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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Epidemiological evidence for metabolic programming in dairy cattle

G. Opsomer A B , M. Van Eetvelde A , M. Kamal A and A. Van Soom A
+ Author Affiliations
- Author Affiliations

A Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan, 133, 9820 Merelbeke Belgium.

B Corresponding author. Email: geert.opsomer@ugent.be

Reproduction, Fertility and Development 29(1) 52-57 https://doi.org/10.1071/RD16410
Published: 2 December 2016

Abstract

In humans, there is evidence that metabolic diseases occurring in later life arise in utero as a result of programming of key endocrine systems during suboptimal intrauterine conditions. The process by which prenatal insults lead to permanent changes in tissue structure and function, and finally to low birthweight (BW), is known as developmental programming. Poor nutrition, environmental temperature, oxygen availability and overnutrition all have been shown to significantly affect intrauterine development. Because the placenta is the organ for communication between mother and fetus, placental insufficiency invariably affects embryonic development and health in later life. In order to optimise their income, dairy farmers inseminate their nulliparous heifers at adolescent age, and subsequently strive for calving intervals not longer than 380 days. Hence, heifers are still growing and multiparous animals are still yielding large quantities of milk while pregnant. Dairy cows heavily selected for milk yield have specific endocrinological characteristics, like low peripheral insulin levels and low peripheral insulin sensitivity, both contributing to safeguard glucose for milk production. The reverse of this advanced selection is the high incidence of a wide range of metabolic diseases. Evidence from epidemiological studies is now available demonstrating that milk yield during gestation and environmental factors, such as season of pregnancy and parturition, affect both the size and the intermediary metabolism of the neonatal calf. The latter suggests that further optimisation in terms of production, reproduction, general health and longevity in the dairy sector may be feasible by taking into account environmental factors occurring during pregnancy.

Additional keywords: developmental origins of health and disease.


References

Banos, G., Brotherstone, S., and Coffey, M. P. (2007). Prenatal maternal effects on body condition score, female fertility, and milk yield of dairy cows. J. Dairy Sci. 90, 3490–3499.
Prenatal maternal effects on body condition score, female fertility, and milk yield of dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntlCksbw%3D&md5=d66090adec68c4bb8f82829ee35d73d8CAS |

Bauman, D. E., and Currie, W. B. (1980). Partitioning of nutrients during pregnancy and lactation – a review of mechanisms involving homeostasis and homeorhesis. J. Dairy Sci. 63, 1514–1529.
Partitioning of nutrients during pregnancy and lactation – a review of mechanisms involving homeostasis and homeorhesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtFygu7s%3D&md5=797f988f04d9c7d1ae34e1dcbe2a5c8fCAS |

Bell, A. W. (1995). Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J. Anim. Sci. 73, 2804–2819.
Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFajsrw%3D&md5=fd4d8aa695764d51b6326ef41129bf57CAS |

Bell, A. W. (2006). Prenatal programming of postnatal productivity and health of livestock: a brief review. Aust. J. Exp. Agric. 46, 725–732.
Prenatal programming of postnatal productivity and health of livestock: a brief review.Crossref | GoogleScholarGoogle Scholar |

Berry, D. P., Lonergan, P., Butler, S. T., Cromie, A. R., Fair, T., Mossa, F., and Evans, A. C. O. (2008). Negative influence of high maternal milk production before and after conception on offspring survival and milk production in dairy cattle. J. Dairy Sci. 91, 329–337.
Negative influence of high maternal milk production before and after conception on offspring survival and milk production in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGisA%3D%3D&md5=2e090fc34baaf35989641b4419b3565eCAS |

Bertram, C. E., and Hanson, M. A. (2001). Animal models and programming of metabolic syndrome. Br. Med. Bull. 60, 103–121.
Animal models and programming of metabolic syndrome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fot12msg%3D%3D&md5=399f406e69c1e62a197a8bbad6b0db7aCAS |

