Generic placeholder image

Reviews on Recent Clinical Trials


ISSN (Print): 1574-8871
ISSN (Online): 1876-1038

Review Article

Gut Alterations in Septic Patients: A Biochemical Literature Review

Author(s): Yaroslava Longhitano*, Christian Zanza, Duraiyah Thangathurai, Samanta Taurone, Daniela Kozel, Fabrizio Racca, Andrea Audo, Enrico Ravera, Alessio Migneco, Andrea Piccioni and Francesco Franceschi

Volume 15, Issue 4, 2020

Page: [289 - 297] Pages: 9

DOI: 10.2174/1574887115666200811105251

Price: $65


Background: Sepsis is a life-threatening organ dysfunction with high mortality and morbidity rate and with the disease progression many alterations are observed in different organs. The gastrointestinal tract is often damaged during sepsis and septic shock and main symptoms are related to increased permeability, bacterial translocation and malabsorption. These intestinal alterations can be both cause and effect of sepsis.

Objective: The aim of this review is to analyze different pathways that lead to intestinal alteration in sepsis and to explore the most common methods for intestinal permeability measurement and, at the same time to evaluate if their use permit to identify patients at high risk of sepsis and eventually to estimate the prognosis.

Material and Methods: The peer-reviewed articles analyzed were selected from PubMed databases using the keywords “sepsis” “gut alteration”, “bowel permeability”, “gut alteration”, “bacterial translocation”, “gut permeability tests”, “gut inflammation”. Among the 321 papers identified, 190 articles were selected, after title - abstract examination and removing the duplicates and studies on pediatric population,only 105 articles relating to sepsis and gut alterations were analyzed.

Results: Integrity of the intestinal barrier plays a key role in the preventing of bacterial translocation and gut alteration related to sepsis. It is obvious that this dysfunction of the small intestine can have serious consequences and the early identification of patients at risk - to develop malabsorption or already malnourished - is very recommended to increase the survivor rate. Until now, in critical patients, the dosage of citrullinemia is easily applied test in clinical setting, in fact, it is relatively easy to administer and allows to accurately assess the functionality of enterocytes.

Conclusion: The sepsis can have an important impact on the gastrointestinal function. In addition, the alteration of the permeability can become a source of systemic infection. At the moment, biological damage markers are not specific, but the dosage of LPS, citrulline, lactulose/mannitol test, FABP and fecal calprotectin are becoming an excellent alternative with high specificity and sensitivity.

Keywords: Sepsis, gut alteration, bowel permeability, bacteria translocation, gut permeability test, gut inflammation.

