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Impact of luminal and systemic endotoxin exposure on gut function, immune response and performance of chickens

Published online by Cambridge University Press:  27 April 2016

K. GHAREEB ,
W.A. AWAD ,
J. BÖHM  and
Q. ZEBELI
K. GHAREEB
Affiliation:
Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria Department of Animal Behaviour and Management, Faculty of Veterinary Medicine, South Valley University, 83523 Qena, Egypt
W.A. AWAD
Affiliation:
Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria Department of Animal Hygiene, Poultry and Environment, Faculty of Veterinary Medicine, South Valley University, 83523 Qena, Egypt
J. BÖHM
Affiliation:
Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
Q. ZEBELI*
Affiliation:
Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
*
Corresponding author: [email protected]
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Abstract

The gastrointestinal tract is a large reservoir of both Gram positive and negative bacteria, of which the Gram negative bacteria act as a source of lipopolysaccharide (LPS). Luminal LPS, commonly known as endotoxin, can enter systemic circulation via paracellular and transcellular permeation. It has been shown that endotoxin exposure can increase intestinal paracellular permeability and alter intestinal structure and function, resulting in impaired absorption and utilisation of nutrients with negative impact on both poultry heath and growth. Acute exposure to large amounts of endotoxin suppresses feed intake in chickens and activation of the innate immune system. Substantial evidence suggests that endotoxin is recognised via toll-like receptor (TLR)-4, located on the surface of immune cells, which activates kinases to enhance the transcription of pro-inflammatory cytokines such as tumour necrosis factor alpha (TNF-α) and interleukin (IL)-1 and 6 which mediate the inhibitory effect of endotoxin on the intestinal nutrient absorption. Inflammation can divert energy and nutrients away from growth supp and into supporting the immune system responses, leading to growth suppression and lowered feed efficiency. In addition, sustained exposure to endotoxin may elicit tolerance, which can make animals refractory against secondary Gram-negative infections. In this review, the effects of endotoxin on intestinal barrier functions and the subsequent negative impacts on the production of chickens are summarised. Overall, this review combines the current knowledge of the chicken's intestinal responses to Gram negative bacterial infection, illustrating the importance of gut health in defence against bacterial infections and improving poultry health, growth and welfare.

Keywords

lipopolysaccharideendotoxinintestinesimmune responsechickens
Type
Reviews
Information
World's Poultry Science Journal , Volume 72 , Issue 2 , June 2016 , pp. 367 - 380
Copyright
Copyright © World's Poultry Science Association 2016 

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References

ABAD, B., MESONERO, J.E., SALVADOR, M.T., GARCIA HERRERA, J. and RODRÍGUEZ-YOLDI, M.J. (2001) The administration of lipopolysaccharide, in vivo, induces alteration in L-leucine intestinal absorption. Life Science 70: 615-628.CrossRefGoogle ScholarPubMed
