Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Mondal D, Minak J, Alam M, Liu Y, Dai J, Korpe P, Liu L, Haque R, Petri WA Jr, 2012. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin Infect Dis 54: 185–192.
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Panter-Brick C, Lunn PG, Langford RM, Maharjan M, Manandhar DS, 2009. Pathways leading to early growth faltering: an investigation into the importance of mucosal damage and immunostimulation in different socio-economic groups in Nepal. Br J Nutr 101: 558–567.
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Cellier C, Delabesse E, Helmer C, Patey N, Matuchansky C, Jabri B, Macintyre E, Cerf-Bensussan N, Brousse N, 2000. Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma. French Coeliac Disease Study Group. Lancet 356: 203–208.
-
15.
Lin A, Arnold BF, Afreen S, Goto R, Huda T, Haque R, Raqib R, Unicomb L, Ahmed T, Colford JM Jr, Luby SP, 2013. Household environmental conditions are associated with enteropathy and impaired growth in rural Bangladesh. Am J Trop Med Hyg 89: 130–137.
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Humphrey JH, 2009. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374: 1032–1035.
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Lee G, Pan W, Penataro Yori P, Paredes Olortegui M, Tilley D, Gregory M, Oberhelman R, Burga R, Chavez CB, Kosek M, 2013. Symptomatic and asymptomatic Campylobacter infections associated with reduced growth in Peruvian children. PLoS Negl Trop Dis 7: e2036.
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Haghighi P, Wolf PL, 1997. Tropical sprue and subclinical enteropathy: a vision for the nineties. Crit Rev Clin Lab Sci 34: 313–341.
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22.
Goto K, Chew F, Torun B, Peerson JM, Brown KH, 1999. Epidemiology of altered intestinal permeability to lactulose and mannitol in Guatemalan infants. J Pediatr Gastroenterol Nutr 28: 282–290.
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23.
van Rheenen PF, Van de Vijver E, Fidler V, 2010. Faecal calprotectin for screening of patients with suspected inflammatory bowel disease: diagnostic meta-analysis. BMJ 341: c3369.
-
24.
Canani RB, Terrin G, Rapacciuolo L, Miele E, Siani MC, Puzone C, Cosenza L, Staiano A, Troncone R, 2008. Faecal calprotectin as reliable non-invasive marker to assess the severity of mucosal inflammation in children with inflammatory bowel disease. Dig Liver Dis 40: 547–553.
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Berni Canani R, Rapacciuolo L, Romano MT, Tanturri de Horatio L, Terrin G, Manguso F, Cirillo P, Paparo F, Troncone R, 2004. Diagnostic value of faecal calprotectin in paediatric gastroenterology clinical practice. Dig Liver Dis 36: 467–470.
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26.
Aomatsu T, Yoden A, Matsumoto K, Kimura E, Inoue K, Andoh A, Tamai H, 2011. Fecal calprotectin is a useful marker for disease activity in pediatric patients with inflammatory bowel disease. Dig Dis Sci 56: 2372–2377.
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Ngure FM, Humphrey JH, Mbuya MN, Majo F, Mutasa K, Govha M, Mazarura E, Chasekwa B, Prendergast AJ, Curtis V, Boor KJ, Stoltzfus RJ, 2013. Formative research on hygiene behaviors and geophagy among infants and young children and implications of exposure to fecal bacteria. Am J Trop Med Hyg 3: 3.
