Animal Reproduction (AR)
https://www.animal-reproduction.org/article/doi/10.21451/1984-3143-AR2019-0053
Animal Reproduction (AR)
Congress Paper

Reproductive physiology of the heat-stressed dairy cow: implications for fertility and assisted reproduction

Peter J. Hansen

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Abstract

Heat stress causes a large decline in pregnancy success per insemination during warm times of the year. Improvements in fertility are possible by exploiting knowledge about how heat stress affects the reproductive process. The oocyte can be damaged by heat stress at the earliest stages of folliculogenesis and remains sensitive to heat stress in the peri-ovulatory period. Changes in oocyte quality due to heat stress are the result of altered patterns of folliculogenesis and, possibly, direct effects of elevated body temperature on the oocyte. While adverse effects of elevated temperature on the oocyte have been observed in vitro, local cooling of the ovary and protective effects of follicular fluid may limit these actions in vivo. Heat stress can also compromise fertilization rate. The first seven days of embryonic development are very susceptible to disruption by heat stress. During these seven days, the embryo undergoes a rapid change in sensitivity to heat stress from being very sensitive (2- to 4-cell stage) to largely resistant (by the morulae stage). Direct actions of elevated temperature on the embryo are likely to be an important mechanism for reduction in embryonic survival caused by heat stress. An effective way to avoid effects of heat stress on the oocyte, fertilization, and early embryo is to bypass the effects through embryo transfer because embryos are typically transferred into females after acquisition of thermal resistance. There may be some opportunity to mitigate effects of heat stress by feeding antioxidants or regulating the endocrine environment of the cow but neither approach has been reduced to practice. The best long-term solution to the problem of heat stress may be to increase genetic resistance of cows to heat stress. Thermotolerance genes exist within dairy breeds and additional genes can be introgressed from other breeds by traditional means or gene editing

Keywords

heat stress, lactating cow, reproduction, fertility, embryo, oocyte.

References

Armengol-Gelonch R, Mallo JM, Ponté D, Jimenez A, Valenza A, Souza AH. 2017. 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, 91:121-126.

Aréchiga CF, Staples CR, McDowell LR, Hansen PJ. 1998. Effects of timed insemination and supplemental -carotene on reproduction and milk yield of dairy cows under heat stress. J Dairy Sci, 81:390-402.

Baruselli PS, Ferreira RM, Sales JN, Gimenes LU, Sá Filho MF, Martins CM, Rodrigues CA, Bó GA. 2011. Timed embryo transfer programs for management of donor and recipient cattle. Theriogenology, 76:1583-1593.

Badinga L, Collier RJ, Thatcher WW, Wilcox CJ. 1985 Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment. J Dairy Sci, 68:78-85.

Basiricò L, Morera P, Primi V, Lacetera N, Nardone A, Bernabucci U. 2011. Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows. Cell Stress Chaperones, 16:441-448.

Biggers BG, Geisert RD, Wetteman RP, Buchanan DS. 1987. Effect of heat stress on early embryonic development in the beef cow. J Anim Sci, 64:1512-1518.

Block J, Hansen PJ. 2007. Interaction between season and culture with insulin-like growth factor-1 on survival of in vitro produced embryos following transfer to lactating dairy cows. Theriogenology, 67:1518-1529.

Carvalho PD, Santos VG, Giordano JO, Wiltbank MC, Fricke PM. 2018. Development of fertility programs to achieve high 21-day pregnancy rates in high-producing dairy cows. Theriogenology, 114:165-172.

Cavallari de Castro F, Leal, CLV, Roth, Z, Hansen PJ. 2019. 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, 27:180-186.

Chebel RC, Demétrio DG, Metzger J. 2008. Factors affecting success of embryo collection and transfer in large dairy herds. Theriogenology, 69:98-106.

Dahl GE, Tao S, Laporta J. 2017. Late gestation heat stress of dairy cattle programs dam and daughter milk production. J Anim Sci, 95:5701-5710.

de Castro e Paula LA, Hansen PJ. 2008. Modification of actions of heat shock on development and apoptosis of cultured preimplantation bovine embryos by oxygen concentration and dithiothreitol. Mol Reprod Dev, 75:1338-1350.

Dikmen S, Cole JB, Null DJ, Hansen PJ. 2012. Heritability of rectal temperature and genetic correlations with production and reproduction traits in dairy cattle. J Dairy Sci, 95:3401-3405.

Dikmen S, Khan FA, Huson HJ, Sonstegard TS, Moss JI, Dahl GE, Hansen PJ. 2014. The SLICK hair locus derived from Senepol cattle confers thermotolerance to intensively managed lactating Holstein cows. J Dairy Sci, 97:5508-5520.

