Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T13:32:43.112Z Has data issue: false hasContentIssue false
  • English
  • Français

Growth and development of adipose tissue and gut and related endocrine status during early growth in the pig: impact of low birth weight

Published online by Cambridge University Press:  01 January 2008

A. Morise ,
I. Louveau  and
I. Le Huërou-Luron
A. Morise
Affiliation:
INRA, UMR1079, Systèmes d’Elevage Nutrition Animale et Humaine, F-35590 Saint Gilles, France
I. Louveau
Affiliation:
INRA, UMR1079, Systèmes d’Elevage Nutrition Animale et Humaine, F-35590 Saint Gilles, France
I. Le Huërou-Luron*
Affiliation:
INRA, UMR1079, Systèmes d’Elevage Nutrition Animale et Humaine, F-35590 Saint Gilles, France
*
E-mail: Isabelle.Luron@rennes.inra.fr
Get access

Abstract

With genetic selection, the increase in litter size has led to higher variation in within-litter birth weights in pigs. This has been associated with a reduction in mean birth weights and a rise in the proportion of piglets weighing less than 1 kg at birth. Low birth weight pigs exhibit lower postnatal growth rates and feed efficiency, which may be explained by an inadequate digestion and/or nutrient use as a consequence of prenatal undernutrition. It is now documented that there is a relationship between birth weight and subsequent pattern of growth and development of tissues and organs. During the neonatal period, the rapid somatic growth is accompanied by tremendous anatomical, physiological and chemical composition changes. The present review focuses primarily on the influence of low birth weight on adipose tissue and the gastrointestinal tract growth and development during the suckling period. The importance of the somatotropic axis, insulin, thyroid hormones, glucocorticoids, epidermal growth factor and leptin in the regulation of these developmental processes is also considered.

Keywords

adipose tissuebirth weightdigestive tracthormonespigs
Type
Full Paper
Information
animal , Volume 2 , Issue 1 , January 2008 , pp. 73 - 83
Copyright
Copyright © The Animal Consortium 2008

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

Ajuwon, KM, Kuske, JL, Ragland, D, Adeola, O, Hancock, DL, Anderson, DB, Spurlock, ME 2003. The regulation of IGF-1 by leptin in the pig is tissue specific and independent of changes in growth hormone. The Journal of Nutritional Biochemistry 14, 522–530.Google Scholar
Alexander, AN, Carey, HV 1999. Oral IGF-I enhances nutrient and electrolyte absorption in neonatal piglet intestine. The American Journal of Physiology 277, G619–G625.Google Scholar
Baker, J, Liu, JP, Robertson, EJ, Efstratiadis, A 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75, 73–82.Google Scholar
Barb, CR, Yan, X, Azain, MJ, Kraeling, RR, Rampacek, GB, Ramsay, TG 1998. Recombinant porcine leptin reduces feed intake and stimulates growth hormone secretion in swine. Domestic Animal Endocrinology 15, 77–86.CrossRefGoogle ScholarPubMed
Barb, CR, Hausman, GJ, Houseknecht, KL 2001. Biology of leptin in the pig. Domestic Animal Endocrinology 21, 297–317.CrossRefGoogle ScholarPubMed
Bauer, R, Walter, B, Hoppe, A, Gaser, E, Lampe, V, Kauf, E, Zwiener, U 1998. Body weight distribution and organ size in newborn swine (Sus scrofa domestica). A study describing an animal model for asymmetrical intrauterine growth retardation. Experimental Toxicology and Pathology 50, 59–65.Google Scholar
Bauer, R, Walter, B, Ihring, W, Kluge, H, Lampe, V, Zwiener, U 2000a. Altered renal function in growth-restricted newborn piglets. Pediatric Nephrology 14, 735–739.Google Scholar
