Influence of heat stress on in vitro oocyte and embryo production in high-yielding Holstein cows

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DOI:

https://doi.org/10.1590/1809-6891v23e-71852E

Abstract

The objective of this study was to evaluate the influence of thermal shock on oocytes used in the production of in vitro embryos (IVP) of high productivity Holstein cows on the day of follicular aspiration (OPU; 0), 30, 60 and 90 days before the OPU. From the mean temperature on day 0 and on the previous 30, 60 and 90 days, they were classified into comfort group (TC; up to 15°C) and heat stress (HS; above 15°C) groups. A negative influence was observed on oocytes and viable embryos (total and grade I). The heat stress in the periods of 30 and 60 days prior to OPU resulted in lower production of viable oocytes (P=0.0028; P=0.0092, respectively). Under stress, on the day of OPU (HS-OPU), cows showed no reduction in the amount of viable oocytes (P=0.5497) and there was no influence of temperature for the group stressed 90 days before OPU (P=0.8287). For total embryos, the difference occurred only in the HS-30 group (P=0.0317), where the groups HS-OPU, HS-60, HS-90 presented, respectively, P=0. 1987, P=0.0596 and P=0.4580. Regarding the production of embryos of grade 1, there was no difference for the groups HS-OPU (P=0.2291) and HS-90 (P=0.2868), but there was a reduction for HS-30 (P=0.0143) and HS-60 (P=0.0253). In summary, heat stress had a negative impact when it occurred 30 or 60 days before follicular aspiration. In addition, 30 days seems to be the period of more susceptibility and that causes the greatest deleterious effects on oocyte viability and IVP.
Keywords: Hyperthermia; Thermal shock; Ovum Pick Up; Dairy cows.

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Author Biography

Ana Carolina dos Santos Oliveira, Universidade Regional de Blumenau (FURB), Blumenau, Santa Catarina, Brasil

Docente da Universidade Regional de Blumenau

References

Rocha DT, Carvalho GR, Resende JC. Cadeia produtiva do leite no Brasil: produção primária [internet]. Embrapa; 2020 Aug [cited 2021 Sep 28]. Available from: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/215880/1/CT-123.pdf. Portuguese.

Ibge. Produção da Pecuária Municipal 2020 [internet]. Ibge; 2021 [cited 2022 May 21]; 48:1-12. Available https://biblioteca.ibge.gov.br/visualizacao/periodicos/84/ppm_2020_v48_br_informativo.pdf.

Embrapa. Anuário de Leite 2019: Sua excelência, o consumidor [internet]. Embrapa; 2019 May [cited 2021 Sep 28]. Available from: https://www.infoteca.cnptia.embrapa.br/handle/doc/1109959.

Mello RRC, Ferreira JE, Sousa SLG, Mello MRB, Palhano HB. Produção in vitro (PIV) de embriões em bovinos. Rev Bras Reprod Anim [internet]. 2016 [cited 2022 Feb 07]; 40(2):58-64. Available from: http://www.cbra.org.br/pages/publicacoes/rbra/v40/n2/p58-64%20(RB602).pdf.

Golçalves PBD, Figueiredo JR, Freitas VJF. Biotécnicas Aplicadas à Reprodução Animal. 2 ed. São Paulo: Roca; 2016. Portuguese.

Rumpf R. Avanços metodológicos na produção in vitro de embriões. R Bras Zootec. [internet]. 2007 [cited 2022 Feb 07]; 36. Available from: https://doi.org/10.1590/S1516-35982007001000021.

Alvim MJ, Paciullo DSC, Carvalho MM, Aroeira LJM, Carvalho LA, Novaes LP, Gomes AT, Miranda JEC, Ribeiro ACCL. Sistema de produção de leite com recria de novilhas em sistemas silvipastoris [internet]. Embrapa. 2005 Dec [Cited 2021 Sep 28]; (7). Available from: https://sistemasdeproducao.cnptia.embrapa.br/FontesHTML/Leite/LeiteRecriadeNovilhas/racas.htm#:~:text=Na%20pecu%C3%A1ria%20leiteira%2C%20considera%2Dse,%2C%20Guzer%C3%A1%2C%20Indubrasil%2C%20Sindi%20ou.