Brickell, J. S., Bourne, N., McGowan, M. M., and Wathes, D. C. (2009). Effect of growth and development during the rearing period on the subsequent fertility of nulliparous Holstein–Friesian heifers. Theriogenology 72, 408–416.
Effect of growth and development during the rearing period on the subsequent fertility of nulliparous Holstein–Friesian heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mvmt1eltA%3D%3D&md5=3b7bd550f8c22c69f42dd11e142ca335CAS |

Burton, G. J., and Fowden, A. L. (2012). Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, S23–S27.
Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation.Crossref | GoogleScholarGoogle Scholar |

Cetin, I., and Alvino, G. (2009). Intrauterine growth restriction: implications for placental metabolism and transport. A review. Placenta 30, S77–S82.
Intrauterine growth restriction: implications for placental metabolism and transport. A review.Crossref | GoogleScholarGoogle Scholar |

Chen, X. K., Wen, S. W., Fleming, N., Demissie, K., Rhoads, G. G., and Walker, M. (2007). Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study. Int. J. Epidemiol. 36, 368–373.
Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVKksbo%3D&md5=8d55e47793c1394f1f78265ef921b307CAS |

De Koster, J. D., and Opsomer, G. (2013). Insulin resistance in dairy cows. Vet. Clin. North Am. Food Anim. Pract. 29, 299–322.
Insulin resistance in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Fowden, A. L., and Moore, T. (2012). Maternal–fetal resource allocation: co-operation and conflict. Placenta 33, e11–e15.
Maternal–fetal resource allocation: co-operation and conflict.Crossref | GoogleScholarGoogle Scholar |

Fowden, A. L., Giussani, D. A., and Forhead, A. J. (2006a). Intrauterine programming of physiological systems: causes and sonsequences. Physiology (Bethesda) 21, 29–37.
Intrauterine programming of physiological systems: causes and sonsequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVWlsrs%3D&md5=63ace120770eecd999227d3bbfeb2082CAS |

Fowden, A. L., Ward, J. W., Wooding, F. P. B., Forhead, A. J., and Constancia, M. (2006b). Programming placental nutrient transport capacity. J. Physiol. 572, 5–15.
Programming placental nutrient transport capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1GhtLw%3D&md5=5ac5a9d38e9295d80b927b33c426b7acCAS |

Fowden, A. L., Forhead, A. J., Coan, P. M., and Burton, G. J. (2008). The placenta and intrauterine programming. J. Neuroendocrinol. 20, 439–450.
The placenta and intrauterine programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslygurc%3D&md5=1ff1c42484475f1bb9e951f2e52577eaCAS |

Fowden, A. L., Ward, J., Wooding, F. B. P., and Forhead, A. J. (2010). Developmental programming of the ovine placenta. Soc. Reprod. Fertil. Suppl. 67, 41–57.
| 1:STN:280:DC%2BC3MnosFegsA%3D%3D&md5=73fb6ca77c758de741266327771b7ac3CAS |

Funston, R. N., and Deutscher, G. H. (2004). Comparison of target breeding weight and breeding date for replacement beef heifers and effects on subsequent reproduction and calf performance. J. Anim. Sci. 82, 3094–3099.
Comparison of target breeding weight and breeding date for replacement beef heifers and effects on subsequent reproduction and calf performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVWks7k%3D&md5=adbf28f40c62ca55f5329113b1412520CAS |

Funston, R. N., Larson, D. M., and Vonnahme, K. A. (2010). Effects of maternal nutrition on conceptus growth and offspring performance: implications for beef cattle production. J. Anim. Sci. 88, E205–E215.
Effects of maternal nutrition on conceptus growth and offspring performance: implications for beef cattle production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3pslOluw%3D%3D&md5=b4878890c9469d4588c37e73b369c81cCAS |

Funston, R. N., Martin, J. L., Larson, D. M., and Roberts, A. J. (2012). Physiology and endocrinology symposium: nutritional aspects of developing replacement heifers. J. Anim. Sci. 90, 1166–1171.
Physiology and endocrinology symposium: nutritional aspects of developing replacement heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFantb4%3D&md5=ee817014555d8ce521f796d9e96404f5CAS |