Bauer, R, Wank, V, Walter, B, Blickhan, R, Zwiener, U 2000b. Reduced muscle vascular resistance in intrauterine growth restricted newborn piglets. Experimental Toxicology and Pathology 52, 271–276.Google Scholar
Bee, G 2004. Effect of early gestation feeding, birth weight and gender of progeny on muscle fiber characteristics of pigs at slaughter. Journal of Animal Science 82, 826–836.Google Scholar
Bell, A, Greenwood, P, Ehrhardt, 2005. Regulation of metabolism and growth during prenatal life. In Biology of metabolism in growing animals (ed. D Burrin and H Mersmann), pp. 3–34. Elsevier, Oxford, UK.Google Scholar
Berthon, D, Herpin, P, Le Dividich, J, Dauncey, MJ 1993. Modification of thermogenic capacity in neonatal pigs by changes in thyroid status during late gestation. Journal of Development and Physiology 19, 253–261.Google Scholar
Berthon, D, Herpin, P, Duchamp, C, Dauncey, MJ, Le Dividich, J 1996. Interactive effects of thermal environment and energy intake on thyroid hormone metabolism in newborn pigs. Biology of the Neonate 69, 51–59.Google Scholar
Biernat, M, Zabielski, R, Yao, G, Marion, J, Le Huërou-Luron, I, Le Dividich, J 2001. Effect of formula v. sow milk feeding on the gut morphology in neonatal piglets. In Digestive physiology of pigs (ed. JE Lindberg and B Ogle), pp. 43–45. CABI Publishing, Wallingford, UK.Google Scholar
Blennemann, B, Moon, YK, Freake, HC 1992. Tissue-specific regulation of fatty acid synthesis by thyroid hormone. Endocrinology 130, 637–643.Google Scholar
Boudry, G, Morise, A, Perrier, C, Sève, B, Luron, I 2006. L’allaitement artificiel modifie le développement post-natal de la barrière épithéliale intestinale et sa régulation nerveuse chez le porcelet de faible poids à la naissance. Nutrition clinique et métabolique 20, S102.Google Scholar
Breier, BH, Gluckman, PD, Blair, HT, McCutcheon, SN 1989. Somatotrophic receptors in hepatic tissue of the developing pig. The Journal of Endocrinology 123, 25–31.CrossRefGoogle Scholar
Burrin, DG, Wester, TJ, Davis, TA, Amick, S, Heath, JP 1996. Orally administered IGF-I increases intestinal mucosal growth in formula-fed neonatal pigs. The American Journal of Physiology 270, R1085–R1091.Google ScholarPubMed
Campbell, RG, Dunkin, AC 1982. The effect of birth weight on the estimated milk intake, growth and body composition of sow-reared piglets. Animal Production 35, 193–197.Google Scholar
Carroll, JA 2001. Dexamethasone treatment at birth enhances neonatal growth in swine. Domestic Animal Endocrinology 21, 97–109.CrossRefGoogle ScholarPubMed
Carroll, JA, Veum, TL, Matteri, RL 1998. Endocrine responses to weaning and changes in post-weaning diet in the young pig. Domestic Animal Endocrinology 15, 183–194.Google Scholar
Carroll, JA, Daniel, JA, Keisler, DH, Matteri, RL 2000. Postnatal function of the somatotrophic axis in pigs born naturally or by caesarian section. Domestic Animal Endocrinology 19, 39–52.Google Scholar
Chen, NX, Hausman, GJ, Wright, JT 1996. Hormonal regulation of insulin-like growth factor binding proteins and insulin-like growth factor I (IGF-I) secretion in porcine stromal-vascular cultures. Journal of Animal Science 74, 2369–2375.CrossRefGoogle ScholarPubMed
Chen, X, Lin, J, Hausman, DB, Martin, RJ, Dean, RG, Hausman, GJ 2000. Alterations in fetal adipose tissue leptin expression correlate with the development of adipose tissue. Biology of the Neonate 78, 41–47.Google Scholar
