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BMC Pediatrics
Published in: BMC Pediatrics 1/2018

Open Access 01-12-2018 | Study protocol

Identifying the etiology and pathophysiology underlying stunting and environmental enteropathy: study protocol of the AFRIBIOTA project

Authors: Pascale Vonaesch, Rindra Randremanana, Jean-Chrysostome Gody, Jean-Marc Collard, Tamara Giles-Vernick, Maria Doria, Inès Vigan-Womas, Pierre-Alain Rubbo, Aurélie Etienne, Emilson Jean Andriatahirintsoa, Nathalie Kapel, Eric Brown, Kelsey E. Huus, Darragh Duffy, B.Brett Finlay, Milena Hasan, Francis Allen Hunald, Annick Robinson, Alexandre Manirakiza, Laura Wegener-Parfrey, Muriel Vray, Philippe J. Sansonetti, for the AFRIBIOTA Investigators

Published in: BMC Pediatrics | Issue 1/2018

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Abstract

Background

Globally one out of four children under 5 years is affected by linear growth delay (stunting). This syndrome has severe long-term sequelae including increased risk of illness and mortality and delayed psychomotor development. Stunting is a syndrome that is linked to poor nutrition and repeated infections. To date, the treatment of stunted children is challenging as the underlying etiology and pathophysiological mechanisms remain elusive. We hypothesize that pediatric environmental enteropathy (PEE), a chronic inflammation of the small intestine, plays a major role in the pathophysiology of stunting, failure of nutritional interventions and diminished response to oral vaccines, potentially via changes in the composition of the pro- and eukaryotic intestinal communities. The main objective of AFRIBIOTA is to describe the intestinal dysbiosis observed in the context of stunting and to link it to PEE. Secondary objectives include the identification of the broader socio-economic environment and biological and environmental risk factors for stunting and PEE as well as the testing of a set of easy-to-use candidate biomarkers for PEE. We also assess host outcomes including mucosal and systemic immunity and psychomotor development. This article describes the rationale and study protocol of the AFRIBIOTA project.

Methods

AFRIBIOTA is a case-control study for stunting recruiting children in Bangui, Central African Republic and in Antananarivo, Madagascar. In each country, 460 children aged 2–5 years with no overt signs of gastrointestinal disease are recruited (260 with no growth delay, 100 moderately stunted and 100 severely stunted). We compare the intestinal microbiota composition (gastric and small intestinal aspirates; feces), the mucosal and systemic immune status and the psychomotor development of children with stunting and/or PEE compared to non-stunted controls. We also perform anthropological and epidemiological investigations of the children’s broader living conditions and assess risk factors using a standardized questionnaire.

Discussion

To date, the pathophysiology and risk factors of stunting and PEE have been insufficiently investigated. AFRIBIOTA will add new insights into the pathophysiology underlying stunting and PEE and in doing so will enable implementation of new biomarkers and design of evidence-based treatment strategies for these two syndromes.
Literature
1.
2.
3.
4.
5.
6.
7.
Wang AZ, Shulman RJ, Crocker AH, Thakwalakwa C, Maleta KM, Devaraj S, et al. A combined intervention of zinc, multiple micronutrients, and Albendazole does not ameliorate environmental enteric dysfunction or stunting in rural Malawian children in a double-blind randomized controlled trial. J Nutr. 2017;147:97–103.PubMedCrossRef
8.
9.
10.
11.
Lunn PG, Northrop-Clewes CA, Downes RM. Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. Lancet. 1991;338:907–10.PubMedCrossRef
12.
Solomons NW. Environmental contamination and chronic inflammation influence human growth potential. J Nutr. 2003;133:1237.PubMedCrossRef
13.
McKay S, Gaudier E, Campbell DI, Prentice AM, Albers R. Environmental enteropathy: new targets for nutritional interventions. Int Health. 2010;2:172–80.PubMedCrossRef
14.
