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Effects of parity and periconceptional metabolic state of Holstein–Friesian dams on the glucose metabolism and conformation in their newborn calves

Published online by Cambridge University Press:  01 April 2014

P. Bossaert*
Affiliation:
Laboratory for Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
E. Fransen
Affiliation:
StatUa Center for Statistics, University of Antwerp, Prinsstraat 13, B-2000 Antwerp, Belgium
A. Langbeen
Affiliation:
Laboratory for Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
M. Stalpaert
Affiliation:
AML. Emiel Vloorsstraat 9, 2020 Antwerp, Belgium
I. Vandenbroeck
Affiliation:
Hooibeekhoeve, Hooibeeksedijk 1, 2440 Geel, Belgium
P. E. Bols
Affiliation:
Laboratory for Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
J. L. Leroy
Affiliation:
Laboratory for Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
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Abstract

The metabolic state of pregnant mammals influences the offspring’s development and risk of metabolic disease in postnatal life. The metabolic state in a lactating dairy cow differs immensely from that in a non-lactating heifer around the time of conception, but consequences for their calves are poorly understood. The hypothesis of this study was that differences in metabolic state between non-lactating heifers and lactating cows during early pregnancy would affect insulin-dependent glucose metabolism and development in their neonatal calves. Using a mixed linear model, concentrations of glucose, IGF-I and non-esterified fatty acids (NEFAs) were compared between 13 non-lactating heifers and 16 high-yielding dairy cows in repeated blood samples obtained during the 1st month after successful insemination. Calves born from these dams were weighed and measured at birth, and subjected to intravenous glucose and insulin challenges between 7 and 14 days of age. Eight estimators of insulin-dependent glucose metabolism were determined: glucose and insulin peak concentration, area under the curve and elimination rate after glucose challenge, glucose reduction rate after insulin challenge, and quantitative insulin sensitivity check index. Effects of dam parity and calf sex on the metabolic and developmental traits were analysed in a two-way ANOVA. Compared with heifers, cows displayed lower glucose and IGF-I and higher NEFA concentrations during the 1st month after conception. However, these differences did not affect developmental traits and glucose homeostasis in their calves: birth weight, withers height, heart girth, and responses to glucose and insulin challenges in the calves were unaffected by their dam’s parity. In conclusion, differences in the metabolic state of heifers and cows during early gestation under field conditions could not be related to their offspring’s development and glucose homeostasis.

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Full Paper
Copyright
© The Animal Consortium 2014 