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Fecal Markers of Environmental Enteropathy are Associated with Animal Exposure and Caregiver Hygiene in Bangladesh
Christine Marie George
Christine Marie George
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Lauren Oldja
Lauren Oldja
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Shwapon K. Biswas
Shwapon K. Biswas
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Jamie Perin
Jamie Perin
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Gwenyth O. Lee
Gwenyth O. Lee
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Shahnawaz Ahmed
Shahnawaz Ahmed
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Rashidul Haque
Rashidul Haque
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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R. Bradley Sack
R. Bradley Sack
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Tahmina Parvin
Tahmina Parvin
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Ishrat J. Azmi
Ishrat J. Azmi
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Sazzadul Islam Bhuyian
Sazzadul Islam Bhuyian
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Kaisar A. Talukder
Kaisar A. Talukder
Johns Hopkins University, Baltimore, Maryland; International Center for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Abu G. Faruque
Abu G. Faruque
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Undernutrition is estimated to be an underlying cause of over half of all deaths in young children globally. There is a growing body of literature suggesting that increased exposure to enteric pathogens is responsible for environmental enteropathy (EE), a disorder associated with impaired growth in children. To determine if household unsanitary environmental conditions were significantly associated with EE and stunting in children, we conducted a cohort of 216 children (≤ 30 months) in rural Bangladesh. Stool was analyzed for four fecal markers of EE: alpha-1-antitrypsin, myeloperoxidase, and neopterin combined to form an EE disease activity score, and calprotectin. We observed a significant association between having an animal corral in a child's sleeping room and elevated EE scores (1.0 point difference, 95% confidence interval [CI]: 0.13, 1.88) and a two times higher odds of stunting (height-for-age z-score < −2) (odds ratio [OR]: 2.53, 95% CI: 1.08, 5.43) after adjusting for potential confounders. In addition, children of caregivers with visibly soiled hands had significantly elevated fecal calprotectin (μg/g) (384.1, 95% CI: 152.37, 615.83). These findings suggest that close contact with animals and caregiver hygiene may be important risk factors for EE in young children. These findings are consistent with the hypothesis that unsanitary environmental conditions can lead to EE in susceptible pediatric populations.
Author Notes
Financial support: This study was funded by a grant from the Johns Hopkins Sherrilyn and Ken Fisher Center for Environmental Infectious Diseases.
Authors' addresses: Christine M. George, Lauren Oldja, Jamie Perin, Gwenyth O. Lee, and R. Bradley Sack, Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, E-mails: cmgeorge@jhsph.edu, loldja@jhsph.edu, jperin@jhu.edu, glee35@jhu.edu, and rsack1@jhu.edu. Shwapon K. Biswas and Sazzadul Islam Bhuyian, Center for Communicable Diseases, International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh, E-mails: drskbiswas2004@yahoo.com and sazzadul.islam@icddrb.org. Shahnawaz Ahmed and Tahmina Parvin, Centre for Nutrition and Food Security (CNFS), icddr,b, Dhaka, Bangladesh, E-mails: shahnawz@icddrb.org and tparvin@icddrb.org. Rashidul Haque, icddr,b, Dhaka, Bangladesh, E-mail: rhaque@icddrb.org. Ishrat J. Azmi and Kaisar A. Talukder, Enteric Microbiology Unit, Centre for Health and Population Research, icddr,b, Dhaka, Bangladesh, E-mails: ishratazmi@icddrb.org and kaisar@icddrb.org. Abu G. Faruque, Clinical Sciences Division, icddr,b, Dhaka, Bangladesh, E-mail: gfaruque@icddrb.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
de Onis M, Blossner M, Borghi E, 2012. Prevalence and trends of stunting among pre-school children, 1990–2020. Public Health Nutr 15: 142–148.
-
2.
Caulfield LE, de Onis M, Blossner M, Black RE, 2004. Undernutrition as an underlying cause of child deaths associated with diarrhea, pneumonia, malaria, and measles. Am J Clin Nutr 80: 193–198.
-
3.
Victora CG, de Onis M, Hallal PC, Blossner M, Shrimpton R, 2010. Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 125: e473–e480.
-
4.
Goto R, Mascie-Taylor CG, Lunn PG, 2009. Impact of anti-Giardia and anthelminthic treatment on infant growth and intestinal permeability in rural Bangladesh: a randomised double-blind controlled study. Trans R Soc Trop Med Hyg 103: 520–529.
