0.857
IF5
0.900
IF
Q3
JCR
0.92
CiteScore
0.405
SJR
Q2
SJR
20
MNiSW
142.18
ICV
REVIEW PAPER
 
CC-BY 4.0
 
 

The contribution of vacuolated foetal-type enterocytes in the process of maturation of the small intestine in piglets. Invited review

T. Skrzypek 1  ,  
K. Ferenc 3,  
 
1
John Paul II Catholic University of Lublin, Center for Interdisciplinary Research, Department of Biotechnology and Environmental Sciences, Laboratory of Confocal and Electron Microscopy, 20-708 Lublin, Poland
2
University of Life Sciences in Lublin, Faculty of Veterinary Medicine, Department of Animal Physiology, 20-950 Lublin, Poland
3
Warsaw University of Life Sciences – SGGW, Faculty of Veterinary Medicine, Department of Large Animal Diseases with Clinic, 02-776 Warsaw, Poland
4
John Paul II Catholic University of Lublin, Center for Interdisciplinary Research, Department of Biotechnology and Environmental Sciences, Laboratory of Biocontrol, Production and Application of Entomopathogenic Nematodes, 20-708 Lublin, Poland
5
University of Life Sciences in Lublin, Faculty of Veterinary Medicine, Institute of Biological Bases of Animal Diseases, Sub-Department of Parasitology and Invasive Diseases, 20-950 Lublin, Poland
J. Anim. Feed Sci. 2018;27(3):187–201
Publish date: 2018-08-31
KEYWORDS:
TOPICS:
ABSTRACT:
In neonates the vacuolated foetal-type enterocytes (VFE) play a key role in the transport of intact colostral and milk proteins from the lumen of the small intestine into the circulation and/or in the intracellular digestion of intestinal nutrients. The absorption of intact colostral macromolecules (including immunoglobulins, hormones and bioactive peptides) is important in the development of the immune and digestive systems of newborn piglets. The digestion of the intestinal content inside the VFE supports the luminal digestion of nutrients. The presence of apical canalicular system, which produces both the transport and the digestive vacuoles, is a key feature of VFE. The VFEs are gradually replaced by adult-type enterocytes. VFEs disappear gradually from the proximal part of the small intestine to the ileum. VFEs containing large (also referred to as giant) transport vacuoles disappear within the first 2–3 days after birth. VFEs containing digestive vacuoles are present for up to week 3 of life. In contrast, VFEs of intrauterine growth retarded piglets show abnormalities in their development of the apical area. The loss of VFEs is a good marker of the small intestine epithelium maturation.
CORRESPONDING AUTHOR:
T. Skrzypek   
John Paul II Catholic University of Lublin, Center for Interdisciplinary Research, Department of Biotechnology and Environmental Sciences, Laboratory of Confocal and Electron Microscopy, 20-708 Lublin, Poland
 
REFERENCES (90):
1. Amdi C., Krogh U., Flummer C., Oksbjerg N., Hansen C.F., Theil P.K., 2013. Intrauterine growth restricted piglets defined by their head shape ingest insufficient amounts of colostrum. J. Anim. Sci. 91, 5605–5613, https://doi.org/10.2527/jas.20....
2. Anderson C.L., Chaudhury C., Kim J., Bronson C.L., Wani M.A., Mohanty S., 2006. Perspective – FcRn transports album: relevance to immunology medicine. Trends Immunol. 27, 343–348, https://doi.org/10.1016/j.it.2....
3. Anderson J.M., Van Itallie C.M., 1995. Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J. Physiol.-Gastroint. Liver Physiol. 269, G467–G475, https://doi.org/10.1152/ajpgi.....
4. Bäckhed F., Roswall J., Peng Y. et al., 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690–703, https://doi.org/10.1016/j.chom....
5. Baintner K. (Editor), 1986. Intestinal Absorption of Macromolecules and Immune Transmission from Mother to Young. CRC Press. Boca Raton, FL (USA).
6. Baintner K., 1994. Demonstration of acidity in intestinal vacuoles of the suckling rat and pig. J. Histochem. Cytochem. 42, 231–238, https://doi.org/10.1177/42.2.7....
7. Baintner K., 2002. Vacuolation of the young. In: R. Zabielski, P.C. Gregory, B. Weström (Editors). Biology of the Intestine in Growing Animals. Elsevier. Amsterdam (The Netherlands), pp. 55–110, https://doi.org/10.1016/S1877-....