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References

Bossaert, P 2010. The role of insulin in the energy conflict between milk production and ovarian activity during the transition period of high-yielding dairy cows. Phd thesis. Faculty of Veterinary Medicine, Ghent University, Belgium.Google Scholar
Bossaert, P, Leroy, JL, De Vliegher, S and Opsomer, G 2008. Interrelations between glucose-induced insulin response, metabolic indicators and time of first ovulation in high yielding dairy cows. Journal of Dairy Science 91, 33633371.Google Scholar
Bossaert, P, Leroy, JL, De Campeneere, S, De Vliegher, S and Opsomer, G 2009. Differences in the glucose-induced insulin response and the peripheral insulin responsiveness between neonatal calves of the Belgian Blue, Holstein–Friesian, and East Flemish breeds. Journal of Dairy Science 92, 44044411.Google Scholar
de Rooij, SR, Painter, RC, Phillips, DIW, Osmond, C, Michels, RPJ, Godsland, IF, Bossuyt, PMM, Bleker, OP and Roseboom, TJ 2006. Impaired insulin secretion after prenatal exposure to the Dutch Famine. Diabetes Care 29, 18971901.CrossRefGoogle Scholar
Drackley, JK, Dann, HM, Douglas, GN, Janovick Guretzky, NA, Litherland, NB, Underwood, JP and Loor, JJ 2005. Physiological and pathological adaptations in dairy cows that may increase susceptibility to periparturient diseases and disorders (invited review). Italian Journal of Animal Science 4, 323344.Google Scholar
Du, M, Tong, J, Zhao, J, Underwood, KR, Zhu, M, Ford, SP and Nathanielsz, PW 2010. Fetal programming of skeletal muscle development in ruminant animals. Journal of Animal Science 88, 5160.CrossRefGoogle ScholarPubMed
Freetly, HC, Ferrell, CL and Jenkins, TG 2000. Timing of realimentation of mature cows that were feed-restricted during pregnancy influences calf birth weights and growth rates. Journal of Animal Science 78, 27902796.Google Scholar
Friggens, NC, Berg, P, Theilgaard, P, Korsgaard, IR, Ingvartsen, KL, Løvendahl, PL and Jensen, J 2007. Breed and parity effects on energy balance profiles through lactation: evidence for genetically driven body reserve change. Journal of Dairy Science 90, 52915305.CrossRefGoogle ScholarPubMed
Gardner, DS, Tingey, K, Van Bon, BWM, Ozanne, SE, Wilson, V, Dandrea, J, Keisler, DH, Stephenson, T and Symonds, ME 2005. Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 289, 947954.CrossRefGoogle ScholarPubMed
Gutierrez, CG, Gong, JG, Bramley, TA and Webb, R 2006. Selection on predicted breeding value for milk production delays ovulation independently of changes in follicular development, milk production and body weight. Animal Reproduction Science 95, 193205.Google Scholar
Hales, C and Barker, D 1992. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595601.Google Scholar
Hammon, HM and Blum, JW 1998. Metabolic and endocrine traits of neonatal calves are influenced by feeding colostrum for different durations or only milk replacer. Journal of Nutrition 128, 624632.CrossRefGoogle ScholarPubMed
Hammon, HM, Bellmann, O, Voigt, J, Schneider, F and Kühn, C 2007. Glucose-dependent insulin response and milk production in heifers within a segregating resource family population. Journal of Dairy Science 90, 32473254.Google Scholar
Jorritsma, R, Wensing, T, Kruip, TAM, Vos, PLAM and Noordhuizen, JPTM 2003. Metabolic changes in early lactation and impaired reproductive performance in dairy cows. Veterinary Research 34, 1126.Google Scholar
Kertz, AF, Reutzel, LF, Barton, BA and Ely, RL 1997. Body weight, body condition score, and wither height of prepartum Holstein cows and birth weight and sex of calves by parity: a database and summary. Journal of Dairy Science 80, 525529.Google Scholar
Leroy, JL, Vanholder, T, Van Knegsel, ATM, Garcia-Ispierto, I and Bols, PE 2008. Nutrient prioritization in dairy cows early postpartum: mismatch between metabolism and fertility? Reproduction in Domestic Animals 43, 96103.Google Scholar
Leroy, JL, Opsomer, G, De Vliegher, S, Vanholder, T, Goossens, L, Geldhof, A, Bols, PE, de Kruif, A and Van Soom, A 2005. Comparison of embryo quality in high yielding dairy cows, in dairy heifers and in beef cows. Theriogenology 64, 20222036.CrossRefGoogle ScholarPubMed