Gilmartin AA, Petri WA. Exploring the role of environmental enteropathy in malnutrition, infant development and oral vaccine response. Philos Trans R Soc Lond Ser B Biol Sci. 2015;370:20140143.CrossRef
15.
Morita T, Perin J, Oldja L, Biswas S, Sack RB, Ahmed S, et al. Mouthing of soil contaminated objects is associated with environmental enteropathy in young children. Tropical Med Int Health. 2017;22:670–8.CrossRef
16.
George CM, Oldja L, Biswas S, Perin J, Lee GO, Kosek M, et al. Geophagy is associated with environmental enteropathy and stunting in children in rural Bangladesh. Am J Trop Med Hyg. 2015;92:1117–24.PubMedPubMedCentralCrossRef
17.
Perin J, Thomas A, Oldja L, Ahmed S, Parvin T, Bhuyian SI, et al. Geophagy is associated with growth faltering in children in rural Bangladesh. J Pediatr. 2016;178:34–39.e1.PubMedCrossRef
18.
George CM, Oldja L, Biswas S, Perin J, Sack RB, Ahmed S, et al. Unsafe child feces disposal is associated with environmental Enteropathy and impaired growth. J Pediatr. 2016;176:43–9.PubMedCrossRef
19.
George CM, Oldja L, Biswas SK, Perin J, Lee GO, Ahmed S, et al. Fecal markers of environmental enteropathy are associated with animal exposure and caregiver hygiene in Bangladesh. Am J Trop Med Hyg. 2015;93:269–75.PubMedPubMedCentralCrossRef
20.
Watanabe K, Petri WA. Environmental enteropathy: elusive but significant subclinical abnormalities in developing countries. EBioMedicine. 2016;10:25–32.PubMedPubMedCentralCrossRef
21.
22.
23.
Keusch GT, Rosenberg IH, Denno DM, Duggan C, Guerrant RL, Lavery JV, et al. Implications of acquired environmental enteric dysfunction for growth and stunting in infants and children living in low- and middle-income countries. Food Nutr Bull. 2013;34:357–64.PubMedPubMedCentralCrossRef
24.
25.
Ahmed T, Auble D, Berkley JA, Black R, Ahern PP, Hossain M, et al. An evolving perspective about the origins of childhood undernutrition and nutritional interventions that includes the gut microbiome. Ann N Y Acad Sci. 2014;1332:22–38.PubMedPubMedCentralCrossRef
26.
Brown EM, Wlodarska M, Willing BP, Vonaesch P, Han J, Reynolds LA, et al. Diet and specific microbial exposure trigger features of environmental enteropathy in a novel murine model. Nat Commun. 2015;6:7806.PubMedPubMedCentralCrossRef
27.
28.
Arndt MB, Richardson BA, Ahmed T, Mahfuz M, Haque R, John-Stewart GC, et al. Fecal markers of environmental enteropathy and subsequent growth in Bangladeshi children. Am J Trop Med Hyg. 2016;95:694–701.PubMedPubMedCentralCrossRef
29.
Harper KM, Mutasa M, Prendergast AJ, Humphrey J, Manges AR. Environmental enteric dysfunction pathways and child stunting: a systematic review. Kosek M, editor. PLoS Negl Trop Dis. 2018;12:e0006205.PubMedPubMedCentralCrossRef
30.
Kelly P, Menzies I, Crane R, Zulu I, Nickols C, Feakins R, et al. Responses of small intestinal architecture and function over time to environmental factors in a tropical population. Am J Trop Med Hyg. 2004;70:412–9.PubMedCrossRef
31.
Kelly P, Besa E, Zyambo K, Louis-Auguste J, Lees J, Banda T, et al. Endomicroscopic and Transcriptomic analysis of impaired barrier function and malabsorption in environmental enteropathy. Petri WA, editor. PLoS Negl Trop Dis. 2016;10:e0004600.PubMedPubMedCentralCrossRef
32.