ALBIN, D.M., WUBBEN, J.E., ROWLETT, J.M., TAPPENDEN, K.A. and NOWAK, R.A. (2007) Changes in small intestinal nutrient transport and barrier function after lipopolysaccharide exposure in two pig breeds. Journal of Animal Science 85: 2517-2523.CrossRefGoogle ScholarPubMed
ALEXANDER, C. and RIETSCHEL, E.T. (2001) Invited review: bacterial lipopolysaccharides and innate immunity. Journal of Endotoxin Research 7: 167-202.Google Scholar
AMADOR, P., GARCÍA-HERRERA, J., MARCA, M.C., DE LA OSADA, J., ACÍN, S., NAVARRO, M.A., SALVADOR, M.T., LOSTAO, M.P. and RODRÍGUEZ-YOLDI, M.J. (2007a) Intestinal D-galactose transport in an endotoxemia model in the rabbit. Journal of Membrane Biology 215: 125-133.Google Scholar
AMADOR, P., GARCÍA-HERRERA, J., MARCA, M.C., DE LA OSADA, J., ACÍN, S., NAVARRO, M.A., SALVADOR, M.T., LOSTAO, M.P. and RODRÍGUEZ-YOLDI, M.J. (2007b) Inhibitory effect of TNF-α on the intestinal absorption of galactose. Journal of Cellular Biochemistry 101: 99-111.Google Scholar
AMADOR, P., MARCA, M.C., GARCÍA-HERRERA, J., LOSTAO, M.P., GUILLÉN, N., DE LA OSADA, J. and RODRÍGUEZ-YOLDI, M.J. (2008) Lipopolysaccharide induces inhibition of galactose intestinal transport in rabbits in vitro. Cellular Physiology and Biochemistry 22: 715-724.Google Scholar
AMETAJ, B.N., SIVARAMAN, S., DUNN, S.M. and ZEBELI, Q. (2012) Repeated oral administration of lipopolysaccharide from Escherichia coli 0111:B4 modulated humoral immune responses in periparturient dairy cows. Innate Immunity 18: 638-647.Google Scholar
AWAD, W.A., GHAREEB, K., PAßLACK, N. and ZENTEK, J. (2013) Dietary inulin alters the intestinal absorptive and barrier function of piglet intestine after weaning. Research in Veterinary Science 95: 249-254.CrossRefGoogle ScholarPubMed
AWAD, W.A., GHAREEB, K. and BÖHM, J. (2011b) Evaluation of the chicory inulin efficacy on ameliorating the intestinal morphology and modulating the intestinal electrophysiological properties in broiler chickens. Journal of Animal Physiology and Animal Nutrition 95: 65-72.Google Scholar
AWAD, W.A., GHAREEB, K., NITSCH, S., PASTEINER, S., ABDEL-RAHEEM, S. and BÖHM, J. (2008b) Effects of dietary inclusion of prebiotic, probiotic and synbiotic on the intestinal glucose absorption of broiler chickens. International Journal of Poultry Science 7: 686-691.Google Scholar
AWAD, W.A., HESS, M., TWARUŻEK, M., GRAJEWSKI, J., KOSICKI, R., BÖHM, J. and ZENTEK, J. (2011c) The impact of the fusarium mycotoxin deoxynivalenol on the health and performance of broiler chickens. International journal of molecular sciences 12: 7996-8012.Google Scholar
AWAD, W.A., MOLNÁR, A., ASCHENBACH, J.R., GHAREEB, K., KHAYAL, B., HESS, C., LIEBHART, D., DUBLECZ, K. and HESS, M. (2015a) Campylobacter infection in chickens modulates the intestinal epithelial barrier function. Innate Immunity 21: 151-160.CrossRefGoogle ScholarPubMed
AWAD, W.A., RAZZAZI-FAZELI, E., BÖHM, J. and ZENTEK, J. (2007) Influence of deoxynivalenol on the D-glucose transport across the isolated epithelium of different intestinal segments of laying hens. Journal of Animal Physiology and Animal Nutrition 91: 175-180.Google Scholar
AWAD, W.A., RAZZAZI-FAZELI, E., BÖHM, J. and ZENTEK, J. (2008a) Effects of B- trichothecenes on luminal glucose transport across the isolated jejunal epithelium of broiler chickens. Journal of Animal Physiology and Animal Nutrition 92: 225-230.CrossRefGoogle ScholarPubMed
