Methods to determine intestinal permeability and bacterial translocation during liver disease

Journal of Immunological Methods

Volumn 421, Issue , 2015, Pages 44-53

  Wang, Lirui ^a,b   Llorente, Cristina ^a,b   Hartmann, Phillipp ^a   Yang, An Ming ^a   Chen, Peng ^a   Schnabl, Bernd ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Endotoxin; Gut liver axis; Intestinal injury; Intestinal leakiness; Microbiome; Microbiota

Indexed keywords

ALBUMIN; ALPHA 1 ANTITRYPSIN; AMINE OXIDASE (COPPER CONTAINING); BOVINE SERUM ALBUMIN; CALGRANULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FATTY ACID BINDING PROTEIN; FLUORESCEIN ISOTHIOCYANATE; MANNITOL; MYOSIN LIGHT CHAIN KINASE; PROTEINASE ACTIVATED RECEPTOR 2; RHAMNOSE; SERUM ALBUMIN; TIGHT JUNCTION PROTEIN; BIOLOGICAL MARKER;

ALBUMIN BLOOD LEVEL; ALCOHOL METABOLISM; BACTERIAL OVERGROWTH; BACTERIAL TRANSLOCATION; BIOLUMINESCENCE; CAPILLARY PERMEABILITY; DISEASE COURSE; ELECTRIC RESISTANCE; ELECTRON MICROSCOPY; FATTY ACID TRANSPORT; HISTOLOGY; HUMAN; IMMUNOFLUORESCENCE TEST; INTESTINAL STEM CELL; INTESTINE CELL; INTESTINE LOOP; INTESTINE MOTILITY; INTESTINE MUCOSA PERMEABILITY; INTESTINE WALL; LIVER DISEASE; MOLECULAR SIZE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMALL INTESTINE; TIGHT JUNCTION; VENOUS BLOOD; ANIMAL; IMMUNOLOGY; INFLAMMATION; INTESTINE ABSORPTION; INTESTINE MUCOSA; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; VASCULARIZATION;

BACTERIA (MICROORGANISMS);

ANIMALS; BACTERIAL TRANSLOCATION; BIOMARKERS; HUMANS; INFLAMMATION; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; LIVER DISEASES; MICE; TIGHT JUNCTIONS;

EID: 84929957703     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2014.12.015     Document Type: Review

References (106)

