Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-06-19T09:52:59.777Z Has data issue: false hasContentIssue false
  • English
  • Français

Environmental factors and dam characteristics associated with insulin sensitivity and insulin secretion in newborn Holstein calves

Published online by Cambridge University Press:  08 May 2015

M. M. Kamal ,
M. Van Eetvelde ,
H. Bogaert ,
M. Hostens ,
L. Vandaele ,
M. Shamsuddin  and
G. Opsomer
M. M. Kamal
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium Department of Surgery and Obstetrics, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
M. Van Eetvelde
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
H. Bogaert
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
M. Hostens
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
L. Vandaele
Affiliation:
Department of Animal Sciences, Institute for Agricultural and Fishery Research (ILVO), Scheldeweg 68, 9090 Melle, Belgium
M. Shamsuddin
Affiliation:
Department of Surgery and Obstetrics, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
G. Opsomer*
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
*
†E-mail: Geert.Opsomer@Ugent.be
Get access

Abstract

The objective of the present retrospective cohort study was to evaluate potential associations between environmental factors and dam characteristics, including level of milk production during gestation, and insulin traits in newborn Holstein calves. Birth weight and gestational age of the calves at delivery were determined. On the next day, heart girth, wither height and diagonal length of both the calves and their dams were measured. Parity, body condition score and age at calving were recorded for all dams. For the cows, days open before last gestation, lactation length (LL), length of dry period (DP) and calving interval were also calculated. The magnitude and shape of the lactation curve both quantified using the MilkBot model based on monthly milk weights, were used to calculate the amount of milk produced during gestation. Using the same procedure, cumulative milk production from conception to drying off (MGEST) was calculated. A blood sample was collected from all calves (n=481; 169 born to heifers and 312 born to cows) at least 5 h after a milk meal on day 3 of life to measure basal glucose and insulin levels. In addition, an intravenous glucose-stimulated insulin secretion test was performed in a subset of the calves (n=316). After descriptive analysis, generalized linear mixed models were used to identify factors that were significantly associated with the major insulin traits (Insb, basal insulin level; QUICKI, quantitative insulin sensitivity check index; AIR, acute insulin response; DI, disposition index) of the newborn calves. The overall average birth weight of the calves was 42.7±5.92 kg. The insulin traits were significantly associated with gender and season of birth when data of all calves were analyzed. In addition, the insulin traits in calves born to cows were significantly associated with MGEST, DP and LL. The Insb was estimated to be higher in calves born to the cows having passed a higher MGEST (P=0.076) and longer DP (P=0.034). The QUICKI was estimated to be lower in calves born to the cows having passed a higher MGEST (P=0.030) and longer DP (P=0.058). Moreover, the AIR (P=0.009) and DI (P=0.049) were estimated to be lower in male compared with female calves. Furthermore, the AIR (P=0.036) and DI (P=0.039) were estimated to be lower in calves born to cows having passed a longer LL. The decisive effects of MGEST, DP and LL in cows on the insulin traits of their calves may provide a basis for developing managerial interventions to improve metabolic health of the offspring.