8. Baintner K., 2007. Transmission of antibodies from mother to young: evolutionary strategies in a proteolytic environment Vet. Immunol. Immunopathol. 117, 153–161, https://doi.org/10.1016/j.veti....
9. Bandrick M., Ariza-Nieto C., Baidoo S.K., Molitor T.W., 2014. Colostral antibody-mediated and cell-mediated immunity contributes to innate and antigen-specific immunity in piglets. Dev. Comp. Immunol. 43, 114–120, https://doi.org/10.1136/gut.37....
10. Bardocz S., Grant G., Ewen S.W.B., Duguid T.J., Brown D.S., Englyst K., Pusztai A., 1995. Reversible effect of phytohaemagglutinin on the growth and metabolism of rat gastrointestinal tract. Gut 37, 353–360, https://doi.org/10.1016/S1877-....
11. Bardocz S., Grant G., Pusztai A., Franklin M.F., Carvalho A.D.F.U., 1996. The effect of phytohaemagglutinin at different dietary concentration on the growth, body compositions and plasma insulin of the rat. Br. J. Nutr. 76, 613–626, https://doi.org/10.1079/BJN199....
12. Benias P.C., Wells R.G., Sackey-Aboagye B. et al., 2018. Structure and distribution of an unrecognized interstitium in human tissues. Sci. Rep. 8, 4947, https://doi.org/10.1038/s41598....
13. Biernat M., 2002. Factors regulating the growth and maturation of the structure and function of the small intestine of the piglets in the early postnatal period. PhD Thesis. The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences. Jabłonna (Poland).
14. Biernat M., Zabielski R., Sysa P., Sosak-Swiderska B., Le Huërou-Luron I., Guilloteau P., 1999. Small intestinal and pancreatic microstructures are modified by an intraduodenal CCK-A receptor antagonist administration in neonatal calves. Regul. Pept. 85, 77–85, https://doi.org/10.1016/S0167-....
15. Brandtzaeg P., Krajci P., 1995. The enterocyte and immunoglobulin transport. In: S. Auricchio, R. Troncone, A. Ferguson (Editors). Mucosal Immunity and the Gut Epithelium: Interactions in Health and Disease. Series: Dynamic Nutrition Research, Volume 4. S. Karger AG. New York, NY (USA).
16. Burton K.A., Smith M.W., 1977. Endocytosis and immunoglobulin transport across the small intestine of the new-born pig. J. Physiol. 270, 473–488, https://doi.org/10.1113/jphysi....
17. Cera K.R., Mahan D.C., Cross R.F., Reinhart G.A., Whitmoyer R.E., 1988. Effect of age, weaning and postweaning diet on small intestinal growth and jejunal morphology in young swine. J. Anim. Sci. 66, 547–584, https://doi.org/10.2527/jas198....
18. Chastant-Maillard S., Freyburger L., Marcheteau E., Thoumire S., Ravier J.F., Reynaud K., 2012. Timing of the intestinal barrier closure in puppies. Reprod. Domest. Anim. 47, 190–193, https://doi.org/10.1111/rda.12....
19. Childs A.C., Mehta D.J., Gerner E.W., 2003. Polyamine-dependent gene expression. Cell. Mol. Life Sci. 60, 1394–1406, https://doi.org/10.1007/s00018....
20. Clarke R.M., Hardy R.N., 1971. Histological changes in the small intestine of the young pig and their relation to macromolecular uptake. J. Anat. 108, 63–77.
21. Danielsen E.M., Hansen G.H., 2016. Small molecule pinocytosis and clathrin-dependent endocytosis at the intestinal brush border: Two separate pathways into the enterocyte. Biochim. Biophys. Acta-Biomembr. 1858, 233–243, https://doi.org/10.1016/j.bbam....
22. Dekaney C.M., Bazer F.W., Jaeger L.A., 1997. Mucosal morphogenesis and cytodifferentiation in fetal porcine small intestine. Anat. Rec. 249, 517–523, https://doi.org/10.1002/(SICI)...<517::AID-AR12>3.0.CO;2-R.
23. Denno D.M., VanBuskirk K., Nelson Z.C., Musser C.A., Hay Burgess D.C., Tarr P.I., 2014. Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review. Clin. Infect. Dis. 59, Suppl. 4, S213–S219, https://doi.org/10.1093/cid/ci....