1. Alam A.N., Sarker S.A., Wahed M.A., Khatun M., Rahaman M.M. Enteric protein loss and intestinal permeability changes in children during acute shigellosis and after recovery: effect of zinc supplementation. Gut 1994, 35:1707.
2. An G., Wei B., Xia B., McDaniel J.M., Ju T., Cummings R.D., Braun J., Xia L. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J. Exp. Med. 2007, 204:1417.
3. Assimakopoulos S.F., Tsamandas A.C., Tsiaoussis G.I., Karatza E., Triantos C., Vagianos C.E., Spiliopoulou I., Kaltezioti V., Charonis A., Nikolopoulou V.N., Scopa C.D., Thomopoulos K.C. Altered intestinal tight junctions' expression in patients with liver cirrhosis: a pathogenetic mechanism of intestinal hyperpermeability. Eur. J. Clin. Invest. 2012, 42:439.
4. Balmer M.L., Slack E., de Gottardi A., Lawson M.A., Hapfelmeier S., Miele L., Grieco A., Van Vlierberghe H., Fahrner R., Patuto N., Bernsmeier C., Ronchi F., Wyss M., Stroka D., Dickgreber N., Heim M.H., McCoy K.D., Macpherson A.J. The liver may act as a firewall mediating mutualism between the host and its gut commensal microbiota. Sci. Transl. Med. 2014, 6. (237ra66.).
5. Bjarnason I., O'Morain C., Levi A.J., Peters T.J. Absorption of 51chromium-labeled ethylenediaminetetraacetate in inflammatory bowel disease. Gastroenterology 1983, 85:318.
6. Bjarnason I., Peters T.J., Levi A.J. Intestinal permeability: clinical correlates. Dig. Dis. 1986, 4:83.
7. Bjarnason I., Peters T.J., Veall N. A persistent defect in intestinal permeability in coeliac disease demonstrated by a 51Cr-labelled EDTA absorption test. Lancet 1983, 1:323.
8. Bjarnason I., Peters T.J., Wise R.J. The leaky gut of alcoholism: possible route of entry for toxic compounds. Lancet 1984, 1:179.
9. Bjarnason I., Williams P., So A., Zanelli G.D., Levi A.J., Gumpel J.M., Peters T.J., Ansell B. Intestinal permeability and inflammation in rheumatoid arthritis: effects of non-steroidal anti-inflammatory drugs. Lancet 1984, 2:1171.
10. Bjerke K., Halstensen T.S., Jahnsen F., Pulford K., Brandtzaeg P. Distribution of macrophages and granulocytes expressing L1 protein (calprotectin) in human Peyer's patches compared with normal ileal lamina propria and mesenteric lymph nodes. Gut 1993, 34:1357.
11. Bode C., Kugler V., Bode J.C. Endotoxemia in patients with alcoholic and non-alcoholic cirrhosis and in subjects with no evidence of chronic liver disease following acute alcohol excess. J. Hepatol. 1987, 4:8.
12. Buffoni F. Histaminase and related amine oxidases. Pharmacol. Rev. 1966, 18:1163.
13. Burri E., Beglinger C. IBD: Faecal calprotectin testing-the need for better standardization. Nat. Rev. Gastroenterol. Hepatol. 2014, 11:583.
14. Chen P., Starkel P., Turner J.R., Ho S.B., Schnabl B. Dysbiosis-induced intestinal inflammation activates TNFRI and mediates alcoholic liver disease in mice. Hepatology 2014.
15. Chen P., Torralba M., Tan J., Embree M., Zengler K., Starkel P., van Pijkeren J.P., DePew J., Loomba R., Ho S.B., Bajaj J.S., Mutlu E.A., Keshavarzian A., Tsukamoto H., Nelson K.E., Fouts D.E., Schnabl B. Supplementation of saturated long-chain fatty acids maintains intestinal eubiosis and reduces ethanol-induced liver injury in mice. Gastroenterology 2015, 148:203.
16. Clayburgh D.R., Barrett T.A., Tang Y., Meddings J.B., Van Eldik L.J., Watterson D.M., Clarke L.L., Mrsny R.J., Turner J.R. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J. Clin. Invest. 2005, 115:2702.
17. Clayburgh D.R., Musch M.W., Leitges M., Fu Y.X., Turner J.R. Coordinated epithelial NHE3 inhibition and barrier dysfunction are required for TNF-mediated diarrhea in vivo. J. Clin. Invest. 2006, 116:2682.
18. Cobden I., Dickinson R.J., Rothwell J., Axon A.T. Intestinal permeability assessed by excretion ratios of two molecules: results in coeliac disease. Br. Med. J. 1978, 2:1060.
19. Coffin P.O., Sharpe B.A. Cause of death in alcoholic hepatitis. J. Hosp. Med. 2007, 2:51.
20. Costa F., Mumolo M.G., Ceccarelli L., Bellini M., Romano M.R., Sterpi C., Ricchiuti A., Marchi S., Bottai M. Calprotectin is a stronger predictive marker of relapse in ulcerative colitis than in Crohn's disease. Gut 2005, 54:364.
