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Animals : an open access journal from MDPI2021; 11(12); doi: 10.3390/ani11123337

Age-Dependent Intestinal Repair: Implications for Foals with Severe Colic.

Abstract: Colic is a leading cause of death in horses, with the most fatal form being strangulating obstruction which directly damages the intestinal barrier. Following surgical intervention, it is imperative that the intestinal barrier rapidly repairs to prevent translocation of gut bacteria and their products and ensure survival of the patient. Age-related disparities in survival have been noted in many species, including horses, humans, and pigs, with younger patients suffering poorer clinical outcomes. Maintenance and repair of the intestinal barrier is regulated by a complex mucosal microenvironment, of which the ENS, and particularly a developing network of subepithelial enteric glial cells, may be of particular importance in neonates with colic. Postnatal development of an immature enteric glial cell network is thought to be driven by the microbial colonization of the gut and therefore modulated by diet-influenced changes in bacterial populations early in life. Here, we review the current understanding of the roles of the gut microbiome, nutrition, stress, and the ENS in maturation of intestinal repair mechanisms after foaling and how this may influence age-dependent outcomes in equine colic cases.
Publication Date: 2021-11-23 PubMed ID: 34944114PubMed Central: PMC8697879DOI: 10.3390/ani11123337Google Scholar: Lookup
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  • Journal Article
  • Review

Summary

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This research article explores the age-related differences in the ability of the intestinal barrier in horses to repair, particularly after surgical intervention following severe colic. It emphasizes the roles of the gut microbiome, nutrition, stress, and the enteric nervous system in this process.

Introduction to the Problem

  • The article departs from the observation that colic is a major cause of death in horses, particularly the form known as strangulating obstruction that severely damages the intestinal barrier.
  • This issue necessitates surgical interventions, after which quick repair of the intestinal barrier is crucial to avoid translocation of gut bacteria and to ensure the patients’ survival.
  • Significantly, the authors note that survival rates vary by age across different species, including horses, humans, and pigs. Younger patients seem to have a worse clinical prognosis.

Role of Enteric Glial Cells and the ENS

  • The research emphasizes the role of the enteric nervous system (ENS) and enteric glial cells in maintaining and healing the intestinal barrier.
  • In particular, the development of the enteric glial cell network in neonates undergoing colic may be key to understanding their condition.
  • The article suggests that the postnatal maturation of these cells is largely driven by the microbial colonization of the gut, which can be modulated by diet-influenced changes in gut bacteria early in life.

The Gut Microbiome, Nutrition, Stress and Colic

  • The authors review current understanding of how the gut microbiome, nutrition, and stress impact the maturation of intestinal repair mechanisms, especially after birth (foaling).
  • They highlight that these factors might play a significant role in explaining age-dependent outcomes in horses suffering from colic.
  • Although the article does not detail specific nutritional or stress-related interventions, the understanding gained from this review might pave the way for more effective treatment strategies for equine colic in the future.

Cite This Article

APA
Erwin SJ, Blikslager AT, Ziegler AL. (2021). Age-Dependent Intestinal Repair: Implications for Foals with Severe Colic. Animals (Basel), 11(12). https://doi.org/10.3390/ani11123337

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 12

Researcher Affiliations

Erwin, Sara J
  • College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27607, USA.
Blikslager, Anthony T
  • College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27607, USA.
Ziegler, Amanda L
  • College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27607, USA.

Grant Funding

  • R01 HD095876 / NIH HHS
  • P30 DK034987 / NIDDK NIH HHS
  • P30 DK034987 / NIH HHS
  • L40 OD028437 / NIH HHS
  • K01 OD028207 / NIH HHS
  • AFRI-006609 / United States Department of Agriculture
  • R01 HD095876 / NICHD NIH HHS