24. Dörfel M., Huber O., 2012. Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. J. Biomed. Biotechnol. 2012, 807356, https://doi.org/10.1155/2012/8....
25. Ekström G.M., Weström B.R., Telemo E., Karlsson B.W., 1988. The uptake of fluorescein-conjugated dextran 70,000 by the small intestinal epithelium of the young rat and pig in relation to macromolecular transmission into the blood. J. Dev. Physiol. 10, 227–233.
26. Elbrønd V.S., Weström B.R., 2007. The early postnatal pattern of vesicle formation in different regions of the porcine small intestine. Livest. Sci. 108, 142–145, https://doi.org/10.1016/j.livs....
27. Fasano A., Baudry B., Pumplin D.W., Wasserman S.S., Tall B.D., Ketley J.M., Kaper J.B., 1991. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc. Natl. Acad. Sci. U. S. A. 88, 5242–5246, https://doi.org/10.1073/pnas.8....
28. Ferenc K., Pilżys T., Skrzypek T. et al., 2017. Structure and function of enterocyte in intrauterine growth retarded pig neonates. Dis. Markers 2017, 5238134, https://doi.org/10.1155/2017/5....
29. Fujita M., Baba R., Shimamoto M., Sakuma Y., Fujimoto S., 2007. Molecular morphology of the digestive tract; macromolecules and food allergens are transferred intact across the intestinal absorptive cells during the neonatal-suckling period. Med. Mol. Morphol. 40, 1–7, https://doi.org/10.1007/s00795....
30. Fujita M., Reinhart F., Neutra M., 1990. Convergence of apical and basolateral endocytic pathways at the apical late endosomes in absorptive cells of suckling rat ileum in vivo. J. Cell Sci. 97, 385–394.
31. Galeano J.A.C., Herrera A.L., Suescún J.P., 2014. E. coli lipopolysaccharide decreases the expression of proteins of tight junctions in the jejunum of weaning piglets. Rev. Fac. Nac. Agron. 67, 7301–7310, https://doi.org/10.15446/rfnam....
32. Godlewski M.M., Słupecka M., Woliński J., Skrzypek T., Skrzypek H., Motyl T., Zabielski R., 2005. Into the unknown – the death pathways in the neonatal gut epithelium. J. Physiol. Pharmacol. 56, Suppl. 3, 7–24.
33. Górka P., Kowalski Z.M., Zabielski R., Guilloteau P., 2018. Use of butyrate to promote gastrointestinal tract development in calves. J. Dairy. Sci. 101, 4785–4800, https://doi.org/10.3168/jds.20....
34. Grognet J.-F., Duvaux-Ponter Ch., 1998. Acquisition of passive immunity in domestic ungulates. J. Anim. Feed Sci. 7, Suppl. 1, 93–114, https://doi.org/10.22358/jafs/....
35. Guilloteau P., Zabielski R., Hammon H.M., Metges C.C., 2010. Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr. Res. Rev. 23, 4–22, https://doi.org/10.1017/S09544....
36. Guyton A.C., Hall J.E., 1996. Digestion and absorption in the gastrointestinal tract. In: Textbook of Medical Physiology. 9th Edition. W.B. Saunders Co. Philadelphia, PA (USA).
37. Heird W.C., Schwarz S.M., Hansen I.H., 1984. Colostrum-induced enteric mucosal growth in beagle puppies. Pediatr. Res. 18, 512–515, https://doi.org/10.1203/000064....
38. Hollander D., 1992. The intestinal permeability barrier. A hypothesis as to its regulation and involvement in Crohn’s Disease. Scand. J. Gastroenterol. 27, 721–726, https://doi.org/10.3109/003655....
39. Jensen A.R., Elnif J., Burrin D.G., Sangild P.T., 2001. Development of intestinal immunoglobulin absorption and enzyme activities in neonatal pigs is diet dependent. J. Nutr. 131, 3259–3265, https://doi.org/10.1093/jn/131....
40. Kacskovics I., 2004. Fc receptors in livestock species. Vet. Immunol. Immunopathol. 102, 351–362, https://doi.org/10.1016/j.veti....
41. Kaouas M., Deloyer P., Gouders I., Peulen O., Dandrifosse G., 1997. Role of interleukin-1β, interleukin-6 and TNF-α in intestinal maturation induced by dietary spermine in rats. Endocrine 6, 187–194, https://doi.org/10.1007/BF0273....