Keywords

insulin traitsdairy calvesrisk factors
Type
Research Article
Information
animal , Volume 9 , Issue 9 , September 2015 , pp. 1490 - 1499
Copyright
© The Animal Consortium 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Accorsi, PA, Govoni, N, Gaiani, R, Pezzi, C, Seren, E and Tamanini, C 2005. Leptin, GH, PRL, insulin and metabolic parameters throughout the dry period and lactation in dairy cows. Reproduction in Domestic Animals 40, 217–223.CrossRefGoogle ScholarPubMed
Albarrán-Portillo, B and Pollott, GE 2013. The relationship between fertility and lactation characteristics in Holstein cows on United Kingdom commercial dairy farms. Journal of Dairy Science 96, 635–646.Google Scholar
Atashi, H, Zamiri, MJ and Dadpasand, M 2013. Association between dry period length and lactation performance, lactation curve, calf birth weight, and dystocia in Holstein dairy cows in Iran. Journal of Dairy Science 96, 3632–3638.Google Scholar
Bergman, RN, Ader, M, Huecking, K and Van Citters, G 2002. Accurate assessment of beta-cell function: the hyperbolic correction. Diabetes 51, S212–S220.CrossRefGoogle ScholarPubMed
Berry, DP, Lonergan, P, Butler, ST, Cromie, AR, Fair, T, Mossa, F and Evans, ACO 2008. Negative influence of high maternal milk production before and after conception on offspring survival and milk production in dairy cattle. Journal of Dairy Science 91, 329–337.CrossRefGoogle ScholarPubMed
Bossaert, P, Leroy, JLMR, 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, 4404–4411.CrossRefGoogle Scholar
Bossaert, P, Fransen, E, Langbeen, A, Stalpaert, M, Vandenbroeck, I, Bols, PEJ and JLMR, Leroy 2014. Effects of parity and periconceptional metabolic state of Holstein-Friesian dams on the glucose metabolism and conformation in their newborn calves. Animal 8, 975–981.CrossRefGoogle ScholarPubMed
Carlsson, GL, Heller, RS, Serup, P and Hyttel, P 2010. Immunohistochemistry of pancreatic development in cattle and pig. Anatomia, Histologia, Embryologia 39, 107–119.Google Scholar
De Blasio, MJ, Gatford, KL, McMillen, IC, Robinson, JS and Owens, JA 2007. Placental restriction of fetal growth increases insulin action, growth, and adiposity in the young lamb. Endocrinology 148, 1350–1358.Google Scholar
De Koster, JD and Opsomer, G 2013. Insulin resistance in dairy cows. Veterinary Clinics of North America: Food Animal Practice 29, 299–322.Google ScholarPubMed
De Rooij, SR, Painter, RC, Phillips, DIW, Osmond, C, Michels, RPJ, Godsland, IF, Bossuyt, PMM, Bleker, OP and Rojeboom, TJ 2006. Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care 29, 1897–1901.CrossRefGoogle Scholar
Edmonson, AJ, Lean, IJ, Weaver, LD, Farver, T and Webster, G 1989. A body condition scoring chart for Holstein dairy cows. Journal of Dairy Science 72, 68–78.CrossRefGoogle Scholar
Ehrlich, J 2011. Quantifying shape of lactation curves, and benchmark curves for common dairy breeds and parities. Bovine Practitioner 45, 88–95.Google Scholar
Fleming, TP, Lucas, ES, Watkins, AJ and Eckert, JJ 2012. Adaptive responses of the embryo to maternal diet and consequences for post-implantation development. Reproduction, Fertility and Development 24, 35–44.Google Scholar
Funston, RN and Summers, AF 2013. Effect of prenatal programming on heifer development. Veterinary Clinics of North America: Food Animal Practice 29, 517–536.Google ScholarPubMed
Geer, EB and Shen, W 2009. Gender differences in insulin resistance, body composition, and energy balance. Gender Medicine 6, 60–75.CrossRefGoogle ScholarPubMed
Gonzalez-Recio, O, Ugarte, E and Bach, A 2012. Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PLoS One 7, e51816.CrossRefGoogle ScholarPubMed
Green, JC, Meyer, JP, Williams, AM, Newsom, EM, Keisler, DH and Lucy, MC 2012. Pregnancy development from day 28 to 42 of gestation in postpartum Holstein cows that were either milked (lactating) or not milked (not lactating) after calving. Reproduction 143, 699–711.Google Scholar
Gutierrez, V, Espasandin, AC, Astessiano, AL, Casal, A, Lopez-Mazz, C and Carriquiry, M 2012. Calf foetal and early life nutrition on grazing conditions: metabolic and endocrine profiles and body composition during the growing phase. Journal of Animal Physiology and Animal Nutrition 97, 720–731.Google Scholar
