Endomicroscopic and Transcriptomic Analysis of Impaired Barrier Function and Malabsorption in Environmental Enteropathy

PLoS Neglected Tropical Diseases

Volumn 10, Issue 4, 2016, Pages

  Kelly, Paul ^a,b   Besa, Ellen ^b   Zyambo, Kanekwa ^b   Louis Auguste, John ^a   Lees, James ^a   Banda, Themba ^b   Soko, Rose ^b   Banda, Rosemary ^b   Amadi, Beatrice ^b   Watson, Alastair ^c  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF ZAMBIA   (Zambia)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 4; DEFENSIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUCAGON LIKE PEPTIDE 2; HLA DR ANTIGEN; INTELECTIN; INTESTINAL TREFOIL FACTOR; LACTOFERRIN; LIPOCALIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; REG 3ALPHA; SERINE PROTEINASE INHIBITOR; SPINK 4; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG; ZINC;

ADULT; ARTICLE; BACTERIAL TRANSLOCATION; BLOOD ANALYSIS; CLINICAL ARTICLE; CONFOCAL LASER MICROSCOPY; ENTEROPATHY; FEMALE; GENE SEQUENCE; GENETIC TRANSCRIPTION; HISTOLOGY; HUMAN; HUMAN TISSUE; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; INTESTINE BIOPSY; INTESTINE CRYPT; INTESTINE INJURY; INTESTINE VILLUS; MALABSORPTION; MALE; MASS SPECTROMETRY; MORPHOMETRICS; ONCOGENE C FOS; URINALYSIS; ZINC UPTAKE TEST; BIOPSY; CHEMISTRY; CYTOCHEMISTRY; ENVIRONMENTAL EXPOSURE; GASTROINTESTINAL DISEASE; GENE EXPRESSION PROFILING; METABOLISM; MICROSCOPY; PATHOLOGY; PLASMA; SEQUENCE ANALYSIS; ZAMBIA;

BIOPSY; ENVIRONMENTAL EXPOSURE; GASTROINTESTINAL DISEASES; GENE EXPRESSION PROFILING; HISTOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MICROSCOPY; PLASMA; SEQUENCE ANALYSIS, RNA; ZAMBIA; ZINC;

EID: 84964846264     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004600     Document Type: Article

References (52)

