{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T11:53:47Z","timestamp":1783511627393,"version":"3.55.0"},"reference-count":33,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2017\/25\/B\/NZ4\/02668"],"award-info":[{"award-number":["2017\/25\/B\/NZ4\/02668"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100008530","name":"European Regional Development Fund","doi-asserted-by":"publisher","award":["RPO WM2007-2013"],"award-info":[{"award-number":["RPO WM2007-2013"]}],"id":[{"id":"10.13039\/501100008530","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Intrauterine growth restricted (IUGR) piglets are born at term but have low birth mass and a characteristic shape of the head. Impaired general condition, especially in intestinal function, leads to an increase in the occurrence of diarrhoea and high mortality in the first days of life. So far, the mechanical and immunological gut barrier functions in IUGR are poorly understood. The aim of this study was to microscopically evaluate the early postnatal changes in the gut mucosa occurring in IUGR piglets. Whole-tissue small intestine samples were collected from littermate pairs (IUGR and normal) on postnatal day (PD) 7, 14 and 180 and analysed by light microscopy. We found that in the IUGR piglets, the percentage of intraepithelial leukocytes was reduced in the duodenum on PD 7, but it increased in the proximal and middle jejunum both on PD 7 and PD 14, which suggested the development of an inflammatory process. The number of goblet cells was also reduced on PD 14. The average size of the Peyer\u2019s patches in the distal jejunum and ileum showed significant reduction on PD 7 as compared to normal pigs; however, on PD 14, it returned to normal. On PD 180, we did not find any differences in the measured parameters between the IUGR and the normal pigs. In conclusion, we found that in one-week-old IUGR pig neonates, the gut barrier and the immune system structures display signs of retarded development but recover within the second postnatal week of life.<\/jats:p>","DOI":"10.3390\/ani11040990","type":"journal-article","created":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T10:44:01Z","timestamp":1617273841000},"page":"990","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Differences in Intestinal Barrier Development between Intrauterine Growth Restricted and Normal Birth Weight Piglets"],"prefix":"10.3390","volume":"11","author":[{"given":"Jaros\u0142aw","family":"Olszewski","sequence":"first","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1725-9783","authenticated-orcid":false,"given":"Romuald","family":"Zabielski","sequence":"additional","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1836-3734","authenticated-orcid":false,"given":"Tomasz","family":"Skrzypek","sequence":"additional","affiliation":[{"name":"Interdisciplinary Research Center, The John Paul II Catholic University of Lublin, 20-950 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Piotr","family":"Matyba","sequence":"additional","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ma\u0142gorzata","family":"Wierzbicka","sequence":"additional","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antoni","family":"Adamski","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawi\u0144skiego 5a, 02-106 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7833-7602","authenticated-orcid":false,"given":"El\u017cbieta","family":"Grzesiuk","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawi\u0144skiego 5a, 02-106 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Sady","sequence":"additional","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8779-5050","authenticated-orcid":false,"given":"Zdzis\u0142aw","family":"Gajewski","sequence":"additional","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0100-9328","authenticated-orcid":false,"given":"Karolina","family":"Ferenc","sequence":"additional","affiliation":[{"name":"Veterinary Research Centre, Centre for Biomedicine Research, Centre for Regenerative Medicine, Department of Large Animal Diseases and Clinic, Institute for Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska 100, 02-797 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.repbio.2014.01.005","article-title":"Intrauterine growth retarded piglet as a model for humans\u2014Studies on the perinatal development of the gut structure and function","volume":"14","author":"Ferenc","year":"2014","journal-title":"Reprod. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Matyba, P., Florowski, T., Dasiewicz, K., Ferenc, K., Olszewski, J., Trela, M., Galemba, G., S\u0142owi\u0144ski, M., Sady, M., and Doma\u0144ska, D. (2021). Performance and Meat Quality of Intrauterine Growth Restricted Pigs. Animals, 11.","DOI":"10.3390\/ani11020254"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2017\/5238134","article-title":"Structure and Function of Enterocyte in Intrauterine Growth Retarded Pig Neonates","volume":"3","author":"Ferenc","year":"2017","journal-title":"Dis. Markers"},{"key":"ref_4","first-page":"225","article-title":"Structural and functional development of small intestine in intrauterine growth retarded porcine offspring born to gilts fed diets with differing protein ratios throughout pregnancy","volume":"63","author":"Mickiewicz","year":"2012","journal-title":"J. Physiol. Pharmacol."},{"key":"ref_5","first-page":"87","article-title":"Gradual disappearance of vacuolated enterocytes in the small intestine of neonatal piglets","volume":"58","author":"Skrzypek","year":"2007","journal-title":"J. Physiol. Pharmacol."},{"key":"ref_6","first-page":"127","article-title":"Mechanisms involved in the development of the small intestine mucosal layer in postnatal piglets","volume":"69","author":"Skrzypek","year":"2018","journal-title":"J. Physiol. Pharmacol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"187","DOI":"10.22358\/jafs\/94167\/2018","article-title":"The contribution of vacuolated foetal-type enterocytes in the process of maturation of the small intestine in piglets. Invited review","volume":"27","author":"Skrzypek","year":"2018","journal-title":"J. Anim. Feed Sci."},{"key":"ref_8","unstructured":"Ferenc, K., Pietrzak, P., Wierzbicka, M., Matyba, P., Grzesiuk, E., Gajewski, Z., and Zabielski, R. (2018). Alterations in the liver of intrauterine growth retarded piglets may predispose to development of insulin resistance and obesity in later life. J. Physiol. Pharmacol., 69."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1369\/0022155414532655","article-title":"Intrauterine growth restriction impairs small intestinal mucosal immunity in neonatal piglets","volume":"62","author":"Dong","year":"2014","journal-title":"J. Histochem. Cytochem."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"925","DOI":"10.3945\/jn.109.116822","article-title":"Intrauterine growth restriction modifies the developmental pattern of intestinal structure. transcriptomic profile. and bacterial colonization in neonatal pigs","volume":"140","author":"Kloareg","year":"2010","journal-title":"J. Nutr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"713","DOI":"10.2174\/1389203720666190124165243","article-title":"Intrauterine growth restriction alters the genome-wide DNA methylation profiles in small intestine. liver and longissimus dorsi muscle of newborn piglets","volume":"20","author":"Tao","year":"2019","journal-title":"Curr. Protein Pept. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/s10142-019-00714-y","article-title":"Membrane proteomic analysis reveals the intestinal development is deteriorated by intrauterine growth restriction in piglets","volume":"20","author":"Huang","year":"2020","journal-title":"Funct. Integr. Genom."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1096\/fj.15-274779","article-title":"Intrauterine growth restriction in neonatal piglets affects small intestinal mucosal permeability and mRNA expression of redox-sensitive genes","volume":"30","author":"Wang","year":"2016","journal-title":"FASEB J."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1152\/ajpgi.00020.2017","article-title":"MicroRNA-29a mediates the impairment of intestinal epithelial integrity induced by intrauterine growth restriction in pig","volume":"312","author":"Zhu","year":"2017","journal-title":"Am. J. Physiol. -Gastrointest. Liver Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5605","DOI":"10.2527\/jas.2013-6824","article-title":"Intrauterine growth restricted piglets defined by their head shape ingest insufficient amounts of colostrum","volume":"91","author":"Amdi","year":"2013","journal-title":"J. Anim. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4991","DOI":"10.2527\/jas.2012-5740","article-title":"Individual physical characteristics of neonatal piglets affect preweaning survival of piglets born in a noncrated system","volume":"91","author":"Hales","year":"2013","journal-title":"J. Anim. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1017\/S0007114515001579","article-title":"Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction","volume":"114","author":"Hu","year":"2015","journal-title":"Br. J. Nutr."