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 75 references
  1. . Baseline Reference of Equine Health and Management in the United States, 2015. .
  2. Vatistas NJ, Snyder JR, Wilson WD, Drake C, Hildebrand S. Surgical treatment for colic in the foal (67 cases): 1980–1992. Equine Vet. J. 1996;28:139–145.
  3. Ziegler AL, Pridgen TA, Mills JK, Gonzalez LM, Van Landeghem L, Odle J, Blikslager AT. Epithelial restitution defect in neonatal jejunum is rescued by juvenile mucosal homogenate in a pig model of intestinal ischemic injury and repair. PLoS ONE 2018;13:e0200674.
  4. Mannoia K, Boskovic DS, Slater L, Plank MS, Angeles DM, Gollin G. Necrotizing enterocolitis is associated with neonatal intestinal injury. J. Pediatr. Surg. 2011;46:81–85.
  5. Lim JC, Golden JM, Ford HR. Pathogenesis of neonatal necrotizing enterocolitis. Pediatr. Surg. Int. 2015;31:509–518.
    doi: 10.1007/s00383-015-3697-9pubmed: 25854935google scholar: lookup
  6. Alvarez J, Sarradell J, Morrison R, Perez A. Impact of Porcine Epidemic Diarrhea on Performance of Growing Pigs. PLoS ONE 2015;10:e0120532.
  7. Cavin JB, Cuddihey H, Macnaughton WK, Sharkey K. Acute regulation of intestinal ion transport and permeability in response to luminal nutrients: The role of the enteric nervous system. Am. J. Physiol. Liver Physiol. 2020;318:G254–G264.
    doi: 10.1152/ajpgi.00186.2019pubmed: 31709828google scholar: lookup
  8. Martini E, Krug SM, Siegmund B, Neurath MF, Becker C. Mend Your Fences: The Epithelial Barrier and its Relationship With Mucosal Immunity in Inflammatory Bowel Disease. Cell. Mol. Gastroenterol. Hepatol. 2017;4:33–46.
    pmc: PMC5439240pubmed: 28560287
  9. McCann C, Alves MM, Brosens E, Natarajan D, Perin S, Chapman C, Hofstra RM, Burns AJ, Thapar N. Neuronal Development and Onset of Electrical Activity in the Human Enteric Nervous System. Gastroenterology 2019;156:1483–1495.e6.
    doi: 10.1053/j.gastro.2018.12.020pubmed: 30610864google scholar: lookup
  10. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am. J. Physiol. Content. 1997;273:C1378–C1385.
  11. White NA, Moore JN, Mair TS. Equine Acute Abdomen. CRC Press; Boca Raton, FL, USA: 2009.
  12. Granger DN, Holm L, Kvietys P. The Gastrointestinal Circulation: Physiology and Pathophysiology. Compreh. Physiol. 2015;5:1541–1583.
    doi: 10.1002/cphy.c150007pubmed: 26140727google scholar: lookup
  13. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. Intestinal Mucosal Lesion in Low-Flow States. Arch. Surg. 1970;101:478–483.
  14. Bellamy JEC, Nielsen NO, Latshaw WK. The Vascular Architecture of the Porcine Small Intestine. Can. J. Comp. Med. Rev. Can. Med. Comp. 1973;37:56–62.
    pmc: PMC1319725pubmed: 4119674
  15. Aharinejad S, Lametschwandtner A, Franz P, Firbas W. The vascularization of the digestive tract studied by scanning electron microscopy with special emphasis on the teeth, esophagus, stomach, small and large intestine, pancreas, and liver. Scanning Microsc. 1991;5:811–849.
    pubmed: 1808716
  16. Blikslager AT, Moeser A, Gookin J, Jones S, Odle J. Restoration of Barrier Function in Injured Intestinal Mucosa. Physiol. Rev. 2007;87:545–564.
    doi: 10.1152/physrev.00012.2006pubmed: 17429041google scholar: lookup
  17. Derikx JPM, Matthijsen RA, De Bruïne AP, Van Bijnen AA, Heineman E, Van Dam RM, DeJong CHC, Buurman WA. Rapid Reversal of Human Intestinal Ischemia-Reperfusion Induced Damage by Shedding of Injured Enterocytes and Reepithelialisation. PLoS ONE 2008;3:e3428.
  18. Li Q, Zhang Q, Wang C, Liu X, Qu L, Gu L, Li N, Li J. Altered distribution of tight junction proteins after intestinal ischaemia/reperfusion injury in rats. J. Cell. Mol. Med. 2009;13:4061–4076.
