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Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

New biomarkers for intestinal permeability induced by lipopolysaccharide in chickens

Saad Gilani A B F , Gordon S. Howarth A , Soressa M. Kitessa C , Rebecca E. A. Forder A , Cuong D. Tran C D and Robert J. Hughes E
+ Author Affiliations
- Author Affiliations

A School of Animal and Veterinary Sciences, The University of Adelaide, Roseworthy Campus, Adelaide, SA 5371, Australia.

B Poultry CRC, PO Box U242, University of New England, Armidale, NSW 2351, Australia.

C Commonwealth Scientific and Industrial Research Organisation, Gate 13 Kintore Avenue, Adelaide, SA 5000, Australia.

D Discipline of Physiology, School of Medicine, The University of Adelaide, Adelaide, SA 5005, Australia.

E South Australian Research and Development Institute.

F Corresponding author. Email: saad.gilani@adelaide.edu.au

Animal Production Science 56(12) 1984-1997 https://doi.org/10.1071/AN15725
Submitted: 15 October 2015  Accepted: 7 April 2016   Published: 8 August 2016

Abstract

Intestinal health is influenced by a complex set of variables involving the intestinal microbiota, mucosal immunity, digestion and absorption of nutrients, intestinal permeability (IP) and intestinal integrity. An increase in IP increases bacterial or toxin translocation, activates the immune system and affects health. IP in chickens is reviewed in three sections. First, intestinal structure and permeability are discussed briefly. Second, the use of lipopolysaccharide (LPS) as a tool to increase IP is discussed in detail. LPS, a glycolipid found in the outer coat of mostly Gram-negative bacteria, has been reported to increase IP in rats, mice and pigs. Although LPS has been used in chickens for inducing systemic inflammation, information regarding LPS effects on IP is limited. This review proposes that LPS could be used as a means to increase IP in chickens. The final section focuses on potential biomarkers to measure IP, proposing that the sugar-recovery method may be optimal for application in chickens.

Additional keywords: anti-trypsin inhibitor, fluorescein isothiocyanate dextran, intestinal fatty acid-binding protein, lactulose, leaky gut, models.


References

Albin DM, Wubben JE, Rowlett JM, Tappenden KA, Nowak RA (2007) Changes in small intestinal nutrient transport and barrier function after lipopolysaccharide exposure in two pig breeds. Journal of Animal Science 85, 2517–2523.
Changes in small intestinal nutrient transport and barrier function after lipopolysaccharide exposure in two pig breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSjtrvE&md5=beab7609c468814835a6af070487ca63CAS | 17526659PubMed |

Awad WA, Ghareeb K, Bohm J (2008) Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides. International Journal of Molecular Sciences 9, 2205–2216.
Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyhsbbL&md5=b1e2a55d05632a661fff5f294acb9938CAS |

Awad WA, Aschenbach JR, Khayal B, Hess C, Hess M (2012) Intestinal epithelial responses to Salmonella enterica serovar enteritidis: effects on intestinal permeability and ion transport. Poultry Science 91, 2949–2957.
Intestinal epithelial responses to Salmonella enterica serovar enteritidis: effects on intestinal permeability and ion transport.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s%2FnsVamtw%3D%3D&md5=302960cd05dbcab5d179656fe6448c9fCAS | 23091155PubMed |

Awad WA, Molnar A, Aschenbach JR, Ghareeb K, Khayal B, Hess C, Liebhart D, Dublecz K, Hess M (2015) Campylobacter infection in chickens modulates the intestinal epithelial barrier function. Innate Immunity 21, 151–160.
Campylobacter infection in chickens modulates the intestinal epithelial barrier function.Crossref | GoogleScholarGoogle Scholar | 24553586PubMed |

Bjarnason I, Macpherson A, Hollander D (1995) Intestinal permeability: an overview. Gastroenterology 108, 1566–1581.
Intestinal permeability: an overview.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3ks12qsQ%3D%3D&md5=c372887e50d4333fe91cb7b14af5aa42CAS | 7729650PubMed |

Bowen OT, Dienglewicz RL, Wideman RF, Erf GF (2009) Altered monocyte and macrophage numbers in blood and organs of chickens injected intravenous with lipopolysaccharide. Veterinary Immunology and Immunopathology 131, 200–210.
Altered monocyte and macrophage numbers in blood and organs of chickens injected intravenous with lipopolysaccharide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFantbnN&md5=13830bc43705afff1bf9483859005b83CAS | 19477023PubMed |

Burke KF, Ruaux CG, Suchodolski JS, Williams DA, Steiner JM (2012) Development and analytical validation of an enzyme-linked immunosorbent assay (ELISA) for the measurement of alpha1-proteinase inhibitor in serum and faeces from cats. Research in Veterinary Science 93, 995–1000.
Development and analytical validation of an enzyme-linked immunosorbent assay (ELISA) for the measurement of alpha1-proteinase inhibitor in serum and faeces from cats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFChtLc%3D&md5=9eb9040e949bcbaf59ce82b943db2159CAS | 22074688PubMed |

Chapman HD (2014) Milestones in avian coccidiosis research: a review. Poultry Science 93, 501–511.
Milestones in avian coccidiosis research: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2crht1eqsA%3D%3D&md5=8bb2d39a5f3b76e9cd3a280ece74ac39CAS | 24604841PubMed |

Chaussé AM, Grépinet O, Bottreau E, Vern YL, Menanteau P, Trotereau J, Robert V, Wu Z, Kerboeuf D, Beaumont C, Velge P (2011) Expression of toll-like receptor 4 and downstream effectors in selected cecal cell subpopulations of chicks resistant or susceptible to Salmonella carrier state. Infection and Immunity 79, 3445–3454.
Expression of toll-like receptor 4 and downstream effectors in selected cecal cell subpopulations of chicks resistant or susceptible to Salmonella carrier state.Crossref | GoogleScholarGoogle Scholar | 21628520PubMed |