Lee GO, McCormick BJJ, Seidman JC, Kosek MN, Haque R, Olortegui MP, et al. Infant nutritional status, feeding practices, enteropathogen exposure, socioeconomic status, and illness are associated with gut barrier function as assessed by the lactulose mannitol test in the MAL-ED birth cohort. Am J Trop Med Hyg. 2017;97:281–90.PubMedPubMedCentralCrossRef
33.
George CM, Burrowes V, Perin J, Oldja L, Biswas S, Sack D, et al. Enteric infections in young children are associated with environmental enteropathy and impaired growth. Tropical Med Int Health. 2018;23:26–33.CrossRef
34.
Rogawski ET, Guerrant RL, Havt A, Lima IFN, Medeiros PHQS, Seidman JC, et al. Epidemiology of enteroaggregative Escherichia coli infections and associated outcomes in the MAL-ED birth cohort. Baker S, editor. PLoS Negl Trop Dis. 2017;11:e0005798.PubMedPubMedCentralCrossRef
35.
Steiner TS, Lima AA, Nataro JP, Guerrant RL. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis. 1998;177:88–96.PubMedCrossRef
36.
Lindenbaum J, Gerson CD, Kent TH. Recovery of small-intestinal structure and function after residence in the tropics. I. Studies in peace corps volunteers. Ann Intern Med. 1971;74:218–22.PubMedCrossRef
37.
Gerson CD, Kent TH, Saha JR, Siddiqi N, Lindenbaum J. 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. 1971;75:41–8.PubMedCrossRef
38.
Kau AL, Planer JD, Liu J, Rao S, Yatsunenko T, Trehan I, et al. Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci Transl Med. 2015;7:276ra24.PubMedPubMedCentralCrossRef
39.
Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from Fur children. Science. 2016;351:aad3311.PubMedCrossRef
40.
Desai HG, Borkar AV, Pathare SM, Dighe PK, Jeejeebhoy KN. “Flat” jejunal mucosa in the tropics. Indian J Med Sci. 1969;23:1–5.PubMed
41.
Chacko CJ, Paulson KA, Mathan VI, Baker SJ. The villus architecture of the small intestine in the tropics: a necropsy study. J Pathol. 1969;98:146–51.PubMedCrossRef
42.
Fagundes-Neto U, Martins MC, Lima FL, Patrício FR, Toledo MR. Asymptomatic environmental enteropathy among slum-dwelling infants. J Am Coll Nutr. 1994;13:51–6.PubMedCrossRef
43.
Fagundes-Neto U, Kallas MR, Patrício FR. Morphometric study of the small bowel mucosa in infants with diarrhea due to enteropathogenic Escherichia coli strains. Hepato-Gastroenterology. 1997;44:1051–6.PubMed
44.
Kallas MR, Patrício FR, Fagundes-Neto U. Morphometrics of the small intestine in children with diarrhea due to classical enteropathogenic Escherichia coli and to environmental asymptomatic enteropathy. Rev Assoc Med Bras (1992). 1995;41:162–6.
45.
Campbell DI, Murch SH, Elia M, Sullivan PB, Sanyang MS, Jobarteh B, et al. Chronic T cell-mediated enteropathy in rural West African children: relationship with nutritional status and small bowel function. Pediatr Res. 2003;54:306–11.PubMedCrossRef
46.
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 Nutr. 2003;133:1332–8.PubMedCrossRef
47.
Lee GO, Olortegui MP, Salas MS, Yori PP, Trigoso DR, Kosek P, et al. Environmental enteropathy is associated with cardiometabolic risk factors in Peruvian children. J Dev Orig Health Dis. 2017;8:337–48.PubMedCrossRef
48.
Ordiz MI, Stephenson K, Agapova S, Wylie KM, Maleta K, Martin J, et al. Environmental enteric dysfunction and the fecal microbiota in Malawian children. Am J Trop Med Hyg. 2017;96:473–6.PubMedPubMedCentralCrossRef
49.