  19. Moore RM, Muir WW, Granger DN. Mechanisms of Gastrointestinal Ischemia-Reperfusion Injury and Potential Therapeutic Interventions: A Review and Its Implications in the Horse. J. Veter. Intern. Med. 1995;9:115–132.
  20. Blikslager AT, Roberts MC, Gerard MP, A Argenzio R. How important is intestinal reperfusion injury in horses?. J. Am. Veter. Med. Assoc. 1997;211:1387–1389.
    pubmed: 9394886
  21. Kalogeris T, Baines CP, Krenz M, Korthuis RJ. Cell Biology of Ischemia/Reperfusion Injury. Int. Rev. Cell Mol. Biol. 2012;298:229–317.
  22. Feil W, Lacy ER, Wong Y-MM, Burger D, Wenzl E, Starlinger M, Schiessel R. Rapid epithelial restitution of human and rabbit colonic mucosa. Gastroenterology 1989;97:685–701.
    doi: 10.1016/0016-5085(89)90640-9pubmed: 2753329google scholar: lookup
  23. Feil W, Wenzl E, Vattay P, Starlinger M, Sogukoglu T, Schiessel R. Repair of rabbit duodenal mucosa after acid injury in vivo and in vitro. Gastroenterology 1987;92:1973–1986.
    doi: 10.1016/0016-5085(87)90632-9pubmed: 3569771google scholar: lookup
  24. Nusrat A, Delp C, Madara JL. Intestinal epithelial restitution. Characterization of a cell culture model and mapping of cytoskeletal elements in migrating cells. J. Clin. Investig. 1992;89:1501–1511.
    doi: 10.1172/JCI115741pmc: PMC443021pubmed: 1569187google scholar: lookup
  25. Jin Y, Blikslager AT. Myosin light chain kinase mediates intestinal barrier dysfunction via occludin endocytosis during anoxia/reoxygenation injury. Am. J. Physiol. Physiol. 2016;311:C996–C1004.
    doi: 10.1152/ajpcell.00113.2016pubmed: 27760753google scholar: lookup
  26. Stamatovic SM, Johnson AM, Sladojevic N, Keep RF, Andjelkovic AV. Endocytosis of tight junction proteins and the regulation of degradation and recycling. Ann. N. Y. Acad. Sci. 2017;1397:54–65.
    doi: 10.1111/nyas.13346pmc: PMC5479724pubmed: 28415156google scholar: lookup
  27. Quiros M, Feier D, Birkl D, Agarwal R, Zhou DW, García AJ, Parkos CA, Nusrat A. Resolvin E1 is a pro-repair molecule that promotes intestinal epithelial wound healing. Proc. Natl. Acad. Sci. USA 2020;117:9477–9482.
    doi: 10.1073/pnas.1921335117pmc: PMC7197018pubmed: 32300016google scholar: lookup
  28. Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T, Zheng X, Ichinose S, Nagaishi T, Okamoto R, Tsuchiya K. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 2012;18:618–623.
    doi: 10.1038/nm.2695pubmed: 22406745google scholar: lookup
  29. Pohl CS, Medland JE, Moeser AJ. Early-life stress origins of gastrointestinal disease: Animal models, intestinal pathophysiology, and translational implications. Am. J. Physiol. Liver Physiol. 2015;309:G927–G941.
    doi: 10.1152/ajpgi.00206.2015pmc: PMC4683303pubmed: 26451004google scholar: lookup
  30. Smith F, Clark JE, Overman BL, Tozel CC, Huang JH, Rivier JEF, Blisklager AT, Moeser AJ. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am. J. Physiol. Liver Physiol. 2010;298:G352–G363.
    doi: 10.1152/ajpgi.00081.2009pmc: PMC2838512pubmed: 19926814google scholar: lookup
  31. Ziegler A, Gonzalez L, Blikslager A. Large Animal Models: The Key to Translational Discovery in Digestive Disease Research. Cell. Mol. Gastroenterol. Hepatol. 2016;2:716–724.
    doi: 10.1016/j.jcmgh.2016.09.003pmc: PMC5235339pubmed: 28090566google scholar: lookup
  32. Blikslager AT, Roberts MC, Rhoads J, A Argenzio R. Is reperfusion injury an important cause of mucosal damage after porcine intestinal ischemia?. Surgery 1997;121:526–534.
