Journal Article
. 2004 Jun; 49(4):621-6.
doi: 10.1023/b:ddas.0000026307.56909.21.

Assessment of intestinal permeability and absorption in cirrhotic patients with ascites using combined sugar probes

Marc J Zuckerman 1 Ian S Menzies  Hoi Ho  Gavin G Gregory  Nancy A Casner  Roger S Crane  Jesus A Hernandez  
Affiliations
  • PMID: 15185867
  •     34 References
  •     21 citations

Abstract

Gastrointestinal dysfunction in patients with cirrhosis may contribute to complications such as malnutrition and spontaneous bacterial peritonitis. To determine whether cirrhotic patients with ascites have altered intestinal function, we compared intestinal permeability and absorption in patients with liver disease and normal subjects. Intestinal permeability and absorption were investigated in 66 cirrhotic patients (48 with ascites, 18 without ascites) and 74 healthy control subjects. Timed recovery of 3-O-methyl-D-glucose, D-xylose, L-rhamnose, and lactulose in urine following oral administration was measured in order to assess active and passive carrier-mediated, and nonmediated, absorptive capacity, as well as intestinal large-pore/small-pore (lactulose/rhamnose) permeability. Test sugars were measured by quantitative thin-layer chromatography and results are expressed as a percentage of test dose recovered in a 5-h urine collection. Sugar excretion ratios relating to small intestinal permeability (lactulose/rhamnose) and absorption (rhamnose/3-O-methyl-D-glucose) were calculated to avoid the effects of nonmucosal factors such as renal clearance, portal hypertension, and ascites on the recovery of sugar probes in urine. Compared with normal subjects, the mean lactulose/rhamnose permeability ratio in cirrhotic patients with ascites was significantly higher (0.058 vs. 0.037, P < 0.001) but not in cirrhotic patients without ascites (0.041 vs. 0.037). Cirrhotic patients with ascites had significantly lower mean recoveries of 3-O-methyl-D-glucose (23.0 vs. 49.1%; P < 0.001), D-xylose (18.8 vs. 34.5%; P < 0.001), L-rhamnose (4.0 vs. 9.1%; P < 0.001), and lactulose (0.202 vs. 0.337%; P < 0.001) than normal subjects. However, the mean rhamnose/3-O-methyl-D-glucose ratio was the same in cirrhotic patients with ascites as normal subjects (0.189 vs. 0.189), indicating that the reduction in probe recovery was due to nonmucosal factors. Compared with normal subjects, cirrhotic patients with ascites have abnormal intestinal permeability, measured by urinary lactulose/rhamnose excretion, and normal small intestinal absorption, assessed by the urinary rhamnose/3-O-methyl-D-glucose ratio. Low urine recovery of sugar probes found in cirrhotic patients appears to be the result of nonintestinal factors affecting clearance rather than reduced intestinal absorption.

Intestinal permeability in liver cirrhosis: relationship with severe septic complications.
B Campillo, P Pernet, +3 authors, C Aussel.
Eur J Gastroenterol Hepatol, 1999 Aug 13; 11(7). PMID: 10445796
Intestinal permeability: an overview.
I Bjarnason, A MacPherson, D Hollander.
Gastroenterology, 1995 May 01; 108(5). PMID: 7729650
Highly Cited. Review.
D-xylose testing.
R M Craig, E D Ehrenpreis.
J Clin Gastroenterol, 1999 Sep 09; 29(2). PMID: 10478874
Review.
Bacterial translocation in cirrhotic rats. Its role in the development of spontaneous bacterial peritonitis.
J M Llovet, R Bartolí, +6 authors, M A Gassull.
Gut, 1994 Nov 01; 35(11). PMID: 7828991    Free PMC article.
Abnormalities of gastric emptying in portal hypertension.
K K Balan, S Grime, +2 authors, S A Jenkins.
Am J Gastroenterol, 1996 Mar 01; 91(3). PMID: 8633503
Quantitative estimation of sugars in blood and urine by paper chromatography using direct densitometry.
I S Menzies.
J Chromatogr, 1973 Jun 27; 81(1). PMID: 4725409
Distribution of d-xylose in sequestered fluid resulting in false-positive tests for malabsorption.
