Environmental Enteropathy: Elusive but Significant Subclinical Abnormalities in Developing Countries

Alemayehu, 2015, Undernutrition status and associated factors in under-5 children, in Tigray, Northern Ethiopia, Nutrition, 31, 964, 10.1016/j.nut.2015.01.013 Asano, 2012, Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice, Am. J. Physiol. Gastrointest. Liver Physiol., 303, G1288, 10.1152/ajpgi.00341.2012 Asfaw, 2015, Prevalence of undernutrition and associated factors among children aged between six to fifty nine months in Bule Hora district, South Ethiopia, BMC Public Health, 15, 41, 10.1186/s12889-015-1370-9 Assis, 2005, Growth faltering in childhood related to diarrhea: a longitudinal community based study, Eur. J. Clin. Nutr., 59, 1317, 10.1038/sj.ejcn.1602245 Barrett, 2012, Gamma-aminobutyric acid production by culturable bacteria from the human intestine, J. Appl. Microbiol., 113, 411, 10.1111/j.1365-2672.2012.05344.x Benzoni, 2015, Plasma endotoxin core antibody concentration and linear growth are unrelated in rural Malawian children aged 2–5years, BMC Res. Notes, 8, 258, 10.1186/s13104-015-1238-1 Berkman, 2002, Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study, Lancet, 359, 564, 10.1016/S0140-6736(02)07744-9 Bhutta, 2008, What works? Interventions for maternal and child undernutrition and survival, Lancet, 371, 417, 10.1016/S0140-6736(07)61693-6 Black, 1984, Effects of diarrhea associated with specific enteropathogens on the growth of children in rural Bangladesh, Pediatrics, 73, 799, 10.1542/peds.73.6.799 Black, 2008, Maternal and child undernutrition: global and regional exposures and health consequences, Lancet, 371, 243, 10.1016/S0140-6736(07)61690-0 Bland, 2010, Enduring consequences of early-life infection on glial and neural cell genesis within cognitive regions of the brain, Brain Behav. Immun., 24, 329, 10.1016/j.bbi.2009.09.012 Boksa, 2010, Effects of prenatal infection on brain development and behavior: a review of findings from animal models, Brain Behav. Immun., 24, 881, 10.1016/j.bbi.2010.03.005 Braniste, 2014, The gut microbiota influences blood-brain barrier permeability in mice, Sci. Transl. Med., 6, 263ra158, 10.1126/scitranslmed.3009759 Brown, 2015, Diet and specific microbial exposure trigger features of environmental enteropathy in a novel murine model, Nat. Commun., 6, 7806, 10.1038/ncomms8806 Campbell, 2003, Growth faltering in rural Gambian infants is associated with impaired small intestinal barrier function, leading to endotoxemia and systemic inflammation, J. Nutr., 133, 1332, 10.1093/jn/133.5.1332 Campbell, 2003, Chronic T cell-mediated enteropathy in rural west African children: relationship with nutritional status and small bowel function, Pediatr. Res., 54, 306, 10.1203/01.PDR.0000076666.16021.5E Checkley, 1998, Effects of Cryptosporidium parvum infection in Peruvian children: growth faltering and subsequent catch-up growth, Am. J. Epidemiol., 148, 497, 10.1093/oxfordjournals.aje.a009675 Checkley, 2003, Effects of acute diarrhea on linear growth in Peruvian children, Am. J. Epidemiol., 157, 166, 10.1093/aje/kwf179 Clough, 2016, Effects of protein malnutrition on tolerance to helminth infection, Biol. Lett., 12, 10.1098/rsbl.2016.0189 Colwell, 1968, Jejunal morphological characteristics in South Vietnamese residents, JAMA, 206, 2273, 10.1001/jama.1968.03150100023004 Cook, 1969, Jejunal morphology of the African in Uganda, J. Pathol., 98, 157, 10.1002/path.1710980302 