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Ghrelin in the gastrointestinal tract and blood circulation of perinatal low and normal weight piglets

Published online by Cambridge University Press:  18 November 2013

S. A. Willemen ,
M. De Vos ,
V. Huygelen ,
E. Fransen ,
B. R. Tambuyzer ,
C. Casteleyn ,
S. Van Cruchten  and
C. Van Ginneken
S. A. Willemen
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
M. De Vos
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
V. Huygelen
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
E. Fransen
Affiliation:
StatUa Center for Statistics, University of Antwerp, Prinsstraat 13, 2000 Antwerp, Belgium
B. R. Tambuyzer
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
C. Casteleyn
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
S. Van Cruchten
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
C. Van Ginneken*
Affiliation:
Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
*
†E-mail: [email protected]
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Abstract

Ghrelin, the ‘hunger’ hormone, is an endogenous growth hormone secretagogue that exerts a wide range of physiological functions. Its perinatal presence suggests that ghrelin might be involved in growth and metabolism processes during intrauterine and postnatal life. Intrauterine growth-restricted (IUGR) neonates have altered endocrine and metabolic pathways because of malnutrition during foetal development. These changes might include an altered gastrointestinal presence of ghrelin cells (GCs). As ghrelin is mainly secreted by the stomach, this altered presence might be reflected in its serum concentrations. Small-for-gestational age (SGA) pigs appear to be a natural occurring model for IUGR children. Therefore, the first aim of this study was to investigate the presence of gastrointestinal GCs expressing active ghrelin in normal weight (NW) foetal and postnatal piglets compared with their SGA littermates using immunohistochemical analysis in combination with stereological methods. Second, total ghrelin serum concentrations of these piglets were analysed with a porcine radioactive immunoassay. In addition, the growth of the gastric pars fundica in the NW and SGA piglets was analysed stereologically. Corresponding with humans and rats, it was shown that opened- and closed-type immunoreactive GCs are distributed along the entire gastrointestinal tract of the perinatal NW and SGA piglets. However, in contrast to the rat’s stomach, the porcine GCs do not disperse from the glandular base to the glandular neck during perinatal development. Furthermore, stereological analysis demonstrated that the NW neonates have a higher amount of gastric cells expressing active ghrelin compared with the SGA piglets that could result in higher milk consumption during the neonatal period. This finding is, however, not reflected in total serum ghrelin levels, which showed no difference between the NW and SGA piglets. Moreover, the stereological volume densities of the fundic layers demonstrate a similar growth pattern in the SGA and NW piglets.

Keywords

ghrelingastrointestinal systemlow birth weightperinatal periodpig
Type
Physiology and functional biology of systems
Information
animal , Volume 7 , Issue 12 , December 2013 , pp. 1978 - 1984
Copyright
Copyright © The Animal Consortium 2013 