G A Marin, M L Clark, J R Senior.
Ann Intern Med, 1968 Dec 01; 69(6). PMID: 5725732
Geography of intestinal permeability and absorption.
I S Menzies, M J Zuckerman, +5 authors, G G Gregory.
Gut, 1999 Mar 17; 44(4). PMID: 10075954    Free PMC article.
Leaky gut in alcoholic cirrhosis: a possible mechanism for alcohol-induced liver damage.
A Keshavarzian, E W Holmes, +3 authors, S Pethkar.
Am J Gastroenterol, 1999 Feb 06; 94(1). PMID: 9934756
Highly Cited.
Abnormalities in proximal small bowel motility in patients with cirrhosis.
J Chesta, C Defilippi, C Defilippi.
Hepatology, 1993 May 01; 17(5). PMID: 8491451
Gastrointestinal dysfunction in liver disease and portal hypertension. Gut-liver interactions revisited.
E M Quigley.
Dig Dis Sci, 1996 Mar 01; 41(3). PMID: 8617136
Review.
Lactulose-L-rhamnose intestinal permeability test in patients with liver cirrhosis.
T Fujii, T Seki, +5 authors, K Inoue.
Hepatol Res, 2001 Feb 13; 19(2). PMID: 11164740
Small intestinal bacterial overgrowth in patients with cirrhosis: prevalence and relation with spontaneous bacterial peritonitis.
T M Bauer, B Steinbrückner, +6 authors, H E Blum.
Am J Gastroenterol, 2001 Nov 06; 96(10). PMID: 11693333
Bacterial translocation to mesenteric lymph nodes is increased in cirrhotic rats with ascites.
G Garcia-Tsao, F Y Lee, +2 authors, A B West.
Gastroenterology, 1995 Jun 01; 108(6). PMID: 7768390
Water and electrolyte movement and mucosal morphology in the jejunum of patients with portal hypertension.
D A Norman, J M Atkins, +2 authors, G J Krejs.
Gastroenterology, 1980 Oct 01; 79(4). PMID: 7409388
Histomorphometric study of portal hypertensive enteropathy.
V Misra, S P Misra, M Dwivedi, S C Gupta.
Am J Clin Pathol, 1997 Dec 31; 108(6). PMID: 9384446
Small intestine dysmotility and bacterial overgrowth in cirrhotic patients with spontaneous bacterial peritonitis.
C S Chang, G H Chen, H C Lien, H Z Yeh.
Hepatology, 1998 Oct 31; 28(5). PMID: 9794900
Simultaneous determination of pulmonary and intestinal permeability in patients with alcoholic liver cirrhosis.
D Huglo, S De Botton, +4 authors, X Marchandise.
Eur J Nucl Med, 2001 Oct 31; 28(10). PMID: 11685493
Intestinal permeability in gastrointestinal disorders. Use of oral [99mTc]DTPA.
R H Resnick, H Royal, +2 authors, T Werth.
Dig Dis Sci, 1990 Feb 01; 35(2). PMID: 2406112
Prevalence of associated infections in community-acquired spontaneous bacterial peritonitis.
H Ho, M J Zuckerman, +3 authors, P R Casner.
Am J Gastroenterol, 1996 Apr 01; 91(4). PMID: 8677940
Quantitative estimation of clinically important monosaccharides in plasma by rapid thin layer chromatography.
I S Menzies, J N Mount, M J Wheeler.
Ann Clin Biochem, 1978 Mar 01; 15(2). PMID: 637512
Intestinal absorption and unmediated permeation of sugars in post-infective tropical malabsorption (tropical sprue).
G C Cook, I S Menzies.
Digestion, 1986 Jan 01; 33(2). PMID: 3949090
Spontaneous bacterial peritonitis.
J Such, B A Runyon.
Clin Infect Dis, 1998 Nov 03; 27(4). PMID: 9798013
Review.
Investigation of intestine and liver function in cirrhosis using combined sugar oral loads.
G Budillon, G Parrilli, +2 authors, I S Menzies.
J Hepatol, 1985 Jan 01; 1(5). PMID: 4056352
Intestinal permeability in dermatitis herpetiformis.