Denno, 2014, Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review, Clin. Infect. Dis., 59, S213, 10.1093/cid/ciu541 Dewey, 2008, Systematic review of the efficacy and effectiveness of complementary feeding interventions in developing countries, Matern. Child Nutr., 4, 24, 10.1111/j.1740-8709.2007.00124.x Dinel, 2014, Inflammation early in life is a vulnerability factor for emotional behavior at adolescence and for lipopolysaccharide-induced spatial memory and neurogenesis alteration at adulthood, J. Neuroinflammation, 11, 155, 10.1186/s12974-014-0155-x Dominguez-Salas, 2014, Maternal nutrition at conception modulates DNA methylation of human metastable epialleles, Nat. Commun., 5, 3746, 10.1038/ncomms4746 Donowitz, 2015, Pediatric small intestine bacterial overgrowth in low-income countries, Trends Mol. Med., 21, 6, 10.1016/j.molmed.2014.11.001 Donowitz, 2016, Small intestine bacterial overgrowth and environmental enteropathy in Bangladeshi children, mBio, 7, e02102, 10.1128/mBio.02102-15 El Aidy, 2015, The small intestine microbiota, nutritional modulation and relevance for health, Curr. Opin. Biotechnol., 32, 14, 10.1016/j.copbio.2014.09.005 Fekadu, 2015, Factors associated with nutritional status of infants and young children in Somali Region, Ethiopia: a cross- sectional study, BMC Public Health, 15, 846, 10.1186/s12889-015-2190-7 Finegold, 2002, Gastrointestinal microflora studies in late-onset autism, Clin. Infect. Dis., 35, S6, 10.1086/341914 Galpin, 2005, Effect of Lactobacillus GG on intestinal integrity in Malawian children at risk of tropical enteropathy, Am. J. Clin. Nutr., 82, 1040, 10.1093/ajcn/82.5.1040 Garcia, 1968, Malabsorption and malnutrition in Mexico, Am. J. Clin. Nutr., 21, 1066, 10.1093/ajcn/21.9.1066 George, 2015, Geophagy is associated with environmental enteropathy and stunting in children in rural Bangladesh, Am.J.Trop. Med. Hyg., 92, 1117, 10.4269/ajtmh.14-0672 Gerson, 1971, Recovery of small-intestinal structure and function after residence in the tropics. II. Studies in Indians and Pakistanis living in New York City, Ann. Intern. Med., 75, 41, 10.7326/0003-4819-75-1-41 Grassly, 2016, The effect of azithromycin on the immunogenicity of oral poliovirus vaccine: a double-blind randomised placebo-controlled trial in seronegative Indian infants, Lancet Infect. Dis., 10.1016/S1473-3099(16)30023-8 Guerrant, 1999, Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in Northeast Brazil, Am.J.Trop. Med. Hyg., 61, 707, 10.4269/ajtmh.1999.61.707 Guerrant, 2013, The impoverished gut–a triple burden of diarrhoea, stunting and chronic disease, Nat. Rev. Gastroenterol. Hepatol., 10, 220, 10.1038/nrgastro.2012.239 Hickman, 2014, The effect of malnutrition on norovirus infection, mBio, 5, 10.1128/mBio.01032-13 Iqbal, 1996, Small intestinal permeability to mannitol and lactulose in the three ethnic groups resident in West Birmingham, Gut, 39, 199, 10.1136/gut.39.2.199 Jaeggi, 2015, Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants, Gut, 64, 731, 10.1136/gutjnl-2014-307720 Jiang, 2014, Febrile illness and pro-inflammatory cytokines are associated with lower neurodevelopmental scores in Bangladeshi infants living in poverty, BMC Pediatr., 14, 50, 10.1186/1471-2431-14-50 Jones, 2014, Mesalazine in the initial management of severely acutely malnourished children with environmental enteric dysfunction: a pilot randomized controlled trial, BMC Med., 12, 133, 10.1186/s12916-014-0133-2 Kelly, 2016, Endomicroscopic and transcriptomic analysis of impaired barrier function and malabsorption in environmental enteropathy, PLoS Negl. Trop. Dis., 10, e0004600, 10.1371/journal.pntd.0004600 Kerac, 2009, Probiotics and prebiotics for severe acute malnutrition (PRONUT study): a double-blind efficacy randomised controlled trial in Malawi, Lancet, 374, 136, 10.1016/S0140-6736(09)60884-9 Keusch, 2013, Implications of acquired environmental enteric dysfunction for growth and stunting in infants and children living in low- and middle-income countries, Food Nutr. Bull., 34, 357, 10.1177/156482651303400308 Khin Maung, 1992, Epidemiology of small bowel bacterial overgrowth and rice carbohydrate malabsorption in Burmese (Myanmar) village children, Am.J.Trop. Med. Hyg., 47, 298, 10.4269/ajtmh.1992.47.298 Korpe, 2012, Environmental enteropathy: critical implications of a poorly understood condition, Trends Mol. Med., 18, 328, 10.1016/j.molmed.2012.04.007 Kosek, 2014, Assessment of environmental enteropathy in the MAL-ED cohort study: theoretical and analytic framework, Clin. Infect. Dis., 59, S239, 10.1093/cid/ciu457 Lin, 2013, Household environmental conditions are associated with enteropathy and impaired growth in rural Bangladesh, Am. J. Trop. Med. Hyg., 89, 130, 10.4269/ajtmh.12-0629 Lindenbaum, 1968, Small intestine dysfunction in Pakistanis and Americans resident in Pakistan, Am. J. Clin. Nutr., 21, 1023, 10.1093/ajcn/21.9.1023 Lindenbaum, 1966, Subclinical small-intestinal disease in East Pakistan, Br. Med. J., 2, 1616, 10.1136/bmj.2.5530.1616 Lindenbaum, 1971, Recovery of small-intestinal structure and function after residence in the tropics. I. Studies in Peace Corps volunteers, Ann. Intern. Med., 74, 218, 10.7326/0003-4819-74-2-218 Lunn, 1991, Intestinal permeability, mucosal injury, and growth faltering in Gambian infants, Lancet, 338, 907, 10.1016/0140-6736(91)91772-M Maier, 2013, Protein-energy malnutrition alters IgA responses to rotavirus vaccination and infection but does not impair vaccine efficacy in mice, Vaccine, 32, 48, 10.1016/j.vaccine.2013.10.072 Mendez, 1999, Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood, J. Nutr., 129, 1555, 10.1093/jn/129.8.1555 Menzies, 1999, Geography of intestinal permeability and absorption, Gut, 44, 483, 10.1136/gut.44.4.483 Molbak, 1997, Risk factors for diarrheal disease incidence in early childhood: a community cohort study from Guinea-Bissau, Am. J. Epidemiol., 146, 273, 10.1093/oxfordjournals.aje.a009263 Mondal, 2012, Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh, Clin. Infect. Dis., 54, 185, 10.1093/cid/cir807 Murray-Kolb, 2013, Iron and brain functions, Curr. Opin. Clin. Nutr. Metab. Care, 16, 703, 10.1097/MCO.0b013e3283653ef8 Naylor, 2015, Environmental enteropathy, oral vaccine failure and growth faltering in infants in Bangladesh, EBioMedicine, 2, 1759, 10.1016/j.ebiom.2015.09.036 Niehaus, 2002, Early childhood diarrhea is associated with diminished cognitive function 4 to 7years later in children in a northeast Brazilian shantytown, Am.J.Trop. Med. Hyg., 66, 590, 10.4269/ajtmh.2002.66.590 Nielsen, 2007, Drug insight: aminosalicylates for the treatment of IBD, Nat. Clin. Pract. Gastroenterol. Hepatol., 4, 160, 10.1038/ncpgasthep0696 O'mahony, 2010, Enteric Microbiota and Small Intestinal Bacterial Overgrowth, 1769 Oria, 2005, APOE4 protects the cognitive development in children with heavy diarrhea burdens in Northeast Brazil, Pediatr. Res., 57, 310, 