Dauncey, MJ 1997. From early nutrition and later development…to underlying mechanisms and optimal health. The British Journal of Nutrition 78, S113–S123.Google Scholar
Dauncey, MJ, Burton, KA, Tivey, DR 1994. Nutritional modulation of insulin-like growth factor-I expression in early postnatal piglets. Pediatric Research 36, 77–84.Google Scholar
Davis, TA, Fiorotto, ML, Burrin, DG, Pond, WG, Nguyen, HV 1997. Intrauterine growth restriction does not alter response of protein synthesis to feeding in newborn pigs. The American Journal of Physiology 272, E877–E884.Google Scholar
Duchamp, C, Burton, KA, Herpin, P, Dauncey, MJ 1994. Perinatal ontogeny of porcine nuclear thyroid hormone receptors and its modulation by thyroid status. The American Journal of Physiology 267, E687–E693.Google ScholarPubMed
Dunshea, FR, Chung, CS, Owens, PC, Ballard, JF, Walton, PE 2002. Insulin-like growth factor-I and analogues increase growth in artificially-reared neonatal pigs. The British Journal of Nutrition 87, 587–593.Google Scholar
Eckert, JE, Gatford, KL, Luxford, BG, Campbell, RG, Owens, PC 2000. Leptin expression in offspring is programmed by nutrition in pregnancy. The Journal of Endocrinology 165, R1–R6.Google Scholar
Estienne, MJ, Harper, AF, Barb, CR, Azain, MJ 2000. Concentrations of leptin in serum and milk collected from lactating sows differing in body condition. Domestic Animal Endocrinology 19, 275–280.CrossRefGoogle ScholarPubMed
Fholenhag, K, Malmlof, K, Skottner, A, Nyberg, F 1999. Effects of human growth hormone on the porto-arterial concentration differences of glucose and amino acids in the newborn piglet. Hormone Metabolism Research 31, 22–26.Google Scholar
Foxcroft, GR, Dixon, WT, Novak, S, Putman, CT, Town, SC, Vinsky, MDA 2006. The biological basis for prenatal programming of postnatal performance in pigs. Journal of Animal Science 84, E105–E112.CrossRefGoogle ScholarPubMed
Friedman, JM, Halaas, JL 1998. Leptin and the regulation of body weight in mammals. Nature 395, 763–770.Google Scholar
Gardan, D, Gondret, F, Louveau, I 2006. Lipid metabolism and secretory function of porcine intramuscular adipocytes in comparison with subcutaneous and perirenal adipocytes. The American Journal of Physiology – Endocrinology and Metabolism 291, E372–E380.CrossRefGoogle Scholar
Gondret, F, Lefaucheur, L, Louveau, I, Lebret, B, Pichodo, X, Le Cozler, Y 2005. Influence of piglet birth weight on postnatal growth performance, tissue lipogenic capacity, and muscle histological traits at market weight. Livestock Production Science 93, 137–146.Google Scholar
Gondret, F, Lefaucheur, L, Juin, H, Louveau, I, Lebret, L 2006. Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. Journal of Animal Science 84, 93–103.Google Scholar
Grégoire, F, Smas, CM, Sul, HS 1998. Understanding adipocyte differentiation. Physiological Reviews 78, 783–809.CrossRefGoogle ScholarPubMed
Grosvenor, CE, Picciano, MF, Baumrucker, CR 1993. Hormones and growth factors in milk. Endocrine Reviews 14, 710–728.Google Scholar
Hales, CN, Barker, DJP 1992. Type 2 (non-insulin dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.Google Scholar
Harrell, RJ, Thomas, MJ, Boyd, RD, Czerwinski, SM, Steele, NC, Bauman, DE 1999. Ontogenic maturation of the somatotropin/insulin-like growth factor axis. Journal of Animal Science 77, 2934–2941.Google Scholar
Hartsock, TG, Graves, HB, Baumgardt, BR 1977. Agonistic behavior and the nursing order in suckling pig: relationship with survival, growth and body composition. Journal of Animal Science 44, 320–330.Google Scholar