MAL-ED Network Investigators. The MAL-ED study: a multinational and multidisciplinary approach to understand the relationship between enteric pathogens, malnutrition, gut physiology, physical growth, cognitive development, and immune responses in infants and children up to 2 years of age in resource-poor environments. Clin Infect Dis. 2014;59(Suppl 4):S193–206.CrossRef
50.
Donowitz JR, Haque R, Kirkpatrick BD, Alam M, Lu M, Kabir M, et al. Small intestine bacterial overgrowth and environmental enteropathy in Bangladeshi children. MBio. 2016;7:e02102–15.PubMedPubMedCentralCrossRef
51.
Lu M, Zhou J, Naylor C, Kirkpatrick BD, Haque R, Petri WA, et al. Application of penalized linear regression methods to the selection of environmental enteropathy biomarkers. Biomark Res. 2017;5:9.PubMedPubMedCentralCrossRef
52.
Guerrant RL, Leite ÁM, Pinkerton R, Medeiros PHQS, Cavalcante PA, DeBoer M, et al. Biomarkers of environmental enteropathy, inflammation, stunting, and impaired growth in children in Northeast Brazil. Weber CR, editor. PLoS ONE. 2016;11:e0158772.PubMedPubMedCentralCrossRef
53.
Johansson MEV, Gustafsson JK, Holmén-Larsson J, Jabbar KS, Xia L, Xu H, et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. 2014;63:281–91.PubMedCrossRef
54.
55.
Lagos R, Fasano A, Wasserman SS, Prado V, San Martin O, Abrego P, et al. Effect of small bowel bacterial overgrowth on the immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR. J Infect Dis. 1999;180:1709–12.PubMedCrossRef
56.
Trehan I, Shulman RJ, Ou C-N, Maleta K, Manary MJ. A randomized, double-blind, placebo-controlled trial of rifaximin, a nonabsorbable antibiotic, in the treatment of tropical enteropathy. Am J Gastroenterol. 2009;104:2326–33.PubMedPubMedCentralCrossRef
57.
Galpin L, Manary MJ, Fleming K, Ou C-N, Ashorn P, Shulman RJ. Effect of lactobacillus GG on intestinal integrity in Malawian children at risk of tropical enteropathy. Am J Clin Nutr. 2005;82:1040–5.PubMedCrossRef
58.
Sanitation Hygiene Infant Nutrition Efficacy (SHINE) Trial Team, Humphrey JH, Jones AD, Manges A, Mangwadu G, Maluccio JA, et al. The Sanitation Hygiene Infant Nutrition Efficacy (SHINE) Trial: Rationale, Design, and Methods. Clin Infect Dis. 2015;61(Suppl 7):S685–702.CrossRef
59.
Kirkpatrick BD, Colgate ER, Mychaleckyj JC, Haque R, Dickson DM, Carmolli MP, et al. The “Performance of Rotavirus and Oral Polio Vaccines in Developing Countries” (PROVIDE) study: description of methods of an interventional study designed to explore complex biologic problems. Am J Trop Med Hyg. 2015;92:744–51.PubMedPubMedCentralCrossRef
60.
Angelakis E, Armougom F, Carrière F, Bachar D, Laugier R, Lagier J-C, et al. A metagenomic investigation of the duodenal microbiota reveals links with obesity. Covasa M, editor. PLoS ONE. 2015;10:e0137784.PubMedPubMedCentralCrossRef
61.
Li G, Yang M, Zhou K, Zhang L, Tian L, Lv S, et al. Diversity of duodenal and rectal microbiota in biopsy tissues and luminal contents in healthy volunteers. J Microbiol Biotechnol. 2015;25:1136–45.PubMedCrossRef
62.
63.
Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, et al. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun. 2008;76:4726–36.PubMedPubMedCentralCrossRef
64.
65.
Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. Eisen JA, editor. PLoS Biol. 2008;6:e280.PubMedPubMedCentralCrossRef
66.
Hill DA, Hoffmann C, Abt MC, Du Y, Kobuley D, Kirn TJ, et al. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 2010;3:148–58.PubMedCrossRef
67.
Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339:548–54.PubMedPubMedCentralCrossRef
68.
Hasan M, Beitz B, Rouilly V, Libri V, Urrutia A, Duffy D, et al. Semi-automated and standardized cytometric procedures for multi-panel and multi-parametric whole blood immunophenotyping. Clin Immunol. 2015;157:261–76.PubMedCrossRef
69.
Duffy D, Rouilly V, Libri V, Hasan M, Beitz B, David M, et al. Functional analysis via standardized whole-blood stimulation systems defines the boundaries of a healthy immune response to complex stimuli. Immunity. 2014;40:436–50.PubMedCrossRef
70.
Kalach N, Kapel N, Waligora-Dupriet A-J, Castelain M-C, Cousin MO, Sauvage C, et al. Intestinal permeability and fecal eosinophil-derived neurotoxin are the best diagnosis tools for digestive non-IgE-mediated cow’s milk allergy in toddlers. Clin Chem Lab Med. 2013;51:351.PubMedCrossRef
71.
Lee GO, Kosek P, Lima AAM, Singh R, Yori PP, Olortegui MP, et al. Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy. J Pediatr Gastroenterol Nutr. 2014;59:544–50.PubMedPubMedCentralCrossRef
72.
Weisz AJ, Manary MJ, Stephenson K, Agapova S, Manary FG, Thakwalakwa C, et al. Abnormal gut integrity is associated with reduced linear growth in rural Malawian children. J Pediatr Gastroenterol Nutr. 2012;55:747–50.PubMedCrossRef
73.
Macpherson AJ, Geuking MB, Slack E, Hapfelmeier S, McCoy KD. The habitat, double life, citizenship, and forgetfulness of IgA. Immunol Rev. 2012;245:132–46.PubMedCrossRef
74.
Maier EA, Weage KJ, Guedes MM, Denson LA, McNeal MM, Bernstein DI, et al. Protein-energy malnutrition alters IgA responses to rotavirus vaccination and infection but does not impair vaccine efficacy in mice. Vaccine. 2013;32:48–53.PubMedCrossRef
75.
Wessells KR, Hess SY, Rouamba N, Ouédraogo ZP, Kellogg M, Goto R, et al. Associations between intestinal mucosal function and changes in plasma zinc concentration following zinc supplementation. J Pediatr Gastroenterol Nutr. 2013;57:348–55.PubMedPubMedCentralCrossRef
76.
Papadia C, Kelly P, Caini S, Corazza GR, Shawa T, Franzè A, et al. Plasma citrulline as a quantitative biomarker of HIV-associated villous atrophy in a tropical enteropathy population. Clin Nutr. 2010;29:795–800.PubMedCrossRef
77.
Crenn P, Messing B, Cynober L. Citrulline as a biomarker of intestinal failure due to enterocyte mass reduction. Clin Nutr. 2008;27:328–39.PubMedCrossRef
78.
Crenn P, Hanachi M, Neveux N, Cynober L. Circulating citrulline levels: a biomarker for intestinal functionality assessment. Ann Biol Clin (Paris). 2011;69:513–21.
79.
McDonald CM, Manji KP, Gosselin K, Tran H, Liu E, Kisenge R, et al. Elevations in serum anti-flagellin and anti-LPS Igs are related to growth faltering in young Tanzanian children. Am J Clin Nutr. 2016;103:1548–54.PubMedPubMedCentralCrossRef
80.
Lin A, Arnold BF, Afreen S, Goto R, Huda TMN, Haque R, et al. Household environmental conditions are associated with enteropathy and impaired growth in rural Bangladesh. Am J Trop Med Hyg. 2013;89:130–7.PubMedPubMedCentralCrossRef
81.
Benzoni N, Korpe P, Thakwalakwa C, Maleta K, Stephenson K, Manary M, et al. Plasma endotoxin core antibody concentration and linear growth are unrelated in rural Malawian children aged 2-5 years. BMC Res Notes. 2015;8:258.PubMedPubMedCentralCrossRef
82.
Ritchie BK, Brewster DR, Davidson GP, Tran CD, McNeil Y, Hawkes JS, et al. 13C-sucrose breath test: novel use of a noninvasive biomarker of environmental gut health. Pediatrics. 2009;124:620–6.PubMedCrossRef
83.
Reis dos JC, de Morais MB, Oliva CAG, Fagundes-Neto U. Breath hydrogen test in the diagnosis of environmental enteropathy in children living in an urban slum. Dig Dis Sci. 2007;52:1253–8.CrossRef
84.
Reis dos JC, de Morais MB, Fagundes-Neto U. Breath hydrogen test to evaluate lactose absorption and small bowel bacterial overgrowth in children. Arq Gastroenterol. 1999;36:169–76.CrossRef
85.
Ghoshal UC, Ghoshal U, Das K, Misra A. Utility of hydrogen breath tests in diagnosis of small intestinal bacterial overgrowth in malabsorption syndrome and its relationship with oro-cecal transit time. Indian J Gastroenterol. 2006;25:6–10.PubMed
86.
Chandra S, Dutta U, Noor MT, Taneja N, Kochhar R, Sharma M, et al. Endoscopic jejunal biopsy culture: a simple and effective method to study jejunal microflora. Indian. J Gastroenterol. 2010;29:226–30.
87.
88.
89.
90.
Semba RD, Gonzalez-Freire M, Moaddel R, Trehan I, Maleta KM, Khadeer M, et al. Environmental enteric dysfunction is associated with altered bile acid metabolism. J Pediatr Gastroenterol Nutr. 2017;64:536–40.PubMedPubMedCentralCrossRef
91.
Gough EK, Stephens DA, Moodie EEM, Prendergast AJ, Stoltzfus RJ, Humphrey JH, et al. Linear growth faltering in infants is associated with Acidaminococcus sp. and community-level changes in the gut microbiota. Microbiome. 2015;3:24.PubMedPubMedCentralCrossRef
92.
Beam CA. Strategies for improving power in diagnostic radiology research. AJR Am J Roentgenol. 2013;159:631–7.CrossRef
93.
Naylor C, Lu M, Haque R, Mondal D, Buonomo E, Nayak U, et al. Environmental enteropathy, oral vaccine failure and growth faltering in infants in Bangladesh. EBioMedicine. 2015;2:1759–66.PubMedPubMedCentralCrossRef
94.
95.
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7.PubMedPubMedCentralCrossRef
96.
Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26:26050.PubMed
97.
Sanders TAB. Establishing of gut microbiota and bacterial colonisation of the gut in early life. Nutrition and development. West Sussex: Wiley; 2013. p. 116–29.
98.
Prentice AM, Ward KA, Goldberg GR, Jarjou LM, Moore SE, Fulford AJ, et al. Critical windows for nutritional interventions against stunting. Am J Clin Nutr. 2013;97:911–8.PubMedPubMedCentralCrossRef
99.
Georgiadis A, Penny ME. Child undernutrition: opportunities beyond the first 1000 days. Lancet Public Health. 2017;2:e399.PubMedCrossRef
100.
101.
Colston JM, Peñataro Yori P, Colantuoni E, Moulton LH, Ambikapathi R, Lee G, et al. A methodologic framework for modeling and assessing biomarkers of environmental enteropathy as predictors of growth in infants: an example from a Peruvian birth cohort. Am J Clin Nutr. 2017;106:245–55.PubMedCrossRef
102.
Vonaesch P, Anderson M, Sansonetti PJ. Pathogens, microbiome and the host: emergence of the ecological Koch’s postulates. FEMS Microbiol Rev. 2018;454:987.