Lopes FFP, Lima RS, Risolia PHB, Ispada J, Assumpção MEOD, Visintin JA. Heat stress induced alteration in bovine oocytes: functional and cellular aspects. Anim Reprod. [internet]. 2012 [cited 2022 Feb 07]; 9(3):395-403. Available from: https://www.animal-reproduction.org/article/5b5a605af7783717068b46f6.

Pizzatto J, Vieira FMC, Macagnan R, Mayer LRR, Oliveira NS, Pilatti JA. Comparação da termorregulação de vacas holandesas em sistema compost barn. Bbiomet [internet]. 2017. Available from: https://cbbiomet.figshare.com/articles/journal_contribution/Compara_o_da_termorregula_o_de_vacas_holandesas_em_sistema_compost_barn/5193268.

Macedo GG, Silva EVC, Pinho RO, Assumpção TI, Jacomini JO, Santos RM, Martins LF. O estresse por calor diminui a fertilidade de fêmeas bovinas por afetar o desenvolvimento oocitário e o embrionário. Rev Bras Reprod Anim. [internet]. 2014 [cited 2022 Feb 07]; 38(2):80-85. Available from: http://www.cbra.org.br/pages/publicacoes/rbra/v38n2/pag80-85%20(RB486).pdf

Ferreira RM, Ayres H, Chiaratti MR, Ferraz ML, Araújo AB, Rodrigues CA, Watanabe YF, Vireque AA, Joaquim DC, Smith LC, Meirelles FV, Baruselli PS. The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts. J Dairy Sci. [internet]. 2011 [cited 2022 Feb 07]; 94(5):2383-2392. Available from: https://doi.org/10.3168/jds.2010-3904.

Klein BG. Cunningham Tratado de Fisiologia Veterinária. 5ed. Rio de Janeiro: Elsevier; 2014.

Lima MTV, Feitosa JV, Oliveira CW, Costa ANL. Influência da temperatura e umidade sobre o conforto térmico bovino em Barbalha, Ceará. Pubvet [internet]. 2019 [cited 2022 May 03]; 13(12): 477, 1-8. Available from: https://doi.org/10.31533/pubvet.v13n12a477.1-8.

Gendelman M, Aroyo A, Yavin S, Roth Z. Seasonal effects on expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction [internet]. 2010 [cited 2022 Feb 07];140(1):73-82. Available from: https://doi.org/10.1530/REP-10-0055.

Rocha A, Randel RD, Broussard JR, Lim JM, Blair RM, Roussel JD, Godke RA, Hansel W. High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows. Theriogenology [internet]. 1998 [cited 2022 Feb 07]; 49(3):657-65. Available from: https://doi.org/10.1016/S0093-691X(98)00016-8.

Pires MFA, Ferreira AM, Saturnino HM, Teodoro RL. Taxa de gestação em fêmeas da raça Holandesa confinadas em free stall, no verão e no inverno. Arq Bras Med Vet Zootec. [internet]. 2002 [cited 2022 Feb 07]; 54(1). Available from: https://doi.org/10.1590/S0102-09352002000100009.

Britt JH. Impacts of Early Postpartum on Follicular Development and Fertility. In: Proceedings of the Twenty-Fourth Annual Conference American Association of Bovine Practitioners [internet]. 1991 Sep [cited 2022 Feb 07]; 18-21. Available from: https://journals.tdl.org/bovine/index.php/AABP/article/view/6706.

Wolfenson D, Roth Z, Meidan R. Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim Reprod Sci [internet]. 2000 [cited 2022 Feb 07]; 60-61:535-47. Available from: https://doi.org/10.1016/S0378-4320(00)00102-0.

Torres-Júnior JRS, Pires MFA, SÁ WF, Ferreira AM, Viana JHM, Camargo LSA, Ramos AA, Folhadella IM, Polisseni J, Freitas C, Clemente CAA, SÁ Filho MF, Paula-Lopes FF, Baruselli PS. Effect of maternal heat stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology [internet]. 2008 [cited 2022 Feb 07]; 69(2):155-66. Available from: https://doi.org/10.1016/j.theriogenology.2007.06.023.

Roth Z. Effect of Heat Stress on Reproduction in Dairy Cows: Insights into the Cellular and Molecular Responses of the Oocyte. Annu Rev Anim Biosci [internet]. 2017 [cited 2022 Feb 07]; 5:151-170. Available from: https://doi.org/10.1146/annurev-animal-022516-022849.

Ferreira RM, Chiaratti MR, Macabelli CH, Rodrigues CA, Ferraza ML. The infertility of repeat-breeder cows during summer is associated with decreased mitochondrial DNA and increased expression of mitochondrial and apoptotic genes in oocytes. Biol Reprod [internet]. 2016 [cited 2022 May 03]; 94(3):66, 1-10. Available from: https://doi.org/10.1095/biolreprod.115.133017.

Lussier JG, Matton P, Dufour JJ. Growth rates of follicles in the ovary of the cow. J Reprod Fert [internet]. 1987 [cited 2022 Feb 07]; 81(2):301-7. Available from: https://doi.org/10.1530/jrf.0.0810301.

Lew BJ, Meidan R, Wolfenson D. Concentrações hormonais e desenvolvimento folicular de vacas leiteiras em hipertermia sazonal e aguda. Arq Bras Med Vet Zootec [internet]. 2006 [cited 2022 Feb 07]; 58(5):816-822. Available from: https://doi.org/10.1590/S0102-09352006000500017.

Roth Z, Meidan R, Braw-Tal R, Wolfenson D. Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J Reprod Fertil [internet]. 2000 [cited 2022 Feb 07]; 120(1):83-90. Available from: https://pubmed.ncbi.nlm.nih.gov/11006149/#:~:text=The%20enhanced%20growth%20of%20follicles,cycle%3B%20P%20%3C%200.05).

Armengol-Gelonch R, Mallo JM, Ponté D, Jimenez A, Valenza A, Souza AH. Impact of phase of the estrous cycle and season on LH surge profile and fertility in dairy cows treated with different GnRH analogs (gonadorelin vs. buserelin). Theriogenology [internet]. 2017 [cited 2022 Feb 07]; 91:121-126. Available from: https://doi.org/10.1016/j.theriogenology.2017.01.001.

Roman-Ponce H, Thatcher WW, Wilcox CJ. Hormonal interelationships and physiological responses of lactating dairy cows to a shade management system in a subtropical environment. Theriogenology [internet]. 1981 [cited 2022 May 03]; 16(2): 139-154. Available from: https://doi.org/10.1016/0093-691X(81)90097-2.

Gilad E, Meidan R, Berman A, Graber Y, Wolfenson D. Effect of heat stress on tonic and GnRH-induced gonadotrophin secretion in relation to concentration of estradiol in plasma of cyclic cows. Journal of Reproduction and Fertility [internet]. 1993. [cited 2022 May 03]; 99(2):315-321. Available from: https://doi.org/10.1530/jrf.0.0990315.

Wise ME, Armstrong DV, Huber JT, Hunter, R, Wiersma F. Hormonal Alterations in the Lactating Dairy Cow in Response to Thermal Stress. J Dairy Sci [internet]. 1988. [cited 2022 May 03]; 71(9): 2480-2485. Available from: https://pubmed.ncbi.nlm.nih.gov/16725628/.