Hauser, N, Mourot, J, De Clercq, L, Genart, C, Remacle, C 1997. The cellularity of developing adipose tissues in Piétrain and Meishan pigs. Reproduction Nutrition Development 37, 617–626.Google Scholar
Hausman, GJ, Hausman, DB 1993. Endocrine regulation of porcine adipose tissue development: cellular and metabolic aspects. In Growth of the pig (ed. GR Hollis), pp. 49–73. CAB International, Wallingford, UK.Google Scholar
Hausman, GJ, Kauffman, RG 1986. The histology of developing porcine adipose tissue. Journal of Animal Science 63, 642–658.CrossRefGoogle ScholarPubMed
Hausman, GJ, Wright, JT 1996. Ontogeny of the response to thyroxine (T-4) in the porcine fetus: Interrelationships between serum T-4, serum insulin-like growth factor-1 (IGF-1) and differentiation of skin and several adipose tissues. Obesity Research 4, 283–292.Google Scholar
Hill, DJ, Milner, RD 1985. Insulin as a growth factor. Pediatric Research 19, 879–886.Google Scholar
Hodin, RA, Meng, S, Chambernain, SM 1994. Thyroid hormone responsiveness is developmentally regulated in the rat small intestine: a possible role for the alpha-2 receptor variant. Endocrinology 135, 564–568.CrossRefGoogle ScholarPubMed
Houle, VM, Schroeder, EA, Odle, J, Donovan, SM 1997. Small intestinal disaccharidase activity and ileal villus height are increased in piglets consuming formula containing recombinant human insulin-like growth factor-I. Pediatric Research 42, 78–86.Google Scholar
Huo, YJ, Wang, T, Xu, RJ, Macdonald, S, Liu, G, Shi, FX 2006. Dietary insulin affects leucine aminopeptidase, growth hormone, insulin-like growth factor I and insulin receptors in the intestinal mucosa of neonatal pigs. Biology of the Neonate 89, 265–273.CrossRefGoogle ScholarPubMed
Jaeger, LA, Lamar, CH 1992. Immunolocalization of epidermal growth factor (EGF) and EGF receptors in the porcine upper gastrointestinal tract. American Journal of Veterinary Research 53, 1685–1692.Google Scholar
Jaquet, D, Leger, J, Tabone, MD, Czernichow, P, Levy-Marchal, C 1999. High serum leptin concentrations during catch-up growth of children born with intrauterine growth retardation. The Journal of Clinical Endocrinology and Metabolism 84, 1949–1953.Google Scholar
Jones G, Edwards SA, Traver S, Jagger S and Hoste S, 1999. Body composition and changes in piglets at weaning to nutritional modification of sow milk composition and effect on post-weaning performance. Proceedings of the 50th Annual Meeting of the EAAP, Zürich, p. 5.Google Scholar
Kaciuba-Uscilko, H 1972. Hormonal regulation of thermogenesis in the new-born pig. The effect of ambient temperature on urinary catecholamine excretion. Biology of the Neonate 21, 245–258.CrossRefGoogle ScholarPubMed
Kajikawa, K, Yasui, W, Sumiyoshi, H, Yoshida, K, Nakayama, H, Ayhan, A, Yokozaki, H, Ito, H, Tahara, E 1991. Expression of epidermal growth factor in human tissues. Immunohistochemical and biochemical analysis. Virchows Archiv. A, Pathological Anatomy and Histology 418, 27–32.CrossRefGoogle ScholarPubMed
Kampman, KA, Ramsay, TG, White, ME 1993. Developmental changes in hepatic IGF-II and IGFBP-2 mRNA levels in intrauterine growth-retarded and control swine. Comparative Biochemistry and Physiology 104B, 415–421.Google Scholar
Kampman, KA, Ramsay, TG, White, ME 1994. Developmental changes in serum IGF-I and IGFBP levels and liver IGFBP-3 mRNA expression in intrauterine growth-retarded and control swine. Comparative Biochemistry and Physiology 108B, 337–347.Google Scholar
Kelly, D 1994. Colostrum, growth factors and intestinal development in pigs. In Digestive physiology in pigs (ed. WB Souffrant and H Hagemeister), pp. 151–166. EAAP Publication No80, Dummerstorf, Germany.Google Scholar