Chen J, Tellez G, Richards JD, Escobar J (2015a) Identification of potential biomarkers for gut barrier failure in broiler chickens. Frontiers in Veterinary Science 2, 14
Identification of potential biomarkers for gut barrier failure in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 26664943PubMed |

Chen SW, Wang PY, Zhu J, Chen GW, Zhang JL, Chen ZY, Zuo S, Liu YC, Pan YS (2015b) Protective effect of 1,25-dihydroxyvitamin d3 on lipopolysaccharide-induced intestinal epithelial tight junction injury in caco-2 cell monolayers. Inflammation 38, 375–383.
Protective effect of 1,25-dihydroxyvitamin d3 on lipopolysaccharide-induced intestinal epithelial tight junction injury in caco-2 cell monolayers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFSntbnJ&md5=78b5b73dab9426cf97b071ffc0f52ce4CAS | 25344656PubMed |

Choct M (2009) Managing gut health through nutrition. British Poultry Science 50, 9–15.
Managing gut health through nutrition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7lvVOisw%3D%3D&md5=8550198431c215e4c6d8b30a18cb6909CAS | 19234925PubMed |

Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. The Journal of Biological Chemistry 274, 10689–10692.
Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXis1Gntbw%3D&md5=5bdda3d49bb678eafd4ba41a721f66aaCAS | 10196138PubMed |

Chun H, Sasaki M, Fujiyama Y, Bamba T (1997) Effect of enteral glutamine on intestinal permeability and bacterial translocation after abdominal radiation injury in rats. Journal of Gastroenterology 32, 189–195.
Effect of enteral glutamine on intestinal permeability and bacterial translocation after abdominal radiation injury in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitlegsb4%3D&md5=752abd4aed6649940bfea4f823820fd8CAS | 9085166PubMed |

Collier CT, van der Klis JD, Deplancke B, Anderson DB, Gaskins HR (2003) Effects of tylosin on bacterial mucolysis, Clostridium perfringens colonization, and intestinal barrier function in a chick model of necrotic enteritis. Antimicrobial Agents and Chemotherapy 47, 3311–3317.
Effects of tylosin on bacterial mucolysis, Clostridium perfringens colonization, and intestinal barrier function in a chick model of necrotic enteritis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVWmtL8%3D&md5=18e9aab764a4ea4999ba7bddee6db14eCAS | 14506046PubMed |

Colman R, Rubin D (2014) Fecal alpha 1-antitrypsin as a biomarker for disease activity in ulcerative colitis. The American Journal of Gastroenterology 109, S434

Cox M, Lewis K, Cooper B (1999) Measurement of small intestinal permeability markers, lactulose, and mannitol in serum (results in celiac disease). Digestive Diseases and Sciences 44, 402–406.
Measurement of small intestinal permeability markers, lactulose, and mannitol in serum (results in celiac disease).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7mtFKqsQ%3D%3D&md5=56f1612092284c81e2aef31b9489b02bCAS | 10063930PubMed |

De Boever S, Croubels S, Meyer E, Sys S, Beyaert R, Ducatelle R, De Backer P (2009) Characterization of an intravenous lipopolysaccharide inflammation model in broiler chickens. Avian Pathology 38, 403–411.
Characterization of an intravenous lipopolysaccharide inflammation model in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVehs77P&md5=a82afaa3815512f6567e028b32da3f1dCAS | 19937527PubMed |

Dong L, Liu X, Li H, Vertel BM, Ebihara L (2006) Role of the N-terminus in permeability of chicken connexin 45.6 gap junctional channels. The Journal of Physiology 576, 787–799.
Role of the N-terminus in permeability of chicken connexin 45.6 gap junctional channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yjtrfM&md5=efed54ea4349b3639a4bf531f60b9df2CAS | 16931554PubMed |

Escala J, Gatherer ME, Voûte L, Love S (2006) Application of the 51Cr–EDTA urinary recovery test for assessment of intestinal permeability in the horse. Research in Veterinary Science 80, 181–185.
Application of the 51Cr–EDTA urinary recovery test for assessment of intestinal permeability in the horse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht12qtb%2FN&md5=41c312cc6dbb0517f1ffa12aa2e4a054CAS | 16143355PubMed |

Fink MP, Antonsson JB, Wang H, Rothschild HR (1991) Increased intestinal permeability in endotoxic pigs: mesenteric hypoperfusion as an etiologic factor. Archives of Surgery 126, 211–218.
Increased intestinal permeability in endotoxic pigs: mesenteric hypoperfusion as an etiologic factor.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7ivVWgsA%3D%3D&md5=f14985b3ecbe6623ece2cca69d1949ebCAS | 1899558PubMed |

Forder REA, Howarth GS, Tivey DR, Hughes RJ (2007) Bacterial modulation of small intestinal goblet cells and mucin composition during early posthatch development of poultry. Poultry Science 86, 2396–2403.
Bacterial modulation of small intestinal goblet cells and mucin composition during early posthatch development of poultry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snivF2rsw%3D%3D&md5=6d41b49daa5d9bf238d11c925999660bCAS |

Frias R, Sankari S, Westermarck E (2004) 51Cr–EDTA absorption blood test: an easy method for assessing small intestinal permeability in dogs. Journal of Veterinary Internal Medicine 18, 156–159.
51Cr–EDTA absorption blood test: an easy method for assessing small intestinal permeability in dogs.Crossref | GoogleScholarGoogle Scholar | 15058765PubMed |

