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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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Luoba AI, Wenzel Geissler P, Estambale B, Ouma JH, Alusala D, Ayah R, Mwaniki D, Magnussen P, Friis H, 2005. Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya. Trop Med Int Health 10: 220–227.
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Geophagy is Associated with Environmental Enteropathy and Stunting in Children in Rural Bangladesh
Christine Marie George
Christine Marie George
Johns Hopkins University, Baltimore, Maryland; International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Lauren Oldja
Lauren Oldja
Johns Hopkins University, Baltimore, Maryland; International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Shwapon Biswas
Shwapon Biswas
Johns Hopkins University, Baltimore, Maryland; International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Jamie Perin
Jamie Perin
Johns Hopkins University, Baltimore, Maryland; International Centre 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 Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Margaret Kosek
Margaret Kosek
Johns Hopkins University, Baltimore, Maryland; International Centre 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 Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Shahnawaz Ahmed
Shahnawaz Ahmed
Johns Hopkins University, Baltimore, Maryland; International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Rashidul Haque
Rashidul Haque
Johns Hopkins University, Baltimore, Maryland; International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Tahmina Parvin
Tahmina Parvin
Johns Hopkins University, Baltimore, Maryland; International Centre 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 Centre 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 Centre 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 Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Shahnaij Mohammad
Shahnaij Mohammad
Johns Hopkins University, Baltimore, Maryland; International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
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Abu G. Faruque
Abu G. Faruque
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There is a growing body of literature indicating an association between stunting and environmental enteropathy (EE), a disorder thought to be caused by repeated exposures to enteric pathogens. To investigate the relationship between exposure to enteric pathogens through geophagy, consumption of soil, EE, and stunting, we conducted a prospective cohort study of 216 children under 5 years of age in rural Bangladesh. Geophagy was assessed at baseline using 5 hour structured observation and caregiver reports. Stool was analyzed for fecal markers of intestinal inflammation: alpha-1-antitrypsin, myeloperoxidase, neopterin (all three combined to form an EE disease activity score), and calprotectin. Eighteen percent of children had observed geophagy events by structured observation and 28% had caregiver reported events in the past week. Nearly all households had Escherichia coli (97%) in soil, and 14% had diarrheagenic E. coli. Children with caregiver-reported geophagy had significantly higher EE scores (0.72 point difference, 95% confidence interval [CI]: 0.01, 1.42) and calprotectin concentrations (237.38 μg/g, 95% CI: 12.77, 462.00). Furthermore, at the 9-month follow-up the odds of being stunted (height-for-age z-score < −2) was double for children with caregiver-reported geophagy (odds ratio [OR]: 2.27, 95% CI: 1.14, 4.51). These findings suggest that geophagy in young children may be an important unrecognized risk factor for EE and stunting.
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, Margaret Kosek, and R. Bradley Sack, Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, E-mails: cmgeorge@jhsph.edu, loldja@gmail.com, jperin@jhu.edu, golee@jhsph.edu, makosek@jhmi.edu, and rsack1@jhu.edu. Shwapon Biswas, Rashidul Haque, and Sazzadul Islam Bhuyian, Center for Communicable Diseases, icddr,b, Dhaka, Bangladesh, E-mails: drskbiswas2004@yahoo.com, rhaque@icddrb.org, 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. 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. Shahnaij Mohammad, Enteric Bacteriology and Epidemiology Unit, icddr,b, Dhaka, Bangladesh, E-mail: shahnawajbmb@gmail.com. Abu G. Faruque, Clinical Sciences Division, icddr,b, Dhaka, Bangladesh, E-mail: gfaruque@icddrb.org.
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-
1.
Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J, 2008. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 371: 243–260.
-
2.
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, 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.
-
3.
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.
-
4.
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.
-
5.
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.
-
6.
Lunn PG, Northrop-Clewes CA, Downes RM, 1991. Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. Lancet 338: 907–910.
-
7.
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.
-
8.
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.
-
9.
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.
-
10.
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.
-
11.
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.
-
12.
Haghighi P, Wolf PL, 1997. Tropical sprue and subclinical enteropathy: a vision for the nineties. Crit Rev Clin Lab Sci 34: 313–341.
-
13.
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.
-
14.
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.
-
15.
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.
-
16.
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.
-
17.
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.
-
18.
Laine L, Garcia F, McGilligan K, Malinko A, Sinatra FR, Thomas DW, 1993. Protein-losing enteropathy and hypoalbuminemia in AIDS. AIDS 7: 837–840.
-
19.
Saiki T, 1998. Myeloperoxidase concentrations in the stool as a new parameter of inflammatory bowel disease. Kurume Med J 45: 69–73.
-
20.
Kawata K, 1978. Water and other environmental interventions—the minimum investment concept. Am J Clin Nutr 31: 2114–2123.
-
21.
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.
-
22.
Shivoga WA, Moturi WN, 2009. Geophagia as a risk factor for diarrhoea. J Infect Dev Ctries 3: 94–98.
-
23.
Geissler PW, Mwaniki D, Thiong F, Friis H, 1998. Geophagy as a risk factor for geohelminth infections: a longitudinal study of Kenyan primary schoolchildren. Trans R Soc Trop Med Hyg 92: 7–11.
-
24.
Luoba AI, Wenzel Geissler P, Estambale B, Ouma JH, Alusala D, Ayah R, Mwaniki D, Magnussen P, Friis H, 2005. Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya. Trop Med Int Health 10: 220–227.
-
25.
Kutalek R, Wewalka G, Gundacker C, Auer H, Wilson J, Haluza D, Huhulescu S, Hillier S, Sager M, Prinz A, 2010. Geophagy and potential health implications: geohelminths, microbes and heavy metals. Trans R Soc Trop Med Hyg 104: 787–795.
-
26.
Glickman LT, Camara AO, Glickman NW, McCabe GP, 1999. Nematode intestinal parasites of children in rural Guinea, Africa: prevalence and relationship to geophagia. Int J Epidemiol 28: 169–174.
-
27.
Miao D, Young SL, Golden CD, 2014. A meta-analysis of pica and micronutrient status. Am J Hum Biol 27: 84–93.
-
28.
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.
-
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.
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