King, RH, Le Dividich, J, Dunshea, FR 1999. Lactation and neonatal growth. In A quantitative biology of the pig (ed. I Kyriazakis), pp. 155–180. CAB International, Oxon, UK.Google Scholar
Lawrence, TLJ, Fowler, VR 2002. Growth of farm animals, second edition. CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
Le Dividich, J 1999. A review. Neonatal and weaner pig: management to reduce variation. In Manipulating pig production VII (ed. PD Cranwell), pp. 135–155. Australasian Pig Science Association, Werribee.Google Scholar
Le Dividich, J, Tivey, D, Blum, JW, Strullu, F, Louat, C 1997. Effect of amount of ingested colostrum on the small intestine growth and lactase activity in the newborn pig. In Digestive Physiology in Pigs (ed. JP Laplace, C Février and A Barbeau), pp. 131–135. EAAP Publication no. 88, INRA, Paris, France.Google Scholar
Lee, CY, Bazer, FW, Etherton, TD, Simmen, FA 1991. Ontogeny of insulin-like growth factors (IGF-I and IGF-II) and IGF-binding proteins in porcine serum during fetal and postnatal development. Endocrinology 128, 2336–2344.Google Scholar
Lee, CY, Chung, CS, Simmen, FA 1993. Ontogeny of the porcine insulin-like growth factor system. Molecular and Cellular Endocrinology 93, 71–80.Google Scholar
Litten, JC, Mostyn, A, Perkins, KS, Corson, AM, Symonds, ME, Clarke, L 2005. Effect of administration of recombinant human leptin during the neonatal period on the plasma concentration and gene expression of leptin in the piglet. Biology of the Neonate 87, 1–7.Google Scholar
Louveau, I, Gondret, F 2004. Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system. Domestic Animal Endocrinology 27, 241–255.CrossRefGoogle ScholarPubMed
Louveau, I, Combes, S, Cochard, A, Bonneau, M 1996. Developmental changes in insulin-like growth factor-I (IGF-I) receptor levels and plasma IGF-I concentrations in Large White and Meishan pigs. General and Comparative Endocrinology 104, 29–36.Google Scholar
Maes, M, Ketelslegers, JM, Underwood, LE 1983. Low plasma somatomedin-C in streptozotocin-induced diabetes mellitus. Correlation with changes in somatogenic and lactogenic liver binding sites. Diabetes 32, 1060–1069.Google Scholar
Marion, J, Le Dividich, J 1999. Utilization of sow milk energy by the piglet. In Manipulating pig production VII (ed. PD Cranwell), pp. 254–260. SR Frankland Pty Ltd, Melbourne, Australia.Google Scholar
Martorell, R, Stein, AD, Schroeder, DG 2001. Early nutrition and later adiposity. The Journal of Nutrition 131, 874S–880S.Google Scholar
McMillen, IC, Robinson, JS 2005. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 85, 571–633.Google Scholar
Mersmann, H, Smith, SB 2005. Development of white adipose tissue lipid metabolism. In Biology of metabolism in growing animals (ed. DG Burrin and H Mersmann), pp. 275–302. Elsevier, London, UK.Google Scholar
Mersmann, HJ, Underwood, MC, Brown, LJ, Houk, JM 1973. Adipose tissue composition and lipogenic capacity in developing swine. The American Journal of Physiology 224, 1130–1135.CrossRefGoogle ScholarPubMed
Mersmann, HJ, Goodman, JR, Brown, LJ 1975. Development of swine adipose tissue: morphology and chemical composition. Journal of Lipid Research 16, 269–279.Google Scholar
Milligan, BN, Fraser, D, Kramer, DL 2002. Within-litter birth weight variation in the domestic pig and its relation to pre-weaning survival, weight gain, and variation in weaning diets. Livestock Production Science 76, 181–191.Google Scholar