Hammon, HM, Steinhoff-Wagner, J, Schonhusen, U, Metges, CC and Blum, JW 2012. Energy metabolism in the newborn farm animal with emphasis on the calf: endocrine changes and responses to milk-born and systemic hormones. Domestic Animal Endocrinology 43, 171–185.CrossRefGoogle ScholarPubMed
Jaquiery, AL, Oliver, MH, Honeyfield-Ross, M, Harding, JE and Bloomfield, FH 2012. Periconceptional undernutrition in sheep affects adult phenotype only in males. Journal of Nutrition and Metabolism 2012, 123610.Google Scholar
Kamal, MM, 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. Journal of Dairy Science 97, 5448–5458.Google Scholar
Limesand, SW, Rozance, PJ, Macko, AR, Anderson, MJ, Kelly, AC and Hay, WWJ 2013. Reductions in insulin concentrations and β-cell mass precede growth restriction in sheep fetuses with placental insufficiency. American Journal of Physiology, Endocrinology and Metabolism 304, E516–E523.Google Scholar
Long, NM, Prado-Cooper, MJ, Krehbiel, CR and Wettemann, RP 2010. Effects of nutrient restriction of bovine dams during early gestation on postnatal growth and regulation of plasma glucose. Journal of Animal Science 88, 3262–3268.Google Scholar
Lucy, MC, Butler, ST and Garverick, HA 2014. Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows. Animal 8, 82–90.Google Scholar
Micke, GC, Sullivan, TM, McMillen, IC, Gentili, S and Perry, VE 2011. Heifer nutrient intake during early- and mid-gestation programs adult offspring adiposity and mRNA expression of growth-related genes in adipose depots. Reproduction 141, 697–706.CrossRefGoogle ScholarPubMed
Morrison, JL 2008. Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clinical and Experimental Pharmacology and Physiology 35, 730–743.CrossRefGoogle ScholarPubMed
Muri, C, Schottstedt, T, Hammon, HM, Meyer, E and Blum, JW 2005. Hematological, metabolic, and endocrine effects of feeding vitamin A and lactoferrin in neonatal calves. Journal of Dairy Science 88, 1062–1077.CrossRefGoogle ScholarPubMed
Owens, JA, Gatford, KL, De Blasio, MJ, Edwards, LJ, McMillen, IC and Fowden, AL 2007. Restriction of placental growth in sheep impairs insulin secretion but not sensitivity before birth. Journal of Physiology 584, 935–949.Google Scholar
Pezeshki, A, Mehrzad, J, Ghorbani, GR, Rahmani, HR, Collier, RJ and Burvenich, C 2007. Effects of short dry periods on performance and metabolic status in Holstein dairy cows. Journal of Dairy Science 90, 5531–5541.Google Scholar
Piccardi, M, Capitaine Funes, A, Balzarini, M and Bó, GA 2013. Some factors affecting the number of days open in Argentinean dairy herds. Theriogenology 79, 760–765.Google Scholar
Radunz, AE, Fluharty, FL, Relling, AE, Felix, TL, Shoup, LM, Zerby, HN and Loerch, SC 2012. Prepartum dietary energy source fed to beef cows: II. Effects on progeny postnatal growth, glucose tolerance, and carcass composition. Journal of Animal Science 90, 4962–4974.Google Scholar
Rozance, PJ, Limesand, SW and Hay, WWJ 2006. Decreased nutrient-stimulated insulin secretion in chronically hypoglycemic late-gestation fetal sheep is due to an intrinsic islet defect. American Journal of Physiology, Endocrinology and Metabolism 291, E404–E411.CrossRefGoogle Scholar
Sattar, N 2013. Gender aspects in type 2 diabetes mellitus and cardiometabolic risk. Best Practice & Research in Clinical Endocrinology & Metabolism 27, 501–507.Google Scholar
Sensosy, W, Zain, AE, Abdel-Razek, AK, Uchiza, M, Tameoka, N, Izaike, Y and Osawa, T 2012. Association between energy status early postpartum and subsequent embryonic mortality in high-yielding recipient cows. Animal Science Journal 83, 284–290.CrossRefGoogle Scholar
Sternbauer, K and Essen-Gustavsson, B 2002. Insulin sensitivity and muscle characteristics in calves at different levels of physical activity. Journal of Veterinary Medicine Series A 49, 449–454.CrossRefGoogle ScholarPubMed
Tao, S, Monteiro, APA, Hayen, MJ and Dahl, GE 2014. Maternal heat stress during the dry period alters postnatal whole-body insulin response of calves. Journal of Dairy Science 97, 897–901.Google Scholar
Wilkin, TJ and Murphy, MJ 2006. The gender insulin hypothesis: why girls are born lighter than boys, and the implications for insulin resistance. International Journal of Obesity 30, 1056–1061.CrossRefGoogle ScholarPubMed
Wu, G, Bazer, FW, Wallace, JM and Spencer, TE 2006. Intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science 84, 2316–2337.CrossRefGoogle ScholarPubMed