-
5.
Kosek M, Haque R, Lima A, Babji S, Shrestha S, Qureshi S, Amidou S, Mduma E, Lee G, Yori PP, Guerrant RL, Bhutta Z, Mason C, Kang G, Kabir M, Amour C, Bessong P, Turab A, Seidman J, Olortegui MP, Quetz J, Lang D, Gratz J, Miller M, Gottlieb M; MAL-ED network, 2013. Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants. Am J Trop Med Hyg 88: 390–396.
-
6.
Liu JR, Sheng XY, Hu YQ, Yu XG, Westcott JE, Miller LV, Krebs NF, Hambidge KM, 2012. Fecal calprotectin levels are higher in rural than in urban Chinese infants and negatively associated with growth. BMC Pediatr 12: 129.
-
7.
Campbell DI, Elia M, Lunn PG, 2003. Growth faltering in rural Gambian infants is associated with impaired small intestinal barrier function, leading to endotoxemia and systemic inflammation. J Nutr 133: 1332–1338.
-
8.
Campbell DI, McPhail G, Lunn PG, Elia M, Jeffries DJ, 2004. Intestinal inflammation measured by fecal neopterin in Gambian children with enteropathy: association with growth failure, Giardia lamblia, and intestinal permeability. J Pediatr Gastroenterol Nutr 39: 153–157.
-
9.
Lunn PG, Northrop-Clewes CA, Downes RM, 1991. Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. Lancet 338: 907–910.
-
10.
Weisz AJ, Manary MJ, Stephenson K, Agapova S, Manary FG, Thakwalakwa C, Shulman RJ, Manary MJ, 2012. Abnormal gut integrity is associated with reduced linear growth in rural Malawian children. J Pediatr Gastroenterol Nutr 55: 747–750.
-
11.
Goto R, Mascie-Taylor CG, Lunn PG, 2009. Impact of intestinal permeability, inflammation status and parasitic infections on infant growth faltering in rural Bangladesh. Br J Nutr 101: 1509–1516.
-
12.
Mondal D, Minak J, Alam M, Liu Y, Dai J, Korpe P, Liu L, Haque R, Petri WA Jr, 2012. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin Infect Dis 54: 185–192.
-
13.
Panter-Brick C, Lunn PG, Langford RM, Maharjan M, Manandhar DS, 2009. Pathways leading to early growth faltering: an investigation into the importance of mucosal damage and immunostimulation in different socio-economic groups in Nepal. Br J Nutr 101: 558–567.
-
14.
Cellier C, Delabesse E, Helmer C, Patey N, Matuchansky C, Jabri B, Macintyre E, Cerf-Bensussan N, Brousse N, 2000. Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma. French Coeliac Disease Study Group. Lancet 356: 203–208.
-
15.
Lin A, Arnold BF, Afreen S, Goto R, Huda T, Haque R, Raqib R, Unicomb L, Ahmed T, Colford JM Jr, Luby SP, 2013. Household environmental conditions are associated with enteropathy and impaired growth in rural Bangladesh. Am J Trop Med Hyg 89: 130–137.
-
16.
Humphrey JH, 2009. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374: 1032–1035.
-
17.
Menzies IS, Zuckerman MJ, Nukajam WS, Somasundaram SG, Murphy B, Jenkins AP, Crane RS, Gregory GG, 1999. Geography of intestinal permeability and absorption. Gut 44: 483–489.
-
18.
Thomas G, Clain DJ, Wicks AC, 1976. Tropical enteropathy in Rhodesia. Gut 17: 888–894.
-
19.
Checkley W, Gilman RH, Epstein LD, Suarez M, Diaz JF, Cabrera L, Black RE, Sterling CR, 1997. Asymptomatic and symptomatic cryptosporidiosis: their acute effect on weight gain in Peruvian children. Am J Epidemiol 145: 156–163.