Graphical Abstract
Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA 2016; 315(8): 801-10.
[] [PMID: 26903338]
Angus DC, van der Poll T. Severe sepsis and septic shock. N Engl J Med 2013; 369(9): 840-51.
[] [PMID: 23984731]
Dellinger RP, Levy MM, Rhodes A, et al. Surviving sepsis campaign guidelines committee including the pediatric subgroup. surviving sepsis campaign: International guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med 2013; 39(2): 165-228.
[] [PMID: 23361625]
Brandtzaeg P. The gut as communicator between environment and host: Immunological consequences. Eur J Pharmacol 2011; 668(Suppl. 1): S16-32.
[] [PMID: 21816150]
Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science 2012; 336(6086): 1268-73.
[] [PMID: 22674334]
Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489(7415): 231-41.
[] [PMID: 22972296]
Scaldaferri F, Pizzoferrato M, Gerardi V, Lopetuso L, Gasbarrini A. The gut barrier: New acquisitions and therapeutic approaches. J Clin Gastroenterol 2012; 46(Suppl): S12-S17.5.
Bischoff SC. ‘Gut health’: A new objective in medicine? BMC Med 2011; 9: 24.
[] [PMID: 21401922]
Camilleri M, Madsen K, Spiller R, Greenwood-Van Meerveld B, Verne GN. Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol Motil 2012; 24(6): 503-12.
[] [PMID: 22583600]
Radeva MY, Waschke J. Mind the gap: Mechanisms regulating the endothelial barrier. Acta Physiol (Oxf) 2018; 222(1): e12860.
[] [PMID: 28231640]
Raleigh DR, Marchiando AM, Zhang Y, et al. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 2010; 21(7): 1200-13.
[] [PMID: 20164257]
Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 2011; 141(5): 769-76.
[] [PMID: 21430248]
McGuckin MA, Lindén SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 2011; 9(4): 265-78.
[] [PMID: 21407243]
Eisenhoffer GT, Loftus PD, Yoshigi M, et al. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 2012; 484(7395): 546-9.
[] [PMID: 22504183]
Gu Y, Forostyan T, Sabbadini R, Rosenblatt J. Epithelial cell extrusion requires the sphingosine-1-phosphate receptor 2 pathway. J Cell Biol 2011; 193(4): 667-76.
[] [PMID: 21555463]
Marchiando AM, Shen L, Graham WV, et al. The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology 2011; 140(4): 1208-1218.e1, 2.
[] [PMID: 21237166]
Garabedian EM, Roberts LJ, McNevin MS, Gordon JI. Examining the role of Paneth cells in the small intestine by lineage ablation in transgenic mice. J Biol Chem 1997; 272(38): 23729-40.
[] [PMID: 9295317]
Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000; 288(5474): 2222-6.
[] [PMID: 10864873]
Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol 2008; 1(1): 11-22.
[] [PMID: 19079156]
Bischoff SC, Mailer R, Pabst O, et al. Role of serotonin in intestinal inflammation: Knockout of serotonin reuptake transporter exacerbates 2,4,6-trinitrobenzene sulfonic acid colitis in mice. Am J Physiol Gastrointest Liver Physiol 2009; 296(3): G685-95.
[] [PMID: 19095763]
Stadnyk AW. Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can J Gastroenterol 2002; 16(4): 241-6.
[] [PMID: 11981577]
Gersemann M, Wehkamp J, Stange EF. Innate immune dysfunction in inflammatory bowel disease. J Intern Med 2012; 271(5): 421-8.
[] [PMID: 22324936]
Dharmani P, Srivastava V, Kissoon-Singh V, Chadee K. Role of intestinal mucins in innate host defense mechanisms against pathogens. J Innate Immun 2009; 1(2): 123-35.
[] [PMID: 20375571]
Schmid-Schönbein GW, Hugli TE. A new hypothesis for microvascular inflammation in shock and multiorgan failure: Self-digestion by pancreatic enzymes. Microcirculation 2005; 12(1): 71-82.
[] [PMID: 15804975]
Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004; 303(5664): 1662-5.
[] [PMID: 15016999]