42. Kelly D., Begbie R., King T.P., 1992. Postnatal intestinal development. In: M.A. Varley, P.E.V. Williams, T.L.J. Lawrence (Editors). Neonatal Survival and Growth. BSAP. Penicuik (UK), pp. 63–79.
43. Kotunia A., Woliński J., Laubitz D., Jurkowska M., Romé V., Guilloteau P., Zabielski R., 2004. Effect of sodium butyrate on the small intestine development in neonatal piglets fed [correction of feed] by artificial sow. J. Physiol. Pharmacol. 55, Suppl. 2, 59–68.
44. König J., Wells J., Cani P.D., García-Ródenas C.L., MacDonald T., Mercenier A., Whyte J., Troost F., Brummer R.-J., 2016. Human intestinal barrier function in health and disease. Clin. Transl. Gastroenterol. 7, e196, https://doi.org/10.1038/ctg.20....
45. Lecce J.G., 1973. Effect of dietary regimen on cessation of uptake of macromolecules by piglet intestinal epithelium (closure) and transport to the blood. J. Nutr. 103, 751–756, https://doi.org/10.1093/jn/103....
46. Lecce J.G., Broughton C.W., 1973. Cessation of uptake of macromolecules by neonatal guinea pig, hamster and rabbit intestinal epithelium (closure) and transport into blood. J. Nutr. 103, 744–750, https://doi.org/10.1093/jn/103....
47. Lecce J.G., Morgan D.O., 1962. Effect of dietary regimen on cessation of intestinal absorption of large molecules (closure) in the neonatal pig and lamb. J. Nutr. 78, 263–268, https://doi.org/10.1093/jn/78.....
48. Marques T.M., Wall R., Ross R.P., Fitzgerald G.F., Ryan C.A., Stanton C., 2010. Programming infant gut microbiota: influence of dietary and environmental factors. Curr. Opin. Biotechnol. 21, 149–156, https://doi.org/10.1016/j.copb....
49. McCarter S.D., Johnson D.L., Kitt K.N., Donohue C., Adams A., Wilson J.M., 2010. Regulation of tight junction assembly and epithelial polarity by a resident protein of apical endosomes. Traffic 11, 856–866, https://doi.org/10.1111/j.1600....
50. Michanek P., Ventrop M., Weström B., 1989. Intestinal transmission of colostral antibodies in newborn dairy calves: Initiation of closure by feeding colostrum. Swed. J. Agric. Res. 19, 125–134.
51. Mickiewicz M., Zabielski R., Grenier B., Le Normand L., Savary G., Holst J.J., Oswald I.P., Metges C.C., Guilloteau P., 2012. Structural and functional development of small intestine in intrauterine growth retarded porcine offspring born to gilts fed diets with differing protein ratios throughout pregnancy. J. Physiol. Pharmacol. 63, 225–239.
52. Moon H.W., 1972. Vacuolated villous epithelium of the small intestine of young pigs. Vet. Pathol. 9, 3–12, https://doi.org/10.1177/030098....
53. Moretti D.B., Nordi W.M., Lima A.L., Pauletti P., Machado-Neto R., 2013. Enterocyte IgG uptake in the small intestine of goat kids during the period of passive immunity acquisition. Small Ruminant Res. 114, 182–187, https://doi.org/10.1016/j.smal....
54. Muza-Moons M.M., Schneeberger E.E., Hecht G.A., 2004. Enteropathogenic Escherichia coli infection leads to appearance of aberrant tight junctions strands in the lateral membrane of intestinal epithelial cells. Cell. Microbiol. 6, 783–793, https://doi.org/10.1111/j.1462....
55. Nechvatalova K., Kudlackova H., Leva L., Babickova K., Faldyna M., 2011. Transfer of humoral and cell-mediated immunity via colostrum in pigs. Vet. Immunol. Immunopathol. 142, 95–100, https://doi.org/10.1016/j.veti....
56. Neu J., Shenoy V., Chakrabarti R., 1996. Glutamine nutrition and metabolism: Where do we go from here? FASEB J. 10, 829–837, https://doi.org/10.1096/fasebj....
57. Pasternak A.J., Hamonic G.M., Van Kessel A., Wilson H.L., 2016. Postnatal regulation of MAMDC4 in the porcine intestinal epithelium is influenced by bacterial colonization. Physiol. Rep. 4, e13018, https://doi.org/10.14814/phy2.....