González-Recio, O., Ugarte, E., and Bach, A. (2012). Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PLoS One 7, e51816.
Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model.Crossref | GoogleScholarGoogle Scholar |

Gutiérrez, V., Espasandin, A. C., Astessiano, A. L., Casal, A., López-Mazz, C., and Carriquiry, M. (2013). Calf foetal and early life nutrition on grazing conditions: metabolic and endocrine profiles and body composition during the growing phase. J. Anim. Physiol. Anim. Nutr. (Berl.) 97, 720–731.
Calf foetal and early life nutrition on grazing conditions: metabolic and endocrine profiles and body composition during the growing phase.Crossref | GoogleScholarGoogle Scholar |

Hales, C. N., and Barker, D. J. P. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty 438 phenotype hypothesis. Diabetologia 35, 595–601.
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty 438 phenotype hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zlsVyhuw%3D%3D&md5=6f1236ea94dd3aed02124b0f182db57fCAS |

Hales, C. N., and Barker, D. J. (2001). The thrifty phenotype hypothesis. Br. Med. Bull. 60, 5–20.
The thrifty phenotype hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fot12mug%3D%3D&md5=ed1028d4d6cfee96cc4c5b22f11f7942CAS |

Ibáñez, L., López-Bermejo, A., Callejo, J., Torres, A., Cabré, S., Dunger, D., and de Zegher, F. (2008). Polycystic ovaries in nonobese adolescents and young women with ovarian androgen excess: relation to prenatal growth. J. Clin. Endocrinol. Metab. 93, 196–199.
Polycystic ovaries in nonobese adolescents and young women with ovarian androgen excess: relation to prenatal growth.Crossref | GoogleScholarGoogle Scholar |

Johanson, J. M., and Berger, P. J. (2003). Birth weight as a predictor of calving ease and perinatal mortality in Holstein cattle. J. Dairy Sci. 86, 3745–3755.
Birth weight as a predictor of calving ease and perinatal mortality in Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFaisrg%3D&md5=3b2b966a98fba89f4ae87a607d6e0939CAS |

Kamal, M. M., Van Eetvelde, M., Depreester, E., Hostens, M., Vandaele, L., and Opsomer, G. (2014). Age at calving in heifers and level of milk production during gestation in cows are associated with the birth size of Holstein calves. J. Dairy Sci. 97, 5448–5458.
Age at calving in heifers and level of milk production during gestation in cows are associated with the birth size of Holstein calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFShu7zK&md5=631cde8f148f1d3f7a89ccf3979ee7a7CAS |

Kamal, M. M., Van Eetvelde, M., Bogaert, H., Hostens, M., Vandaele, L., Shamsuddin, M., and Opsomer, G. (2015). Environmental factors and dam characteristics associated with insulin sensitivity and insulin secretion in newborn Holstein calves. Animal 9, 1490–1499.
Environmental factors and dam characteristics associated with insulin sensitivity and insulin secretion in newborn Holstein calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlOnurnM&md5=17b12ed33ba323b4beaac4d187f19e0aCAS |

Leroy, J. L. M. R., Opsomer, G., Van Soom, A., Goovaerts, I. G. F., and Bols, P. E. J. (2008a). Reduced fertility in high‐yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high‐yielding dairy cows. Reprod. Domest. Anim. 43, 612–622.
Reduced fertility in high‐yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high‐yielding dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnksVeqsg%3D%3D&md5=3b63dbf7a5b9c082c10142577964c5b6CAS |

Leroy, J. L. M. R., Van Soom, A., Opsomer, G., Goovaerts, I. G. F., and Bols, P. E. J. (2008b). Reduced fertility in high‐yielding dairy cows: are the oocyte and embryo in danger? Part II. Mechanisms linking nutrition and reduced oocyte and embryo quality in high‐yielding dairy cows. Reprod. Domest. Anim. 43, 623–632.
Reduced fertility in high‐yielding dairy cows: are the oocyte and embryo in danger? Part II. Mechanisms linking nutrition and reduced oocyte and embryo quality in high‐yielding dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnksVeruw%3D%3D&md5=4b6d47815f590130edc0048a16c67972CAS |