AWAD, W.A., VAHJEN, W., ASCHENBACH, J.R. and ZENTEK, J. (2011a) A diet naturally contaminated with the Fusarium mycotoxin deoxynivalenol down regulates gene Expression of glucose transporters in the intestine of broiler chickens. Livestock Science 140: 72-79.Google Scholar
AWAD, W.A. and ZENTEK, J. (2015) The feed contaminant deoxynivalenol affects the intestinal barrier permeability through inhibition of protein synthesis. Archive of Toxicology 89: 961-965.Google Scholar
AWAD, W.A., HESS, C., KHAYAL, B., ASCHENBACH, J.R. and HESS, M. (2014a) In vitro exposure to Escherichia coli decreases ion conductance in the jejunal epithelium of broiler chickens. PLOS ONE 9: e92156.CrossRefGoogle ScholarPubMed
AWAD, W.A., ASCHENBACH, J.R., KHAYAL, B., HESS, C. and HESS, M. (2012) Intestinal epithelial responses to Salmonella enterica serovar Enteritidis: effects on the intestinal permeability and ion transport. Poultry Science 91: 2949-2957.Google Scholar
AWAD, W.A., ASCHENBACH, J.R., GHAREEB, K., KHAYAL, B., HESS, C. and HESS, M. (2014b) Campylobacter jejuni influences the expression of nutrient transporter genes in the intestine of chickens. Veterinary Microbiology 172: 195-201.Google Scholar
AWAD, W.A., SMORODCHENKO, A., HESS, C., ASCHENBACH, J.R., MOLNÁR, A., DUBLECZ, K., KHAYAL, B., POHL, E.E. and HESS, M. (2015b) Increased intracellular calcium level and impaired nutrient absorption are important pathogenicity traits in the chicken intestinal epithelium during Campylobacter jejuni colonisation. Applied Microbiology and Biotechnology 99: 6431-6441.Google Scholar
BISWAS, S.K. and LOPEZ-COLLAZO, E. (2009) Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends in Immunology 30: 475-487.Google Scholar
BRAUDE, A.T., CAREY, F.J., SUTHERLAND, D. and ZALESKY, M. (1955) Studies with radioactive endotoxin. II. Correlation of physiologic effects with distribution of radioactivity in rabbits injected with lethal doses of E coli endotoxin labelled with radioactive sodium chromate. Journal of Clinical Investigation 34: 858.Google Scholar
CAVAILLON, J. and ADIB-CONQUY, M. (2006) Bench-to-bedside review: endotoxin tolerance as a model of leukocyte reprogramming in sepsis. Critical Care 10: 233.CrossRefGoogle Scholar
CAVAILLON, J.M., ADRIE, C., FITTING, C. and ADIB-CONQUY, M. (2003) Endotoxin tolerance: is there a clinical relevance? Journal of Endotoxin Research 9: 101-107.Google Scholar
DELMASTRO-GREENWOOD, M.M. and PIGANELLI, J.D. (2013) Changing the energy of an immune response. American Journal of Clinical and Experimental Immunology 27: 30-54.Google Scholar
EVOCK-CLOVER, C.M., MYERS, M.J. and STEELE, N.C. (1997) Effects of an endotoxin challenge on growth performance, carcass accretion rates, and serum hormone and metabolite concentrations in control pigs and those treated with recombinant porcine somatotropin. Journal of Animal Science 75: 1784-1790.Google Scholar
FAN, H. and COOK, J.A. (2004) Molecular mechanisms of endotoxin tolerance. Journal of Endotoxin Research 10: 71-84.Google Scholar
FERNANDES, F.C. (2005) Endotoxinas em aviários. Revista Brasileira de Medicina do Trabalho 3: 22-28.Google Scholar
FLINN, A., MANI, V., JEFFREY, M., SPENCER, J.D. and GABLER, N.K. (2010) Dietary n-3 fatty acids differentially alter ileum nutrient transport in growing pigs under immune challenge. Midwest Joint ADSA-ASAS Meetings 88: 122.Google Scholar