    doi: 10.1016/S0039-6060(97)90107-0pubmed: 9142151google scholar: lookup
  33. Pohl CS, Medland JE, Mackey E, Edwards LL, Bagley KD, Dewilde MP, Williams KJ, Moeser AJ. Early weaning stress induces chronic functional diarrhea, intestinal barrier defects, and increased mast cell activity in a porcine model of early life adversity. Neurogastroenterol. Motil. 2017;29:e13118.
    doi: 10.1111/nmo.13118pmc: PMC5650513pubmed: 28573751google scholar: lookup
  34. Medland JE, Pohl CS, Edwards LL, Frandsen S, Bagley K, Li Y, Moeser AJ. Early life adversity in piglets induces long-term upregulation of the enteric cholinergic nervous system and heightened, sex-specific secretomotor neuron responses. Neurogastroenterol. Motil. 2016;28:1317–1329.
    doi: 10.1111/nmo.12828pmc: PMC5002263pubmed: 27134125google scholar: lookup
  35. Furness JB. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol. 2012;9:286–294.
    doi: 10.1038/nrgastro.2012.32pubmed: 22392290google scholar: lookup
  36. Koliaraki V, Pallangyo CK, Greten FR, Kollias G. Mesenchymal Cells in Colon Cancer. Gastroenterology 2017;152:964–979.
    doi: 10.1053/j.gastro.2016.11.049pubmed: 28111227google scholar: lookup
  37. Gong W, Guo M, Han Z, Wang Y, Yang P, Xu C, Wang Q, Du L, Li Q, Zhao H. Mesenchymal stem cells stimulate intestinal stem cells to repair radiation-induced intestinal injury. Cell Death Dis. 2016;7:e2387.
    doi: 10.1038/cddis.2016.276pmc: PMC5059875pubmed: 27685631google scholar: lookup
  38. Sémont A, Mouiseddine M, François A, Demarquay C, Mathieu N, Chapel A, Saché A, Thierry D, Laloi P, Gourmelon P. Mesenchymal stem cells improve small intestinal integrity through regulation of endogenous epithelial cell homeostasis. Cell Death Differ. 2009;17:952–961.
    doi: 10.1038/cdd.2009.187pubmed: 20019749google scholar: lookup
  39. Ocansey DW, Wang L, Wang J, Yan Y, Qian H, Zhang X, Xu W, Mao F. Mesenchymal stem cell–gut microbiota interaction in the repair of inflammatory bowel disease: An enhanced therapeutic effect. Clin. Transl. Med. 2019;8:31.
    doi: 10.1186/s40169-019-0251-8pmc: PMC6928179pubmed: 31872304google scholar: lookup
  40. Swerlick RA, Lawley TJ. Role of Microvascular Endothelial Cells in Inflammation. J. Investig. Dermatol. 1993;100:S111–S115.
    doi: 10.1038/jid.1993.33pubmed: 8423379google scholar: lookup
  41. Saps M, Miranda A. Gastrointestinal Pharmacology. Mediat. Drugs Gastrointest. Motil. I. 2017;239:147–176.
    doi: 10.1007/164_2016_119pubmed: 28236087google scholar: lookup
  42. Tamburini S, Shen N, Wu HC, Clemente STNSJC. The microbiome in early life: Implications for health outcomes. Nat. Med. 2016;22:713–722.
    doi: 10.1038/nm.4142pubmed: 27387886google scholar: lookup
  43. Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG, Ilhan ZE, Challis C, Schretter CE, Rocha S, Gradinaru V. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson’s Disease. Cell. 2016;167:1469–1480.e12.
    doi: 10.1016/j.cell.2016.11.018pmc: PMC5718049pubmed: 27912057google scholar: lookup
  44. Qin X, Caputo FJ, Xu DZ, Deitch EA. Hydrophobicity of mucosal surface and its relationship to gut barrier function. Shock. 2008;29:372–376.
    doi: 10.1097/SHK.0b013e3181453f4epubmed: 17693944google scholar: lookup
  45. Rupani B, Caputo FJ, Watkins A, Vega D, Magnotti LJ, Lu Q, Xu DZ, Deitch EA. Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock. Surgery 2007;141:481–489.
    doi: 10.1016/j.surg.2006.10.008pubmed: 17383525google scholar: lookup
  46. Nagy N, Goldstein AM. Enteric nervous system development: A crest cell’s journey from neural tube to colon. Semin. Cell Dev. Biol. 2017;66:94–106.