Leroy, J. L., Valckx, S. D., Jordaens, L., De Bie, J., Desmet, K. L., Van Hoeck, V., Britt, J. H., Marei, W. F., and Bols, P. E. (2015). Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model. Reprod. Fertil. Dev. 27, 693–703.
Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVWntbc%3D&md5=0f001f409eef63c3ce1a8ed972449410CAS |

Linden, T. C., Bicalho, R. C., and Nydam, D. V. (2009). Calf birth weight and its association with calf and cow survivability, disease incidence, reproductive performance, and milk production. J. Dairy Sci. 92, 2580–2588.
Calf birth weight and its association with calf and cow survivability, disease incidence, reproductive performance, and milk production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsFenu70%3D&md5=b459a751ef364806278295fdbad9e084CAS |

Long, N. M., Vonnahme, K. A., Hess, B. W., Nathanielsz, P. W., and Ford, S. P. (2009). Effects of early gestational undernutrition on fetal growth, organ development, and placentomal composition in the bovine. J. Anim. Sci. 87, 1950–1959.
Effects of early gestational undernutrition on fetal growth, organ development, and placentomal composition in the bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1eju74%3D&md5=bb9ce562903c5d27d6614b28d1cd54d4CAS |

McMillen, I. C., MacLaughlin, S. M., Muhlhausler, B. S., Gentili, S., Duffield, J. L., and Morrison, J. L. (2008). Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin. Pharmacol. Toxicol. 102, 82–89.
Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvF2gsrg%3D&md5=369230a772feba9d732e5dfa2d484564CAS |

Norman, H. D., Wright, J. R., Kuhn, M. T., Hubbard, S. M., Cole, J. B., and VanRaden, P. M. (2009). Genetic and environmental factors that affect gestation length in dairy cattle. J. Dairy Sci. 92, 2259–2269.
Genetic and environmental factors that affect gestation length in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFymsLg%3D&md5=1504c448152638bcac6c09c0ed89494cCAS |

Pascottini, O. B., Hostens, M., Dini, P., Van Eetvelde, M., Vercauteren, P., and Opsomer, G. (2016). Prevalence of cytological endometritis and effect on pregnancy outcomes at the time of insemination in nulliparous dairy heifers. J. Dairy Sci. 99, .
| 1:CAS:528:DC%2BC28XhsVKqsr7F&md5=5fcc69ee9af3f9cfbd43a003f09d9cf7CAS |

Raboisson, D., Delor, F., Cahuzac, E., Gendre, C., Sans, P., and Allaire, G. (2013). Perinatal, neonatal, and rearing period mortality of dairy calves and replacement heifers in France. J. Dairy Sci. 96, 2913–2924.
Perinatal, neonatal, and rearing period mortality of dairy calves and replacement heifers in France.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFahtLo%3D&md5=69c0369c83f6e99442993658905b085aCAS |

Ribeiro, E. S., Gomes, G., Greco, L. F., Cerri, R. L. A., Vieira-Neto, A., Monteiro, P. L. J., Lima, F. S., Bisinotto, R. S., Thatcher, W. W., and Santos, J. E. P. (2016). Carryover effect of postpartum inflammatory diseases on developmental biology and fertility in lactating dairy cows. J. Dairy Sci. 99, 2201–2220.
Carryover effect of postpartum inflammatory diseases on developmental biology and fertility in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitV2jur%2FO&md5=edc6f78d15a957fef96e6d40900a52dbCAS |

Simerl, N. A., Wilcox, C. J., Thatcher, W. W., and Martin, F. G. (1991). Prepartum and peripartum reproductive performance of dairy heifers freshening at young ages. J. Dairy Sci. 74, 1724–1729.
Prepartum and peripartum reproductive performance of dairy heifers freshening at young ages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzkvFektA%3D%3D&md5=f2a28208142f587c32a1954a37f5ae6dCAS |