21. Crossley J.R., Elliott R.B. Simple method for diagnosing protein-losing enteropathies. Br. Med. J. 1977, 1:428.
22. Cuenca S., Sanchez E., Santiago A., El Khader I., Panda S., Vidal S., Camilo Nieto J., Juarez C., Sancho F., Guarner F., Soriano G., Guarner C., Manichanh C. Microbiome composition by pyrosequencing in mesenteric lymph nodes of rats with CCl4-induced cirrhosis. J. Innate Immun. 2014, 6:263.
23. Dale I., Brandtzaeg P., Fagerhol M.K., Scott H. Distribution of a new myelomonocytic antigen (L1) in human peripheral blood leukocytes. Immunofluorescence and immunoperoxidase staining features in comparison with lysozyme and lactoferrin. Am. J. Clin. Pathol. 1985, 84:24.
24. Dale I., Fagerhol M.K., Naesgaard I. Purification and partial characterization of a highly immunogenic human leukocyte protein, the L1 antigen. Eur. J. Biochem. 1983, 134:1.
25. Dastych M., Dastych M., Novotna H., Cihalova J. Lactulose/mannitol test and specificity, sensitivity, and area under curve of intestinal permeability parameters in patients with liver cirrhosis and Crohn's disease. Dig. Dis. Sci. 2008, 53:2789.
26. Elamin E., Jonkers D., Juuti-Uusitalo K., van Ijzendoorn S., Troost F., Duimel H., Broers J., Verheyen F., Dekker J., Masclee A. Effects of ethanol and acetaldehyde on tight junction integrity: in vitro study in a three dimensional intestinal epithelial cell culture model. PLoS One 2012, 7:e35008.
27. Evans T.W. 'Review article: albumin as a drug-biological effects of albumin unrelated to oncotic pressure. Aliment. Pharmacol. Ther. 2002, 16(Suppl. 5):6.
28. Fanali G., di Masi A., Trezza V., Marino M., Fasano M., Ascenzi P. Human serum albumin: from bench to bedside. Mol. Asp. Med. 2012, 33:209.
29. Farquhar M.G., Palade G.E. Junctional complexes in various epithelia. J. Cell Biol. 1963, 17:375.
30. Fasano A. Intestinal zonulin: open sesame!. Gut 2001, 49:159.
31. Fasano A. Intestinal permeability and its regulation by zonulin: diagnostic and therapeutic implications. Clin. Gastroenterol. Hepatol. 2012, 10:1096.
32. Foulke-Abel J., In J., Kovbasnjuk O., Zachos N.C., Ettayebi K., Blutt S.E., Hyser J.M., Zeng X.L., Crawford S.E., Broughman J.R., Estes M.K., Donowitz M. Human enteroids as an ex-vivo model of host-pathogen interactions in the gastrointestinal tract. Exp. Biol. Med. 2014, 239:1124.
33. Fouts D.E., Torralba M., Nelson K.E., Brenner D.A., Schnabl B. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J. Hepatol. 2012, 56:1283.
34. Fukui H., Brauner B., Bode J.C., Bode C. Plasma endotoxin concentrations in patients with alcoholic and non-alcoholic liver disease: reevaluation with an improved chromogenic assay. J. Hepatol. 1991, 12:162.
35. Furuta G.T., Turner J.R., Taylor C.T., Hershberg R.M., Comerford K., Narravula S., Podolsky D.K., Colgan S.P. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 2001, 193:1027.
36. Garcia-Martinez R., Caraceni P., Bernardi M., Gines P., Arroyo V., Jalan R. Albumin: pathophysiologic basis of its role in the treatment of cirrhosis and its complications. Hepatology 2013, 58:1836.
37. Gollin G., Marks C., Marks W.H. Intestinal fatty acid binding protein in serum and urine reflects early ischemic injury to the small bowel. Surgery 1993, 113:545.
38. Granger D.N., Taylor A.E. Permeability of intestinal capillaries to endogenous macromolecules. Am. J. Physiol. 1980, 238:H457.
39. Grivennikov S.I., Wang K., Mucida D., Stewart C.A., Schnabl B., Jauch D., Taniguchi K., Yu G.Y., Osterreicher C.H., Hung K.E., Datz C., Feng Y., Fearon E.R., Oukka M., Tessarollo L., Coppola V., Yarovinsky F., Cheroutre H., Eckmann L., Trinchieri G., Karin M. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012, 491:254.
40. Halme L., Turunen U., Tuominen J., Forsstrom T., Turpeinen U. Comparison of iohexol and lactulose-mannitol tests as markers of disease activity in patients with inflammatory bowel disease. Scand. J. Clin. Lab. Invest. 2000, 60:695.
41. Hartmann P., Chen P., Wang H.J., Wang L., McCole D.F., Brandl K., Starkel P., Belzer C., Hellerbrand C., Tsukamoto H., Ho S.B., Schnabl B. Deficiency of intestinal mucin-2 ameliorates experimental alcoholic liver disease in mice. Hepatology 2013, 58:108.