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.nut.2018.07.114","article-title":"l-Threonine improves intestinal mucin synthesis and immune function of intrauterine growth\u2013retarded weanling piglets","volume":"59","author":"Zhang","year":"2019","journal-title":"Nutrition"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1021\/pr900747d","article-title":"Temporal Proteomic Analysis Reveals Continuous Impairment of Intestinal Development in Neonatal Piglets with Intrauterine Growth Restriction","volume":"9","author":"Wang","year":"2010","journal-title":"J. Proteome Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1007\/s12275-019-8690-x","article-title":"Characteristics of the gut microbiota colonization, inflammatory profile, and plasma metabolome in intrauterine growth restricted piglets during the first 12 hours after birth","volume":"57","author":"Huang","year":"2019","journal-title":"J. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4683","DOI":"10.1038\/s41598-020-61623-w","article-title":"Intrauterine growth restriction in piglets alters blood cell counts and impairs cytokine responses in peripheral mononuclear cells 24 days post-partum","volume":"10","author":"Amdi","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Zhang, H., Chen, Y., Li, Y., and Wang, T. (2020). Protective Effect of Polydatin on Jejunal Mucosal Integrity, Redox Status, Inflammatory Response, and Mitochondrial Function in Intrauterine Growth-Retarded Weanling Piglets. Oxidative Med. Cell. Longev., 7178123.","DOI":"10.1155\/2020\/7178123"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"630","DOI":"10.3389\/fimmu.2015.00630","article-title":"Weaning Markedly Affects Transcriptome Profiles and Peyer\u2019s Patch Development in Piglet Ileum","volume":"6","author":"Inoue","year":"2015","journal-title":"Front. Immunol."},{"key":"ref_24","first-page":"269","article-title":"The Mammary Gland in Mucosal and Regional Immunity","volume":"2","author":"Butler","year":"2015","journal-title":"Mucosal Immunol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1051\/animres:2004020","article-title":"Postnatal development of intestinal immune system in piglets: Implications for the process of weaning","volume":"53","author":"Stokes","year":"2004","journal-title":"Anim. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1046\/j.1365-3083.1999.00557.x","article-title":"The influence of age and breeding conditions on the number and proliferation of intraepithelial lymphocytes in pigs","volume":"50","author":"Pabst","year":"1999","journal-title":"Scand. J. Immunol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1046\/j.1365-2567.2000.00013.x","article-title":"Antibody repertoire development in fetal and newborn piglets, III. Colonization of the gastrointestinal tract selectively diversifies the preimmune repertoire in mucosal lymphoid tissues","volume":"100","author":"Butler","year":"2000","journal-title":"Immunology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/j.chom.2012.09.009","article-title":"Intestinal Commensal Microbes as Immune Modulators","volume":"12","author":"Ivaylo","year":"2012","journal-title":"Cell Host Microbe"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1111\/rda.13463","article-title":"The challenge of large litters on the immune system of the sow and the piglets","volume":"54","author":"Oliviero","year":"2019","journal-title":"Reprod. Dom. Anim."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1038\/nri2707","article-title":"Toll-like receptor signalling in the intestinal epithelium: How bacterial recognition shapes intestinal function","volume":"10","author":"Abreu","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1111\/j.1365-2249.2012.04602.x","article-title":"Lymph node dissection\u2013understanding the immunological function of lymph nodes","volume":"169","author":"Buettner","year":"2012","journal-title":"Clin. Exp. Immunol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Maroilley, T., Berri, M., Lemonnier, G., Esquerr\u00e9, D., Chevaleyre, C., M\u00e9lo, S., Meurens, F., Coville, J.L., Leplat, J.J., and Rau, A. (2018). Immunome differences between porcine ileal and jejunal Peyer\u2019s patches revealed by global transcriptome sequencing of gut-associated lymphoid tissues. Sci. Rep., 8.","DOI":"10.1038\/s41598-018-27019-7"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"660","DOI":"10.3389\/fendo.2019.00660","article-title":"Post-natal Growth Retardation Associated With Impaired Gut Hormone Profiles, Immune and Antioxidant Function in Pigs","volume":"10","author":"Qi","year":"2019","journal-title":"Front. Endocrinol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/4\/990\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:58:05Z","timestamp":1760363885000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/4\/990"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,1]]},"references-count":33,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4]]}},"alternative-id":["ani11040990"],"URL":"https:\/\/doi.org\/10.3390\/ani11040990","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,1]]}}}