Sullivan, T. M., Micke, G. C., Magalhaes, R. S., Phillips, N. J., and Perry, V. E. (2009). Dietary protein during gestation affects placental development in heifers. Theriogenology 72, 427–438.
Dietary protein during gestation affects placental development in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2nsr4%3D&md5=cf0deb380b4e8e3db5b31f592455f7b4CAS |

Swali, A., and Wathes, D. C. (2006). Influence of the dam and sire on size at birth and subsequent growth, milk production and fertility in dairy heifers. Theriogenology 66, 1173–1184.
Influence of the dam and sire on size at birth and subsequent growth, milk production and fertility in dairy heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vps1yitA%3D%3D&md5=56e197d52db82210a11de727e1907485CAS |

Swali, A., and Wathes, D. C. (2007). Influence of primiparity on size at birth, growth, the somatotrophic axis and fertility in dairy heifers. Anim. Reprod. Sci. 102, 122–136.
Influence of primiparity on size at birth, growth, the somatotrophic axis and fertility in dairy heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snitFOjsQ%3D%3D&md5=d25f35924078141769568be8bb40d9caCAS |

Van Eetvelde, M., Kamal, M. M., Hostens, M., Vandaele, L., Fiems, L. O., and Opsomer, G. (2016). Evidence for placental compensation in cattle. Animal 10, 1342–1350.
Evidence for placental compensation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC28jms1CltA%3D%3D&md5=cf7ee31e4068e28f19ac6ea27ab8fc3eCAS |

Vaughan, O. R., Sferruzzi-Perri, A. N., Coan, P. M., and Fowden, A. L. (2012). Environmental regulation of placental phenotype: implications for fetal growth. Reprod. Fertil. Dev. 24, 80–96.
Environmental regulation of placental phenotype: implications for fetal growth.Crossref | GoogleScholarGoogle Scholar |

Vonnahme, K. A., Zhu, M. J., Borowicz, P. P., Geary, T. W., Hess, B. W., Reynolds, L. P., Caton, J. S., Means, W. J., and Ford, S. P. (2007). Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome. J. Anim. Sci. 85, 2464–2472.
Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSjtrvO&md5=7a8ce74ba7e9a89a63a000821c9bb98fCAS |

Wallace, J. M., Luther, J. S., Milne, J. S., Aitken, R. P., Redmer, D. A., Reynolds, L. P., and Hay, W. W. (2006). Nutritional modulation of adolescent pregnancy outcome – a review. Placenta 27, S61–S68.
Nutritional modulation of adolescent pregnancy outcome – a review.Crossref | GoogleScholarGoogle Scholar |

Wathes, D. C. (2012). Mechanisms linking metabolic status and disease with reproductive outcome in the dairy cow. Reprod. Domest. Anim. 47, 304–312.
Mechanisms linking metabolic status and disease with reproductive outcome in the dairy cow.Crossref | GoogleScholarGoogle Scholar |

Wathes, D. C., Brickell, J. S., Bourne, N. E., Swali, A., and Cheng, Z. (2008). Factors influencing heifer survival and fertility on commercial dairy farms. Animal 2, 1135–1143.
Factors influencing heifer survival and fertility on commercial dairy farms.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vptFSitg%3D%3D&md5=bb66da1ad792fc09bd7ff89a22dbc453CAS |

Wathes, D. C., Pollott, G. E., Johnson, K. F., Richardson, H., and Cooke, J. S. (2014). Heifer fertility and carry over consequences for life time production in dairy and beef cattle. Animal 8, 91–104.
Heifer fertility and carry over consequences for life time production in dairy and beef cattle.Crossref | GoogleScholarGoogle Scholar |

Wilcox, A. J. (2001). On the importance and unimportance of birth weight. Int. J. Epidemiol. 30, 1233–1241.
On the importance and unimportance of birth weight.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387gtF2itA%3D%3D&md5=d1bb5d4268996ce3620a4b0d02ae0c27CAS |

Wiltbank, M. C., Baez, G. M., Garcia-Guerra, A., Toledo, M. Z., Monteiro, P. L., Melo, L. F., Ochoa, J. C., Santos, J. E., and Sartori, R. (2016). Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. Theriogenology 86, 239–253.
Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |