Injectable progesterone in 13-month-old prepubertal Nellore heifers: effects on in vitro embryo production and pregnancy rate.

Publisher: Springer Country of Publication: United States NLM ID: 1277355 Publication Model: Electronic Cited Medium: Internet ISSN: 1573-7438 (Electronic) Linking ISSN: 00494747 NLM ISO Abbreviation: Trop Anim Health Prod Subsets: MEDLINE

Publication: 2005- : Heidelberg : Springer
Original Publication: Edinburgh, Livingstone.

Progesterone*/administration & dosage ; Pregnancy Rate*; Animals ; Cattle/physiology ; Female ; Pregnancy ; Fertilization in Vitro/veterinary ; Embryo Transfer/veterinary ; Injections, Intramuscular/veterinary ; Random Allocation ; Oocytes/drug effects

The aim of this study was to evaluate the effect of injectable progesterone administration before ovum pick-up (OPU) on in vitro embryo production (IVEP) and pregnancy rate in prepubertal Nellore heifers. Twenty-three Nellore females, 13.04 ± 0.8 months of age, were randomly assigned to two groups: control group (no progesterone application) and progesterone group (intramuscular administration of 1 mL [150 mg/mL] progesterone 7 days before OPU). The second OPU was performed after 28 days (crossover between groups). After OPU, oocytes were selected for IVEP and a sample was fixed in 4% paraformaldehyde. Viable oocytes were subjected to immunofluorescence staining for IGFBP2 and caspase-3. For each oocyte, one image was generated per channel (A555 and A488 filters) and analyzed with the ImageJ program for the quantification of fluorescence intensity (in pixels). The produced embryos were transferred to multiparous Nellore cows and pregnancy was diagnosed by ultrasound 30 days after transfer. Data were analyzed using the MIXED and GLIMMIX procedure of SAS ^® . Treatment with injectable progesterone had no effect on the number or size of the antral follicles of heifers. No differences between the control and progesterone groups were observed for total number of aspirated oocytes (P = 0.78), viable oocytes (P = 0.80), cleavage rate (P = 0.60), or blastocyst rate (P = 0.56). There were no differences in pixel intensity between the two groups, nor in the levels of IGFBP2 or caspase-3. However, a difference was observed in the pregnancy rate of embryos produced from heifers of the progesterone group (42.1%; 32/76) when compared to the rate of embryos produced from control heifers (28.4%; 23/81) (P = 0.02). The use of injectable progesterone before OPU in prepubertal Nellore heifers does not improve IVEP but increases the pregnancy rate after transfer.
(© 2024. The Author(s), under exclusive licence to Springer Nature B.V.)

Abeni F, Petrera F, Le Cozler Y (2019) Effects of feeding treatment on growth rates, metabolic profiles and age at puberty, and their relationships in dairy heifers. Animal 13(5):1020–1029. (PMID: 3030147910.1017/S1751731118002422)
Akison L, Robker R (2012) The critical roles of progesterone receptor (PGR) in ovulation, oocyte developmental competence and oviductal transport in mammalian reproduction. Reprod Domest Anim 47:288–296. (PMID: 2282738310.1111/j.1439-0531.2012.02088.x)
Alexopoulos NI, Maddox-Hyttel P, Tveden-Nyborg P, D’Cruz NT, Tecirlioglu TR, Cooney MA, Schauser K, Holland MK, French AJ (2008) Developmental disparity between in vitro-produced and somatic cell nuclear transfer bovine days 14 and 21 embryos: implications for embryonic loss. Reprod Domest Anim 136:433–445.
Aparicio IM, Garcia-Herreros M, O’Shea LC, Hensey C, Lonergan P, Fair T (2011) Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol Reprod 84:910–921. (PMID: 2122821610.1095/biolreprod.110.087411)
Argudo DE, Tenemaza MA, Merchán SL, Balvoa JA, Méndez MS, Soria ME, Perea FP (2020) Intraovarian influence of bovine corpus luteum on oocyte morphometry and developmental competence, embryo production and cryotolerance. Theriogenology 155:232–239. (PMID: 3275899410.1016/j.theriogenology.2020.05.044)
Batista EO, Guerreiro BM, Freitas BG, Silva JC, Vieira LM, Ferreira RM, Rezende RG, Basso AC, Lopes RN, Rennó FP, Souza AH, Baruselli PS (2016) Plasma anti-Müllerian hormone as a predictive endocrine marker to select Bos taurus (Holstein) and Bos indicus (Nelore) calves for in vitro embryo production. Domest Anim Endocrinol 54:1–9. (PMID: 2637909910.1016/j.domaniend.2015.08.001)
Borman SM, Chaffin CL, Schwinof KM, Stouffer RL, Zelinski-Wooten MB (2004) Progesterone promotes oocyte maturation, but not ovulation, in nonhuman primate follicles without a gonadotropin surge. Biol Reprod 71:366–373. (PMID: 1498524210.1095/biolreprod.103.023390)
Cerri RLA, Chebel RC, Rivera F, Narciso CD, Oliveira RA, Amstalden M, Santos JEP (2011) Concentration of progesterone during the development of the ovulatory follicle: II. Ovarian and uterine responses. J Dairy Sci 94:3352–3365. (PMID: 2170002110.3168/jds.2010-3735)
Costa CCM, Maia ASC, Brandl TMB, Chiquitelli Neto M, de França VCF (2018) Thermal equilibrium of Nellore cattle in tropical conditions: an investigation of circadian pattern. J Therm Biol 74:317–324. (PMID: 10.1016/j.jtherbio.2018.04.014)
Crosier AE, Farin PW, Dykstra MJ, Alexander JE, Farin CE (2000) Ultrastructural morphometry of bovine compact morulae produced in vivo or in vitro. Biol Reprod 62:1459–1465. (PMID: 1077520110.1095/biolreprod62.5.1459)
Currin L, Baldassarre H, Bordignon V (2021) Vitro vitro production of embryos from prepubertal holstein cattle and mediterranean water buffalo: problems, progress and potential. Anim (Basel) 11:2275.
Day ML, Anderson LH (1998) Current concepts on the control of puberty in cattle. J Anim Sci 76(3):1–15. (PMID: 10.2527/1998.76suppl_31x)
Domiciano LF, Mombach MA, Carvalho P, da Silva NMF, Pereira DH, Cabral LS, Lopes LB, Pedreira BC (2018) Desempenho E comportamento de novilhos nelore em sistemas integrados. Anim Prod Sci 58:920–929. (PMID: 10.1071/AN16351)
Erdem H, Karasahin T, Alkan H (2020) Effect of embryo quality and developmental stages on pregnancy rate during fresh embryo transfer in beef heifers. Trop Anim Health Prod 52:2541–2547. (PMID: 3244515510.1007/s11250-020-02287-6)
Fair T, Lonergan P (2012) The role of progesterone in oocyte acquisition of developmental competence. Reprod Domest Anim 47:142–147. (PMID: 2282736310.1111/j.1439-0531.2012.02068.x)
Fair T, Hyttel P, Greve T (1995) Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 42:437–442. (PMID: 860797310.1002/mrd.1080420410)
FAO (2020) Food and Agriculture commodities production. Food and Agriculture Organization of the United Nations.
Ferguson CE, Kesler DJ, Godke RA (2012) Progesterone enhances in vitro development of bovine embryos. Theriogenology 77:108–114. (PMID: 2187231310.1016/j.theriogenology.2011.07.022)
Fortes MRS, Li Y, Collis E, Zhang Y, Hawken RJ (2012) The IGF1 pathway genes and their association with age of puberty in cattle. Anim Genet 44:91–95. (PMID: 2255419810.1111/j.1365-2052.2012.02367.x)
Gordon I (1994) Laboratory production of cattle embryos. Wallingford, UK: CABI International, 640.
IETS (2018) Statistics of embryo production and transfer in domestic farm animals. Embryo Technol Newsl 36(4):1–26.
Ikeda S, Imai H, Yamada M (2003) Apoptosis in cumulus cells during in vitro maturation of bovine cumulus-enclosed oocytes. Reproduction 125:369–376. (PMID: 1261160010.1530/rep.0.1250369)
Jerez ERM, García AA, Caccia M, Rodríguez AC, Gonzales SJR, Waltero EMM, Marín DFD (2022) Effect of the presence and location of corpus luteum on competence of bovine cumulus-oocyte complexes. Anim Reprod 19(2):e20210074.
Jiang J, Ma L, Prakapenka D, VanRaden PM, Cole JB, Da Y (2019) A large-scale genome-wide Association study in U.S. Holstein cattle. Front Genet 10:412. (PMID: 31139206652778110.3389/fgene.2019.00412)
Jo M, Komar CM, Fortune JE (2002) Gonadotropin surge induces two separate increases in messenger RNA for progesterone receptor in bovine preovulatory follicles. Biol Reprod 67:1981–1988. (PMID: 1244407710.1095/biolreprod.102.004366)
Kaniyamattam K, Block J, Hansen PJ, De Vries A (2017) Comparison between an exclusive in vitro-produced embryo transfer system and artificial insemination for genetic, technical, and financial herd performance. J Dairy Sci 100:5729–5745. (PMID: 10.3168/jds.2016-11979)
Kauffold J, Amer HAH, Bergfeld U, Weber W, Sobiraj A (2005) The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter. J Reprod Dev 51(3):325–332. (PMID: 1600086610.1262/jrd.17002)
Kawamoto TS, Viana JHM, Pontelo TP, Franco MM, De Faria OAC, Fidelis AAG, Vargas LN, Figueiredo RA (2022) Dynamics of the reproductive changes and acquisition of oocyte competence in Nelore (bos taurus indicus) calves during the early and intermediate prepubertal periods. Animals 12:2137. (PMID: 36009727940510710.3390/ani12162137)
Kubisch HM, Larson MA, Roberts RM (1998) Relationship between age of blastocyst formation and interferon-τ secretion by in vitro-derived bovine embryos. Mol Reprod Dev 49:254–260. (PMID: 949137710.1002/(SICI)1098-2795(199803)49:3<254::AID-MRD5>3.0.CO;2-N)
Landry DA, Bellefleur A, Labrecque R, Grand F, Vigneault C, Blondin P, Sirard M (2016) Effect of cow age on the in vitro developmental competence of oocytes obtained after FSH stimulation and coasting treatments. Theriogenology 86:1240–1246. (PMID: 2721566910.1016/j.theriogenology.2016.04.064)
Larson JE, Krisher RL, Lamb GC (2011) Effects of supplemental progesterone on the development, metabolism and blastocyst cell number of bovine embryos produced in vitro. Reprod Fertility Dev 23:311–318. (PMID: 10.1071/RD10106)
Liszewska E, Rekawiecki R, Kotwica J (2005) Effect of progesterone on the expression of BAX and BCL-2 and on caspase activity in bovine luteal cells. Prostaglandins Other Lipid Mediat 78:67–81. (PMID: 1630360610.1016/j.prostaglandins.2005.03.003)
Lonergan P (2011) Influence of progesterone on oocyte quality and embryo development in cows. Theriogenology 76:1594–1601. (PMID: 2185598510.1016/j.theriogenology.2011.06.012)
Lonergan P (2015) New insights into the function of progesterone in early pregnancy. Anim Front 5:12–17. (PMID: 10.2527/af.2015-0003)
Menchaca A, Cuadro F, Santos-Neto D, Bosolasco PC, Barrera D, De Brun N, Crispo V, M (2018) Oocyte developmental competence is improved by relatively greater circulating progesterone concentrations during preovulatory follicular growth. Anim Reprod Sci 195:321–328. (PMID: 3126240510.1016/j.anireprosci.2018.06.010)
Michalovic L, Currin L, Gutierrez K, Bellefleur AM, Glanzner WG, Schuermann Y, de Macedo MP, Bohrer RC, Dicks N, Lopez R, Taibi M, Madogwe E, St-Yves A, Mondadori RG, Gourdon J, Vigneault C, Baldassarre H, Bordignon V (2018) Granulosa cells of prepubertal cattle respond to gonadotropin signaling and upregulate genes that promote follicular growth and prevent cell apoptosis. Mol Reprod Dev 85:909–920. (PMID: 3029896610.1002/mrd.23066)
Monteiro FM, Mercadante MEZ, Barros CM, Satrapa RA, Silva JAV, Oliveira LZ, Saraiva NZ, Oliveira CS, Garcia JM (2013) Reproductive tract development and puberty in two lines of Nellore heifers selected for postweaning weight. Theriogenology 80(1):10–17. (PMID: 2362316310.1016/j.theriogenology.2013.02.013)
Nicholas B, Alberio R, Fouladi-Nashta AA, Webb R (2005) Relationship between low-molecular-weight insulin-like Growth factor-binding proteins, Caspase-3 activity, and Oocyte Quality. Biol Reprod 72:796–804. (PMID: 1556459610.1095/biolreprod.104.036087)
Nivet AL, Bunel A, Labrecque R, Belanger J, Vigneault C, Blondin P, Sirard MA (2012) FSH withdrawal improves developmental competence of oocytes in the bovine model. Reproduction 143(2):165–171. (PMID: 2208014110.1530/REP-11-0391)
Pereira RM, Marques CC, Baptista MC, Vasques MI, Horta AEM (2009) Embryos and culture cells: a model for studying the effect of progesterone. Anim Reprod Sci 111:31–40. (PMID: 1837452510.1016/j.anireprosci.2008.02.004)
Pieterse MC, Kappen KA, Kruip TAM, Taverne MAM (1988) Aspiration of bovine oocytes during transvaginal ultrasound scanning of the ovaries. Theriogenology 30:751–762. (PMID: 1672651710.1016/0093-691X(88)90310-X)
Pontes JH, Sterza M, Basso FA, Ferreira AC, Sanches CR, Rubin BV, Seneda KC, M.M (2011) Ovum pick up, in vitro embryo production, and pregnancy rates from a large-scale commercial program using Nelore cattle (Bos indicus) donors. Theriogenology 75(9):1640–1646. (PMID: 2133405510.1016/j.theriogenology.2010.12.026)
Presicce GA, Jiang S, Simkin M, Zhang L, Looney CR, Godke RA, Yang X (1997) Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves. Biol Reprod 56(2):386–392. (PMID: 911613710.1095/biolreprod56.2.386)
Rawlings NC, Evans ACO, Honaramooz A, Bartlewski PM (2003) Antral follicle growth and endocrine changes in prepubertal cattle sheep and goats. Anim Reprod Sci 78:259–270. (PMID: 1281864810.1016/S0378-4320(03)00094-0)
Revel F, Mermillod P, Peynot N, Renard JP, Heyman Y (1995) Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows. J Reprod Infertil 103:115–120. (PMID: 10.1530/jrf.0.1030115)
Saad M, Sarwar Z, Saleem M, Arshad U, Shahzad M, Hassan Mushtaq M, Ahmad N (2019) Effect of plasma progesterone on oocyte recovery, oocyte quality, and early in-vitro developmental competence of embryos in Bos indicus dairy cows. Anim Reprod Sci 202:80–86. (PMID: 3076511110.1016/j.anireprosci.2019.02.001)
Salehi E, Aflatoonian R, Moeini A, Yamini N, Asadi E, Khosravizadeh Z, Abolhassani F (2017) Apoptotic biomarkers in cumulus cells in relation to embryo quality in polycystic ovary syndrome. Arch Gynecol Obstet 296:1219–1227. (PMID: 2898832110.1007/s00404-017-4523-5)
Silva LG (2020) Produção in vitro de embriões de novilhas Nelore (Bos indicus) de 12 e 24 meses de idade tratadas ou não com FSH [dissertation]. São Paulo: Universidade de São Paulo.
Silva MO, Borges MS, Fernandes LG, Rodrigues NN, Watanabe YF, Joaquim DC, Oliveira CS, Feuchard VLS, Cyrillo JNSG, Mercadante MEZ, Monteiro FM (2022) Effect of Nellore (Bos indicus) donor age on in-vitro embryo production and pregnancy rate. Reprod Domest Anim 57(9):980–988. (PMID: 3561298110.1111/rda.14164)
Snel-Oliveira MV, Pereira DC, Malagoli Junior D, Rumpf R (2003) Hormonal stimulation and ultrasound guided transvaginal follicle aspiration and oocyte recovery in Nelore (Bos taurus indicus) prepubertal calves. Revista Brasileira De Zootecnia 32(1):106–114. (PMID: 10.1590/S1516-35982003000100014)
Viana JHM, Silva BDM, Moura RM, Féres LFR, Figueiredo RA (2024) Oocyte developmental potential and embryo production before puberty in cattle. Anim Reprod 21(3):e20240069.
Warzych E, Pawlak P, Pszczola M, Cieslak A, Lechniak D (2017) Prepubertal heifers versus cows—the differences in the follicular environment. Theriogenology 87:36–47. (PMID: 2763439610.1016/j.theriogenology.2016.08.007)
Watanabe YF, Watanabe MR, Vila RA, Galerani MAV, Lôbo RB (1999) The influence of B2 and a modified CR-2 medium on the in vitro production of bovine embryos with cumulus and oviduct co-culture. Theriogenology 51:259. (PMID: 10.1016/S0093-691X(99)91818-6)
Watanabe OY, Schmitt E, Meirellles FV, Oliveira A, bos-Mikich A, Watanabe YF (2014) Vitrification system (open and closed) in new incubator with reduced oxygen. Reprod Fertility Dev 27:158. (PMID: 10.1071/RDv27n1Ab132)
Yaka M, Çil N, Kabukçu C, Şenol H, Mete GA (2022) Relationship between embryo development and apoptotic gene expression of cumulus cells in poor responders and polycystic ovary syndrome. Reprod Biomed Online 45:935–942. (PMID: 3609687010.1016/j.rbmo.2022.06.018)
Yuan YQ, Van Soom A, Leroy JLMR, Dewulf J, Van Zeveren A, De Kruif A, Peelman LJ (2005) Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 63:2147–2163. (PMID: 1582668010.1016/j.theriogenology.2004.09.054)
Zacarias TA, Kawamoto TS, Scaliante Júnior JR, Silva Guimarães AL, Franco MM, Figueiredo RA (2018) Hormonal stimulation in 4 to 7 months old Nelore (Bos taurus indicus) females improved ovarian follicular responses but not the in vitro embryo production. Theriogenology 6:118–130.

2017/50339-5 Fundação de Amparo à Pesquisa do Estado de São Paulo; 001 Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Keywords: Animal reproduction; Follicular aspiration; IVEP

4G7DS2Q64Y (Progesterone)

Date Created: 20241024 Date Completed: 20241024 Latest Revision: 20241210

20241210

10.1007/s11250-024-04205-6

39448424