Schmid-Schönbein GW, Penn A, Kistler E. The autodigestion hypothesis in shock and multi-organ failure: Degrading protease activity. Bol Soc Port Hemorreol Microcirc 2011; 26(3): 6-15.
[PMID: 25284955]
Bermejo-Martin JF, Andaluz-Ojeda D, Almansa R, et al. Defining immunological dysfunction in sepsis: A requisite tool for precision medicine. J Infect 2016; 72(5): 525-36.
[] [PMID: 26850357]
Bianchi ME. DAMPs, PAMPs and alarmins: All we need to know about danger. J Leukoc Biol 2007; 81(1): 1-5.
[] [PMID: 17032697]
Schnoor M, García Ponce A, Vadillo E, Pelayo R, Rossaint J, Zarbock A. Actin dynamics in the regulation of endothelial barrier functions and neutrophil recruitment during endotoxemia and sepsis. Cell Mol Life Sci 2017; 74(11): 1985-97.
[] [PMID: 28154894]
Wells JM, Brummer RJ, Derrien M, et al. Homeostasis of the gut barrier and potential biomarkers. Am J Physiol Gastrointest Liver Physiol 2017; 312(3): G171-93.
[] [PMID: 27908847]
Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: Recent insights and progress. Curr Gastroenterol Rep 2010; 12(5): 319-30.
[] [PMID: 20703838]
Altshuler AE, Lamadrid I, Li D, et al. Transmural intestinal wall permeability in severe ischemia after enteral protease inhibition. PLoS One 2014; 9(5): e96655.
[] [PMID: 24805256]
Shimizu K, Ogura H, Hamasaki T, et al. Altered gut flora are associated with septic complications and death in critically ill patients with systemic inflammatory response syndrome. Dig Dis Sci 2011; 56(4): 1171-7.
[] [PMID: 20931284]
Wang L, Bastarache JA, Ware LB. The coagulation cascade in sepsis. Curr Pharm Des 2008; 14: 1860-9.
Jiang LY, Zhang M, Zhou TE, Yang ZF, Wen LQ, Chang JX. Changes of the immunological barrier of intestinal mucosa in rats with sepsis. World J Emerg Med 2010; 1(2): 138-43.
[PMID: 25214957]
Spronk PE, Zandstra DF, Ince C. Bench-to-bedside review: Sepsis is a disease of the microcirculation. Crit Care 2004; 8(6): 462-8.
[] [PMID: 15566617]
Theuer CJ, Wilson MA, Steeb GD, Garrison RN. Microvascular vasoconstriction and mucosal hypoperfusion of the rat small intestine during bacteremia. Circ Shock 1993; 40(1): 61-8.
[PMID: 8324891]
Amalakuhan B, Habib SA, Mangat M, et al. Endothelial adhesion molecules and multiple organ failure in patients with severe sepsis. Cytokine 2016; 88: 267-73.
[] [PMID: 27701021]
Silswal N, Reddy NS, Qureshi AA, Qureshi N. Resveratrol downregulates biomarkers of sepsis via inhibition of proteasome’s proteases. Shock 2018; 50(5): 579-88.
[] [PMID: 29240645]
Ellis CG, Jagger J, Sharpe M. The microcirculation as a functional system. Crit Care 2005; 9(Suppl. 4): S3-8.
[] [PMID: 16168072]
Deitch EA. Bacterial translocation or lymphatic drainage of toxic products from the gut: What is important in human beings? Surgery 2002; 131(3): 241-4.
[] [PMID: 11894026]
Gustot T. Multiple organ failure in sepsis: Prognosis and role of systemic inflammatory response. Curr Opin Crit Care 2011; 17(2): 153-9.
[] [PMID: 21346564]
Moore FA, Moore EE, Poggetti R, et al. Gut bacterial translocation via the portal vein: A clinical perspective with major torso trauma. J Trauma 1991; 31(5): 629-36.
[] [PMID: 2030509]
Chang M, Alsaigh T, Kistler EB, Schmid-Schonbein GW. Breakdown of mucin as barrier to digestive enzymes in the ischemic rat small intestine. PLoS ONE 2012; 7: e40087.
Defazio J, Fleming ID, Shakhsheer B, Zaborina O, Alverdy JC. The opposing forces of the intestinal microbiome and the emerging pathobiome. Surg Clin North Am 2014; 94(6): 1151-61.
[] [PMID: 25440116]
Li KY, Jiang LY, Zhang M, Zhong M, Xie WZ. Effects of ulinastatin on gut mucosal apoptosis and bacterial translocation in rats with sepsis. Nan Fang Yi Ke Da Xue Xue Bao 2008; 28(7): 1244-6.
[PMID: 18676274]
Dempfle CE. Coagulopathy of sepsis. Thromb Haemost 2004; 91(2): 213-24.
[] [PMID: 14961146]
De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002; 166(1): 98-104.