10.1203/01.PDR.0000148719.82468.CA Oria, 2010, ApoE polymorphisms and diarrheal outcomes in Brazilian shanty town children, Braz. J. Med. Biol. Res., 43, 249, 10.1590/S0100-879X2010007500003 Oria, 2016, Early-life enteric infections: relation between chronic systemic inflammation and poor cognition in children, Nutr. Rev., 74, 374, 10.1093/nutrit/nuw008 Petri, 2014, Environmental enteropathy and malnutrition: do we know enough to intervene?, BMC Med., 12, 187, 10.1186/s12916-014-0187-1 Qadri, 2013, Immune responses and protection in children in developing countries induced by oral vaccines, Vaccine, 31, 452, 10.1016/j.vaccine.2012.11.012 Sanchez, 2013, Duodenal-mucosal bacteria associated with celiac disease in children, Appl. Environ. Microbiol., 79, 5472, 10.1128/AEM.00869-13 Silva, 2015, An overview of molecular basis of iron metabolism regulation and the associated pathologies, Biochim. Biophys. Acta, 1852, 1347, 10.1016/j.bbadis.2015.03.011 Spadoni, 2015, A gut-vascular barrier controls the systemic dissemination of bacteria, Science, 350, 830, 10.1126/science.aad0135 Spencer, 2011, Neonatal programming of innate immune function, Am. J. Physiol. Endocrinol. Metab., 300, E11, 10.1152/ajpendo.00516.2010 Subramanian, 2014, Persistent gut microbiota immaturity in malnourished Bangladeshi children, Nature, 510, 417, 10.1038/nature13421 Trehan, 2009, A randomized, double-blind, placebo-controlled trial of rifaximin, a nonabsorbable antibiotic, in the treatment of tropical enteropathy, Am. J. Gastroenterol., 104, 2326, 10.1038/ajg.2009.270 Tussing-Humphreys, 2012, Rethinking iron regulation and assessment in iron deficiency, anemia of chronic disease, and obesity: introducing hepcidin, J. Acad. Nutr. Diet., 112, 391, 10.1016/j.jada.2011.08.038 Urrutia, 2013, Inflammation alters the expression of DMT1, FPN1 and hepcidin, and it causes iron accumulation in central nervous system cells, J. Neurochem., 126, 541, 10.1111/jnc.12244 Valentiner-Branth, 2001, Community-based controlled trial of dietary management of children with persistent diarrhea: sustained beneficial effect on ponderal and linear growth, Am. J. Clin. Nutr., 73, 968, 10.1093/ajcn/73.5.968 Victora, 2008, Maternal and child undernutrition: consequences for adult health and human capital, Lancet, 371, 340, 10.1016/S0140-6736(07)61692-4 Wacklin, 2013, The duodenal microbiota composition of adult celiac disease patients is associated with the clinical manifestation of the disease, Inflamm. Bowel Dis., 19, 934, 10.1097/MIB.0b013e31828029a9 Wacklin, 2014, Altered duodenal microbiota composition in celiac disease patients suffering from persistent symptoms on a long-term gluten-free diet, Am. J. Gastroenterol., 109, 1933, 10.1038/ajg.2014.355 Wang, 2000, Human zonulin, a potential modulator of intestinal tight junctions, J. Cell Sci., 113, 4435, 10.1242/jcs.113.24.4435 Wood, 1991, Small bowel morphology in British Indian and Afro-Caribbean subjects: evidence of tropical enteropathy, Gut, 32, 256, 10.1136/gut.32.3.256 Yano, 2015, Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis, Cell, 161, 264, 10.1016/j.cell.2015.02.047 Yisak, 2015, Prevalence and risk factors for under nutrition among children under five at Haramaya district, Eastern Ethiopia, BMC Pediatr., 15, 212, 10.1186/s12887-015-0535-0 Yu, 2016, Environmental enteric dysfunction includes a broad spectrum of inflammatory responses and epithelial repair processes, Cell. Mol. Gastroenterol. Hepatol., 2, e1