1. Cook GC, Cook GC, Malabsorption in the tropics. In: Tropical Gastroenterology. Oxford: Oxford University Press, 1980.
2. Keusch GT, Denno DM, Black RE, et al. Environmental Enteric Dysfunction: Pathogenesis, Diagnosis, and Clinical Consequences. Clin Infect Dis2014; 59: S207–12. doi: 10.1093/cid/ciu48525305288
3. Prendergast A, Kelly P, Enteropathies in the developing world; neglected effects on global health. Am J Trop Med Hyg2012; 86: 756–763. doi: 10.4269/ajtmh.2012.11-074322556071
4. Guerrant RL, DeBoer MD, Moore SR, Scharf RJ, Lima AAM, The impoverished gut—a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol2013; 10, 220–229. doi: 10.1038/nrgastro.2012.23923229327
5. Central Statistical Office (CSO)Ministry of Health (MOH)Tropical Diseases Research Centre (TDRC)University of ZambiaMacro International Inc.2015. Zambia Demographic and Health Survey 2014. Calverton, Maryland, USA: CSO and Macro International Inc.
6. Humphrey JH, Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet2009; 374: 1032–35. doi: 10.1016/S0140-6736(09)60950-819766883
7. Kosek M, Guerrant RL, Kang G, et al. Assessment of Environmental Enteropathy in the MAL-ED cohort Study: theoretical and analytic framework. Clin Infect Dis2014; 59: S239–47. doi: 10.1093/cid/ciu45725305293
8. Levine MM, Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biology2010; 8: 129. doi: 10.1186/1741-7007-8-12920920375
9. Campbell DI, Elia M, Lunn PG, Growth faltering in rural Gambian infants is associated with impaired small intestinal barrier function, leading to endotoxemia and systemic inflammation. J Nutr2003; 133: 1332–1338. 12730419
10. Brenchley J, Douek DC, Microbial translocation across the GI tract. Annu Rev Immunol2012; 30: 149–73. doi: 10.1146/annurev-immunol-020711-07500122224779
11. Prendergast AJ, Rukobo S, Chasekwa B, et al. Stunting Is Characterized by Chronic Inflammation in Zimbabwean Infants. PLoS ONE2014; 9: e86928. doi: 10.1371/journal.pone.008692824558364
12. Kimer N, Krag A, Moller S, et al. Systematic review with meta-analysis: the effects of rifaximin in hepatic encephalopathy. Aliment Pharmacol Ther2014; 40: 123–132. doi: 10.1111/apt.1280324849268
13. Bellot P, García-Pagán JC, Francés R, et al. Bacterial DNA translocation is associated with systemic circulatory abnormalities and intrahepatic endothelial dysfunction in patients with cirrhosis. Hepatology2010; 52: 2044–2052. doi: 10.1002/hep.2391820979050
14. Vesterbacka J, Barqasho B, Häggblom A, et al. Effects of Co-Trimoxazole on Microbial Translocation in HIV-1-Infected Patients Initiating Antiretroviral Therapy. AIDS Res Hum Retroviruses. 2015; 31: 830–6. doi: 10.1089/AID.2014.036626059763
15. Tenorio AR, Chan ES, Bosch RJ, et al. Rifaximin has a Marginal Impact on Microbial Translocation, T-cell Activation and Inflammation in HIV-Positive Immune Non-responders to Antiretroviral Therapy–ACTG A5286. J Infect Dis2015; 211:780–90. doi: 10.1093/infdis/jiu51525214516
16. Giorgio V, Miele L, Principessa L, et al. Intestinal permeability is increased in children with non-alcoholic fatty liver disease, and correlates with liver disease severity. Dig Liver Dis2014; 46: 556–60. doi: 10.1016/j.dld.2014.02.01024631029
17. Marchiando AM, Graham WV, Turner JR, Epithelial Barriers in Homeostasis and Disease. Annu. Rev. Pathol. Mech. Dis.2010. 5:119–44
18. Mizuno T, Yokoyama Y, Nishio H, et al. Intraoperative bacterial translocation detected by bacterium-specific ribosomal RNA-targeted reverse-transcriptase polymerase chain reaction for the mesenteric lymph node strongly predicts postoperative infectious complications after major hepatectomy for biliary malignancies. Ann Surg2010; 252: 1013–1019. doi: 10.1097/SLA.0b013e3181f3f35521107112
19. Salazar-Lindo E, Allen S, Brewster DR, et al. Intestinal Infections and Environmental Enteropathy: Working Group Report of the Second World Congress of Pediatric Gastroenterology, Hepatology, and Nutrition. J Ped Gastrenterol Nutr2003; 39: S662–S669.
20. Kelly P, Menzies I, Crane R, et al. Responses of small intestinal architecture and function over time to environmental factors in a tropical population. Am J Trop Med Hyg2004; 70: 412–419. 15100456
21. Turner JR, Intestinal mucosal barrier function in health and disease. Ann Rev Immunol2009; 9: 799–809.
22. Gunzel D, Yu ASL, Claudins and the modulation of tight junction permeability. Physiol Rev2013; 93: 525–569. doi: 10.1152/physrev.00019.201223589827
23. Marchiando AM, Shen L, Graham WV, et al. Caveolin-1–dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol2010; 189: 111–126. doi: 10.1083/jcb.20090215320351069
24. Kiesslich R, Goetz M, Angus EM, et al. Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology2007;133:1769–78. 18054549
25. Kiesslich R, Duckworth CA, Moussata D, et al. Local barrier dysfunction identified by confocal laser endomicroscopy predicts relapse in inflammatory bowel disease. Gut2012; 61: 1146–1153. doi: 10.1136/gutjnl-2011-30069522115910
26. Kelly P, Shawa T, Mwanamakondo S, et al. Gastric and intestinal barrier impairment in tropical enteropathy and HIV: limited impact of micronutrient supplementation during a randomised controlled trial. BMC Gastroenterology2010; 10: 72. doi: 10.1186/1471-230X-10-7220604937
27. Zulu J, Mwansa-Lisulo M, Besa E, et al. Improving validity of informed consent for biomedical research in Zambia using a laboratory exposure intervention. PLOS One2014; 9: e108305. doi: 10.1371/journal.pone.010830525254378
28. Valberg LS, Flanagan PR, Brennan J, et al. Does the oral zinc tolerance test measure zinc absorption?Am J Clin Nutr1985; 41: 37–42. 3966423
29. Tarazona S, García-Alcalde F, Dopazo J, et al. Differential expression in RNA-seq: a matter of depth. Genome Res. 2011; 21: 2213–23. doi: 10.1101/gr.124321.11121903743
30. Lim LG, Neumann J, Hansen T, et al. Confocal endomicroscopy identifies loss of local barrier function in the duodenum of patients with Crohn’s disease and Ulcerative Colitis. Inflamm Bowel Dis2014;20:892–900. doi: 10.1097/MIB.000000000000002724691113
31. Zevallos VF, Herencia LI, Chang F, Donnelly S, Ellis HJ, Ciclitira PJ, Gastrointestinal effects of eating quinoa (Chenopodium quinoa Willd.) in celiac patients. Am J Gastroenterol. 2014; 109: 270–8. doi: 10.1038/ajg.2013.43124445568
32. 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: 1208–1218.e1-2. doi: 10.1053/j.gastro.2011.01.00421237166
33. Petri WA, Naylor C, Haque R, Environmental enteropathy and malnutrition: do we know enough to intervene?BMC Medicine2014; 12: 187. doi: 10.1186/s12916-014-0187-125604120
34. Guan Y, Watson AJM, Marchiando AM, et al. Redistribution of the tight junction protein ZO-1 during physiologic shedding of mouse intestinal epithelial cells. American Journal of Physiology: Cell Physiology2011; 300: C1404–14. doi: 10.1152/ajpcell.00270.201021346149
35. Williams JM, Duckworth CA, Watson AJ, et al. A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Dis Model Mech. 2013; 6: 1388–99. doi: 10.1242/dmm.01328424046352
36. Marchetti G, Tincati C, Silvestri G, Microbial Translocation in the Pathogenesis of HIV Infection and AIDS. Clin Microbiol Rev2013; 26: 2–18. doi: 10.1128/CMR.00050-1223297256
37. Manary MJ, Hotz C, Krebs NF, et al. Zinc homeostasis in Malawian children consuming a high-phytate, maize-based diet. Am J Clin Nutr2002;75:1057–61. 12036813
38. Illing AC, Shawki A, Cunningham CL, et al. Substrate Profile and Metal-ion Selectivity of Human Divalent Metal-ion Transporter-1. J Biol Chem2012; 287: 30485–30496. doi: 10.1074/jbc.M112.36420822736759
39. Kelly P, Shawa T, Mwanamakondo S, et al. Gastric and intestinal barrier impairment in tropical enteropathy and HIV: limited impact of micronutrient supplementation during a randomised controlled trial. BMC Gastroenterology2010; 10: 72. doi: 10.1186/1471-230X-10-7220604937
40. Sandström B, Abrahamsson H, Zinc absorption and achlorhydria. Eur J Clin Nutr. 1989; 43: 877–9. 2697554
41. Janssen P, Rotondo A, Mule F, Tack J, Review article: a comparison of glucagon-like peptides 1 and 2. Aliment Pharmacol Ther2013; 37: 18–36. doi: 10.1111/apt.1209223121085
42. Baldassano S, Amato A, GLP-2: What do we know? What are we going to discover?Regulatory Peptides2014; 194–5; 6–10.
43. Jeppesen PB, Pertkiewicz M, Messing B, et al. Teduglutide reduced need for parenteral support among patients with short bowel syndrome with intestinal failure. Gastroenterology2012; 143: 1473–1481. doi: 10.1053/j.gastro.2012.09.00722982184
44. Wojcik MH, Meenaghan E, Lawson EA, Misra M, Klibanski A, Miller KK, Reduced amylin levels are associated with low bone mineral density in women with anorexia nervosa. Bone. 2010; 46: 796–800. doi: 10.1016/j.bone.2009.11.01419931436
45. Bremholm L, Hornum M, Andersen UB, et al. The effect of Glucagon-Like Peptide-2 on mesenteric blood flow and cardiac parameters in end-jejunostomy short bowel patients. Regulatory Peptides2011; 168: 32–38. doi: 10.1016/j.regpep.2011.03.00321421014
46. Xiao Q, Boushey RP, Cino M, et al. Circulating levels of glucagon-like peptide-2 in human subjects with inflammatory bowel disease. Am J Physiol Regulatory Integrative Comp Physiol2000; 278: R1057–R1063.
47. Trautvetter U, Jahreis G, Effect of supplementary calcium phosphate on plasma gastrointestinal hormones in a double-blind, placebo-controlled, cross-over human study. Br J Nutr2014; 111: 287–293. doi: 10.1017/S000711451300234123871132
48. Dhaliwal W, Bajaj-Elliott M, Kelly P, Intestinal defensin gene expression in human populations. Mol Immunol2003; 40: 469–475. 14568394
49. Veitch A, Kelly P, Zulu I, et al. Tropical enteropathy: a T cell mediated crypt hyperplastic enteropathy. Eur J Gastroenterol Hepatol2001; 13: 1175–1181. 11711773
50. Wapenaar MS, Monsuur AJ, Poell J, et al. The SPINK gene family and celiac disease susceptibility. Immunogenetics2007; 59: 349–357. 17333166
51. Aamann L, Vestergaard EM, Gronbaek H, Trefoil factors in inflammatory bowel disease. World J Gastroenterol2014; 20: 3223–3230. doi: 10.3748/wjg.v20.i12.322324696606
52. Vestergaard EM, Nexo E, Wendt A, et al. Trefoil factors in human milk. Early Hum Dev2008; 84: 631–635. doi: 10.1016/j.earlhumdev.2008.04.00118502057