Mills, SE 1999. Regulation of porcine adipocyte metabolism by insulin and adenosine. Journal of Animal Science 77, 3201–3207.CrossRefGoogle ScholarPubMed
Morgan, CJ, Coutts, AGP, McFadyen, MC, King, TP, Kelly, D 1996. Characterization of IGF-I receptors in the porcine small intestine during postnatal development. The Journal of Nutritional Biochemistry 7, 339–347.Google Scholar
Mostyn, A, Litten, JC, Perkins, KS, Euden, PJ, Corson, AM, Symonds, ME, Clarke, L 2005. Influence of size at birth on the endocrine profiles and expression of uncoupling proteins in subcutaneous adipose tissue, lung, and muscle of neonatal pigs. The American Journal of Physiology 288, R1536–R1542.Google Scholar
Murphy, VE, Smith, R, Giles, WB, Clifton, VL 2006. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocrine Reviews 27, 141–169.Google Scholar
Noblet, J, Etienne, M 1987. Body composition, metabolic rate and utilisation of milk nutrients in suckling piglets. Reproduction Nutrition Development 27, 829–839.Google Scholar
Ong, KK, Dunger, DB 2004. Birth weight, infant growth and insulin resistance. European Journal of Endocrinology 151 (Suppl. 3), U131–U139.Google Scholar
Peng, M, Palin, MF, Veronneau, S, Lebel, D, Pelletier, G 1997. Ontogeny of epidermal growth factor (EGF), EGF receptor (EGFR) and basic fibroblast growth factor (bFGF) mRNA levels in pancreas, liver, kidney, and skeletal muscle of pig. Domestic Animal Endocrinology 14, 286–294.Google Scholar
Phillips, LS, Young, HS 1976. Nutrition and somatomedin. II. Serum somatomedin activity and cartilage growth activity in streptozotocin-diabetic rats. Diabetes 25, 516–527.Google Scholar
Phillips, DI, Fall, CH, Cooper, C, Norman, RJ, Robinson, JS, Owens, PC 1999. Size at birth and plasma leptin concentrations in adult life. International Journal of Obesity and Related Metabolic Disorders 23, 1025–1029.Google Scholar
Poore, KR, 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, Fowden, AL 2003. The effect of birth weight on hypothalamo-pituitary-adrenal axis function in juvenile and adult pigs. The Journal of Physiology 547, 107–116.Google Scholar
Poore, KR, Fowden, AL 2004a. 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
Poore, KR, Fowden, AL 2004b. Insulin sensitivity in juvenile and adult Large White pigs of low and high birth weight. Diabetologia 47, 340–348.Google Scholar
Powell, SE, Aberle, ED 1980. Effects of birth weight on growth and carcass composition of swine. The Journal of Animal Science 50, 860–868.Google Scholar
Powell, SE, Aberle, ED 1981. Skeletal muscle and adipose tissue cellularity in runt and normal birth weight swine. Journal of Animal Science 52, 748–756.Google Scholar
Qian, H, Barb, CR, Compton, MM, Hausman, GJ, Azain, MJ, Kraeling, RR, Baile, CA 1999. Leptin mRNA expression and serum leptin concentrations as influenced by age, weight and estradiol in pigs. Domestic Animal Endocrinology 16, 135–143.CrossRefGoogle ScholarPubMed
Quiniou, N, Dagorn, J, Gaudré, D 2002. Variation of piglets’ birth weight and consequences on subsequent performance. Livestock Production Science 78, 63–70.Google Scholar
Ramsay, TG, Bush, JA, McMurtry, JP, Thivierge, MC, Davis, TA 2004. Peripheral leptin administration alters hormone and metabolite levels in the young pig. Comparative Biochemistry and Physiology A 138, 17–25.Google Scholar
Randall, GC 1983. Changes in the concentrations of corticosteroids in the blood of fetal pigs and their dams during late gestation and labor. Biology of Reproduction 29, 1077–1084.Google Scholar