-
20.
Lee G, Pan W, Penataro Yori P, Paredes Olortegui M, Tilley D, Gregory M, Oberhelman R, Burga R, Chavez CB, Kosek M, 2013. Symptomatic and asymptomatic Campylobacter infections associated with reduced growth in Peruvian children. PLoS Negl Trop Dis 7: e2036.
-
21.
Haghighi P, Wolf PL, 1997. Tropical sprue and subclinical enteropathy: a vision for the nineties. Crit Rev Clin Lab Sci 34: 313–341.
-
22.
Goto K, Chew F, Torun B, Peerson JM, Brown KH, 1999. Epidemiology of altered intestinal permeability to lactulose and mannitol in Guatemalan infants. J Pediatr Gastroenterol Nutr 28: 282–290.
-
23.
van Rheenen PF, Van de Vijver E, Fidler V, 2010. Faecal calprotectin for screening of patients with suspected inflammatory bowel disease: diagnostic meta-analysis. BMJ 341: c3369.
-
24.
Canani RB, Terrin G, Rapacciuolo L, Miele E, Siani MC, Puzone C, Cosenza L, Staiano A, Troncone R, 2008. Faecal calprotectin as reliable non-invasive marker to assess the severity of mucosal inflammation in children with inflammatory bowel disease. Dig Liver Dis 40: 547–553.
-
25.
Berni Canani R, Rapacciuolo L, Romano MT, Tanturri de Horatio L, Terrin G, Manguso F, Cirillo P, Paparo F, Troncone R, 2004. Diagnostic value of faecal calprotectin in paediatric gastroenterology clinical practice. Dig Liver Dis 36: 467–470.
-
26.
Aomatsu T, Yoden A, Matsumoto K, Kimura E, Inoue K, Andoh A, Tamai H, 2011. Fecal calprotectin is a useful marker for disease activity in pediatric patients with inflammatory bowel disease. Dig Dis Sci 56: 2372–2377.
-
27.
Laine L, Garcia F, McGilligan K, Malinko A, Sinatra FR, Thomas DW, 1993. Protein-losing enteropathy and hypoalbuminemia in AIDS. AIDS 7: 837–840.
-
28.
Saiki T, 1998. Myeloperoxidase concentrations in the stool as a new parameter of inflammatory bowel disease. Kurume Med J 45: 69–73.
-
29.
Marquis GS, Ventura G, Gilman RH, Porras E, Miranda E, Carbajal L, Pentafiel M, 1990. Fecal contamination of shanty town toddlers in households with non-corralled poultry, Lima, Peru. Am J Public Health 80: 146–149.
-
30.
Ngure FM, Humphrey JH, Mbuya MN, Majo F, Mutasa K, Govha M, Mazarura E, Chasekwa B, Prendergast AJ, Curtis V, Boor KJ, Stoltzfus RJ, 2013. Formative research on hygiene behaviors and geophagy among infants and young children and implications of exposure to fecal bacteria. Am J Trop Med Hyg 3: 3.
-
31.
Halder A, Tronchet C, Akhter S, Bhuiya A, Johnston R, Luby S, 2010. Observed hand cleanliness and other measures of handwashing behavior in rural Bangladesh. BMC Public Health 10: 545.
-
32.
World Health Organization, 2008. Child Growth Standards 2006. Available at: www.who.int/childgrowth/en.
-
33.
de Onis M, Blössner M, 1997. WHO Global Database on Child Growth and Malnutrition. Geneva, Switzerland: World Health Organization.
-
34.
Smith KE, Stenzel SA, Bender JB, Wagstrom E, Soderlund D, Leano FT, Taylor CM, Belle-Isle PA, Danila R, 2004. Outbreaks of enteric infections caused by multiple pathogens associated with calves at a farm day camp. Pediatr Infect Dis J 23: 1098–1104.
-
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