GARCÍA-HERRERA, J., MARCA, M.C., BROT-LAROCHE, E., GUILLEN, N., ACIN, S., NAVARRO, M.A., DE LA OSADA, J. and RODRIGUEZ-YOLDI, M.J. (2008) Protein kinases, TNF-α, and proteasome contribute in the inhibition of fructose intestinal transport by sepsis in vivo. American Journal of Physiology - Gastrointestinal and Liver Physiology 294: G155-G164.CrossRefGoogle ScholarPubMed
GARCÍA-HERRERA, J., ABAD, B. and RODRÍGUEZ-YOLDI, M.J. (2003) Effect of lipopolysaccharide on D-fructose transport across rabbit jejunum. Inflammation Research 52: 177-184.Google Scholar
GARDINER, K.R., HALLIDAY, M.I., BARCLAY, G.R., MILNE, L., BROWN, D., STEPHENS, S., MAXWELL, R.J. and ROWLANDS, B.J. (1995) Significance of systemic endotoxaemia in inflammatory bowel disease. Gut 36: 897-901.Google Scholar
GHAREEB, K., AWAD, W.A., BÖHM, J. and 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.CrossRefGoogle ScholarPubMed
GHAREEB, K., AWAD, W.A., MOHNL, M., PORTA, R., BIARNÉS, M., BÖHM, J. and SCHATZMAYR, G. (2012) Evaluating the efficacy of an avian-specific probiotic to reduce the colonisation of Campylobacter jejuni in broiler chickens. Poultry Science 91: 1825-1832.CrossRefGoogle ScholarPubMed
GHAREEB, K., AWAD, W.A., MOHNL, M., BÖHM, J. and SCHATZMAYR, G. (2013a) Control strategies for Campylobacter infection in poultry production. World's Poultry Science Journal 69: 57-76.CrossRefGoogle Scholar
GHAREEB, K., AWAD, W.A., SOODOI, C., SASGARY, S., STRASSER, A. and BÖHM, J. (2013b) Effects of feed contaminant deoxynivalenol on plasma cytokines and mRNA expression of immune genes in the intestine of broiler chickens. PLOS ONE 8: e71492.Google Scholar
GHOSHAL, S., WITTA, J., ZHONG, J., DE VILLIERS, W. and ECKHARDT, E. (2009) Chylomicrons promote intestinal absorption of lipopolysaccharides. Journal of Lipid Research 50: 90-97.CrossRefGoogle ScholarPubMed
GREISMAN, S.E. and HORNICK, R.B. (1975) The nature of endotoxin tolerance. Transactions of the American Clinical and Climatological Association 86: 43-50.Google Scholar
GIANNENAS, I., TONTIS, D., TSALIE, E., CHRONIS, E.F., DOUKAS, D. and KYRIAZAKIS, I. (2010) Influence of dietary mushroom agaricus bisporus on intestinal morphology and microflora composition in broiler chickens. Research in Veterinary Science 89: 78-84.Google Scholar
HANSSEN, S.A., HASSELQUIST, D., FOLSTAD, I. and ERIKSTAD, K.E. (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society B: Biological Sciences 271: 925-930.Google Scholar
HARRIS, H.W., GRUNFELD, C., FEINGOLD, K.R., , READ, T.E., KANE, J.P., JONES, A.L., EICHBAUM, E.B., BLAND, G.F. and RAPP, J.H. (1993) Chylomicrons alter the fate of endotoxin, decreasing tumor necrosis factor release and preventing death. Journal of Clinical Investigation 91: 1028-1034.CrossRefGoogle ScholarPubMed
HU, X.F., GUO, Y.M., LI, J.H., YAN, G.L., BUN, S. and HUANG, B.Y. (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.Google Scholar
HURLEY, J.C. (1995) Endotoxemia: methods of detection and clinical correlates. Clinical Microbiology Reviews 8: 268-292.Google Scholar
JING, M., MUNYAKA, P.M., TACTACAN, G.B., RODRIGUEZ-LECOMPTE, J.C., O, K. and HOUSE, J.D. (2014) Performance, serum biochemical responses, and gene expression of intestinal folate transporters of young and older laying hens in response to dietary folic acid supplementation and challenge with Escherichia coli lipopolysaccharide. Poultry Science 93: 122-131.Google Scholar
KAISER, M.G., BEACH, E., CIRACI, C. and LAMONT, S.J. (2010) Bacterial lipopolysaccharide and dietary natural source vitamin e effects on broiler chick immune response. Animal Industry Report AS 656: ASL R2480.Google Scholar
KAMBOH, A.A. and ZHU, W.Y. (2014) Individual and combined effects of genistein and hesperidin on immunity and intestinal morphometry in lipopolysacharide-challenged broiler chickens. Poultry Science 93: 2175-2183.Google Scholar
KANNO, S., EMIL, S., KOSI, M., MONFORTE-MUNOZ, H. and ATKINSON, J. (1996) Small intestinal absorption during endotoxemia in swine. American Journal of Surgery 62: 793-799.Google Scholar
KHIAOSA-ARD, R. and ZEBELI, Q. (2014) Cattle's variation in rumen ecology and metabolism and its contributions to feed efficiency. Livestock Science 162: 66-75.Google Scholar
LAI, H.T.L., NIEUWLAND, M.G.B., KEMP, B., AARNINK, A.J.A. and PARMENTIER, H.K. (2009) Effects of dust and airborne dust components on antibody responses, body weight gain, and heart morphology of broilers. Poultry Science 88: 1838-1849.Google Scholar
LEW, W.Y.W., BAYNA, E., MOLLE, E.D., DALTON, N.D., LAI, N.C., BHARGAVA, V., MENDIOLA, V., CLOPTON, P. and TANG, T. (2013) Recurrent exposure to subclinical lipopolysaccharide increases mortality and induces cardiac fibrosis in mice. PLOS ONE 8: e61057.Google Scholar
LIEBERS, V., RAULF-HEIMSOTH, M. and BRÜNING, T. (2008) Health effects due to endotoxin inhalation (review). Archive of Toxicology 82: 203-210.CrossRefGoogle ScholarPubMed
LÓRÁND, B. (2004) Bile acids in physico-chemical host defence. Pathophysiology 11: 139-145.Google Scholar
LU, M., ZHANG, M., TAKASHIMA, A., WEISS, J., APICELLA, M.A., LI, X.H., YUAN, D. and MUNFORD, R.S. (2005) Lipopolysaccharide deacylation by an endogenous lipase controls innate antibody responses to Gram negative bacteria. Nature Immunology 6: 989-994.Google Scholar
LUYENDYK, J.P., SHORES, K.C., GANEY, P.E. and ROTH, R.A. (2002) Bacterial lipopolysaccharide exposure alters aflatoxin B1 hepatotoxicity: Benchmark dose analysis for markers of liver injury. Toxicological Science 68: 220-225.Google Scholar
MALONEY, S.K. and GRAY, D.A. (1998) Characteristics of the febrile response in Pekin ducks. Journal of Comparative Physiology B 168: 177-182.CrossRefGoogle ScholarPubMed
MANI, V., WEBER, T.E., BAUMGARD, L.H. and GABLER, N.K. (2012) Endotoxin, inflammation, and intestinal function in livestock. Journal of Animal Science 90: 1452-1465.Google Scholar
MARAIS, M., MALONEY, S.K. and GRAY, D.A. (2011) The development of endotoxin tolerance, and the role of hypothalamo-pituitary-adrenal function and glucocorticoids in Pekin ducks. Journal of Experimental Biology 214: 3378-3385.CrossRefGoogle ScholarPubMed
MENG, Q., CHOUDRY, H.A., SOUBA, W.W., KARINCH, A.M., HUANG, J., LIN, C., VARY, T.C. and PAN, M. (2005) Regulation of amino acid arginine transport by lipopolysaccharide and nitric oxide in intestinal epithelial IEC-6 cells. Journal of Gastrointestinal Surgery 9: 1276-1285Google Scholar
MIRELES, A.J., KIM, S.M. and KLASING, K.C. (2005) An acute inflammatory response alters bone homeostasis, body composition, and the humoral immune response of broiler chickens. Poultry Science 84: 553-560.CrossRefGoogle ScholarPubMed
MITCHELL, M.A. and CARLISLE, A.J. (1992) The effects of chronic exposure to elevated environmental temperature on intestinal morphology and nutrient absorption in the domestic fowl (Gallus domesticus). Comparative Biochemistry and Physiology - Part A: Physiology 101: 137-142.Google Scholar
MUELLER, M., LINDNER, B., KUSUMOTO, S., FUKASE, K., SCHROMM, A.B. and SEYDEL, U. (2004) Aggregates are the biologically active units of endotoxin. Journal of Biological Chemistry 279: 26307-26313.CrossRefGoogle ScholarPubMed
NETEA, M.G., VAN DEUREN, M., KULLBERG, B.J., CAVAILLON, J.M. and VAN DER MEER, J.W. (2002) Does the shape of lipid A determine the interaction of LPS with toll-like receptors?. Trends in Immunology 23: 135-139.Google Scholar
NOLAN, J.P. (1981) Endotoxin, reticuloendothelial (RES) function and liver injury. Hepatology 1: 458-465.Google Scholar
PARRA, J., AGUDELO, J., ORTIZ, L., RAMÍREZ, M.C., RODRÍGUEZ, B. and LÓPEZ, A. (2011) Lipopolysaccharide (LPS) from E. coli has detrimental effects on the intestinal morphology of weaned pigs. Colombian Journal of Animal Science and Veterinary Medicine 24: 598-608.Google Scholar
PLATA-SALAMÁN, C.R., SONTI, G., BORKOSKI, J.P., WILSON, C.D. and FRENCH-MULLEN, J.M.H. (1996) Anorexia induced by chronic central administration of cytokines at estimated pathophysiological concentrations. Physiology & Behaviour 60: 867-875.Google Scholar
PLOEGAERT, T.C.W., DE VRIES REILINGH, G., NIEUWLAND, M.G.B., LAMMERS, A., SAVELKOUL, H.F.J. and PARMENTIER, H.K. (2007) Intratracheally administered pathogen-associated molecular patterns affect antibody responses of poultry. Poultry Science 86: 1667-1676.Google Scholar
RAUBER, R.H., PERLIN, V.J., FIN, C.D., MALLMANN, A.L., MIRANDA, D.P., GIACOMINI, L.Z. and NASCIMENTO, V.P. (2014) Interference of Salmonella typhimurium lipopolysaccharide on performance and biological parameters of broiler chickens . Brazilian Journal of Poultry Science 16: 67-76.Google Scholar
RIETSCHEL, E.T., KIRIKAE, T., SCHADE, F.U., MAMAT, U., SCHMIDT, G., LOPPNOW, H., ULMER, A.J., ZAHRINGER, U., SEYDEL, U. and DI PADOVA, F. (1994) Bacterial endotoxin: molecular relationships of structure to activity and function. The FASEB Journal 8: 217-225.Google Scholar
RIETSCHEL, E.T., BRADE, H., HOLST, O., BRADE, L., MUELLER-LOENNIES, S., MAMAT, U., ZAHRINGER, U., BECKMANN, F., SEYDEL, U., BRANDENBURG, K., ULMER, A.J., MATTERN, T., HEINE, H., SCHLETTER, J., LOPPNOW, H., SCHONBECK, U., FLAD, H.D., HAUSCHILDT, S., SCHADE, U.F., DI PADOVA, F., KUSUMOTO, S. and SCHUMANN, R.R. (1996) Bacterial endotoxin: chemical constitution, biological recognition, host response, and immunological detoxification. Current Topics in Microbiology and Immunology 216: 39-81.Google Scholar
ROTH, J., ASLAN, T., STORR, B. and ZEISBERGER, E. (1997) Lack of cross tolerance between LPS and muramyl dipeptide in induction of circulation TNF-a and IL-6 in guinea pigs. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 273: 1529-1533.Google Scholar
RUITER, D.J., VAN DER MEULEN, J., BROUWER, A., HUMMEL, M.J., MAUW, B.J., VAN DER PLOEG, J.C. and WISSE, E. (1981) Uptake by liver cells of endotoxin following its intravenous injection. Laboratory Investigation 45: 38-45.Google Scholar
SHEN, L., WEBER, C.R., RALEIGH, D.R., YU, D. and TURNER, J.R. (2011) Tight junction pore and leak pathways: A dynamic duo. Annual Review of Physiology 73: 283-309.Google Scholar
SHINI, S., KAISER, P., SHINI, A. and BRYDEN, W.L. (2008) Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comparative Biochemistry and Physiology - Part B 149: 324-333.Google Scholar
SILHAVY, T.J., KAHNE, D. and WALKER, S. (2010) The bacterial cell envelope. Cold Spring Harbor Perspectives in Biology 2: a000414.Google Scholar