Ranke, MB 1987. A note on adults with growth hormone deficiency. Acta Paediatrica Scandinavica Supplementum 331, 80–82.Google Scholar
Reeds, PG, Burrin, DG, Davis, TA, Fiorotto, MA, Mersmann, HJ, Pond, WG 1993. Growth regulation with reference to the pig. In Growth of the pig (ed. GR Hollis), pp. 1–32. CAB International, Wallingford, UK.Google Scholar
Rehfeldt, C, Kuhn, G 2006. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. Journal of Animal Science 84, E113–E123.Google Scholar
Ritacco, G, Radecki, SV, Schoknecht, PA 1997. Compensatory growth in runt pigs is not mediated by insulin-like growth factor-I. Journal of Animal Science 75, 1237–1243.Google Scholar
Romsos, DR, Leveille, GA, Allee, GL 1971a. Alloxan diabetes in the pig (Sus domesticus). Response to glucose, tolbutamide and insulin administration. Comparative Biochemistry and Physiology A 40, 557–568.Google Scholar
Romsos, DR, Leveille, GA, Allee, GL 1971b. In vitro lipogenesis in adipose tissue from alloxan-diabetic pigs (Sus domesticus). Comparative Biochemistry and Physiology A 40, 569–578.Google Scholar
Sangild, PT, Xu, RJ, Trahair, JF 2002. Maturation of intestinal function: the role of cortisol and birth. In Biology of the Intestine in Growing Animals (ed. R Zabielski, PC Gregory and B Weström), pp. 111–144. Elsevier, Oxford, UK.Google Scholar
Scanes, CG, Lazarus, D, Bowen, S, Buonomo, FC, Gilbreath, RL 1987. Postnatal changes in circulating concentrations of growth hormone, somatomedin C and thyroid hormones in pigs. Domestic Animal Endocrinology 4, 253–257.Google Scholar
Schnoebelen-Combes, S, Louveau, I, Postel-Vinay, MC, Bonneau, M 1996. Ontogeny of GH receptor and GH-binding protein in the pig. The Journal of Endocrinology 148, 249–255.CrossRefGoogle ScholarPubMed
Schober, DA, Simmen, FA, Hadsell, DL, Baumrucker, CR 1990. Perinatal expression of type I IGF receptors in porcine small intestine. Endocrinology 126, 1125–1132.Google Scholar
Schoknecht, PA, Ebner, S, Skottner, A, Burrin, DG, Davis, TA, Ellis, K, Pond, WG 1997. Exogenous insulin-like growth factor-I increases weight gain in intrauterine growth-retarded neonatal pigs. Pediatric Research 42, 201–207.Google Scholar
Serrero, G, Mills, D 1991. Physiological role of epidermal growth factor on adipose tissue development in vivo. Proceedings of the National Academy of Sciences of the United States of America 88, 3912–3916.CrossRefGoogle ScholarPubMed
Shulman, RJ 1990. Oral insulin increases small intestinal mass and disaccharidase activity in the newborn miniature pig. Pediatric Research 28, 171–175.Google Scholar
Shulman, RJ, Tivey, DR, Sunitha, I, Dudley, MA, Henning, SJ 1992. Effect of oral insulin on lactase activity, mRNA and posttranscriptional processing in the newborn pig. Journal of Pediatric Gastroenterology and Nutrition 14, 166–172.Google Scholar
Shulman, RJ, Wong, WW, Smith, EO 2005. Influence of changes in lactase activity and small-intestinal mucosal growth on lactose digestion and absorption in pre-term infants. The American Journal of Clinical Nutrition 81, 472–479.Google Scholar
Singhal, A, Farooqi, IS, O’Rahilly, S, Cole, TJ, Fewtrell, M, Lucas, A 2002. Early nutrition and leptin concentrations in later life. The American Journal of Clinical Nutrition 75, 993–999.Google Scholar
Slebodzinski, AB 1981. Sequential observation of changes in thyroxine, triiodothyronine and reverse triiodothyronine during the postnatal adaptation of the pig. Biology of the Neonate 39, 191–199.Google Scholar