C E Griffiths, I S Menzies, +2 authors, L Fry.
J Invest Dermatol, 1988 Aug 01; 91(2). PMID: 3397588
Effect of selective bowel decontamination with norfloxacin on spontaneous bacterial peritonitis, translocation, and survival in an animal model of cirrhosis.
B A Runyon, M Borzio, +3 authors, M A Runyon.
Hepatology, 1995 Jun 01; 21(6). PMID: 7768517
Intestinal permeability in liver cirrhosis.
G Ersöz, A Aydin, +3 authors, K Kumanlioglu.
Eur J Gastroenterol Hepatol, 1999 May 13; 11(4). PMID: 10321758
THE EFFECT OF PORTAL HYPERTENSION ON INTESTINAL ABSORPTION.
I F ENQUIST, M R GOLDING, +2 authors, N A SOLOMON.
Surg Gynecol Obstet, 1965 Jan 01; 120. PMID: 14259791
Small bowel bacterial overgrowth in patients with alcoholic cirrhosis.
F Casafont Morencos, G de las Heras Castaño, +3 authors, F Pons Romero.
Dig Dis Sci, 1996 Mar 01; 41(3). PMID: 8617135
Malabsorption and nutritional abnormalities in patients with liver cirrhosis.
A Romiti, M Merli, +6 authors, G Budillon.
Ital J Gastroenterol, 1990 Jun 01; 22(3). PMID: 2131941
Bacterial infections in liver disease.
M Navasa, A Rimola, J Rodés.
Semin Liver Dis, 1997 Jan 01; 17(4). PMID: 9408968
Review.
Translocation of gut bacteria in rats with cirrhosis to mesenteric lymph nodes partially explains the pathogenesis of spontaneous bacterial peritonitis.
B A Runyon, S Squier, M Borzio.
J Hepatol, 1994 Nov 01; 21(5). PMID: 7890896
Sugar absorption tests, with special reference to 3-0-methyl-d-glucose and d-xylose.
J S FORDTRAN, P H CLODI, K H SOERGEL, F J INGELFINGER.
Ann Intern Med, 1962 Dec 01; 57. PMID: 13958713
Liver disease and malabsorption.
M S Losowsky, B E Walker.
Gastroenterology, 1969 Mar 01; 56(3). PMID: 4886030
Review.
Gut flora and bacterial translocation in chronic liver disease.
John Almeida, Sumedha Galhenage, +2 authors, Stephen M Riordan.
World J Gastroenterol, 2006 Mar 30; 12(10). PMID: 16570339    Free PMC article.
Review.
Increased intestinal macromolecular permeability and urine nitrite excretion associated with liver cirrhosis with ascites.
Soong Lee, Seung-Cheol Son, +6 authors, Myung-Geun Shin.
World J Gastroenterol, 2008 Jul 09; 14(24). PMID: 18609714    Free PMC article.
Pharmacokinetics and dosage adjustment in patients with hepatic dysfunction.
Roger K Verbeeck.
Eur J Clin Pharmacol, 2008 Sep 03; 64(12). PMID: 18762933
Highly Cited. Review.
Uptake of 18F-labeled 6-fluoro-6-deoxy-D-glucose by skeletal muscle is responsive to insulin stimulation.
Chandra Spring-Robinson, Visvanathan Chandramouli, +5 authors, Raymond F Muzic.
J Nucl Med, 2009 May 16; 50(6). PMID: 19443592    Free PMC article.
Impaired glucose and nutrient absorption in critical illness: is gastric emptying only a piece of the puzzle?
Alain Dive.
Crit Care, 2009 Oct 13; 13(5). PMID: 19818163    Free PMC article.
Analysis of metabolism of 6FDG: a PET glucose transport tracer.
Raymond F Muzic, Visvanathan Chandramouli, +3 authors, Faramarz Ismail-Beigi.
Nucl Med Biol, 2011 Jul 02; 38(5). PMID: 21718942    Free PMC article.
Potential drug-drug interactions and adverse drug reactions in patients with liver cirrhosis.
Carmen C Franz, Sabin Egger, +2 authors, Stephan Krähenbühl.
