5 | |||
Transferrable embryo | 5.0 ± 0.6 | 5.4 ± 0.7 | 3.5 ± 0.8 | |||
Santa Inês | Ovulation rate | 7.5 ± 4.8 a | 3.0 ± 5.0 b | 2.2 ± 3.5 b | 200 mg FSH in multiple dose | [167] |
Embryo recovery | 5.4 ± 4.4 a | 1.8 ± 4.0 b | 1.2 ± 2.3 b | |||
Transferrable embryo | 4.0 ± 3.5 a | 1.2 ± 3.0 b | 1.1 ± 2.1 b | |||
Santa Inês | Ovulation rate | 7.2 ± 6.1 a | 6.3 ± 6.8 a | 7.5 ± 7.3 a | pFSH in six decreasing dose | [23] |
Embryo recovery | 1.4 ± 2.4 a | 2.4 ± 3.4 a | 1.2 ± 2.4 a |
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Khan, S.U.; Jamal, M.A.; Su, Y.; Wei, H.-J.; Qing, Y.; Cheng, W. Towards Improving the Outcomes of Multiple Ovulation and Embryo Transfer in Sheep, with Particular Focus on Donor Superovulation. Vet. Sci. 2022, 9, 117. https://doi.org/10.3390/vetsci9030117
Khan SU, Jamal MA, Su Y, Wei H-J, Qing Y, Cheng W. Towards Improving the Outcomes of Multiple Ovulation and Embryo Transfer in Sheep, with Particular Focus on Donor Superovulation. Veterinary Sciences. 2022; 9(3):117. https://doi.org/10.3390/vetsci9030117
Chicago/Turabian StyleKhan, Sami Ullah, Muhammad Ameen Jamal, Yanhua Su, Hong-Jiang Wei, Yubo Qing, and Wenmin Cheng. 2022. "Towards Improving the Outcomes of Multiple Ovulation and Embryo Transfer in Sheep, with Particular Focus on Donor Superovulation" Veterinary Sciences 9, no. 3: 117. https://doi.org/10.3390/vetsci9030117