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References

Aydin, S, Ozkan, Y and Kumru, S 2006. Ghrelin is present in human colostrum, transitional and mature milk. Peptides 27, 878–882.Google Scholar
Barker, DJ 1998. In utero programming of chronic disease. Clinical Science 95, 115–128.CrossRefGoogle ScholarPubMed
Cooper, JE 1975. The use of the pig as an animal model to study problems associated with low birthweight. Laboratory Animals 9, 329–336.Google Scholar
Depassille, AMB, Rushen, J and Hartsock, TG 1988. Ontogeny of teat fidelity in pigs and its relation to competition at suckling. Canadian Journal of Animal Science 68, 325–338.Google Scholar
Devillers, N, Farmer, C, Le Dividich, J and Prunier, A 2007. Variability of colostrum yield and colostrum intake in pigs. Animal 1, 1033–1041.Google Scholar
D’Inca, R, Kloareg, M, Gras-Le Guen, C and Le Huerou-Luron, I 2010b. Intrauterine growth restriction modifies the developmental pattern of intestinal structure, transcriptomic profile, and bacterial colonization in neonatal pigs. The Journal of Nutrition 140, 925–931.Google Scholar
D’Inca, R, Che, L, Thymann, T, Sangild, PT and Le Huerou-Luron, I 2010a. Intrauterine growth restriction reduces intestinal structure and modifies the response to colostrum in preterm and term piglets. Livestock Science 133, 20–22.Google Scholar
Du, GM, Shi, ZM, Wei, XH, Liu, MJ, Zhang, L and Zhao, RQ 2007. Expression of gastric ghrelin and H(+)-K(+)-ATPase mRNA in weanling piglets and effects of ghrelin on H(+)-K(+)-ATPase expression and activity in gastric mucosal cells in vitro. Research in Veterinary Science 82, 99–104.CrossRefGoogle Scholar
Evans, HE and Sack, WO 1973. Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Zentralblatt für Veterinärmedicin C 2, 11–45.Google Scholar
Farquhar, J, Heiman, M, Wong, AC, Wach, R, Chessex, P and Chanoine, JP 2003. Elevated umbilical cord ghrelin levels in small for gestational age neonates. Journal of Clinical Endocrinology and Metabolism 88 4324–4327.CrossRefGoogle ScholarPubMed
Frappier, BL 2006. Digestive system. In Dellmann's textbook of veterinary histology, 6th edition (ed. Eurell, JA and Frappier, BL), p. 187. Blackwell Publishing, Iowa, US.Google Scholar
Gundersen, HJ and Jensen, EB 1987. The efficiency of systematic sampling in stereology and its prediction. Journal of Microscopy 147, 229–263.Google Scholar
Hales, CN and Barker, DJ 1992. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.Google Scholar
Hayashida, T, Murakami, K, Mogi, K, Nishihara, M, Nakazato, M, Mondal, MS, Horii, Y, Kojima, M, Kangawa, K and Murakami, N 2001. Ghrelin in domestic animals: distribution in stomach and its possible role. Domestic Animal Endocrinology 21, 17–24.Google Scholar
Hendrix, WF, Kelley, KW, Gaskins, CT and Hinrichs, DJ 1978. Porcine neonatal survival and serum gamma globulins. Journal of Animal Science 47, 1281–1286.Google Scholar
Kojima, M, Hosoda, H, Date, Y, Nakazato, M, Matsuo, H and Kangawa, K 1999. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402, 656–660.Google Scholar
Kotunia, A and Zabielski, R 2006. Ghrelin in the postnatal development of the gastrointestinal tract. Journal of Physiology and Pharmacology 57 (suppl. 5), 97–111.Google Scholar
Kyriakakou, M, Malamitsi-Puchner, A, Mastorakos, G, Boutsikou, T, Hassiakos, D, Papassotiriou, I and Kanaka-Gantenbein, C 2009. The role of IGF-1 and ghrelin in the compensation of intrauterine growth restriction. Reproductive Sciences 16, 1193–1200.Google Scholar
Lee, MJ, Conner, EL, Charafeddine, L, Woods, JR Jr and Del Priore, G 2001. A critical birth weight and other determinants of survival for infants with severe intrauterine growth restriction. Annals of the New York Academy of Sciences 943, 326–339.Google Scholar
Lewis, NJ and Hurnik, JF 1986. An approach response of piglets to the sows nursing vocalizations. Canadian Journal of Animal Science 66, 537–539.Google Scholar
Milligan, BN, Fraser, D and Kramer, DL 2001. Birth weight variation in the domestic pig: effects on offspring survival, weight gain and suckling behaviour. Applied Animal Behaviour Science 73, 179–191.Google Scholar
Poore, KR and Fowden, AL 2002. The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age. Diabetologia 45, 1247–1254.Google Scholar
Poore, KR and Fowden, AL 2004. The effects of birth weight and postnatal growth patterns on fat depth and plasma leptin concentrations in juvenile and adult pigs. The Journal of Physiology 558, 295–304.Google Scholar
Rindi, G, Necchi, V, Savio, A, Torsello, A, Zoli, M, Locatelli, V, Raimondo, F, Cocchi, D and Solcia, E 2002. Characterisation of gastric ghrelin cells in man and other mammals: studies in adult and fetal tissues. Histochemistry and Cell Biology 117, 511–519.CrossRefGoogle ScholarPubMed
Sakata, I, Nakamura, K, Yamazaki, M, Matsubara, M, Hayashi, Y, Kangawa, K and Sakai, T 2002a. Ghrelin-producing cells exist as two types of cells, closed- and opened-type cells, in the rat gastrointestinal tract. Peptides 23, 531–536.Google Scholar
Sakata, I, Tanaka, T, Matsubara, M, Yamazaki, M, Tani, S, Hayashi, Y, Kangawa, K and Sakai, T 2002b. Postnatal changes in ghrelin mRNA expression and in ghrelin-producing cells in the rat stomach. Journal of Endocrinology 174, 463–471.Google Scholar
Salfen, BE, Carroll, JA, Keissler, DH and Strauch, TA 2004. Effects of exogenous ghrelin on feed intake, weight gain, behavior, and endocrine responses in weanling pigs. Journal of Animal Science 82, 1957–1966.Google Scholar
Sangild, PT 2006. Gut responses to enteral nutrition in preterm infants and animals. Experimental Biology and Medicine 231, 1695–1711.Google Scholar
Slupecka, M, Wolinski, J and Pierzynowski, SG 2012. The effects of enteral ghrelin administration on the remodeling of the small intestinal mucosa in neonatal piglets. Regulatory Peptides 174, 38–45.CrossRefGoogle ScholarPubMed
Toshinai, K, Yamaguchi, H, Sun, Y, Smith, RG, Yamanaka, A, Sakurai, T, Date, Y, Mondal, MS, Shimbara, T and Kawagoe, T 2006. Des-acyl ghrelin induces food intake by a mechanism independent of the growth hormone secretagogue receptor. Endocrinology 147, 2306–2314.Google Scholar
Vitari, F, Di Giancamillo, A, Deponti, D, Carollo, V and Domeneghini, C 2012. Distribution of ghrelin-producing cells in the gastrointestinal tract of pigs at different ages. Veterinary Research Communications 36, 71–80.Google Scholar
Wang, T, Huo, YJ, Shi, F, Xu, RJ and Hutz, RJ 2005. Effects of intrauterine growth retardation on development of the gastrointestinal tract in neonatal pigs. Biology of the Neonate 88, 66–72.Google Scholar
Wierup, N, Bjorkqvist, M, Westrom, B, Pierzynowski, S, Sundler, F and Sjolund, K 2007. Ghrelin and motilin are cosecreted from a prominent endocrine cell population in the small intestine. Journal of Clinical Endocrinology and Metabolism 92, 3573–3581.Google Scholar
Xu, RJ, Mellor, DJ, Birtles, MJ, Reynolds, GW and Simpson, HV 1994. Impact of intrauterine growth retardation on the gastrointestinal tract and the pancreas in newborn pigs. Journal of Pediatric Gastroenterology and Nutrition 18, 231–240.Google Scholar
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