42. Hartmann P., Haimerl M., Mazagova M., Brenner D.A., Schnabl B. Toll-like receptor 2-mediated intestinal injury and enteric tumor necrosis factor receptor I contribute to liver fibrosis in mice. Gastroenterology 2012, 143(1330-40):e1.
43. Hober R. Ueber Resorption im Dunndarm Zweite Mittheilung, Pflugers Arch. 1899, 74:246.
44. Honzawa Y., Nakase H., Matsuura M., Chiba T. Clinical significance of serum diamine oxidase activity in inflammatory bowel disease: importance of evaluation of small intestinal permeability. Inflamm. Bowel Dis. 2011, 17:E23.
45. Iqbal T.H., Lewis K.O., Gearty J.C., Cooper B.T. Small intestinal permeability to mannitol and lactulose in the three ethnic groups resident in west Birmingham. Gut 1996, 39:199.
46. Johne B., Fagerhol M.K., Lyberg T., Prydz H., Brandtzaeg P., Naess-Andresen C.F., Dale I. Functional and clinical aspects of the myelomonocyte protein calprotectin. Mol. Pathol. 1997, 50:113.
47. Juby L.D., Rothwell J., Axon A.T. Cellobiose/mannitol sugar test-a sensitive tubeless test for coeliac disease: results on 1010 unselected patients. Gut 1989, 30:476.
48. Kanda T., Fujii H., Tani T., Murakami H., Suda T., Sakai Y., Ono T., Hatakeyama K. Intestinal fatty acid-binding protein is a useful diagnostic marker for mesenteric infarction in humans. Gastroenterology 1996, 110:339.
49. Kanda T., Nakatomi Y., Ishikawa H., Hitomi M., Matsubara Y., Ono T., Muto T. Intestinal fatty acid-binding protein as a sensitive marker of intestinal ischemia. Dig. Dis. Sci. 1992, 37:1362.
50. Keller K.M., Knobel R., Ewe K. Fecal alpha 1-antitrypsin in newborn infants. J. Pediatr. Gastroenterol. Nutr. 1997, 24:271.
51. Klingberg T.D., Pedersen M.H., Cencic A., Budde B.B. Application of measurements of transepithelial electrical resistance of intestinal epithelial cell monolayers to evaluate probiotic activity. Appl. Environ. Microbiol. 2005, 71:7528.
52. Konikoff M.R., Denson L.A. Role of fecal calprotectin as a biomarker of intestinal inflammation in inflammatory bowel disease. Inflamm. Bowel Dis. 2006, 12:524.
53. Kosek M., Haque R., Lima A., Babji S., Shrestha S., Qureshi S., Amidou S., Mduma E., Lee G., Yori P.P., Guerrant R.L., Bhutta Z., Mason C., Kang G., Kabir M., Amour C., Bessong P., Turab A., Seidman J., Olortegui M.P., Quetz J., Lang D., Gratz J., Miller M., Gottlieb M., network, M.-E. Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants. Am.J.Trop. Med. Hyg. 2013, 88:390.
54. Laine L., Garcia F., McGilligan K., Malinko A., Sinatra F.R., Thomas D.W. Protein-losing enteropathy and hypoalbuminemia in AIDS. Aids 1993, 7:837.
55. Langhorst J., Elsenbruch S., Koelzer J., Rueffer A., Michalsen A., Dobos G.J. Noninvasive markers in the assessment of intestinal inflammation in inflammatory bowel diseases: performance of fecal lactoferrin, calprotectin, and PMN-elastase, CRP, and clinical indices. Am. J. Gastroenterol. 2008, 103:162.
56. Li N., DeMarco V.G., West C.M., Neu J. Glutamine supports recovery from loss of transepithelial resistance and increase of permeability induced by media change in Caco-2 cells. J. Nutr. Biochem. 2003, 14:401.
57. Lin R.S., Lee F.Y., Lee S.D., Tsai Y.T., Lin H.C., Lu R.H., Hsu W.C., Huang C.C., Wang S.S., Lo K.J. Endotoxemia in patients with chronic liver diseases: relationship to severity of liver diseases, presence of esophageal varices, and hyperdynamic circulation. J. Hepatol. 1995, 22:165.
58. Luk G.D., Bayless T.M., Baylin S.B. Diamine oxidase (histaminase). A circulating marker for rat intestinal mucosal maturation and integrity. J. Clin. Invest. 1980, 66:66.
59. Ma T.Y., Nguyen D., Bui V., Nguyen H., Hoa N. Ethanol modulation of intestinal epithelial tight junction barrier. Am. J. Physiol. 1999, 276:G965.
60. Marchiando A.M., Graham W.V., Turner J.R. Epithelial barriers in homeostasis and disease. Annu. Rev. Pathol. 2010, 5:119.
61. Marchiando A.M., Shen L., Graham W.V., Weber C.R., Schwarz B.T., Austin J.R., Raleigh D.R., Guan Y., Watson A.J., Montrose M.H., Turner J.R. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 2010, 189:111.