Hansen PJ. Antecedents of mammalian fertility: Lessons from the heat-stressed cow regarding the importance of oocyte competence for fertilization and embryonic development. Animal Frontiers [internet]. 2013 [cited 2022 Feb 07]; 3(4): 34–39. Available from: https://doi.org/10.2527/af.2013-0031.

Roth Z, Meidan R, Shaham-Albalancy U, Braw-Tal, R, Wolfenson D. Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles. Reproduction [internet]. 2001 [cited 2022 Feb 07]; 121(5):745-51. Available from: https://pubmed.ncbi.nlm.nih.gov/11427162/.

Hansen PJ. Reproductive physiology of the heat-stressed dairy cow: implications for fertility and assisted reproduction. Anim Reprod [internet]. 2019 [cited 2022 Feb 07]; 16(3):497-507. Available from: http://dx.doi.org/10.21451/1984-3143-AR2019-0053.

Al-katanani YM, Paula-Lopes FF, Hansen PJ. Effect of season and exposure to heat stress on oocyte competence in Holstein cows. J Dairy Sci [internet]. 2002 [cited 2022 Feb 07]; 85(2):390-6. Available from: https://doi.org/10.3168/jds.S0022-0302(02)74086-1.

Fialho ALL, Souza-cáceres MB, Silva WAL, Arruda EDS, Kischel H, Ribeiro-Ferreira MGC, Medeiros CF, Silva JR, Oliveira MVM, Ferraz ALJ, Melo-Sterz, F. A. Efeito do estresse térmico calórico agudo e crônico sobre a qualidade oocitária de bovinos de raças adaptadas. Arq Bras Med Vet Zootec [internet]. 2018 [cited 2022 Feb 07]; 70(1):64-72. Available from: https://doi.org/10.1590/1678-4162-9494.

Putney DJ, Mullins S, Thatcher WW, Drost M, Gross TS. Embryonic Development in Superovulated Dairy Cattle Exposed to Elevated Ambient Temperatures Between the Onset of Estrus and Insemination. Anim Reprod Sci [internet]. 1989 [cited 2022 Feb 07]; 19(1–2):37-51. Available from: https://doi.org/10.1016/0378-4320(89)90045-6.

Luciano AM, Franciosi F, Modina SC, Lodde V. Gap Junction-Mediated Communications Regulate Chromatin Remodeling During Bovine Oocyte Growth and Differentiation Through cAMP-Dependent Mechanism(s). Biology of Reproduction [internet]. 2011 [cited 2022 May 03]; 85(6): 1252-1259. Available from: https://doi.org/10.1095/biolreprod.111.092858.

Lodde V, Modina S, Galbusera C, Franciosi F, Luciano AM. Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol Reprod Dev [internet]. 2007 [cited 2022 May 03]; 74(6):740-9. Available from: https://pubmed.ncbi.nlm.nih.gov/17075796/.

Campen KA, Abbott CR, Rispoli LA, Payton RR, Saxton AM, Edwards JL. Heat stress impairs gap junction communication and cumulus function of bovine oocytes. J Reprod Dev [internet]. 2018 [cited 2022 May 03]; 64(5):385-392. Available from: https://pubmed.ncbi.nlm.nih.gov/29937465/.

Putney DJ, Drost M, Thatcher WW. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between Days 1 to 7 post insemination. Theriogenology [internet]. 1988 [cited 2022 Feb 07]; 30(2):195-209. Available from: https://doi.org/10.1016/0093-691X(88)90169-0.

Putney DJ, Drost M, Thatcher WW. Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology [internet]. 1989 [cited 2022 Feb 07]; 31(4):765-78. Available from: https://doi.org/10.1016/0093-691X(89)90022-8.

Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A. Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction [internet]. 2001 [cited 2022 Feb 07]; 121(3):447-54. Available from: https://pubmed.ncbi.nlm.nih.gov/11226071/.