58. Pasternak J.A., Kent-Dennis C., Van Kessel A.G., Wilson H.L., 2015. Claudin-4 undergoes age-dependent change in cellular localization on pig jejunal villous epithelial cells, independent of bacterial colonization. Mediat. Inflamm. 2015, e263629, https://doi.org/10.1155/2015/2....
59. Patel R.M., Myers L.S., Kurundkar A.R., Maheshwari A., Nusrat A., Lin P.W., 2012. Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am. J. Pathol. 180, 626–635, https://doi.org/10.1016/j.ajpa....
60. Pierzynowski S.G., Sjodin A., 1998. Perspectives of glutamine and its derivatives as feed additives for farm animals. J. Anim. Feed Sci. 7, Suppl. 1, 79–91, https://doi.org/10.22358/jafs/....
61. Pluske J., Hampson D., Williams I.H., 1997. Factors influencing the structure and function of the small intestine in weaned pigs: a review. Livest. Prod. Sci. 51, 215–236, https://doi.org/10.1016/S0301-....
62. Rådberg K., Biernat M., Linderoth A., Zabielski R., Pierzynowski S.G., Weström B.R., 2001. Enternal exposure to crude red kidney bean lectin induces maturation of the gut in suckling pigs. J. Anim. Sci. 79, 2669–2678, https://doi.org/10.2527/2001.7....
63. Salmon H., 2012. Colostral and lactogenic maternal immunity: Humoral and cellular factors of induction and transmission to the neonate. In: B. Rekik (Editor). Milk Production. Food Science and Technology Series. Nova Science Publishers. Hauppauge, NY (USA), pp. 37–73.
64. Salmon H., Berri M., Gerdts V., Meurens F., 2009. Humoral and cellular factors of maternal immunity in swine. Dev. Comp. Immunol. 33, 384–393, https://doi.org/10.1016/j.dci.....
65. Sangild P.T., 2001. Transitions in the life of the gut at birth. In: J.E. Lindberg, B. Ogle (Editors). Digestive Physiology of Pigs. Proceedings of the 8th Symposium, Swedish University of Agricultural Sciences, Uppsala, Sweden, 20–22 June 2000. CABI Publishing. Wallingford (UK), pp. 3–16, https://doi.org/10.1079/978085....
66. Sangild P.T., 2003. Uptake of colostral immunoglobulins by the compromised newborn farm animal. Acta Vet. Scand. 44, Suppl. 1, S105, https://doi.org/10.1186/1751-0....
67. Sangild P.T., Xu R.J., Trahair J.F., 2002. Maturation of intestinal function: the role of cortisol and birth. In: R. Zabielski, P.C. Gregory, B.R. Weström (Editors). Biology of the Small Intestine in Growing Animals. Elsevier. Amsterdam (The Netherlands), pp. 111–144, https://doi.org/10.1016/S1877-....
68. Seiler N., Raul F., 2005. Polyamines and apoptosis. J. Cell. Mol. Med. 9, 632–642, https://doi.org/10.1111/j.1582....
69. Simister N.E., 2003. Placental transport of immunoglobulin G. Vaccine 21, 3365–3369, https://doi.org/10.1016/S0264-....
70. Skrzypek T., Valverde Piedra J.L., Skrzypek H., Kazimierczak W., Biernat M., Zabielski R., 2007a. Gradual disappearance of vacuolated enterocytes in the small intestine of neonatal piglets. J. Physiol. Pharmacol. 58, Suppl. 3, 87–95.
71. Skrzypek T., Valvedre Piedra J.L., Skrzypek H., Kazimierczak W., Szymańczyk S., Pawłowska M., Zabielski R., 2007b. Intestinal villi structure during the development of pig and wild boar crossbreed neonates. Livest. Sci. 109, 38–41, https://doi.org/10.1016/j.livs....
72. Skrzypek T., Valverde Piedra J.L., Skrzypek H., Woliński J., Kazimierczak W., Szymańczyk S., Pawłowska M., Zabielski R., 2005. Light and scanning electron microscopy evaluation of the postnatal small intestinal mucosa development in pigs. J. Physiol. Pharmacol. 56, Suppl. 3, 71–87.
73. Skrzypek T., Kazimierczak W., Skrzypek H., Valverde Piedra J.L., Godlewski M.M., Zabielski R., 2018. Mechanisms involved in the development of the small intestine mucosal layer in postnatal piglets. J. Physiol. Pharmacol. 69, 127–138, https://doi.org/10.26402/jpp.2....
