Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-19T15:22:19.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Intestinal permeability induced by lipopolysaccharide and measured by lactulose, rhamnose and mannitol sugars in chickens

Published online by Cambridge University Press:  24 November 2016

S. Gilani ,
G. S. Howarth ,
S. M. Kitessa ,
C. D. Tran ,
R. E. A. Forder  and
R. J. Hughes
S. Gilani*
Affiliation:
School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy Campus, Adelaide, SA 5371, Australia Poultry Cooperative Research Centre, University of New England, PO Box U242, Armidale, NSW 2351, Australia
G. S. Howarth
Affiliation:
School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy Campus, Adelaide, SA 5371, Australia
S. M. Kitessa
Affiliation:
PPPI Nutrition Research Laboratory, South Australian Research & Development Institute, Roseworthy, SA 5371, Australia Commonwealth Scientific and Industrial Research Organisation, Health and Bio-security, Adelaide, SA, Australia
C. D. Tran
Affiliation:
Commonwealth Scientific and Industrial Research Organisation, Health and Bio-security, Adelaide, SA, Australia School of Medicine, Faculty of Health Sciences, University of Adelaide, Adelaide, SA 5005, Australia
R. E. A. Forder
Affiliation:
School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy Campus, Adelaide, SA 5371, Australia
R. J. Hughes
Affiliation:
School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy Campus, Adelaide, SA 5371, Australia PPPI Nutrition Research Laboratory, South Australian Research & Development Institute, Roseworthy, SA 5371, Australia
*
†E-mail: saad.gilani@adelaide.edu.au
Get access

Abstract

Increased intestinal permeability (IP) can lead to compromised health. Limited in vivo IP research has been conducted in chickens. The objectives of the current study were to develop a model of increased IP utilizing lipopolysaccharide (LPS Escherichia coli O55:B5) and to evaluate IP changes using the lactulose, mannitol and rhamnose (LMR) sugar permeability test. In addition, fluorescein isothiocyanate dextran (FITC-d), d-lactate, zonula occludens (ZO-1) and diamine oxidase (DAO) permeability tests were employed. Male Ross chickens were reared until day 14 on the floor in an animal care facility and then transferred to individual cages in three separate experiments. In each of experiments 1 and 2, 36 chicks were randomly allocated to receive either saline (control) or LPS (n=18/group). Lactulose, mannitol and rhamnose sugar concentration in blood was measured at 0, 30, 60, 90, 120 and 180 min in experiment 1, at 60, 90 and 120 min in experiment 2 and at 90 min in experiment 3 (n=16/group). Lipopolysaccharide was injected intraperitoneally at doses of 0.5, 1 and 1 mg/kg BW in experiments 1, 2 and 3, respectively, on days 16, 18 and 20, whereas control received sterile saline. On day 21, only birds in experiments 1 and 2 were fasted for 19.5 h. Chicks were orally gavaged with the LMR sugars (0.25 gL, 0.05 gM, 0.05 gR/bird) followed by blood collection (from the brachial vein) as per time point for each experiment. Only in experiment 3, were birds given an additional oral gavage of FITC-d (2.2 mg/ml per bird) 60 min after the first gavage. Plasma d-lactate, ZO-1 and DAO concentrations were also determined by ELISA in experiment 3 (n=10). Administration of LPS did not affect IP as measured by the LMR sugar test compared with control. This was also confirmed by FITC-d and DAO levels in experiment 3 (P>0.05). The plasma levels of d-lactate were decreased (P<0.05). Plasma levels of ZO-1 were increased in the third experiment only and did not change in the first two experiments. Lipopolysaccharide at doses of 0.5 and 1 mg/kg did not increase IP in this model system. In conclusion, the LMR sugar can be detected in blood 90 min after the oral gavage. Further studies are needed for the applicability of LMR sugars tests.