Vanholder T, Leroy JLMR, Van Soom A, Opsomer G, Maes D, Coryn M, Kruif A. Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim Reprod Sci [internet]. 2005 [cited 2022 Feb 07]; 87(1-2):33-44. Available from: https://doi.org/10.1016/j.anireprosci.2004.09.006.

Ispada J, Rodrigues TA, Risolia PHB, Lima RS, Gonçalves DR, Rettori D, Nichi M, Feitosa WB, Paula-Lopes FF. Astaxanthin counteracts the effects of heat shock on the maturation of bovine oocyte. Reprod Fertil Dev [internet]. 2018 [cited 2022 Feb 07]; 30(9):1169-1179. Available from: https://doi.org/10.1071/RD17271.

Rodrigues TA, Tuna KM, Alli AA, Tribulo P, Hansen PJ, Koh J, Paula-Lopes FF. Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock. Reprod Fertil Dev [internet]. 2019 [cited 2022 Feb 07]; 31(5):888-897. Available from: https://doi.org/10.1071/RD18450.

Rivera RM, Hansen PJ. Development of cultured bovine embryos after exposure to high temperatures in the physiological range. Reproduction [internet]. 2001 [cited 2022 Feb 07]; 121(1):107-15. Available from: https://pubmed.ncbi.nlm.nih.gov/11226033/.

Roth Z, Hansen PJ. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod [internet]. 2004 [cited 2022 Feb 07]; 71(6):1898-906. Available from: https://doi.org/10.1095/biolreprod.104.031690.

Hyttel P, Callesen H, Greve T. Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J Reprod Fert [internet]. 1986 [cited 2022 Feb 07]; 76(2):645-56. Available from: https://doi.org/10.1530/jrf.0.0760645.

Edwards JL, Hansen P J. Differential responses of bovine oocytes and preimplantation embryos to heat shock.Mol Reprod Dev [internet]. 1997 [cited 2022 Feb 07]; 46(2):138-45. Available from: https://doi.org/10.1002/(SICI)1098-2795(199702)46:2<138::AID-MRD4>3.0.CO;2-R.

Baumgartner AP, Chrisman CL. Cytogenetic analysis of ovulated mouse oocytes following hyperthermic stress during meiotic maturation. Exp Cell Res [internet]. 1981 [cited 2022 Feb 07]; 32(2):359-366. Available from: https://doi.org/10.1016/0014-4827(81)90111-7.

Roth Z, Hansen PJ. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction [internet]. 2005 [cited 2022 Feb 07]; 129(2):235-44. Available from: https://doi.org/10.1530/rep.1.00394.

Roth Z, Arav A, Bor A, Zeron Y, Braw-Tal R, Wolfenson D. Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction [internet]. 2001 [cited 2022 Feb 07]; 122(5):737-44. Available from: https://pubmed.ncbi.nlm.nih.gov/11690534/#:~:text=The%20results%20show%20a%20delayed,quality%20oocytes%20in%20the%20autumn.

Cavallari, F. C.; Leal, C. L. V.; Zvi, R.; Hansen, P. J. Effects of melatonin on production of reactive oxygen species and developmental competence of bovine oocytes exposed to heat shock and oxidative stress during in vitro maturation. Zygote [internet]. 2019 [cited 2022 May 03]; 27(4):262. Available from: https://pubmed.ncbi.nlm.nih.gov/31171044/.

Published

2022-07-05

How to Cite

BERLING, F.; CASTRO, F. C. de; OLIVEIRA, A. C. dos S. Influence of heat stress on in vitro oocyte and embryo production in high-yielding Holstein cows. Brazilian Animal Science/ Ciência Animal Brasileira, Goiânia, v. 23, 2022. DOI: 10.1590/1809-6891v23e-71852E. Disponível em: https://revistas.ufg.br/vet/article/view/71852. Acesso em: 22 dec. 2024.

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MEDICINA VETERINÁRIA