Garnaut SM, Howarth GS, Read LC (2002) Effects of Insulin-like growth factor-I and its analogue, long-R 3-IGF-I, on intestinal absorption of 3-O-methyl-d-glucose are less pronounced than gut mucosal growth responses. Growth Factors 20, 17–25.
Effects of Insulin-like growth factor-I and its analogue, long-R 3-IGF-I, on intestinal absorption of 3-O-methyl-d-glucose are less pronounced than gut mucosal growth responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvV2gt7Y%3D&md5=df239b61db337974c79f6bb0332a3761CAS | 11999215PubMed |

Ghareeb K, Awad WA, Bohm J, Zebeli Q (2015) Impacts of the feed contaminant deoxynivalenol on the intestine of monogastric animals: poultry and swine. Journal of Applied Toxicology 35, 327–337.
Impacts of the feed contaminant deoxynivalenol on the intestine of monogastric animals: poultry and swine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXivFamtrk%3D&md5=b91ea6a2e02d9bae6c775402326eb4fcCAS | 25352520PubMed |

Golab K, Gawel A, Warwas M, Mazurkiewicz M (2007) Serum concentration of cystatin and antitrypsin activity in chicken infection diseases. Medycyna Weterynaryjna 63, 1216–1219.

Groschwitz KR, Hogan SP (2009) Intestinal barrier function: molecular regulation and disease pathogenesis. The Journal of Allergy and Clinical Immunology 124, 3–20, quiz 21–22.
Intestinal barrier function: molecular regulation and disease pathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsl2gu7k%3D&md5=9d2ae71f911146dde2acf5183b2f52d0CAS | 19560575PubMed |

Guo S, Al-Sadi R, Said HM, Ma TY (2013) Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. American Journal of Pathology 182, 375–387.
Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFOisL4%3D&md5=3ed52c4413d48301596d40343b5749beCAS | 23201091PubMed |

Hamilton MK, Boudry G, Lemay DG, Raybould HE (2015) Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent. American Journal of Physiology. Gastrointestinal and Liver Physiology 308, G840–G851.
Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVGgtL7K&md5=05c0ae2096f8c993d37c8a1759674c0aCAS | 25747351PubMed |

Han K, Kim K, Wang J, Kim H (2013) Effect of unfermented and fermented atractylodes macrocephalae on gut permeability and lipopolysaccharide-induced inflammation. Journal of Korean Medicine for Obesity Research 13, 24–32.

Hang CH, Shi JX, Sun BW, Li JS (2007) Apoptosis and functional changes of dipeptide transporter (PepT1) in the rat small intestine after traumatic brain injury. The Journal of Surgical Research 137, 53–60.
Apoptosis and functional changes of dipeptide transporter (PepT1) in the rat small intestine after traumatic brain injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12ktb7M&md5=9c709ffe69e8aaab795d69a36a6a0e88CAS | 17081567PubMed |

Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings. Biological Sciences 271, 925–930.
Costs of immunity: immune responsiveness reduces survival in a vertebrate.Crossref | GoogleScholarGoogle Scholar |

He C, Yang S, Yu W, Chen Q, Shen J, Hu Y, Shi J, Wu X, Li J, Li N (2014) Effects of continuous renal replacement therapy on intestinal mucosal barrier function during extracorporeal membrane oxygenation in a porcine model. Journal of Cardiothoracic Surgery 9, 72
Effects of continuous renal replacement therapy on intestinal mucosal barrier function during extracorporeal membrane oxygenation in a porcine model.Crossref | GoogleScholarGoogle Scholar | 24758270PubMed |

Hollander D (1999) Intestinal permeability, leaky gut, and intestinal disorders. Current Gastroenterology Reports 1, 410–416.
Intestinal permeability, leaky gut, and intestinal disorders.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FitVOktQ%3D%3D&md5=2638cebdc1f53f594b87d223481a0053CAS | 10980980PubMed |

Hornef MW, Normark BH, Vandewalle A, Normark S (2003) Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. The Journal of Experimental Medicine 198, 1225–1235.
Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVGqt7c%3D&md5=d2989736dc25d639d4465d94504a4c8bCAS | 14568981PubMed |

Hu X, Guo Y, Li J, Yan G, Bun S, Huang B (2011) Effects of an early lipopolysaccharide challenge on growth and small intestinal structure and function of broiler chickens. Canadian Journal of Animal Science 91, 379–384.
Effects of an early lipopolysaccharide challenge on growth and small intestinal structure and function of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1OisL7K&md5=91c9e52ccc1badb6947d1b4bc19c0f87CAS |

Ilan Y (2012) Leaky gut and the liver: a role for bacterial translocation in nonalcoholic steatohepatitis. World Journal of Gastroenterology 18, 2609–2618.
Leaky gut and the liver: a role for bacterial translocation in nonalcoholic steatohepatitis.Crossref | GoogleScholarGoogle Scholar | 22690069PubMed |

Jeurissen S, Lewis F, van der Klis J, Mroz Z, Rebel J, ter Huurne A (2002) Parameters and techniques to determine intestinal health of poultry as constituted by immunity, integrity, and functionality. Current Issues in Intestinal Microbiology 3, 1–14.

Karcher DM, Applegate T (2008) Survey of enterocyte morphology and tight junction formation in the small intestine of avian embryos. Poultry Science 87, 339–350.
Survey of enterocyte morphology and tight junction formation in the small intestine of avian embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FlslCrtg%3D%3D&md5=6a84c0309f61ae392581e08d6e97009cCAS | 18212379PubMed |

Katouzian F, Sblattero D, Not T, Tommasini A, Giusto E, Meiacco D, Stebel M, Marzari R, Fasano A, Ventura A (2005) Dual sugar gut-permeability testing on blood drop in animal models. Clinica Chimica Acta 352, 191–197.
Dual sugar gut-permeability testing on blood drop in animal models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvFamuw%3D%3D&md5=09639c1face86f613c2cd7f14b650f16CAS |

Kimura M, Sawada N, Kimura H, Isomura H, Hirata K, Mori M (1996) Comparison between the distribution of 7H6 tight junction-associated antigen and occludin during the development of chick intestine. Cell Structure and Function 21, 91–96.
Comparison between the distribution of 7H6 tight junction-associated antigen and occludin during the development of chick intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivVKjurc%3D&md5=0edd974b4c1cbc307eee768b0a256dd4CAS | 8726478PubMed |

Kitessa SM, Nattrass GS, Forder REA, McGrice HA, Wu S-B, Hughes RJ (2014) Mucin gene mRNA levels in broilers challenged with Eimeria and/or Clostridium perfringens. Avian Diseases 58, 408–414.
Mucin gene mRNA levels in broilers challenged with Eimeria and/or Clostridium perfringens.Crossref | GoogleScholarGoogle Scholar | 25518436PubMed |

Klunker LR, Kahlert S, Panther P, Diesing A-K, Reinhardt N, Brosig B, Kersten S, Dänicke S, Rothkötter H-J, Kluess JW (2013) Deoxynivalenol and E.coli lipopolysaccharide alter epithelial proliferation and spatial distribution of apical junction proteins along the small intestinal axis1. Journal of Animal Science 91, 276–285.
Deoxynivalenol and E.coli lipopolysaccharide alter epithelial proliferation and spatial distribution of apical junction proteins along the small intestinal axis1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFKiurg%3D&md5=98e063a257f2e999a7e0dba2c95c9c93CAS | 23100596PubMed |

Kosek M, Haque R, Lima A, Babji S, Shrestha S, Qureshi S, Amidou S, Mduma E, Lee G, Yori PP, Guerrant RL, Bhutta Z, Mason C, Kang G, Kabir M, Amour C, Bessong P, Turab A, Seidman J, Olortegui MP, Quetz J, Lang D, Gratz J, Miller M, Gottlieb M, MAL-ED network (2013) Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants. The American Journal of Tropical Medicine and Hygiene 88, 390–396.
Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants.Crossref | GoogleScholarGoogle Scholar | 23185075PubMed |

Kurundkar AR, Killingsworth CR, McIlwain RB, Timpa JG, Hartman YE, He D, Karnatak RK, Neel ML, Clancy JP, Anantharamaiah G (2010) Extracorporeal membrane oxygenation causes loss of intestinal epithelial barrier in the newborn piglet. Pediatric Research 68, 128–133.
Extracorporeal membrane oxygenation causes loss of intestinal epithelial barrier in the newborn piglet.Crossref | GoogleScholarGoogle Scholar | 20442689PubMed |

Kuttappan VA, Berghman LR, Vicuña EA, Latorre JD, Menconi A, Wolchok JD, Wolfenden AD, Faulkner OB, Tellez GI, Hargis BM, Bielke LR (2015) Poultry enteric inflammation model with dextran sodium sulfate mediated chemical induction and feed restriction in broilers. Poultry Science 94, 1220–1226.
Poultry enteric inflammation model with dextran sodium sulfate mediated chemical induction and feed restriction in broilers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MjktlOjsA%3D%3D&md5=933c6a9387089caaf0404c3906ee49e4CAS | 25877409PubMed |

Laxminarayan R, T Van Boeckel, Teillant A (2015) ‘The economic costs of withdrawing antimicrobial growth promoters from the livestock sector.’ OECD food, agriculture and fisheries papers, 78. (OECD Publishing: Paris)

Lea T (2015) Caco-2 cell line. In ‘The impact of food bioactives on health: in vitro and ex vivo models’. (Eds K Verhoeckx, P Cotter, I López-Expósito, C Kleiveland, T Lea, A Mackie, T Requena, D Swiatecka, H Wichers) pp. 103–113. (Springer Link)

Lei K, Li YL, Yu DY, Rajput IR, Li WF (2013) Influence of dietary inclusion of Bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens. Poultry Science 92, 2389–2395.
Influence of dietary inclusion of Bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeqs7vE&md5=88e21a515dd3f74f477be6325699ae71CAS | 23960122PubMed |

Lei Q, Qiang F, Chao D, Di W, Guoqian Z, Bo Y, Lina Y (2014) Amelioration of hypoxia and LPS-induced intestinal epithelial barrier dysfunction by emodin through the suppression of the NF-κB and HIF-1α signaling pathways. International Journal of Molecular Medicine 34, 1629–1639.

Li Y, Wang X, Li N, Li J (2014) The study of n-3 PUFAs protecting the intestinal barrier in rat HS/R model. Lipids in Health and Disease 13, 146
The study of n-3 PUFAs protecting the intestinal barrier in rat HS/R model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXms1SmtLw%3D&md5=b99be729ca627769f4937c28b5579093CAS | 25200333PubMed |

Li Y, Zhang H, Chen YP, Yang MX, Zhang LL, Lu ZX, Zhou YM, Wang T (2015) Bacillus amyloliquefaciens supplementation alleviates immunological stress and intestinal damage in lipopolysaccharide-challenged broilers. Animal Feed Science and Technology 208, 119–131.
Bacillus amyloliquefaciens supplementation alleviates immunological stress and intestinal damage in lipopolysaccharide-challenged broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFemt7bK&md5=504d9eddef811855eebbc9d41ac1e7a2CAS |

Liu D, Guo Y, Wang Z, Yuan J (2010) Exogenous lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens. Avian Pathology 39, 17–24.
Exogenous lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 20390532PubMed |

Liu Y, Chen F, Odle J, Lin X, Jacobi SK, Zhu H, Wu Z, Hou Y (2012) Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge. The Journal of Nutrition 142, 2017–2024.
Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Siu7%2FM&md5=90b31a656ca9a36d68d8897b96a4a281CAS | 23014495PubMed |

Liu X, Yang G, Geng X-R, Cao Y, Li N, Ma L, Chen S, Yang P-C, Liu Z (2013) Microbial products induce claudin-2 to compromise gut epithelial barrier function. PLoS One 8, e68547
Microbial products induce claudin-2 to compromise gut epithelial barrier function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlyhsrnI&md5=cbb98fbe43333f0d3c079a2888f683cbCAS | 23990874PubMed |

Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98.
Trade-offs in evolutionary immunology: just what is the cost of immunity?Crossref | GoogleScholarGoogle Scholar |

Mani V, Weber TE, Baumgard LH, Gabler NK (2012) Growth and development symposium: endotoxin, inflammation, and intestinal function in livestock. Journal of Animal Science 90, 1452–1465.
Growth and development symposium: endotoxin, inflammation, and intestinal function in livestock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xns1eis7Y%3D&md5=8fd05af9ec89cb019b4f13558fe6cbe0CAS | 22247110PubMed |

Meddings JB, Swain MG (2000) Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the rat. Gastroenterology 119, 1019–1028.
Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gsrY%3D&md5=970d39a906de7d6107feba570496a755CAS | 11040188PubMed |

Mercer DW, Smith GS, Cross JM, Russell DH, Chang L, Cacioppo J (1996) Effects of lipopolysaccharide on intestinal injury: potential role of nitric oxide and lipid peroxidation. The Journal of Surgical Research 63, 185–192.
Effects of lipopolysaccharide on intestinal injury: potential role of nitric oxide and lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksVOmsrw%3D&md5=81f4991081a2dfd2ba37ffc87d6175c8CAS | 8661195PubMed |

Meyer B, Zentek J, Harlander-Matauschek A (2013) Differences in intestinal microbial metabolites in laying hens with high and low levels of repetitive feather-pecking behavior. Physiology & Behavior 110–111, 96–101.
Differences in intestinal microbial metabolites in laying hens with high and low levels of repetitive feather-pecking behavior.Crossref | GoogleScholarGoogle Scholar |

Mohr AJ, Leisewitz AL, Jacobson LS, Steiner JM, Ruaux CG, Williams DA (2003) Effect of early enteral nutrition on intestinal permeability, intestinal protein loss, and outcome in dogs with severe parvoviral enteritis. Journal of Veterinary Internal Medicine 17, 791–798.
Effect of early enteral nutrition on intestinal permeability, intestinal protein loss, and outcome in dogs with severe parvoviral enteritis.Crossref | GoogleScholarGoogle Scholar | 14658714PubMed |

Murphy KF, German AJ, Ruaux CG, Steiner JM, Williams DA, Hall EJ (2003) Fecal α1-proteinase inhibitor concentration in dogs with chronic gastrointestinal disease. Veterinary Clinical Pathology 32, 67–72.
Fecal α1-proteinase inhibitor concentration in dogs with chronic gastrointestinal disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szgsFenug%3D%3D&md5=c74fc7c3edcacef0511b5cd8d89fe7a9CAS | 12833220PubMed |

Murugesan GR, Gabler NK, Persia ME (2014) Effects of direct-fed microbial supplementation on broiler performance, intestinal nutrient transport and integrity under experimental conditions with increased microbial challenge. British Poultry Science 55, 89–97.
Effects of direct-fed microbial supplementation on broiler performance, intestinal nutrient transport and integrity under experimental conditions with increased microbial challenge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslymu7vJ&md5=4addb60e9529aa9ed6e1aa07caae7e8aCAS | 24219515PubMed |

Naughton J, Duggan G, Bourke B, Clyne M (2014) Interaction of microbes with mucus and mucins. Gut Microbes 5, 48–52.
Interaction of microbes with mucus and mucins.Crossref | GoogleScholarGoogle Scholar | 24149677PubMed |

Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ (2006) Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. Journal of Immunology (Baltimore, MD.: 1950) 176, 3070–3079.
Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1erurk%3D&md5=835f545506117d5089614f6319dd4517CAS |

Nébot-Vivinus M, Harkat C, Bzioueche H, Cartier C, Plichon-Dainese R, Moussa L, Eutamene H, Pishvaie D, Holowacz S, Seyrig C, Piche T, Theodorou V (2014) Multispecies probiotic protects gut barrier function in experimental models. World Journal of Gastroenterology 20, 6832–6843.
Multispecies probiotic protects gut barrier function in experimental models.Crossref | GoogleScholarGoogle Scholar | 24944474PubMed |

Neirinckx E, Vervaet C, Michiels J, De Smet S, Van Den Broeck W, Remon JP, De Backer P, Croubels S (2011) Feasibility of the Ussing chamber technique for the determination of in vitro jejunal permeability of passively absorbed compounds in different animal species. Journal of Veterinary Pharmacology and Therapeutics 34, 290–297.

Ni L, Chen Q, Zhu K, Shi J, Shen J, Gong J, Gao T, Yu W, Li J, Li N (2015) The influence of extracorporeal membrane oxygenation therapy on intestinal mucosal barrier in a porcine model for post-traumatic acute respiratory distress syndrome. Journal of Cardiothoracic Surgery 10, 20
The influence of extracorporeal membrane oxygenation therapy on intestinal mucosal barrier in a porcine model for post-traumatic acute respiratory distress syndrome.Crossref | GoogleScholarGoogle Scholar | 25884385PubMed |

Niewold TA (2015) Intestinal health biomarkers in vivo. In ‘Intestinal health: key to maximise growth performance in livestock’. Chapter 9. (Ed. TA Niewold) pp. 219–228. (Wageningen Academic Publishers: Wageningen, The Netherlands)

Niewold TA, Meinen M, van der Meulen J (2004) Plasma intestinal fatty acid binding protein (IFABP) concentrations increase following intestinal ischemia in pigs. Research in Veterinary Science 77, 89–91.
Plasma intestinal fatty acid binding protein (IFABP) concentrations increase following intestinal ischemia in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1Cgt7o%3D&md5=0b54ca3ab7f6d18b05a9a3cfb2be8059CAS | 15120958PubMed |

Osselaere A, Santos R, Hautekiet V, De Backer P, Chiers K, Ducatelle R, Croubels S (2013) Deoxynivalenol impairs hepatic and intestinal gene expression of selected oxidative stress, tight junction and inflammation proteins in broiler chickens, but addition of an adsorbing agent shifts the effects to the distal parts of the small intestine. PLoS One 8, e69014
Deoxynivalenol impairs hepatic and intestinal gene expression of selected oxidative stress, tight junction and inflammation proteins in broiler chickens, but addition of an adsorbing agent shifts the effects to the distal parts of the small intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1CmtLzM&md5=75888de6c262702c7f2d88ddd77e9c3fCAS | 23922676PubMed |

Ozden O, Black BL, Ashwell CM, Tipsmark CK, Borski RJ, Grubb BJ (2010) Developmental profile of claudin-3, -5, and -16 proteins in the epithelium of chick intestine. The Anatomical Record 293, 1175–1183.
Developmental profile of claudin-3, -5, and -16 proteins in the epithelium of chick intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVSltbzO&md5=e9e8b9b375cb6a86d7b167288c3ee366CAS | 20583258PubMed |

Parambeth JC, Suchodolski JS, Steiner JM (2015) Purification and partial characterization of alpha1-proteinase inhibitor in the common marmoset (Callithrix jacchus). Research in Veterinary Science 99, 17–22.
Purification and partial characterization of alpha1-proteinase inhibitor in the common marmoset (Callithrix jacchus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXivFahtrc%3D&md5=8595d0f8756191ca132bf35a9b5b78ddCAS | 25745866PubMed |

Piton G, Cypriani B, Regnard J, Patry C, Puyraveau M, Capellier G (2015) Catecholamine use is associated with enterocyte damage in critically ill patients. Shock 43, 437–442.
Catecholamine use is associated with enterocyte damage in critically ill patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmsl2ntrs%3D&md5=6ae61c5667e4269ac2becb917b562dddCAS | 25565647PubMed |

Powell D (1981) Barrier function of epithelia. American Journal of Physiology. Gastrointestinal and Liver Physiology 241, G275–G288.

Prisciandaro LD, Geier MS, Butler RN, Cummins AG, Howarth GS (2011) Evidence supporting the use of probiotics for the prevention and treatment of chemotherapy-induced intestinal mucositis. Critical Reviews in Food Science and Nutrition 51, 239–247.
Evidence supporting the use of probiotics for the prevention and treatment of chemotherapy-induced intestinal mucositis.Crossref | GoogleScholarGoogle Scholar | 21390944PubMed |

Rose ME, Long PL (1969) Immunity to coccidiosis: gut permeability changes in response to sporozoite invasion. Experientia 25, 183–184.
Immunity to coccidiosis: gut permeability changes in response to sporozoite invasion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M3gvVyrsA%3D%3D&md5=618959610914a95533902396ec82e0d0CAS | 5786101PubMed |

Rosero O, Onody P, Kovacs T, Molnar D, Lotz G, Toth S, Turoczi Z, Fulop A, Garbaisz D, Harsanyi L, Szijarto A (2014) Impaired intestinal mucosal barrier upon ischemia-reperfusion: patching holes in the shield with a simple surgical method BioMed Research International 41, 1615–1623.

Ruan Z, Liu S, Zhou Y, Mi S, Liu G, Wu X, Yao K, Assaad H, Deng Z, Hou Y, Wu G, Yin Y (2014) Chlorogenic acid decreases intestinal permeability and increases expression of intestinal tight junction proteins in weaned rats challenged with LPS. PLoS One 9, e97815
Chlorogenic acid decreases intestinal permeability and increases expression of intestinal tight junction proteins in weaned rats challenged with LPS.Crossref | GoogleScholarGoogle Scholar | 24887396PubMed |

Ruhnke I, Rohe I, Meyer W, Kroger S, Neumann K, Zentek J (2013) Method for the preparation of mucosal flaps from the jejunum of laying hens for transporter studies in Ussing chambers. Archives of Animal Nutrition 67, 161–168.
Method for the preparation of mucosal flaps from the jejunum of laying hens for transporter studies in Ussing chambers.Crossref | GoogleScholarGoogle Scholar | 23521695PubMed |

Schokker D (2012) Chicken intestinal development in health and disease In transcriptomic and modelling approach. PhD Thesis, Wageningen Institute of Animal Sciences, Wageningen, The Netherlands.

Shen LJ, Guan YY, Wu XP, Wang Q, Wang L, Xiao T, Wu HR, Wang JG (2015) Serum citrulline as a diagnostic marker of sepsis-induced intestinal dysfunction. Clinics and Research in Hepatology and Gastroenterology 39, 230–236.
Serum citrulline as a diagnostic marker of sepsis-induced intestinal dysfunction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVart7rP&md5=90af76f2263a544aef94e2e237b6d8a5CAS | 25457562PubMed |

Shi H, Wu B, Wan J, Liu W, Su B (2015) The role of serum intestinal fatty acid binding protein levels and D-lactate levels in the diagnosis of acute intestinal ischemia. Clinics and Research in Hepatology and Gastroenterology 39, 373–378.
The role of serum intestinal fatty acid binding protein levels and D-lactate levels in the diagnosis of acute intestinal ischemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXovVSjtg%3D%3D&md5=f35b1efd07eae4ca0e23c66d693ce94eCAS | 25683524PubMed |

Song J, Jiao LF, Xiao K, Luan ZS, Hu CH, Shi B, Zhan XA (2013) Cello-oligosaccharide ameliorates heat stress-induced impairment of intestinal microflora, morphology and barrier integrity in broilers. Animal Feed Science and Technology 185, 175–181.
Cello-oligosaccharide ameliorates heat stress-induced impairment of intestinal microflora, morphology and barrier integrity in broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVKgtbfF&md5=2aa9f68b08abd78981581a3f9fcc72bcCAS |

Song J, Xiao K, Ke YL, Jiao LF, Hu CH, Diao QY, Shi B, Zou XT (2014) Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poultry Science 93, 581–588.
Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjs1Gjt70%3D&md5=282422d1e4201235bb85cabfef4914dfCAS | 24604851PubMed |

Sørensen SH, Proud FJ, Rutgers HC, Markwell P, Adam A, Batt RM (1997) A blood test for intestinal permeability and function: a new tool for the diagnosis of chronic intestinal disease in dogs. Clinica Chimica Acta 264, 103–115.
A blood test for intestinal permeability and function: a new tool for the diagnosis of chronic intestinal disease in dogs.Crossref | GoogleScholarGoogle Scholar |

Stanley D, Denman S, Hughes R, Geier M, Crowley T, Chen H, Haring V, Moore R (2012) Intestinal microbiota associated with differential feed conversion efficiency in chickens. Applied Microbiology and Biotechnology 96, 1361–1369.
Intestinal microbiota associated with differential feed conversion efficiency in chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1ektL7P&md5=aacd341817859f5df02ee4281426ee0aCAS | 22249719PubMed |

Stenman LK, Holma R, Eggert A, Korpela R (2013) A novel mechanism for gut barrier dysfunction by dietary fat: epithelial disruption by hydrophobic bile acids. American Journal of Physiology. Gastrointestinal and Liver Physiology 304, G227–G234.
A novel mechanism for gut barrier dysfunction by dietary fat: epithelial disruption by hydrophobic bile acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFKrt7g%3D&md5=f309938c57ca88d3435d17475f68f4a7CAS | 23203158PubMed |

Suchodolski JS, Heilmann RM, Steiner JM, Meyer DJ (2012) Laboratory approach. In ‘Canine and feline gastroenterology’. (Ed. J Steiner) pp. 177–204. (Saunders, Elsevier: USA)

Sun T, Gao GZ, Li RF, Li X, Li DW, Wu SS, Yeo AET, Jin B (2015) Bone marrow-derived mesenchymal stem cell transplantation ameliorates oxidative stress and restores intestinal mucosal permeability in chemically induced colitis in mice. American Journal of Translational Research 7, 891–901.

Tan J, Liu S, Guo Y, Applegate TJ, Eicher SD (2014) Dietary L-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens. British Journal of Nutrition 111, 1394–1404.
Dietary L-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkslSls7o%3D&md5=e8d903a693fbafe36e8eca3ff8a1b411CAS | 24330949PubMed |

Tan S, Yu W, Lin Z, Chen Q, Shi J, Dong Y, Duan K, Bai X, Xu L, Yu Z, Li J, Li N (2015) Berberine ameliorates intestinal mucosal barrier damage induced by peritoneal air exposure. Biological & Pharmaceutical Bulletin 38, 122–126.
Berberine ameliorates intestinal mucosal barrier damage induced by peritoneal air exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsl2gtr8%3D&md5=176a353bec9d99711906febff31c4260CAS |

Tellez G, Latorre JD, Kuttappan VA, Kogut MH, Wolfenden A, Hernandez-Velasco X, Hargis BM, Bottje WG, Bielke LR, Faulkner OB (2014) Utilization of rye as energy source affects bacterial translocation, intestinal viscosity, microbiota composition, and bone mineralization in broiler chickens. Frontiers in Genetics 5, 339
Utilization of rye as energy source affects bacterial translocation, intestinal viscosity, microbiota composition, and bone mineralization in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 25309584PubMed |

Tellez G, Latorre JD, Kuttappan VA, Hargis BM, Hernandez-Velasco X (2015) Rye affects bacterial translocation, intestinal viscosity, microbiota composition and bone mineralization in turkey poults. PLoS One 10, e0122390
Rye affects bacterial translocation, intestinal viscosity, microbiota composition and bone mineralization in turkey poults.Crossref | GoogleScholarGoogle Scholar | 25849537PubMed |

Tooley KL, Howarth GS, Butler RN (2009) Mucositis and non-invasive markers of small intestinal function. Cancer Biology & Therapy 8, 753–758.
Mucositis and non-invasive markers of small intestinal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFOns7g%3D&md5=efb9d8c7ceb7bd06e1841d69defa29e1CAS |

Tran AX, Whitfield C (2009) ‘Lipopolysaccharides (endotoxins). In ‘Encyclopedia of microbiology’. (Ed. M Schaechter) pp. 513–528. (Elsevier: UK)

Uni Z, Platin R, Sklan D (1998) Cell proliferation in chicken intestinal epithelium occurs both in the crypt and along the villus. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 168, 241–247.
Cell proliferation in chicken intestinal epithelium occurs both in the crypt and along the villus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czhtVClug%3D%3D&md5=259c3070d4ffdd90f5594a6c47443ac0CAS | 9646500PubMed |

Vicuña EA, Kuttappan VA, Tellez G, Hernandez-Velasco X, Seeber-Galarza R, Latorre JD, Faulkner OB, Wolfenden AD, Hargis BM, Bielke LR (2015) Dose titration of FITC-D for optimal measurement of enteric inflammation in broiler chicks. Poultry Science 94, 1353–1359.
Dose titration of FITC-D for optimal measurement of enteric inflammation in broiler chicks.Crossref | GoogleScholarGoogle Scholar | 25877413PubMed |

Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews. Genetics 13, 227–232.