103.
104.
Breurec S, Vanel N, Bata P, Chartier L, Farra A, Favennec L, et al. Etiology and epidemiology of diarrhea in hospitalized children from low income country: a matched case-control study in Central African Republic. Ryan ET, editor. PLoS Negl Trop Dis. 2016;10:e0004283.PubMedPubMedCentralCrossRef
105.
Vonaesch P, Tondeur L, Breurec S, Bata P, Nguyen LBL, Frank T, et al. Factors associated with stunting in healthy children aged 5 years and less living in Bangui (RCA). Wieringa F, editor. PLoS ONE. 2017;12:e0182363.PubMedPubMedCentralCrossRef
106.
Donowitz JR, Petri WA. Pediatric small intestine bacterial overgrowth in low-income countries. Trends Mol Med. 2015;21:6–15.PubMedCrossRef
107.
108.
Khin-Maung-U, Bolin TD, Duncombe VM, Myo-Khin, Nyunt-Nyunt-Wai, Pereira SP, et al. Epidemiology of small bowel bacterial overgrowth and rice carbohydrate malabsorption in Burmese (Myanmar) village children. Am J Trop Med Hyg. 1992;47:298–304.PubMedCrossRef
109.
Yu J, Ordiz MI, Stauber J, Shaikh N, Trehan I, Barnell E, et al. Environmental enteric dysfunction includes a broad spectrum of inflammatory responses and epithelial repair processes. Cell Mol Gastroenterol Hepatol. 2016;2:158–174.e1.PubMedCrossRef
110.
Parker EP, Ramani S, Lopman BA, Church JA, Iturriza-Gómara M, Prendergast AJ, et al. Causes of impaired oral vaccine efficacy in developing countries. Future Microbiol. 2018;13:97–118.PubMedCrossRef
111.
Becker-Dreps S, Vilchez S, Bucardo F, Twitchell E, Choi WS, Hudgens MG, et al. The association between fecal biomarkers of environmental enteropathy and rotavirus vaccine response in Nicaraguan infants. Pediatr Infect Dis J. 2017;36:412–6.PubMedCrossRef
112.
Oriá RB, Murray-Kolb LE, Scharf RJ, Pendergast LL, Lang DR, Kolling GL, et al. Early-life enteric infections: relation between chronic systemic inflammation and poor cognition in children. Nutr Rev. 2016;74:374–86.PubMedPubMedCentralCrossRef
113.
Guernier V, Brennan B, Yakob L, Milinovich G, Clements ACA, Soares Magalhaes RJ. Gut microbiota disturbance during helminth infection: can it affect cognition and behaviour of children? BMC Infect Dis. 2017;17:58.PubMedPubMedCentralCrossRef
114.
Ngure FM, Reid BM, Humphrey JH, Mbuya MN, Pelto G, Stoltzfus RJ. Water, sanitation, and hygiene (WASH), environmental enteropathy, nutrition, and early child development: making the links. Black MM, Dewey KG, editors. Ann N Y Acad Sci. 2014;1308:118–28.PubMedCrossRef
Metadata
Title
Identifying the etiology and pathophysiology underlying stunting and environmental enteropathy: study protocol of the AFRIBIOTA project
Authors
Pascale Vonaesch
Rindra Randremanana
Jean-Chrysostome Gody
Jean-Marc Collard
Tamara Giles-Vernick
Maria Doria
Inès Vigan-Womas
Pierre-Alain Rubbo
Aurélie Etienne
Emilson Jean Andriatahirintsoa
Nathalie Kapel
Eric Brown
Kelsey E. Huus
Darragh Duffy
B.Brett Finlay
Milena Hasan
Francis Allen Hunald
Annick Robinson
Alexandre Manirakiza
Laura Wegener-Parfrey
Muriel Vray
Philippe J. Sansonetti
for the AFRIBIOTA Investigators
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Pediatrics / Issue 1/2018
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/s12887-018-1189-5

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