  47. Yoo BB, Mazmanian SK. The Enteric Network: Interactions between the Immune and Nervous Systems of the Gut. Immunity 2017;46:910–926.
  48. Heuckeroth R, Pachnis V. Getting to the guts of enteric nervous system development. Development 2006;133:2287–2290.
    doi: 10.1242/dev.02418pubmed: 16720873google scholar: lookup
  49. Husso A, Jalanka J, Alipour MJ, Huhti P, Kareskoski M, Pessa-Morikawa T, Iivanainen A, Niku M. The composition of the perinatal intestinal microbiota in horse. Sci. Rep. 2020;10:1–12.
    doi: 10.1038/s41598-019-57003-8pmc: PMC6965133pubmed: 31949191google scholar: lookup
  50. Rose E, Odle J, Blikslager A, Ziegler A. Probiotics, Prebiotics and Epithelial Tight Junctions: A Promising Approach to Modulate Intestinal Barrier Function. Int. J. Mol. Sci. 2021;22:6729.
    doi: 10.3390/ijms22136729pmc: PMC8268081pubmed: 34201613google scholar: lookup
  51. Nighot M, Al-Sadi R, Guo S, Rawat M, Nighot P, Watterson MD, Ma TY. Lipopolysaccharide-Induced Increase in Intestinal Epithelial Tight Permeability Is Mediated by Toll-Like Receptor 4/Myeloid Differentiation Primary Response 88 (MyD88) Activation of Myosin Light Chain Kinase Expression. Am. J. Pathol. 2017;187:2698–2710.
  52. Ye L, Li G, Goebel A, Raju AV, Kong F, Lv Y, Li K, Zhu Y, Raja S, He P. Caspase-11–mediated enteric neuronal pyroptosis underlies Western diet–induced colonic dysmotility. J. Clin. Investig. 2020;130:3621–3636.
    doi: 10.1172/JCI130176pmc: PMC7324173pubmed: 32484462google scholar: lookup
  53. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 2007;19:59–69.
    doi: 10.1016/j.smim.2006.10.002pubmed: 17118672google scholar: lookup
  54. Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano G, Gasbarrini A, Mele M. What Is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019;7:14.
  55. Cossais F, Durand T, Chevalier J, Boudaud M, Kermarrec L, Aubert P, Neveu I, Naveilhan P, Neunlist M. Postnatal development of the myenteric glial network and its modulation by butyrate. Am. J. Physiol. Liver Physiol. 2016;310:G941–G951.
    doi: 10.1152/ajpgi.00232.2015pubmed: 27056724google scholar: lookup
  56. Kabouridis PS, Lasrado R, McCallum S, Chng SH, Snippert HJ, Clevers H, Pettersson S, Pachnis V. Microbiota Controls the Homeostasis of Glial Cells in the Gut Lamina Propria. Neuron 2015;85:289–295.
  57. Kabouridis PS, Pachnis V. Emerging roles of gut microbiota and the immune system in the development of the enteric nervous system. J. Clin. Investig. 2015;125:956–964.
    doi: 10.1172/JCI76308pmc: PMC4362252pubmed: 25729852google scholar: lookup
  58. Cammarota G, Ianiro G, Cianci R, Bibbò S, Gasbarrini A, Curro’ D. The involvement of gut microbiota in inflammatory bowel disease pathogenesis: Potential for therapy. Pharmacol. Ther. 2015;149:191–212.
  59. Scott FW, Pound LD, Patrick C, Eberhard CE, Crookshank JA. Where genes meet environment—integrating the role of gut luminal contents, immunity and pancreas in type 1 diabetes. Transl. Res. 2017;179:183–198.
    doi: 10.1016/j.trsl.2016.09.001pubmed: 27677687google scholar: lookup
  60. Losurdo G, Principi M, Iannone A, Ierardi E, Di Leo A. The Interaction Between Celiac Disease and Intestinal Microbiota. J. Clin. Gastroenterol. 2016;50:S145–S147.
    doi: 10.1097/MCG.0000000000000682pubmed: 27741160google scholar: lookup
  61. Tang WW, Hazen SL. The contributory role of gut microbiota in cardiovascular disease. J. Clin. Investig. 2014;124:4204–4211.
    doi: 10.1172/JCI72331pmc: PMC4215189pubmed: 25271725google scholar: lookup