62. Mattioli F., Fucile C., Marini V., Isola L., Montanaro F., Savarino V., Martelli A. Assessment of intestinal permeability using sugar probes: influence of urinary volume. Clin. Lab. 2011, 57:909.
63. Maxton D.G., Bjarnason I., Reynolds A.P., Catt S.D., Peters T.J., Menzies I.S. Lactulose, 51Cr-labelled ethylenediaminetetra-acetate, l-rhamnose and polyethyleneglycol 400 [corrected] as probe markers for assessment in vivo of human intestinal permeability. Clin. Sci. 1986, 71:71.
64. Menard S., Cerf-Bensussan N., Heyman M. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol. 2010, 3:247.
65. Menzies I.S. Absorption of intact oligosaccharide in health and disease, Biochem. Soc. Trans. 1974, 1042.
66. Menzies I.S. Transmucosal passage of inert molecules in health and disease. Intestinal Absorption and Secretion 1984, 527. MTP Press, Lancaster. E. Skadhauge (Ed.).
67. Menzies I.S., Laker M.F., Pounder R., Bull J., Heyer S., Wheeler P.G., Creamer B. Abnormal intestinal permeability to sugars in villous atrophy. Lancet 1979, 2:1107.
68. Munkholm P., Langholz E., Hollander D., Thornberg K., Orholm M., Katz K.D., Binder V. Intestinal permeability in patients with Crohn's disease and ulcerative colitis and their first degree relatives. Gut 1994, 35:68.
69. Napolitano L.M., Koruda M.J., Meyer A.A., Baker C.C. The impact of femur fracture with associated soft tissue injury on immune function and intestinal permeability. Shock 1996, 5:202.
70. Nicholson J.P., Wolmarans M.R., Park G.R. The role of albumin in critical illness. Br. J. Anaesth. 2000, 85:599.
71. Niewold T.A., Meinen M., van der Meulen J. Plasma intestinal fatty acid binding protein (I-FABP) concentrations increase following intestinal ischemia in pigs. Res. Vet. Sci. 2004, 77:89.
72. Palma P., Mihaljevic N., Hasenberg T., Keese M., Koeppel T.A. Intestinal barrier dysfunction in developing liver cirrhosis: an in vivo analysis of bacterial translocation. Hepatol. Res. 2007, 37:6.
73. Peeters M., Hiele M., Ghoos Y., Huysmans V., Geboes K., Vantrappen G., Rutgeerts P. Test conditions greatly influence permeation of water soluble molecules through the intestinal mucosa: need for standardisation. Gut 1994, 35:1404.
74. Peters T.J. Serum albumin. The Impact of Protein Chemistry on Biological Sciences: Adventures of Circulating Proteins 1984, 39. Academic Press, New York. A.N. Schechter (Ed.).
75. Rangachari P.K. Histamine: mercurial messenger in the gut. Am. J. Physiol. 1992, 262:G1.
76. Rao A.S., Camilleri M., Eckert D.J., Busciglio I., Burton D.D., Ryks M., Wong B.S., Lamsam J., Singh R., Zinsmeister A.R. Urine sugars for in vivo gut permeability: validation and comparisons in irritable bowel syndrome-diarrhea and controls. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301:G919.
77. Pijls K.E., Koek G.H., Elamin E.E., de Vries H., Masclee A.A., Jonkers D.M. Large intestine permeability is increased in patients with compensated liver cirrhosis. Am. J. Physiol. Gastrointestinal. Liver Physiol. 2014, 306:G147.
78. Rao R.K. Acetaldehyde-induced barrier disruption and paracellular permeability in Caco-2 cell monolayer. Methods Mol. Biol. 2008, 447:171.
79. Salaspuro M. Bacteriocolonic pathway for ethanol oxidation: characteristics and implications. Ann. Med. 1996, 28:195.
80. Sandler N.G., Koh C., Roque A., Eccleston J.L., Siegel R.B., Demino M., Kleiner D.E., Deeks S.G., Liang T.J., Heller T., Douek D.C. Host response to translocated microbial products predicts outcomes of patients with HBV or HCV infection. Gastroenterology 2011, 141:1220. (1230 e1-3).
81. Sapone A., de Magistris L., Pietzak M., Clemente M.G., Tripathi A., Cucca F., Lampis R., Kryszak D., Carteni M., Generoso M., Iafusco D., Prisco F., Laghi F., Riegler G., Carratu R., Counts D., Fasano A. Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 2006, 55:1443.
82. Schnabl B. Linking intestinal homeostasis and liver disease. Curr. Opin. Gastroenterol. 2013, 29:264.
83. Schnabl B., Brenner D.A. Interactions between the intestinal microbiome and liver diseases. Gastroenterology 2014, 146:1513.
84. Schoepfer A.M., Beglinger C., Straumann A., Trummler M., Renzulli P., Seibold F. Ulcerative colitis: correlation of the Rachmilewitz endoscopic activity index with fecal calprotectin, clinical activity, C-reactive protein, and blood leukocytes. Inflamm. Bowel Dis. 2009, 15:1851.
85. Seki E., Schnabl B. Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut. J. Physiol. 2012, 590:447.
86. Sequeira I.R., Lentle R.G., Kruger M.C., Hurst R.D. Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability. PLoS One 2014, 9:e99256.
87. Shakir K.M., Margolis S., Baylin S.B. Localization of histamine (diamine oxidase) in rat small intestinal mucosa: site of release by heparin. Biochem. Pharmacol. 1977, 26:2343.
88. Sharp H.L. The current status of alpha-1-antityrpsin, a protease inhibitor, in gastrointestinal disease. Gastroenterology 1976, 70:611.
89. Sipponen T. Diagnostics and prognostics of inflammatory bowel disease with fecal neutrophil-derived biomarkers calprotectin and lactoferrin. Dig. Dis. 2013, 31:336.
90. Spiller R.C., Jenkins D., Thornley J.P., Hebden J.M., Wright T., Skinner M., Neal K.R. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome. Gut 2000, 47:804.
91. Sun Z., Wang X., Andersson R. Role of intestinal permeability in monitoring mucosal barrier function. History, methodology, and significance of pathophysiology. Dig. Surg. 1998, 15:386.
92. Szabo S., Trier J.S., Brown A., Schnoor J. Early vascular injury and increased vascular permeability in gastric mucosal injury caused by ethanol in the rat. Gastroenterology 1985, 88:228.
93. Thuijls G., van Wijck K., Grootjans J., Derikx J.P., van Bijnen A.A., Heineman E., Dejong C.H., Buurman W.A., Poeze M. Early diagnosis of intestinal ischemia using urinary and plasma fatty acid binding proteins. Ann. Surg. 2011, 253:303.
94. Tripathi A., Lammers K.M., Goldblum S., Shea-Donohue T., Netzel-Arnett S., Buzza M.S., Antalis T.M., Vogel S.N., Zhao A., Yang S., Arrietta M.C., Meddings J.B., Fasano A. Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16799.
95. Turner J.R. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am. J. Pathol. 2006, 169:1901.
96. Ulluwishewa D., Anderson R.C., McNabb W.C., Moughan P.J., Wells J.M., Roy N.C. Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr. 2011, 141:769.
97. van Elburg R.M., Uil J.J., Kokke F.T., Mulder A.M., van de Broek W.G., Mulder C.J., Heymans H.S. Repeatability of the sugar-absorption test, using lactulose and mannitol, for measuring intestinal permeability for sugars. J. Pediatr. Gastroenterol. Nutr. 1995, 20:184.
98. van Elburg R.M., Uil J.J., Mulder C.J., Heymans H.S. Intestinal permeability in patients with coeliac disease and relatives of patients with coeliac disease. Gut 1993, 34:354.
99. van Nieuwenhoven M.A., Geerling B.J., Deutz N.E., Brouns F., Brummer R.J. The sensitivity of the lactulose/rhamnose gut permeability test. Eur. J. Clin. Investig. 1999, 29:160.
100. van Wijck K., Verlinden T.J., van Eijk H.M., Dekker J., Buurman W.A., Dejong C.H., Lenaerts K. Novel multi-sugar assay for site-specific gastrointestinal permeability analysis: a randomized controlled crossover trial. Clin. Nutr. 2013, 32:245.
101. Vanuytsel T., Vermeire S., Cleynen I. The role of Haptoglobin and its related protein, Zonulin, in inflammatory bowel disease. Tissue barriers 2013, 1:e27321.
102. Vogelsang H., Wyatt J., Penner E., Lochs H. Screening for celiac disease in first-degree relatives of patients with celiac disease by lactulose/mannitol test. Am. J. Gastroenterol. 1995, 90:1838.
103. Vojdani A. For the assessment of intestinal permeability, size matters. Altern. Ther. Health Med. 2013, 19:12.
104. Wang W., Uzzau S., Goldblum S.E., Fasano A. Human zonulin, a potential modulator of intestinal tight junctions. J. Cell Sci. 2000, 113(Pt 24):4435.
105. Xiang J.Y., Ouyang Q., Li G.D., Xiao N.P. Clinical value of fecal calprotectin in determining disease activity of ulcerative colitis. World J. Gastroenterol. 2008, 14:53.
106. Yan A.W., Fouts D.E., Brandl J., Starkel P., Torralba M., Schott E., Tsukamoto H., Nelson K.E., Brenner D.A., Schnabl B. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 2011, 53:96.