Lucy, MC 2008. Functional differences in the growth hormone and insulin-like growth factor axis in cattle and pigs: implications for postpartum nutrition and reproduction. Reproduction in Domestic Animals 43, 3139.Google Scholar
Martin, BC, Warram, JH, Krolewski, AS, Bergman, RN, Soeldner, JS and Kahn, CR 1992. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. The Lancet 340, 925929.Google Scholar
McMillen, C, MacLaughlin, SM, Muhlhausler, BS, Gentili, S, Duffield, JL and Morrison, JL 2008. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic & Clinical Pharmacology & Toxicology 102, 8289.Google Scholar
Micke, GC, Sullivan, TM, Gatford, GL, Owens, JA and Perry, VE 2010. Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits. Animal Reproduction Science 121, 208217.Google Scholar
Micke, GC, Sullivan, TM, Soares Magalhaes, RJ, Rolls, PJ, Norman, ST and Perry, VEA 2009. Heifer nutrition during early- and mid-pregnancy alters fetal growth trajectory and birth weight. Animal Reproduction Science 117, 110.Google Scholar
Mossa, F, Carter, F, Walsh, SW, Kenny, DA, Smith, GW, Ireland, JLH, Hildebrandt, TB, Lonergan, P, Ireland, JJ and Evans, ACO 2013. Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biology of Reproduction 88, 19.Google Scholar
Oikawa, S and Oetzel, GR 2006. Decreased insulin response in dairy cows following a four-day fast to induce hepatic lipidosis. Journal of Dairy Science 88, 29993005.CrossRefGoogle Scholar
Owens, JA, Thavaneswaran, P, De Blasio, MJ, McMillen, IC, Robinson, JS and Gatford, KI 2007. Sex-specific effects of placental restriction on components of the metabolic syndrome in young adult sheep. American Journal of Physiology – Endocrinology and Metabolism 292, 18791889.Google Scholar
Ozanne, SE and Hales, CN 2002. Early programming of glucose–insulin metabolism. Trends in Endocrinology & Metabolism 13, 368373.CrossRefGoogle ScholarPubMed
Pires, JAA, Souza, AH and Grummer, RR 2007. Induction of hyperlipidemia by intravenous infusion of tallow emulsion causes insulin resistance in Holstein cows. Journal of Dairy Science 90, 27352744.Google Scholar
Rabasa-Lhoret, R, Bastard, JP, Jan, V, Ducluzeau, PH, Andreelli, F, Guebre, F, Bruzeau, J, Louche-Pellissier, C, Maitrepierre, C, Peyrat, J, Chagne, J, Vidal, H and Laville, M 2003. Modified quantitative insulin sensitivity check index is better correlated to hyperinsulinemic glucose clamp than other fasting-based index of insulin sensitivity in different insulin-resistant states. The Journal of Clinical Endocrinology & Metabolism 88, 49174923.Google Scholar
Rauprich, ABE, Hammon, HM and Blum, JW 2000. Effects of feeding colostrum and a formula with nutrient contents as colostrum on metabolic and endocrine traits in neonatal calves. Biology of the Neonate 78, 5364.Google Scholar
Ravelli, ACJ, van der Meulen, JHP, Michels, RPJ, Osmond, C, Barker, DJP, Hales, CN and Bleker, OP 1998. Glucose tolerance in adults after prenatal exposure to famine. The Lancet 351, 173177.CrossRefGoogle ScholarPubMed
Stocker, CJ, Arch, JRS and Cawthorne, MA 2005. Fetal origins of insulin resistance and obesity. Proceedings of the Nutrition Society 64, 143151.Google Scholar
Taylor, VJ, Cheng, Z, Pushpakumara, PGA, Wathes, DC and Beever, DE 2004. Relationships between the plasma concentrations of insulin-like growth factor-I in dairy cows and their fertility and milk yield. Veterinary Record 155, 583588.Google Scholar
Todd, SE, Oliver, MH, Jaquiery, AL, Bloomfield, FH and Harding, JE 2009. Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatric Research 65, 409413.Google Scholar
Van Hoeck, V, Sturmey, RG, Bermejo-Alvarez, P, Rizos, D, Gutierrez-Adan, A, Leese, HJ, Bols, PE and Leroy, JL 2011. Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6(8), doi:10.1371/journal.pone.0023183, Published online by Epub.Google Scholar
Van Hoeck, V, JL, Leroy, Alvarez, MA, Rizos, D, Gutierrez-Adan, A, Schnorbusch, K, Bols, PE, Leese, HJ and Sturmey, RG 2013. Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 145, 3344.Google Scholar
Wathes, DC, Reynolds, TS, Robinson, RS and Stevenson, KR 1998. Role of the insulin-like growth factor system in uterine function and placental development in ruminants. Journal of Dairy Science 81, 17781789.Google Scholar