Drost M, Ambrose JD, Thatcher MJ, Cantrell CK, Wolfsdorf KE, Hasler JF, Thatcher WW. 1999. Conception rates after artificial insemination or embryo transfer in lactating dairy cows during summer in Florida. Theriogenology, 52:1161-1167.

Ealy AD, Drost M, Hansen PJ. 1993. Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J Dairy Sci, 76:2899-2905.

Ealy AD, Aréchiga CF, Bray DR, Risco CA, Hansen PJ. 1994. Effectiveness of short-term cooling and vitamin E for alleviation of infertility induced by heat stress in dairy cows. J Dairy Sci, 77:3601-3607.

Ealy AD, Howell JL, Monterroso VH, Arechiga CF, Hansen PJ. 1995. Developmental changes in sensitivity of bovine embryos to heat shock and use of antioxidants as thermoprotectants. J Anim Sci, 73:1401 -1407.

Eberhardt BG, Satrapa RA, Capinzaiki CR, Trinca LA, Barros CM. 2009. Influence of the breed of bull (Bos taurus indicus vs. Bos taurus taurus) and the breed of cow (Bos taurus indicus, Bos taurus taurus and crossbred) on the resistance of bovine embryos to heat. Anim Reprod Sci, 114:54-61.

Edwards JL, Ealy AD, Monterroso VH, Hansen PJ. 1997. Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos, Mol Reprod Dev, 48: 25-33.

El-Tarabany MS, El-Tarabany AA. 2015. Impact of maternal heat stress at insemination on the subsequent reproductive performance of Holstein, Brown Swiss, and their crosses. Theriogenology, 84:1523-1529.

Ferraz PA, Burnley C, Karanja J, Viera-Neto A, Santos JE, Chebel RC, Galvão KN. 2016. Factors affecting the success of a large embryo transfer program in Holstein cattle in a commercial herd in the southeast region of the United States. Theriogenology, 86:1834-1841.

Ferreira RM, Ayres H, Chiaratti MR, Ferraz ML, Araújo AB, Rodrigues CA, Watanabe YF, Vireque AA, Joaquim DC, Smith LC, Meirelles FV, Baruselli PS. 2011. 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, 94:2383-2392.

Flamenbaum I, Galon N. 2010. Management of heat stress to improve fertility in dairy cows in Israel. J Reprod Dev, 56 (Suppl):S36-41.

Friedman E, Voet H, Reznikov D, Dagoni I, Roth Z. 2011. Induction of successive follicular waves by gonadotropin-releasing hormone and prostaglandin F to improve fertility of high-producing cows during the summer and autumn. J Dairy Sci, 94:2393-2402.

Friedman E, Roth Z, Voet H, Lavon Y, Wolfenson D. 2012. Progesterone supplementation postinsemination improves fertility of cooled dairy cows during the summer. J Dairy Sci, 95:3092-3099.

García-Ispierto I, Abdelfatah A, López-Gatius F. 2013. Melatonin treatment at dry-off improves reproductive performance postpartum in high-producing dairy cows under heat stress conditions. Reprod Domest Anim, 48: 577-583.

García-Ispierto I, López-Gatius F, Santolaria P, Yániz JL, Nogareda C, López-Béjar M, De Rensis F. 2006. Relationship between heat stress during the peri-implantation period and early fetal loss in dairy cattle. Theriogenology, 65:799-807.

García-Ispierto I, De Rensis F, Pérez-Salas JA, Nunes JM, Pradés B, Serrano-Pérez B, López-Gatius F. 2019. The GnRH analogue dephereline given in a fixed-time AI protocol improves ovulation and embryo survival in dairy cows. Res Vet Sci, 122:170-174.

Gilad E, Meidan R, Berman A, Graber Y, Wolfenson D. 1993. Effect of tonic and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in plasma of cyclic cows. J Reprod Fertil, 99:315-321.

Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. 2014. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci USA, 111:4139-4144.

Gwazdauskas FC, Thatcher WW, Wilcox CJ. 1973. Physiological, environmental, and hormonal factors at insemination which may affect conception. J Dairy Sci, 56:873-877.

Gwazdauskas FC, Thatcher WW, Kiddy CA, Paape MJ, Wilcox CJ. 1981. Hormonal patterns during heat stress following PGF2α-tham salt induced luteal regression in heifers. Theriogenology, 16:271-285.

Hackbart KS, Ferreira RM, Dietsche AA, Socha MT, Shaver RD, Wiltbank MC, Fricke PM. 2010. Effect of dietary organic zinc, manganese, copper, and cobalt supplementation on milk production, follicular growth, embryo quality, and tissue mineral concentrations in dairy cows. J Anim Sci, 88:3856-3870.

Hansen PJ, Block J. 2004. Towards an embryocentric world: the current and potential uses of embryo technologies in dairy production. Reprod Fertil Dev, 16:1-14.

Hansen PJ. 2013a. Antecedents of mammalian fertility: Lessons from the heat-stressed cow regarding the importance of oocyte competence for fertilization and embryonic development. Anim Frontiers, 3: 34-28.

Hansen PJ. 2013b. Cellular and molecular basis of therapies to ameliorate effects of heat stress on embryonic development in cattle. Anim Reprod, 10: 322-333.

Hansen PJ. 2017. Physiological approaches to improving fertility during heat stress. In Large Herd Dairy Management, 3rd. ed., Beede, D.K. (ed.), American Dairy Science Assn, Champaign-Urbana, Illinois, chapter 7-24.

Her E, Wolfenson D, Flamenbaum I, Folman Y, Kaim M, Berman A. 1988. Thermal, productive, and reproductive responses of high yielding cows exposed to short-term cooling in summer. J Dairy Sci, 71:1085 -1092.

Hernández-Cerón J, Chase CC Jr, Hansen PJ. 2004. Differences in heat tolerance between preimplantation embryos from Brahman, Romosinuano, and Angus Breeds. J Dairy Sci, 87:53-58

Howell JL, Fuquay JW, Smith AE. 1994. Corpus luteum growth and function in lactating Holstein cows during spring and summer. J Dairy Sci, 77:735-739.

Ispada J, Rodrigues TA, Risolia PHB, Lima RS, Gonçalves DR, Rettori D, Nichi M, Feitosa WB, Paula-Lopes FF. 2018. Astaxanthin counteracts the effects of heat shock on the maturation of bovine oocytes. Reprod Fertil Dev, 30:1169-1179.

Lamp O, Derno M, Otten W, Mielenz M, Nürnberg G, Kuhla B. 2015. Metabolic heat stress adaption in transition cows: differences in macronutrient oxidation between late-gestating and early-lactating German Holstein dairy cows. PLoS One, 10:e0125264.

Lawrence JL, Payton RR, Godkin JD, Saxton AM, Schrick FN, Edwards JL. 2004. Retinol improves development of bovine oocytes compromised by heat stress during maturation. J Dairy Sci, 87:2449-2454.

López-Gatius F, Hunter R. 2017. Clinical relevance of pre-ovulatory follicular temperature in heat-stressed lactating dairy cows. Reprod Domest Anim, 52:366-370.

López-Gatius F, Hunter RHF. 2019a. Pre-ovulatory follicular cooling correlates positively with the potential for pregnancy in dairy cows: Implications for human IVF. J Gynecol Obstet Hum Reprod, 48:419-422.

López-Gatius F, Hunter RHF. 2019b. Pre-ovulatory follicular temperature in bi-ovular cows. J Reprod Dev, 65:191-194.

López-Gatius F, López-Béjar M, Fenech M, Hunter RH. 2005b. Ovulation failure and double ovulation in dairy cattle: risk factors and effects. Theriogenology, 63:1298-307.

López-Gatius F, Santolaria P, Martino A, Delétang F, De Rensis F. 2005c. The effects of GnRH treatment at the time of AI and 12 days later on reproductive performance of high producing dairy cows during the warm season in northeastern Spain. Theriogenology, 65:820-830.

López-Gatius F, Santolaria P, Mundet I, Yániz JL. 2005a. Walking activity at estrus and subsequent fertility in dairy cows. Theriogenology, 63:1419-1429.

Loureiro B, Bonilla L, Block J, Fear JM, Bonilla AQ, Hansen PJ. 2009. Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology, 150:5046-5054.

Mendonça LGD, Mantelo FM, Stevenson JS. 2017. Fertility of lactating dairy cows treated with gonadotropin-releasing hormone at AI, 5 days after AI, or both, during summer heat stress. Theriogenology, 91:9-16.

Nabenishi H, Ohta H, Nishimoto T, Morita T, Ashizawa K, Tsuzuki Y. 2012. The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote 20:249-259.

Nebel RL, Jobst SM, Dranfield MBG, Pandolfi SM, Bailey, TL. 1997. Use of radio frequency data communication system, HeatWatch®, to describe behavioral estrus in dairy cattle. J Dairy Sci. 80 (Suppl. 1):179 (Abstract).

Nguyen TTT, Bowman PJ, Haile-Mariam M, Pryce JE, Hayes BJ. 2016. Genomic selection for tolerance to heat stress in Australian dairy cattle. J Dairy Sci, 99:2849-2862.

Ortega MS, Rocha-Frigoni NAS, Mingoti GZ, Roth Z, Hansen PJ, 2016. Modification of embryonic resistance to heat shock in cattle by melatonin and genetic variation in HSPA1L. J Dairy Sci, 99:9152-9164.

Ortiz-Colón G, Fain SJ, Parés IK, Curbelo-Rodríguez J, Jiménez-Cabán E, Pagán-Morales M, Gould WA. 2018. Assessing climate vulnerabilities and adaptive strategies for resilient beef and dairy operations in the tropics. Climate Change, 146:47-58.

Paula-Lopes FF, Chase CC Jr, Al-Katanani YM, Krininger CE III, Rivera RM, Tekin S, Majewski AC, Ocon OM, Olson TA, Hansen PJ. 2003b. Genetic divergence in cellular resistance to heat shock in cattle: Differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction, 125:285-294.

Paula-Lopes FF, Al-Katanani YM, Majewski AC, Mc Dowell LR, Hansen PJ. 2003a. Manipulation of antioxidant status fails to improve fertility of lactating cows or survival of heat-shocked embryos. J Dairy Sci, 86:2343 -2351.

Pegorer MF, Vasconcelos JL, Trinca LA, Hansen PJ, Barros CM. 2007. Influence of sire and sire breed (Gyr versus Holstein) on establishment of pregnancy and embryonic loss in lactating Holstein cows during summer heat stress. Theriogenology, 67:692-697.

Pereira MH, Rodrigues AD, Martins T, Oliveira WV, Silveira PS, Wiltbank MC, Vasconcelos JL. 2013. Timed artificial insemination programs during the summer in lactating dairy cows: comparison of the 5-d Cosynch protocol with an estrogen/progesterone-based protocol. J Dairy Sci, 96:6904-6914.

Pinedo PJ, De Vries A. 2017. Season of conception is associated with future survival, fertility, and milk yield of Holstein cows. J Dairy Sci, 100:6631-6639.

Porto-Neto LR, Bickhart DM, Landaeta-Hernandez AJ, Utsunomiya YT, Pagan M, Jimenez E, Hansen PJ, Dikmen S, Schroeder SG, Kim ES, Sun J, Crespo E, Amati N, Cole JB, Null DJ, Garcia JF, Reverter A, Barendse W, Sonstegard TS. 2018. Convergent evolution of slick coat in cattle through truncation mutations in the prolactin receptor. Front Genet, 9:57.

Putney DJ, Drost M, Thatcher WW. 1988a. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between Days 1 to 7 post insemination. Theriogenology, 30:195-209.

Putney DJ, Drost M, Thatcher WW. 1989b. Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology, 31:765-778.

Putney DJ, Mullins S, Thatcher WW, Drost M, Gross TS. 1989a. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Anim Reprod Sci, 19:37-51.

Putney DJ, Thatcher WW, Drost M, Wright JM, DeLorenzo MA. 1988b. Influence of environmental temperature on reproductive performance of bovine embryo donors and recipients in the southwest region of the United States. Theriogenology, 30:905-922.

Richards JI. 1985. Effect of high daytime temperatures on the intake and utilization of water in lactating Friesian cows. Trop Anim Health Prod, 17:209-217.

Rocha de Zouza, F, Campos CC, Marques da Silva NA, dos Santos RM. 2016. Influence of seasonality, timing of insemination and rectal temperature on conception rate of crossbred dairy cows. Semina: Ciências Agrárias, Londrina, 37:155-162.

Rodrigues TA, Tuna KM, Alli AA, Tribulo P, Hansen PJ, Koh J, Paula-Lopes FF. 2019. Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock. Reprod Fertil Dev, 31:888-897.

Roth Z. 2017. Effect of heat stress on reproduction in dairy cows: insights into the cellular and molecular responses of the oocyte. Annu Rev Anim Biosci, 5:151-170.

Roth Z, Arav A, Bor A, Zeron Y, Braw-Tal R, Wolfenson D. 2001b. Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction, 122:737-744.

Roth Z, Arav A, Braw-Tai R, Bor A, Wolfenson D. 2002. Effect of treatment with follicle-stimulating hormone or bovine somatotropin on the quality of oocytes aspirated in the autumn from previously heat-stressed cows. J Dairy Sci, 85:1398-1405.

Roth Z, Meidan R, Braw-Tal R, Wolfenson D. 2000. Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J Reprod Fertil, 120:83-90.

Roth Z, Meidan R, Shaham-Albalancy A, Braw-Tal R, Wolfenson D. 2001a. Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles. Reproduction, 121:745-751.

Sakatani M, Alvarez NV, Takahashi M, Hansen PJ. 2012. Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle. J Dairy Sci, 95:3080-3091.

Sakatani M, Kobayashi S, Takahashi M. 2004. Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Mol Reprod Dev, 67:77-82.

Sakatani M, Yamanaka K, Kobayashi S, Takahashi M. 2008. Heat shock-derived reactive oxygen species induce embryonic mortality in in vitro early stage bovine embryos. J Reprod Dev, 54:496-501.

Santolaria P, López-Gatius F, García-Ispierto I, Bech-Sàbat G, Angulo E, Carretero T, Sánchez-Nadal JA, Yániz J. 2010. Effects of cumulative stressful and acute variation episodes of farm climate conditions on late embryo/early fetal loss in high producing dairy cows. Int J Biometeorol, 54:93-98.

Sartori R, Sartor-Bergfelt R, Mertens SA, Guenther JN, Parrish JJ, Wiltbank, MC. 2002. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J Dairy Sci, 85:2803-2812.

Skibiel AL, Peñagaricano F, Amorín R, Ahmed BM, Dahl GE, Laporta J. 2018. In utero heat stress alters the offspring epigenome. Sci Rep, 8:14609.

Shabankareh HK, Zandi M, Ganjali M. 2010. First service pregnancy rates following post-AI use of HCG in Ovsynch and Heatsynch programmes in lactating dairy cows. Reprod Domest Anim, 45:711-716.

Silva CF, Sartorelli ES, Castilho AC, Satrapa RA, Puelker RZ, Razza EM, Ticianelli JS, Eduardo HP, Loureiro B, Barros CM. 2013. Effects of heat stress on development, quality and survival of Bos indicus and Bos taurus embryos produced in vitro. Theriogenology, 79:351-357.

Stewart BM, Block J, Morelli P, Navarette AE, Amstalden M, Bonilla L, Hansen PJ, Bilby TR. 2011. Efficacy of embryo transfer in lactating dairy cows during summer using fresh or vitrified embryos produced in vitro with sex-sorted semen. J Dairy Sci, 94:3437-3445.

Stott GH, Wiersma F. 1976. Short term thermal relief for improved fertility in dairy cattle during hot weather. Int J Biometeorol, 20:344-350.

Thatcher WW, Collier RJ. 1986. Effects of climate on bovine reproduction. In: Current Therapy in Theriogenology 2. (D. A. Morrow, ed.), W. B. Saunders, Philadelphia pp. 301-309.

Torres-Júnior JR de S, Pires M de FA Pires, de Sá WF, Ferreira A de M, Viana JH, Camargo LS, Ramos AA, Folhadella IM, Polisseni J, de Freitas C, Clemente CA, de Sá Filho MF, Paula-Lopes FF, Baruselli PS. 2008. Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology, 69:155-166.

Trout JP, McDowell LR, Hansen PJ. 1998. Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress. J Dairy Sci, 81:1244-1250.

Vasconcelos JL, Jardina DT, Sá Filho OG, Aragon FL, Veras MB. 2011. Comparison of progesterone-based protocols with gonadotropin-releasing hormone or estradiol benzoate for timed artificial insemination or embryo transfer in lactating dairy cows. Theriogenology, 75:1153-1160.

Voelz BE, Rocha L, Scortegagna F, Stevenson JS, Mendonça LGD. 2016. Treatment of lactating dairy cows with gonadotropin-releasing hormone before first insemination during summer heat stress. J Dairy Sci, 99:7612-7623.

Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC. 1998. Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. J Dairy Sci, 81:2124-2131.

Wolfenson D, Flamenbaum I, Berman A. 1988. Hyperthermia and body energy store effects on estrous behavior, conception rate, and corpus luteum function in dairy cows. J Dairy Sci, 71:3497-3504.

Wolfenson D, Thatcher WW, Badinga L, Savio JD, Meidan R, Lew BJ, Braw-Tal R, Berman A. 1995. Effect of heat stress on follicular development during the estrous cycle in lactating dairy cattle. Biol Reprod, 52:1106-1113.

Wolff LK, Monty DE, Jr. 1974. Physiologic response to intense summer heat and its effect on the estrous cycle of nonlactating and lactating Holstein-Friesian cows in Arizona. Am J Vet Res, 35:187-192.

Zolini AM, Ortiz WG, Estrada-Cortes E, Ortega MS, Dikmen S, Sosa F, Giordano JO, Hansen PJ. 2019. Interactions of human chorionic gonadotropin with genotype and parity on fertility responses of lactating dairy cows. J Dairy Sci, 102:846-856.

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