Wang X, Shen J, Li S, Zhi L, Yang X, Yao J (2014) Sulfated Astragalus polysaccharide regulates the inflammatory reaction in LPS-infected broiler chicks. International Journal of Biological Macromolecules 69, 146–150.
Sulfated Astragalus polysaccharide regulates the inflammatory reaction in LPS-infected broiler chicks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOqu7fF&md5=dd03d6555177436c64af50be66d08059CAS | 24820152PubMed |

Williams RB (2005) Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathology 34, 159–180.
Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MrhvVSksQ%3D%3D&md5=4a3c58b977b994f9edfd30716a0554e9CAS | 16191699PubMed |

Williams JM, Duckworth CA, Watson AJ, Frey MR, Miguel JC, Burkitt MD, Sutton R, Hughes KR, Hall LJ, Caamano JH, Campbell BJ, Pritchard DM (2013) A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Disease Models & Mechanisms 6, 1388–1399.
A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Sgsr4%3D&md5=2b46acfea88f67bc6c5910de587d6650CAS |

Wu QJ, Zhou YM, Wu YN, Zhang LL, Wang T (2013) The effects of natural and modified clinoptilolite on intestinal barrier function and immune response to LPS in broiler chickens. Veterinary Immunology and Immunopathology 153, 70–76.
The effects of natural and modified clinoptilolite on intestinal barrier function and immune response to LPS in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFOqurY%3D&md5=599ed28edf60e5ec510182a78df0f739CAS | 23453767PubMed |

Xie H, Rath N, Huff G, Huff W, Balog J (2000) Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens. Poultry Science 79, 33–40.
Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslSrtA%3D%3D&md5=0762995b41fd4d5632de46d76db9f909CAS | 10685886PubMed |

Xun W, Shi L, Zhou H, Hou G, Cao T, Zhao C (2015) Effects of curcumin on growth performance, jejunal mucosal membrane integrity, morphology and immune status in weaned piglets challenged with enterotoxigenic Escherichia coli. International Immunopharmacology 27, 46–52.
Effects of curcumin on growth performance, jejunal mucosal membrane integrity, morphology and immune status in weaned piglets challenged with enterotoxigenic Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnsVWltL0%3D&md5=d6ec5cfdc29504ed31e34863cda4772eCAS | 25937483PubMed |

Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, Sitaraman SV, Merlin D (2009) Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One 4, e6073–8.
Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis.Crossref | GoogleScholarGoogle Scholar | 19562033PubMed |

Yegani M, Korver DR (2008) Factors affecting intestinal health in poultry. Poultry Science 87, 2052–2063.
Factors affecting intestinal health in poultry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnitVKhtg%3D%3D&md5=1097e8c8d629244e91cf548d49939becCAS | 18809868PubMed |

Yue C, Wang W, Tian WL, Huang Q, Zhao RS, Zhao YZ, Li QR, Li JS (2013) Lipopolysaccharide-induced failure of the gut barrier is site-specific and inhibitable by growth hormone. Inflammation Research 62, 407–415.
Lipopolysaccharide-induced failure of the gut barrier is site-specific and inhibitable by growth hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktVGhtbo%3D&md5=37991c288ff782dd8369aa733bc805bcCAS | 23340865PubMed |

Yuh EL, Shulman SG, Mehta SA, Xie J, Chen L, Frenkel V, Bednarski MD, Li KCP (2005) Delivery of systemic chemotherapeutic agent to tumors by using focused ultrasound: study in a murine model. Radiology 234, 431–437.
Delivery of systemic chemotherapeutic agent to tumors by using focused ultrasound: study in a murine model.Crossref | GoogleScholarGoogle Scholar | 15671000PubMed |

Zhang Q, Piao XL, Piao XS, Lu T, Wang D, Kim SW (2011) Preventive effect of coptis chinensis and berberine on intestinal injury in rats challenged with lipopolysaccharides. Food and Chemical Toxicology 49, 61–69.
Preventive effect of coptis chinensis and berberine on intestinal injury in rats challenged with lipopolysaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1agtr7L&md5=2d2220a0a4e7253e27eb138811c48f61CAS | 20932871PubMed |

Zhang L, Fan X, Zhong Z, Xu G, Shen J (2015) Association of plasma diamine oxidase and intestinal fatty acid-binding protein with severity of disease in patient with heat stroke. The American Journal of Emergency Medicine 33, 867–871.
Association of plasma diamine oxidase and intestinal fatty acid-binding protein with severity of disease in patient with heat stroke.Crossref | GoogleScholarGoogle Scholar | 25913083PubMed |

Zhu C, Wu Y, Jiang Z, Zheng C, Wang L, Yang X, Ma X, Gao K, Hu Y (2015) Dietary soy isoflavone attenuated growth performance and intestinal barrier functions in weaned piglets challenged with lipopolysaccharide. International Immunopharmacology 28, 288–294.
Dietary soy isoflavone attenuated growth performance and intestinal barrier functions in weaned piglets challenged with lipopolysaccharide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotlKjsro%3D&md5=a2cd964194ec83bbed88836b5252c565CAS | 25979760PubMed |

Zuidhof MJ, Schneider BL, Carney VL, Korver DR, Robinson FE (2014) Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005. Poultry Science 93, 2970–2982.
Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M7kvFeksg%3D%3D&md5=810194ebd378e2ecfd10468490685790CAS | 25260522PubMed |