Keywords

lactuloserhamnosemannitollipopolysaccharideFITC-d
Type
Research Article
Information
animal , Volume 11 , Issue 7 , July 2017 , pp. 1174 - 1179
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Araujo, G, Yunta, C, Terre, M, Mereu, A, Ipharraguerre, I and Bach, A 2015. Intestinal permeability and incidence of diarrhea in newborn calves. Journal of Dairy Science 98, 7309–7317.Google Scholar
Chapman, HD 2014. Milestones in avian coccidiosis research: a review. Poultry Science 93, 501–511.Google Scholar
Chen, J, Tellez, G, Richards, JD and Escobar, J 2015. Identification of potential biomarkers for gut barrier failure in broiler chickens. Frontiers in Veterinary Science 2, article no. 14.Google Scholar
Cox, M, Lewis, K and 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.CrossRefGoogle ScholarPubMed
Fink, MP 2003. Intestinal epithelial hyper permeability: update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Current Opinion in Critical Care 9, 143–151.Google Scholar
Gilani, S, Howarth, GS, Kitessa, SM, Forder, REA, Tran, CD and Hughes, RJ 2016. New biomarkers for intestinal permeability induced by lipopolysaccharide in chickens. Animal Production Science 56, 1984–1997.CrossRefGoogle Scholar
Hu, X, Guo, Y, Li, J, Yan, G, Bun, S and 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.Google Scholar
Klaus, DA, Motal, MC, Burger-Klepp, U, Marschalek, C, Schmidt, EM, Lebherz-Eichinger, D, Krenn, CG and Roth, GA 2013. Increased plasma zonulin in patients with sepsis. Biochemia Medica 23, 107–111.Google Scholar
Kuttappan, VA, Berghman, LR, Vicuna, EA, Latorre, JD, Menconi, A, Wolchok, JD, Wolfenden, AD, Faulkner, OB, Tellez, GI, Hargis, BM and Bielke, LR 2015. Poultry enteric inflammation model with dextran sodium sulfate mediated chemical induction and feed restriction in broilers. Poultry Science 94, 1220–1226.Google Scholar
Lei, K, Li, YL, Yu, DY, Rajput, IR and 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.CrossRefGoogle ScholarPubMed
Li, Y, Zhang, H, Chen, YP, Yang, MX, Zhang, LL, Lu, ZX, Zhou, YM and Wang, T 2015. Bacillus amyloliquefaciens supplementation alleviates immunological stress and intestinal damage in lipopolysaccharide-challenged broilers. Animal Feed Science and Technology 208, 119–131.Google Scholar
Ni, L, Chen, Q, Zhu, K, Shi, J, Shen, J, Gong, J, Gao, T, Yu, W, Li, J and 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.Google Scholar
Perše, M and Cerar, A 2012. Dextran sodium sulphate colitis mouse model: traps and tricks. Journal of Biomedicine and Biotechnology 2012, 1–12.CrossRefGoogle ScholarPubMed
Piton, G, Cypriani, B, Regnard, J, Patry, C, Puyraveau, M and Capellier, G 2015. Catecholamine use is associated with enterocyte damage in critically ill patients. Shock 43, 437–442.Google Scholar
Ruan, Z, Liu, S, Zhou, Y, Mi, S, Liu, G, Wu, X, Yao, K, Assaad, H, Deng, Z, Hou, Y, Wu, G and 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.CrossRefGoogle ScholarPubMed
Skouroliakou, M, Ntountaniotis, D, Kastanidou, O and Massara, P 2016. Evaluation of Barley’s beta-glucan food fortification through investigation of intestinal permeability in healthy adults. Journal of the American College of Nutrition 35, 13–19.CrossRefGoogle ScholarPubMed
Shaikh, M, Rajan, K, Forsyth, CB, Voigt, RM and Keshavarzian, A 2015. Simultaneous gas-chromatographic urinary measurement of sugar probes to assess intestinal permeability: use of time course analysis to optimize its use to assess regional gut permeability. Clinica Chimica Acta 442, 24–32.Google Scholar
Shi, H, Wu, B, Wan, J, Liu, W and 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 Hepatology and Gastroenterology 39, 373–378.Google Scholar
Shini, S, Kaiser, P, Shini, A and Bryden, WL 2008. Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology 149, 324–333.Google Scholar
Sørensen, SH, Proud, FJ, Rutgers, HC, Markwell, P, Adam, A and 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.Google Scholar
Sun, T, Gao, G-Z, Li, R-F, Li, X, Li, D-W, Wu, S-S, Yeo, AET and 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.Google Scholar
Tan, J, Liu, S, Guo, Y, Applegate, TJ and Eicher, SD 2014. Dietary L-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens. British Journal of Nutrition 111, 1394–1404.Google Scholar
Tran, A and Whitfield, C 2009. Lipopolysaccharides (Endotoxins). In Encyclopaedia of microbiology (ed. M Schaechter), pp. 513–528. Elsevier, Oxford, UK.Google Scholar
Tran, CD, Hawkes, J, Graham, RD, Kitchen, JL, Symonds, EL, Davidson, GP and Butler, RN 2015. Zinc-fortified oral rehydration solution improved intestinal permeability and small intestinal mucosal recovery. Clinical Pediatrics 54, 676–682.Google Scholar
van Wijck, K, Verlinden, TJM, van Eijk, HMH, Dekker, J, Buurman, WA, Dejong, CHC and Lenaerts, K 2013. Novel multi-sugar assay for site-specific gastrointestinal permeability analysis: a randomized controlled crossover trial. Clinical Nutrition 32, 245–251.CrossRefGoogle ScholarPubMed
Vicuna, EA, Kuttappan, VA, Galarza-Seeber, R, Latorre, JD, Faulkner, OB, Hargis, BM, Tellez, G and Bielke, LR 2015a. Effect of dexamethasone in feed on intestinal permeability, differential white blood cell counts, and immune organs in broiler chicks. Poultry Science 94, 2075–2080.Google Scholar
Vicuna, EA, Kuttappan, VA, Tellez, G, Hernandez-Velasco, X, Seeber-Galarza, R, Latorre, JD, Faulkner, OB, Wolfenden, AD, Hargis, BM and Bielke, LR 2015b. Dose titration of FITC-D for optimal measurement of enteric inflammation in broiler chicks. Poultry Science 94, 1353–1359.CrossRefGoogle ScholarPubMed
Wang, L, Llorente, C, Hartmann, P, Yang, AM, Chen, P and Schnabl, B 2015. Methods to determine intestinal permeability and bacterial translocation during liver disease. Journal of Immunological Methods 421, 44–53.Google Scholar
Wang, LC, Zhang, TT, Wen, C, Jiang, ZY, Wang, T and Zhou, YM 2012. Protective effects of zinc-bearing clinoptilolite on broilers challenged with Salmonella pullorum . Poultry Science 91, 1838–1845.Google Scholar
Wideman, RF Jr, Hamal, KR, Stark, JM, Blankenship, J, Lester, H, Mitchell, KN, Lorenzoni, G and Pevzner, I 2012. A wire-flooring model for inducing lameness in broilers: evaluation of probiotics as a prophylactic treatment. Poultry Science 91, 870–883.Google Scholar
Wijtten, P, Verstijnen, J, van Kempen, T, Perdok, H, Gort, G and Verstegen, M 2011. Lactulose as a marker of intestinal barrier function in pigs after weaning. Journal of Animal Science 89, 1347–1357.Google Scholar
Williams, JM, Duckworth, CA, Watson, AJ, Frey, MR, Miguel, JC, Burkitt, MD, Sutton, R, Hughes, KR, Hall, LJ, Caamano, JH, Campbell, BJ and Pritchard, DM 2013. A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Disease Models and Mechanisms 6, 1388–1399.Google Scholar
Wu, QJ, Zhou, YM, Wu, YN, Zhang, LL and 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.Google Scholar
Xun, W, Shi, L, Zhou, H, Hou, G, Cao, T and 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.Google Scholar
Zhu, C, Wu, Y, Jiang, Z, Zheng, C, Wang, L, Yang, X, Ma, X, Gao, K and Hu, Y 2015. Dietary soy isoflavone attenuated growth performance and intestinal barrier functions in weaned piglets challenged with lipopolysaccharide. International Immunopharmacology 28, 288–294.Google Scholar
Zuidhof, MJ, Schneider, BL, Carney, VL, Korver, DR and Robinson, FE 2014. Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005. Poultry Science 93, 2970–2982.Google Scholar