[] [PMID: 12091178]
Prin M, Bakker J, Wagener G. Hepatosplanchnic circulation in cirrhosis and sepsis. World J Gastroenterol 2015; 21(9): 2582-92.
[] [PMID: 25759525]
Hoyt DB. Looking forward. The trauma, critical care and acute care surgery program. Bull Am Coll Surg 2012; 97(2): 4-5.
[PMID: 24010247]
Ince C. The microcirculation is the motor of sepsis. Crit Care 2005; 9(Suppl. 4): S13-9.
[] [PMID: 16168069]
Farquhar I, Martin CM, Lam C, Potter R, Ellis CG, Sibbald WJ. Decreased capillary density in vivo in bowel mucosa of rats with normotensive sepsis. J Surg Res 1996; 61(1): 190-6.
[] [PMID: 8769965]
Lemaire LC, van Lanschot JB, Stoutenbeek CP, et al. Thoracic duct in patients with multiple organ failure: No major route of bacterial translocation. Ann Surg 1999; 229(1): 128-36.
[] [PMID: 9923810]
Trzeciak S, Cinel I, Phillip Dellinger R, et al. Microcirculatory Alterations in Resuscitation and Shock (MARS) Investigators. Resuscitating the microcirculation in sepsis: the central role of nitric oxide, emerging concepts for novel therapies, and challenges for clinical trials. Acad Emerg Med 2008; 15(5): 399-413.
[] [PMID: 18439194]
Sielenkämper AW, Meyer J, Kloppenburg H, Eicker K, Van Aken H. The effects of sepsis on gut mucosal blood flow in rats. Eur J Anaesthesiol 2001; 18(10): 673-8.
[] [PMID: 11553244]
Moon R, Parikh AA, Szabo C, Fischer JE, Salzman AL, Hasselgren PO. Complement C3 production in human intestinal epithelial cells is regulated by interleukin 1beta and tumor necrosis factor alpha. Arch Surg 1997; 132(12): 1289-93.
[] [PMID: 9403532]
Sünderhauf A, Skibbe K, Preisker S, et al. Regulation of epithelial cell expressed C3 in the intestine - Relevance for the pathophysiology of inflammatory bowel disease? Mol Immunol 2017; 90: 227-38.
[] [PMID: 28843904]
Sipola S, Ala-Kokko TI, Laurila JJ, et al. Colon epithelial injury in critically ill colectomized patients: Aberration of tight junction proteins and Toll-like receptors. Minerva Anestesiol 2017; 83(10): 1017-25.
[] [PMID: 28409518]
Li Q, Zhang Q, Wang C, Liu X, Li N, Li J. Disruption of tight junctions during polymicrobial sepsis in vivo. J Pathol 2009; 218(2): 210-21.
[] [PMID: 19235836]
Klaus DA, Motal MC, Burger-Klepp U, et al. Increased plasma zonulin in patients with sepsis. Biochem Med (Zagreb) 2013; 23(1): 107-11.
[] [PMID: 23457771]
Yu P, Martin CM. Increased gut permeability and bacterial translocation in Pseudomonas pneumonia-induced sepsis. Crit Care Med 2000; 28(7): 2573-7.
[] [PMID: 10921597]
van Vliet MJ, Tissing WJ, Rings EH, et al. Citrulline as a marker for chemotherapy induced mucosal barrier injury in pediatric patients. Pediatr Blood Cancer 2009; 53(7): 1188-94.
[] [PMID: 19688831]
Lutgens LC, Blijlevens NM, Deutz NE, Donnelly JP, Lambin P, de Pauw BE. Monitoring myeloablative therapy-induced small bowel toxicity by serum citrulline concentration: A comparison with sugar permeability tests. Cancer 2005; 103(1): 191-9.
[] [PMID: 15573372]
Fredenburgh LE, Velandia MM, Ma J, et al. Cyclooxygenase-2 deficiency leads to intestinal barrier dysfunction and increased mortality during polymicrobial sepsis. J Immunol 2011; 187(10): 5255-67.
[] [PMID: 21967897]
Meng J, Yu H, Ma J, et al. Morphine induces bacterial translocation in mice by compromising intestinal barrier function in a TLR-dependent manner. PLoS One 2013; 8(1): : e54040..
[] [PMID: 23349783]
Yoseph BP, Klingensmith NJ, Liang Z, et al. Mechanisms of intestinal barrier dysfunction in sepsis. Shock 2016; 46(1): 52-9.
[] [PMID: 27299587]
Hunninghake GW, Doerschug KC, Nymon AB, Schmidt GA, Meyerholz DK, Ashare A. Insulin-like growth factor-1 levels contribute to the development of bacterial translocation in sepsis. Am J Respir Crit Care Med 2010; 182(4): 517-25.