SONESSON, H.R.A., ZÄHRINGER, U., GRIMMECKE, H.D., WESTPHAL, O. and RIETSCHEL, E.T. (1994) Bacterial endotox: chemical structure and biological activity, in: BRINGHAM, K.L. (Ed) Endotoxin and the Lungs, pp. 1-20 (Marcel Dekker Inc. NY, NY).Google Scholar
STAR, L., KEMP, B., VAN DEN ANKER, I. and PARMENTIER, H.K. (2008) Effect of single or combined climatic and hygienic stress in four layer lines: 1. Performance. Poultry Science 87: 1022-1030.Google Scholar
STEIGER, M., SENN, M., ALTREUTHER, G., WERLING, D., SUTTER, F., KREUZER, M. and LANGHANS, W. (1999) Effect of a prolonged low-dose lipopolysaccharide infusion on feed intake and metabolism in heifers. Journal of Animal Science 77: 2523-2532.Google Scholar
TODAR, K. (2010) Online textbook of bacteriology. http://www.textbookofbacteriology.net (Last accessed 01.09.11).Google Scholar
TOMITA, M., OHKUBO, R. and HAYASHI, M. (2004) Lipopolysaccharide transport system across colonic epithelial cells in normal and infective rat. Drug Metabolism and Pharmacokinetics 19: 33-40.Google Scholar
TURNER, J.R. (2009) Intestinal mucosal barrier function in health and disease. Nature Reviews Immunology 9: 799-809.Google Scholar
ULEVITCH, R.J., JOHNSTON, A.R. and WEINSTEIN, D.B. (1979) New function for high density lipoproteins: Their participation in intravascular reactions of bacterial lipopolysaccharides. The Journal of Clinical Investigation 64: 1516-1524.Google Scholar
ULEVITCH, R.J. and JOHNSTON, A.R. (1978) The modification of biophysical and endotoxic properties of bacterial lipopolysaccharides by serum. The Journal of Clinical Investigation 62: 1313-1324.Google Scholar
VREUGDENHIL, A.C.E., ROUSSEAU, C.H., HARTUNG, T., GREVE, J.W.M., VAN'T VEER, C. and BUURMAN, W.A. (2003) Lipopolysaccharide (lps)-binding protein mediates lps detoxification by chylomicrons. Journal of Immunology 170: 1399-1405.Google Scholar
WELLS, J.E. and RUSSELL, J. (1996) The effect of growth and starvation on the lysis of the ruminal cellulolytic bacterium Fibrobacter succinogenes. Applied and Environmental Microbiology 62: 1342-1346.Google Scholar
WEST, M. and HEAGY, W. (2002) Endotoxin tolerance: a review. Critical Care Medicine 30: S54-S73.Google Scholar
XIE, H., RATH, N.C., HUFF, G.R., HUFF, W.E. and BALOG, J.M. (2000) Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens. Poultry Science 79: 33-40.Google Scholar
YANG, X.J., GUO, Y.M., HE, X., YUAN, J.M., YANG, Y. and WANG, Z. (2008) Growth performance and immune responses in chickens after challenge with lipopolysaccharide and modulation by dietary different oils. Animal 2: 216-223.Google Scholar
ZÄHRINGER, U., LINDNER, B. and RIETSCHEL, E.T. (1999) Chemical structure of lipid A: recent advances in structural analysis of biologically active molecules, in: BRADE, H., OPAL, S., VOGEL, S. & MORRISON, D.C. (Eds) Endotoxin in Health and Disease, pp. 93-114 (Marcel Dekker, New York).Google Scholar
ZEBELI, Q. and METZLER-ZEBELI, B.U. (2012) Interplay between rumen digestive disorders and diet-induced inflammation in dairy cattle. Research in Veterinary Science 93: 1099-1108.Google Scholar
ZHANG, X., ZHAO, L., CAO, F., AHMAD, H., WANG, G. and WANG, T. (2013) Effects of feeding fermented Ginkgo biloba leaves on small intestinal morphology, absorption, and immunomodulation of early lipopolysaccharide-challenged chicks. Poultry Science 92: 119-130.Google Scholar