Steele, NC, Etherton, TD 1983. Nutrient partitioning in the young pig as affected by dietary protein intake and insulin treatment. Journal of Animal Science 57, 208.Google Scholar
Symonds, ME, Pearce, S, Bispham, J, Gardner, DS, Stephenson, T 2004. Timing of nutrient restriction and programming of fetal adipose tissue development. The Proceedings of the Nutrition Society 63, 397–403.Google Scholar
Thieriot-Prevost, G, Boccara, JF, Francoual, C, Badoual, J, Job, JC 1988. Serum insulin-like growth factor 1 and serum growth-promoting activity during the first postnatal year in infants with intrauterine growth retardation. Pediatric Research 24, 380–383.Google Scholar
Tilley, RE, McNeil, CJ, Ashworth, CJ, Page, KR, McArdle, HJ 2007. Altered muscle development and expression of the insulin-like growth factor system in growth-retarded fetal pigs. Domestic Animal Endocrinology 32, 167–177.CrossRefGoogle ScholarPubMed
Vaughan, TJ, James, PS, Pascall, JC, Brown, KD 1992. Expression of the genes for TGF alpha, EGF and the EGF receptor during early pig development. Development 116, 663–669.Google Scholar
Vickers, MH, Reddy, S, Ikenasio, BA, Breier, BH 2001. Dysregulation of the adipoinsular axis – a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming. The Journal of Endocrinology 170, 323–332.Google Scholar
Vickers, MH, Gluckman, PD, Coveny, AH, Hofman, PL, Cutfield, WS, Gertler, A, Breier, BH, Harris, M 2005. Neonatal leptin treatment reverses developmental programming. Endocrinology 146, 4211–4216.Google Scholar
Wang, T, Huo, YJ, Shi, F, Xu, RJ, 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
Weström, BR, Ekman, R, Svendsen, L, Svendsen, J, Karlsson, BW 1987. Levels of immunoreactive insulin, neurotensin and bombesin in porcine colostrum and milk. Journal of Pediatric Gastroenterology and Nutrition 6, 460–465.Google ScholarPubMed
Widdowson, EM 1971. Intra-uterine growth retardation in the pig. I. Organ size and cellular development at birth and after growth to maturity. Biology of the Neonate 19, 329–340.Google Scholar
Wolinski, J, Biernat, M, Guilloteau, P, Weström, BR, Zabielski, R 2003. Exogenous leptin controls the development of the small intestine in neonatal piglets. The Journal of Endocrinology 177, 215–222.Google Scholar
Wolter, BF, Ellis, M, Corrigan, BP, DeDecker, JM 2002. The effect of birth weight on feeding of supplemental milk replacer to piglets during lactation on pre-weaning and post-weaning growth performance and carcass characteristics. Journal of Animal Science 80, 301–308.Google Scholar
Wu, G, Bazer, FW, Wallace, JM, Spencer, TE 2006. Intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science 84, 2316–2337.Google Scholar
Xu, RJ 1996. Development of the newborn GI tract and its relation to colostrum/milk intake: a review. Reproduction Fertility Development 8, 35–48.Google Scholar
Xu, RJ, Mellor, DJ, Birtles, MJ, Reynolds, GW, 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
Xu, RJ, Wang, F, Zhang, SH 2000. Postnatal adaptation of the gastrointestinal tract in neonatal pigs: a possible role of milk-borne growth factors. Livestock Production Science 66, 95–107.Google Scholar
Zabielski, R, Laubitz, D, Wolinski, J, Guilloteau, P 2005. Nutritional and hormonal control of gut epithelium remodeling in neonatal piglets. Journal of Animal Feeding Sciences 14, 99–112.Google Scholar
Zijlstra, RT, Odle, J, Hall, WF, Petschow, BW, Gelberg, HB, Litov, RE 1994. Effect of orally administered epidermal growth factor on intestinal recovery of neonatal pigs infected with rotavirus. Journal of Pediatric Gastroenterology and Nutrition 19, 382–390.Google Scholar