74. Svendsen L.S., Weström B.R., Svendsen J., Ohlsson B.G., Ekman R., Karlsson B.W., 1986. Insulin involvement in intestinal macromolecular transmission and closure in neonatal pigs. J. Pediatr. Gastroenterol. Nutr. 5, 299–304, https://doi.org/10.1097/000051....
75. Teichberg S., Wapnir R.A., Moyse J., Lifshitz F., 1992. Development of the neonatal rat small intestinal barrier to nonspecific macromolecular absorption. II. Role of dietary corticosterone. Pediatr. Res. 32, 50–57, https://doi.org/10.1203/000064....
76. Trahair J.F., 1993. Review: Is fetal enteral nutrition important for normal gastrointestinal growth? A discussion. J. Parenter. Enter. Nutr. 17, 82–85, https://doi.org/10.1177/014860....
77. Trahair J.F., Sangild P.T., 1997. Systemic and luminal influences on the perinatal development of the gut. Equine Vet. J. 29, Suppl. 24, 40–50, https://doi.org/10.1111/j.2042....
78. Travis S., Menzies I., 1992. Intestinal permeability: functional assessment and significance. Clin. Sci. 82, 471–488, https://doi.org/10.1042/cs0820....
79. Tyler H., Ramsey H., 1993. Effect of insulin-induced hypoglycemia on cessation of macromolecular transport in the neonatal calf. J. Dairy Sci. 76, 2736–2741, https://doi.org/10.3168/jds.S0....
80. Vukavić T., 1984. Timing of the gut closure. J. Pediatr. Gastroenterol. Nutr. 3, 700–703, https://doi.org/10.1097/000051....
81. Wang W., Degroote J., Van Ginneken C., Van Poucke M., Vergauwen H., Dam T.M.T., Vanrompay D., Peelman L.J., De Smet S., Michiels J., 2016. Intrauterine growth restriction in neonatal piglets affects small intestinal mucosal permeability and mRNA expression of redox-sensitive genes. FASEB J. 30, 863–873, https://doi.org/10.1096/fj.15-....
82. Wang X., Lin G., Liu C., Feng. C., Zhou H., Wang T., Li D., Wu G., Wang J., 2014. Temporal proteomic analysis reveals defects in small-intestinal development of porcine fetuses with intrauterine growth restriction. J. Nutr. Biochem. 25, 785–795, https://doi.org/10.1016/j.jnut....
83. Weaver L.T., Walker W.A., 1989. Uptake of macromolecules in the neonate. In: E. Lebenthal, (Editor). Human Gastrointestinal Development. Raven Press, New York (USA), pp. 731–748.
84. Weström B.R., Svendsen J., Ohlsson B.G., Tagesson C., Karlsson B.W., 1984. Intestinal transmission of macromolecules (BSA and FITC-labelled dextran) in the neonatal pig: influence of age of piglet and molecular weight of markers. Biol. Neonate. 46, 20–26, https://doi.org/10.1159/000242....
85. Widdowson E.M., Colombo V.E., Artavanis C.A., 1976. Changes in the organs of pigs in response to feeding for the first 24 h after birth. II. The digestive tract. Biol. Neonate. 28, 272–281, https://doi.org/10.1159/000240....
86. Wilson J.M., Whitney J.A., Neutra M.R., 1987. Identification of an endosomal antigen specific to absorptive cells of suckling rat ileum. J. Cell Biol. 105, 691–703, https://doi.org/10.1083/jcb.10....
87. Xu R.J., Mellor D.J., Tungthanathanich P., Birtles M.J., Reynolds G.W., Simpson H.V., 1992. Growth and morphological changes in the small intestine in piglets during the first three days after birth. J. Dev. Physiol. 18, 161–172.
88. Yamashiro Y., Sato M., Shimizu T., Oguchi S., Maruyama K., Kitamura S., 1989. Possible biological growth factors in breast milk and postnatal development of the gastrointestinal tract. Pediatr. Int. 31, 417–423, https://doi.org/10.1111/j.1442....
89. Zabielski R., 1998. Regulatory peptides in milk, food and in the gastrointestinal lumen of young animals and children. J. Anim. Feed Sci. 7, 65–78, https://doi.org/10.22358/jafs/....
90. Zabielski R., 2007. Hormonal and neural regulation of intestinal function in pigs. Livest. Sci. 108, 32–40, https://doi.org/10.1016/j.livs....
Copy url
Share
 
 
ISSN:1230-1388