  62. Fintl C, Lindberg R, Press CM. Myenteric networks of interstitial cells of Cajal are reduced in horses with inflammatory bowel disease. Equine Veter. J. 2020;52:298–304.
    doi: 10.1111/evj.13160pubmed: 31397916google scholar: lookup
  63. Mullen KR, Yasuda K, Divers TJ, Weese JS. Equine faecal microbiota transplant: Current knowledge, proposed guidelines and future directions. Equine Veter. Educ. 2016;30:151–160.
    doi: 10.1111/eve.12559pmc: PMC7159401pubmed: 32313396google scholar: lookup
  64. Garber A, Hastie P, Murray JA. Factors Influencing Equine Gut Microbiota: Current Knowledge. J. Equine Veter. Sci. 2020;88:102943.
    doi: 10.1016/j.jevs.2020.102943pubmed: 32303307google scholar: lookup
  65. Quercia S, Freccero F, Castagnetti C, Soverini M, Turroni S, Biagi E, Rampelli S, Lanci A, Mariella J, Chinellato E. Early colonisation and temporal dynamics of the gut microbial ecosystem in Standardbred foals. Equine Veter. J. 2019;51:231–237.
    doi: 10.1111/evj.12983pubmed: 29931762google scholar: lookup
  66. Costa MC, Stampfli HR, Allenvercoe E, Weese JS. Development of the faecal microbiota in foals. Equine Veter. J. 2016;48:681–688.
    doi: 10.1111/evj.12532pubmed: 26518456google scholar: lookup
  67. Van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, De Vos WM, Visser CE, Kuijper EJ, Bartelsman JFWM, Tijssen JGP. Duodenal Infusion of Donor Feces for Recurrent Clostridium difficile. N. Engl. J. Med. 2013;368:407–415.
    doi: 10.1056/NEJMoa1205037pubmed: 23323867google scholar: lookup
  68. Pothoulakis C, Lamont JT. Microbes and microbial toxins: Paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am. J. Physiol. Gastrointest. Liver Physiol. 2001;280:G178–G183.
    doi: 10.1152/ajpgi.2001.280.2.G178pubmed: 11208538google scholar: lookup
  69. Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell. Mol. Life Sci. 2013;70:631–659.
    doi: 10.1007/s00018-012-1070-xpmc: PMC11113843pubmed: 22782113google scholar: lookup
  70. Woliński J, Słupecka M, Weström B, Prykhodko O, Ochniewicz P, Arciszewski M, Ekblad E, Szwiec K, Ushakova, Skibo G. Effect of feeding colostrum versus exogenous immunoglobulin G on gastrointestinal structure and enteric nervous system in newborn pigs1. J. Anim. Sci. 2012;90:327–330.
    doi: 10.2527/jas.53926pubmed: 23365369google scholar: lookup
  71. Jacobi SK, Odle J. Nutritinal Factors Influencing Intestinal Health of the Neonate. Adv. Nutr. 2012;3:687–696.
    doi: 10.3945/an.112.002683pmc: PMC3648750pubmed: 22983847google scholar: lookup
  72. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 2011;108((Suppl. 1)):4578–4585.
    doi: 10.1073/pnas.1000081107pmc: PMC3063592pubmed: 20668239google scholar: lookup
  73. Moeser A, Klok CV, Ryan KA, Wooten JG, Little D, Cook VL, Blikslager A. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am. J. Physiol. Liver Physiol. 2007;292:G173–G181.
    doi: 10.1152/ajpgi.00197.2006pubmed: 16901995google scholar: lookup
  74. Lansade L, Foury A, Reigner F, Vidament M, Guettier E, Bouvet G, Soulet D, Parias C, Ruet A, Mach N. Progressive habituation to separation alleviates the negative effects of weaning in the mother and foal. Psychoneuroendocrinology 2018;97:59–68.
  75. Ziegler AL, Pridgen TA, Blikslager AT. Environmental stressors affect intestinal permeability and repair responses in a pig intestinal ischemia model. Tissue Barriers 2020;8:1832421.

Citations

This article has been cited 1 times.
  1. Gomez DE, Wong D, MacNicol J, Dembek K. The fecal bacterial microbiota of healthy and sick newborn foals. J Vet Intern Med 2023 Jan;37(1):315-322.
    doi: 10.1111/jvim.16596pubmed: 36519210google scholar: lookup