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Evidence for placental compensation in cattle

Published online by Cambridge University Press:  03 March 2016

M. Van Eetvelde ,
M. M. Kamal ,
M. Hostens ,
L. Vandaele ,
L. O. Fiems  and
G. Opsomer
M. Van Eetvelde*
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
M. M. Kamal
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
L. O. Fiems
Affiliation:
Department of Animal Sciences, Institute for Agricultural and Fishery Research (ILVO), Scheldeweg 68, 9090 Melle, Belgium
G. Opsomer
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
*
†E-mail: [email protected]
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Abstract

Prenatal development is known to be extremely sensitive to maternal and environmental challenges. In this study, we hypothesize that body growth and lactation during gestation in cattle reduce nutrient availability for the pregnant uterus, with consequences for placental development. Fetal membranes of 16 growing heifers and 27 fully grown cows of the Belgian Blue (BB) breed were compared to determine the effect of body growth on placental development. Furthermore, the fetal membranes of 49 lactating Holstein Friesian (HF) cows and 27 HF heifers were compared to study the impact of dam lactation compared to dam body growth. After parturition, calf birth weight and body measurements of dam and calf were recorded, as well as weight of total fetal membranes, cotyledons and intercotyledonary membranes. All cotyledons were individually measured to calculate both the surface of each individual cotyledon and the total cotyledonary surface per placenta. Total cotyledonary surface was unaffected by breed or the breed×parity interaction. Besides a 0.3 kg lower cotyledonary weight (P=0.007), heifer placentas had a smaller total cotyledonary surface compared with placentas of cows (0.48±0.017 v. 0.54±0.014 m2, respectively, P<0.001). Within the BB breed, fetal membranes of heifers had a 1.5 kg lower total weight and 1.0 kg lower intercotyledonary membrane weight (P<0.005) compared with cows. A cotyledon number of only 91±5.4 was found in multiparous BB dams, while growing BB heifers had a higher cotyledon number (126±6.7, P<0.001), but a greater proportion of smaller cotyledons (<40 cm2). Within the HF breed, no parity effect on intercotyledonary membrane weight, cotyledon number and individual cotyledonary surface was found. Placental efficiency (calf weight/total cotyledonary surface) was similar in HF and BB heifers but significantly higher in multiparous BB compared with multiparous HF dams (106.0±20.45 v. 74.3±12.27 kg/m2, respectively, P<0.001). Furthermore, a seasonal effect on placental development was found, with winter and spring placentas having smaller cotyledons than summer and fall placentas (P<0.001). Main findings of the present study are that lactation and maternal growth during gestation entail a comparable nutrient diverting constraint, which might alter placental development. However, results suggest that the placenta is able to manage this situation through two potential compensation mechanisms. In early pregnancy the placenta might cope by establishing a higher number of cotyledons, while in late gestation a compensatory expansion of the cotyledonary surface is suggested to meet the nutrient demand of the fetus.

Keywords

placental developmentmaternal factorscalving seasonHolstein FriesianBelgian Blue
Type
Research Article
Information
animal , Volume 10 , Issue 8 , August 2016 , pp. 1342 - 1350
Copyright
© The Animal Consortium 2016 

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References

Adeyinka, FD 2012. The development of the bovine placentome and associated structures during gestation: a thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Veterinary Science, Massey University, Palmerston North, New Zealand.Google Scholar
Allen, W, Wilsher, S, Turnbull, C, Stewart, F, Ousey, J, Rossdale, P and Fowden, A 2002. Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero. Reproduction 123, 445–453.CrossRefGoogle ScholarPubMed
Barker, D, Thornburg, K, Osmond, C, Kajantie, E and Eriksson, J 2010. Beyond birthweight: the maternal and placental origins of chronic disease. Journal of Developmental Origins of Health and Disease 1, 360–364.CrossRefGoogle ScholarPubMed
Bertolini, M, Mason, JB, Beam, SW, Carneiro, GF, Sween, ML, Kominek, DJ, Moyer, AL, Famula, TR, Sainz, RD and Anderson, GB 2002. Morphology and morphometry of in vivo-and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology 58, 973–994.CrossRefGoogle ScholarPubMed
Clarke, L, Heasman, L, Juniper, DT and Symonds, ME 1998. Maternal nutrition in early-mid gestation and placental size in sheep. British Journal of Nutrition 79, 359–364.CrossRefGoogle ScholarPubMed
Constância, M, Angiolini, E, Sandovici, I, Smith, P, Smith, R, Kelsey, G, Dean, W, Ferguson-Smith, A, Sibley, CP and Reik, W 2005. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proceedings of the National Academy of Sciences of the United States of America 102, 19219–19224.CrossRefGoogle ScholarPubMed
Coopman, F, Van Zeveren, A, Verhoeven, G and De Smet, S 2007. Parameters for the estimation of live weight and for the visual appraisal of the muscular conformation in the (double-muscled) Belgian Blue beef breed. Archiv Fur Tierzucht-Archives of Animal Breeding 50, 348–355.CrossRefGoogle Scholar
Early, R, McBride, B, Vatnick, I and Bell, A 1991. Chronic heat stress and prenatal development in sheep: II. Placental cellularity and metabolism. Journal of Animal Science 69, 3610–3616.CrossRefGoogle ScholarPubMed
Fiems, L and Ampe, B 2015. Importance of dam BW change and calf birth weight in double-muscled Belgian Blue cattle and its relationship with parity and calving interval. Animal 9, 94–103.CrossRefGoogle ScholarPubMed
Fleming, T, Velazquez, M, Eckert, J, Lucas, E and Watkins, A 2012. Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Animal Reproduction Science 130, 193–197.CrossRefGoogle ScholarPubMed
Fowden, A, Ward, J, Wooding, F and Forhead, A 2011. Developmental programming of the ovine placenta. Reproduction in Domestic Ruminants VII, 41.Google Scholar
Funston, RN, Larson, DM and Vonnahme, KA 2010. Effects of maternal nutrition on conceptus growth and offspring performance: implications for beef cattle production. Journal of Animal Science 88, E205–E215.CrossRefGoogle ScholarPubMed
Grobet, L, Martin, LJ, Poncelet, D, Pirottin, D, Brouwers, B, Riquet, J, Schoeberlein, A, Dunner, S, Menissier, F, Massabanda, J, Fries, R, Hanset, R and Georges, M 1997. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genetics 17, 71–74.CrossRefGoogle ScholarPubMed
Heasman, L, Clarke, L, Stephenson, T and Symonds, M 1999. The influence of maternal nutrient restriction in early to mid-pregnancy on placental and fetal development in sheep. Proceedings of the Nutrition Society 58, 283–288.CrossRefGoogle ScholarPubMed
Kamal, 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. Journal of Dairy Science 97, 5448–5458.CrossRefGoogle ScholarPubMed
Kolkman, I, Opsomer, G, Aerts, S, Hoflack, G, Laevens, H and Lips, D 2010. Analysis of body measurements of newborn purebred Belgian Blue calves. Animal 4, 661–671.CrossRefGoogle ScholarPubMed
Laven, R and Peters, A 2001. Gross morphometry of the bovine placentome during gestation. Reproduction in Domestic Animals 36, 289–296.CrossRefGoogle ScholarPubMed
Miglino, M, Pereira, F, Visintin, J, Garcia, J, Meirelles, F, Rumpf, R, Ambrósio, C, Papa, P, Santos, T and Carvalho, A 2007. Placentation in cloned cattle: structure and microvascular architecture. Theriogenology 68, 604–617.CrossRefGoogle ScholarPubMed
Neto, ACD, Morceli, JAB, da Fonseca, R, Ambrosio, CE, Pereira, FTV and Miglino, MA 2009. Biometrics evolution of the embryonic and fetal annexes in cows obtained by natural mating, at 10 to 70 days of gestation. Pesquisa Veterinária Brasileira 29, 859–862.Google Scholar
Neville, W, Mullinix, B, Smith, J and McCormick, W 1978. Growth patterns for pelvic dimensions and other body measurements of beef females. Journal of Animal Science 47, 1080–1088.CrossRefGoogle Scholar
NRC 2000. National research council: nutrient requirements of Beef cattle. National Academy Press, Washington, DC.Google Scholar
NRC 2001. National research council: nutrient requirements of dairy cattle. National Academy Press, Washington, DC.Google Scholar
Peugnet, P, Wimel, L, Duchamp, G, Sandersen, C, Camous, S, Guillaume, D, Dahirel, M, Dubois, C, Jouneau, L and Reigner, F 2014. Enhanced or reduced fetal growth induced by embryo transfer into smaller or larger breeds alters post-natal growth and metabolism in pre-weaning horses. PLoS One 9, e102044.CrossRefGoogle ScholarPubMed
Redmer, D, Wallace, J and Reynolds, L 2004. Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development. Domestic Animal Endocrinology 27, 199–217.CrossRefGoogle ScholarPubMed
Reynolds, L, Millaway, D, Kirsch, J, Infeld, J and Redmer, D 1990. Growth and in-vitro metabolism of placental tissues of cows from day 100 to day 250 of gestation. Journal of Reproduction and Fertility 89, 213–222.CrossRefGoogle ScholarPubMed
Reynolds, LP and Redmer, D 1995. Utero-placental vascular development and placental function. Journal of Animal Science 73, 1839–1851.CrossRefGoogle ScholarPubMed
Reynolds, LP, Caton, JS, Redmer, DA, Grazul-Bilska, AT, Vonnahme, KA, Borowicz, PP, Luther, JS, Wallace, JM, Wu, G and Spencer, TE 2006. Evidence for altered placental blood flow and vascularity in compromised pregnancies. Journal of Physiology 572, 51–58.CrossRefGoogle ScholarPubMed
Schlafer, D, Fisher, P and Davies, C 2000. The bovine placenta before and after birth: placental development and function in health and disease. Animal Reproduction Science 60, 145–160.CrossRefGoogle ScholarPubMed
Shahin, KA, Berg, RT and Price, MA 1991. Muscle and bone distribution in mature normal and double muscled cows. Livestock Production Science 28, 291–303.CrossRefGoogle Scholar
Tao, S, Bubolz, J, Do Amaral, B, Thompson, I, Hayen, M, Johnson, S and Dahl, G 2011. Effect of heat stress during the dry period on mammary gland development. Journal of Dairy Science 94, 5976–5986.CrossRefGoogle ScholarPubMed
Wallace, J, Bourke, D and Aitken, R 1998. Nutrition and fetal growth: paradoxical effects in the overnourished adolescent sheep. Journal of Reproduction and Fertility 54, 385–399.Google Scholar
Walton, A and Hammond, J 1938. The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proceedings of the Royal Society of London. Series B, Biological Sciences 125, 311–335.Google Scholar
Wooding, P and Burton, G 2008. Comparative placentation: structures, functions and evolution. Springer-Verlag, Berlin Heidelberg, Germany.CrossRefGoogle Scholar