[] [PMID: 20413631]
Penn AH, Hugli TE, Schmid-Schönbein GW. Pancreatic enzymes generate cytotoxic mediators in the intestine. Shock 2007; 27(3): 296-304.
[] [PMID: 17304111]
O’Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep 2006; 7: 688-93.
O’Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC. Microbiology of bacterial translocation in humans. Gut 1998; 42(1): 29-35.
[] [PMID: 9505882]
Reino DC, Pisarenko V, Palange D, et al. Trauma hemorrhagic shock-induced lung injury involves a gut-lymph-induced TLR4 pathway in mice. PLoS One 2011. 6(8), e14829.
[] [PMID: 21829592]
Cabrera-Perez J, Badovinac VP, Griffith TS. Enteric immunity, the gut microbiome, and sepsis: rethinking the germ theory of disease. Exp Biol Med 2017; 242: 127-39.
Meng J, Banerjee S, Li D, et al. Opioid exacerbation of gram-positive sepsis, induced by gut microbial modulation, is rescued by IL-17A neutralization. Sci Rep 2015; 5: 10918.
[] [PMID: 26039416]
Deshmukh HS, Liu Y, Menkiti OR, et al. The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat Med 2014; 20(5): 524-30.
[] [PMID: 24747744]
Anderson AD, Jain PK, Fleming S, Poon P, Mitchell CJ, MacFie J. Evaluation of a triple sugar test of colonic permeability in humans. Acta Physiol Scand 2004; 182(2): 171-7.
[] [PMID: 15450113]
van Wijck K, Verlinden TJ, van Eijk HM, et al. Novel multi-sugar assay for site-specific gastrointestinal permeability analysis: A randomized controlled crossover trial. Clin Nutr 2013; 32(2): 245-51.
[] [PMID: 22892368]
Harris CE, Griffiths RD, Freestone N, Billington D, Atherton ST, Macmillan RR. Intestinal permeability in the critically ill. Intensive Care Med 1992; 18(1): 38-41.
[] [PMID: 1578045]
Ohri SK, Somasundaram S, Koak Y, et al. The effect of intestinal hypoperfusion on intestinal absorption and permeability during cardiopulmonary bypass. Gastroenterology 1994; 106(2): 318-23.
[] [PMID: 8299899]
Kerckhoffs AP, Akkermans LM, de Smet MB, et al. Intestinal permeability in irritable bowel syndrome patients: Effects of NSAIDs. Dig Dis Sci 2010; 55(3): 716-23.
[] [PMID: 19255843]
Ammori BJ, Leeder PC, King RF, et al. Early increase in intestinal permeability in patients with severe acute pancreatitis: Correlation with endotoxemia, organ failure, and mortality. J Gastrointest Surg 1999; 3(3): 252-62.
[] [PMID: 10481118]
Lee S, Son SC, Han MJ, et al. Increased intestinal macromolecular permeability and urine nitrite excretion associated with liver cirrhosis with ascites. World J Gastroenterol 2008; 14(24): 3884-90.
[] [PMID: 18609714]
Solligård E, Juel IS, Spigset O, Romundstad P, Grønbech JE, Aadahl P. Gut luminal lactate measured by microdialysis mirrors permeability of the intestinal mucosa after ischemia. Shock 2008; 29(2): 245-51.
[PMID: 17693938]
Jenkins RT, Ramage JK, Jones DB, Collins SM, Goodacre RL, Hunt RH. Small bowel and colonic permeability to 51Cr-EDTA in patients with active inflammatory bowel disease. Clin Invest Med 1988; 11(2): 151-5.
[PMID: 3135136]
Bates DW, Parsonnet J, Ketchum PA, et al. AMCC Sepsis Project Working Group. Limulus amebocyte lysate assay for detection of endotoxin in patients with sepsis syndrome. Clin Infect Dis 1998; 27(3): 582-91.
[] [PMID: 9770160]
Bergheim I, Weber S, Vos M, et al. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: Role of endotoxin. J Hepatol 2008; 48(6): 983-92.
[] [PMID: 18395289]
Thuy S, Ladurner R, Volynets V, et al. Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr 2008; 138(8): 1452-5.
[] [PMID: 18641190]
Strutz F, Heller G, Krasemann K, Krone B, Müller GA. Relationship of antibodies to endotoxin core to mortality in medical patients with sepsis syndrome. Intensive Care Med 1999; 25(5): 435-44.
[] [PMID: 10401935]