Eur J Clin Pharmacol, 2011 Aug 16; 68(2). PMID: 21842337
Gut microbiota and inflammation.
Asa Hakansson, Goran Molin.
Nutrients, 2012 Jan 19; 3(6). PMID: 22254115    Free PMC article.
Highly Cited. Review.
Microbial translocation in chronic liver diseases.
Marilia Rita Pinzone, Benedetto Maurizio Celesia, +2 authors, Giuseppe Nunnari.
Int J Microbiol, 2012 Aug 01; 2012. PMID: 22848224    Free PMC article.
Relevance of Liver Failure for Anti-Infective Agents: From Pharmacokinetic Alterations to Dosage Adjustments.
Fiona V Bϋdingen, Daniel Gonzalez, Amelia N Tucker, Hartmut Derendorf.
Ther Adv Infect Dis, 2014 Jun 21; 2(1). PMID: 24949199    Free PMC article.
Gastrointestinal dysfunction in liver cirrhosis.
Evangelos Kalaitzakis.
World J Gastroenterol, 2014 Oct 31; 20(40). PMID: 25356031    Free PMC article.
Review.
Gut-liver axis in liver cirrhosis: How to manage leaky gut and endotoxemia.
Hiroshi Fukui.
World J Hepatol, 2015 Apr 08; 7(3). PMID: 25848468    Free PMC article.
Review.
Low risk of bacteremia after endoscopic variceal therapy for esophageal varices: a systematic review and meta-analysis.
Yi Jia, Alok Dwivedi, +3 authors, Marc Zuckerman.
Endosc Int Open, 2015 Nov 04; 3(5). PMID: 26528494    Free PMC article.
Review.
Gut epithelial barrier dysfunction in human immunodeficiency virus-hepatitis C virus coinfected patients: Influence on innate and acquired immunity.
Mercedes Márquez, Clotilde Fernández Gutiérrez del Álamo, José Antonio Girón-González.
World J Gastroenterol, 2016 Jan 29; 22(4). PMID: 26819512    Free PMC article.
Review.
Intestinal permeability in a patient with liver cirrhosis.
Jonathan Manuel Aguirre Valadez, Liliana Rivera-Espinosa, +3 authors, Aldo Torre.
Ther Clin Risk Manag, 2016 Dec 07; 12. PMID: 27920543    Free PMC article.
Review.
Changes of Intestinal Functions in Liver Cirrhosis.
Hiroshi Fukui, Reiner Wiest.
Inflamm Intest Dis, 2016 Apr 01; 1(1). PMID: 29922655    Free PMC article.
Review.
Taurocholic acid is an active promoting factor, not just a biomarker of progression of liver cirrhosis: evidence from a human metabolomic study and in vitro experiments.
Zhimin Liu, Zhifeng Zhang, +5 authors, Zhijun Duan.
BMC Gastroenterol, 2018 Jul 13; 18(1). PMID: 29996772    Free PMC article.
Dietary approach and gut microbiota modulation for chronic hepatic encephalopathy in cirrhosis.
Daniela Campion, Ilaria Giovo, +3 authors, Carlo Alessandria.
World J Hepatol, 2019 Jul 12; 11(6). PMID: 31293718    Free PMC article.
Review.
Regulatory T Cells Restrict Permeability to Bacterial Antigen Translocation and Preserve Short-Chain Fatty Acids in Experimental Cirrhosis.
Oriol Juanola, Paula Piñero, +8 authors, Rubén Francés.
Hepatol Commun, 2018 Dec 18; 2(12). PMID: 30556045    Free PMC article.
Evaluation of Serum-Derived Bovine Immunoglobulin Protein Isolate in Subjects With Decompensated Cirrhosis With Ascites.
Matthew J Stotts, Amanda Cheung, +6 authors, Charlene Prather.
Cureus, 2021 Jul 13; 13(6). PMID: 34249551    Free PMC article.
Leaky Gut and Gut-Liver Axis in Liver Cirrhosis: Clinical Studies Update.
Hiroshi Fukui.
Gut Liver, 2020 Oct 20; 15(5). PMID: 33071239    Free PMC article.
Review.