Pascal C, Bernard M, Luc C. Cytrulline as biomarker of intestinal failure due to enterocyte mass reduction. Clin Nutr 2008; 27(3): 328-39.
Bennett-Guerrero E, Barclay GR, Weng PL, et al. Endotoxin-neutralizing capacity of serum from cardiac surgical patients. J Cardiothorac Vasc Anesth 2001; 15(4): 451-4.
[] [PMID: 11505348]
Crenn P, Coudray-Lucas C, Thuillier F, Cynober L, Messing B. Postabsorptive plasma citrulline concentration is a marker of absorptive enterocyte mass and intestinal failure in humans. Gastroenterology 2000; 119(6): 1496-505.
[] [PMID: 11113071]
Relja B, Szermutzky M, Henrich D, et al. Intestinal-FABP and liver-FABP: Novel markers for severe abdominal injury. Acad Emerg Med 2010; 17(7): 729-35.
[] [PMID: 20653587]
Pedersen L, Nybo M, Poulsen MK, Henriksen JE, Dahl J, Rasmussen LM. Plasma calprotectin and its association with cardiovascular disease manifestations, obesity and the metabolic syndrome in type 2 diabetes mellitus patients. BMC Cardiovasc Disord 2014; 14: 196.
[] [PMID: 25527236]
Reisinger KW, Derikx JP, Thuijls G, et al. Noninvasive measurement of intestinal epithelial damage at time of refeeding can predict clinical outcome after necrotizing enterocolitis. Pediatr Res 2013; 73(2): 209-13.
[] [PMID: 23154757]
Monbaliu D, de Vries B, Crabbé T, et al. Liver fatty acid-binding protein: an early and sensitive plasma marker of hepatocellular damage and a reliable predictor of graft viability after liver transplantation from non-heart-beating donors. Transplant Proc 2005; 37(1): 413-6.
[] [PMID: 15808662]
Vreugdenhil AC, Wolters VM, Adriaanse MP, et al. Additional value of serum I-FABP levels for evaluating celiac disease activity in children. Scand J Gastroenterol 2011; 46(12): 1435-41.
[] [PMID: 22029621]
Fagerhol MK. Calprotectin, a faecal marker of organic gastrointestinal abnormality. Lancet 2000; 356(9244): 1783-4.
[] [PMID: 11117904]
Lundberg JO, Hellström PM, Fagerhol MK, Weitzberg E, Roseth AG. Technology insight: Calprotectin, lactoferrin and nitric oxide as novel markers of inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol 2005; 2(2): 96-102.
[] [PMID: 16265127]
Thuijls G, Derikx JP, van Wijck K, et al. Non-invasive markers for early diagnosis and determination of the severity of necrotizing enterocolitis. Ann Surg 2010; 251(6): 1174-80.
[] [PMID: 20485148]
Damms A, Bischoff SC. Validation and clinical significance of a new calprotectin rapid test for the diagnosis of gastrointestinal diseases. Int J Colorectal Dis 2008; 23(10): 985-92.
[] [PMID: 18629518]
van Wijck K, Lenaerts K, van Loon LJ, Peters WH, Buurman WA, Dejong CH. Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men. PLoS One 2011; 6(7): e22366.
[] [PMID: 21811592]
Thuijls G, van Wijck K, Grootjans J, et al. Early diagnosis of intestinal ischemia using urinary and plasma fatty acid binding proteins. Ann Surg 2011; 253(2): 303-8.
[] [PMID: 21245670]
Grootjans J, Hodin CM, de Haan JJ, et al. Level of activation of the unfolded protein response correlates with Paneth cell apoptosis in human small intestine exposed to ischemia/reperfusion. Gastroenterology 2011; 140(2): 529-539.e3.
[] [PMID: 20965186]
Grootjans J, Hundscheid IH, Lenaerts K, et al. Ischaemia-induced mucus barrier loss and bacterial penetration are rapidly counteracted by increased goblet cell secretory activity in human and rat colon. Gut 2013; 62(2): 250-8.
[] [PMID: 22637697]
Rayes N, Seehofer D, Hansen S, et al. Early enteral supply of lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation 2002; 74(1): 123-7.
[] [PMID: 12134110]
Rayes N, Seehofer D, Theruvath T, et al. Supply of pre- and probiotics reduces bacterial infection rates after liver transplantation- a randomized, double-blind trial. Am J Transplant 2005; 5(1): 125-30.
[] [PMID: 15636620]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy