Geophagy is associated with environmental enteropathy and stunting in children in rural Bangladesh

American Journal of Tropical Medicine and Hygiene

Volumn 92, Issue 6, 2015, Pages 1117-1124

  George, Christine Marie ^a,b   Oldja, Lauren ^a,b   Biswas, Shwapon ^a,c   Perin, Jamie ^a,b   Lee, Gwenyth O ^a,b   Kosek, Margaret ^a,b   Sack, R Bradley ^a,b   Ahmed, Shahnawaz ^a,c   Haque, Rashidul ^a,c   Parvin, Tahmina ^a,c   Azmi, Ishrat J ^a,d   Bhuyian, Sazzadul Islam ^a,c   Talukder, Kaisar A ^a,d   Mohammad, Shahnaij ^a,c   Faruque, Abu G ^a,e  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^d ICDDR B Centre for Health and Population Research   (Bangladesh)

^e ICDDRB Clinical Sciences Division   (Bangladesh)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; CALGRANULIN; MYELOPEROXIDASE; NEOPTERIN; SOIL;

ANTHROPOMETRIC PARAMETERS; ARTICLE; CAREGIVER; CHILD; DIARRHEAGENIC ESCHERICHIA COLI; DISEASE ASSOCIATION; ENTERITIS; ENTEROPATHY; ENVIRONMENTAL ENTEROPATHY; ESCHERICHIA COLI; FEEDING BEHAVIOR; FEMALE; FOLLOW UP; GEOPHAGY; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PRESCHOOL CHILD; STUNTING; BANGLADESH; COMPLICATION; FECES; GROWTH DISORDERS; INTESTINAL DISEASES; MICROBIOLOGY; PICA; PROSPECTIVE STUDY; RURAL POPULATION; SOIL; STATISTICS AND NUMERICAL DATA;

ESCHERICHIA COLI;

BANGLADESH; CHILD, PRESCHOOL; ESCHERICHIA COLI; FECES; FEMALE; GROWTH DISORDERS; HUMANS; INFANT; INTESTINAL DISEASES; MALE; PICA; PROSPECTIVE STUDIES; RURAL POPULATION; SOIL; SOIL MICROBIOLOGY;

EID: 84930604110     PISSN: 00029637     EISSN: None     Source Type: Journal    
DOI: 10.4269/ajtmh.14-0672     Document Type: Article

References (52)

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.
30. World Health Organization, 2008. Child Growth Standards 2006. Available at: http://www.who.int/childgrowth/en/.
31. De Onis M, Blössner M, 1997. WHO Global Database on Child Growth and Malnutrition. Geneva, Switzerland: World Health Organization.
32. Dewey KG, Begum K, 2011. Long-term consequences of stunting in early life. Matern Child Nutr 7(Suppl 3):5-18.
33. 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 89:709-716.
34. Houpt E, Gratz J, Kosek M, Zaidi AK, Qureshi S, Kang G, Babji S, Mason C, Bodhidatta L, Samie A, Bessong P, Barrett L, Lima A, Havt A, Haque R, Mondal D, Taniuchi M, Stroup S, McGrath M, Lang D; MAL-ED Network Investigators, 2014. Microbiologic methods utilized in the MAL-ED Cohort Study. Clin Infect Dis 59(Suppl 4):S225-S232.
35. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM, 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209-222.
36. Tulve NS, Suggs JC, McCurdy T, Cohen Hubal EA, Moya J, 2002. Frequency of mouthing behavior in young children. J Expo Anal Environ Epidemiol 12:259-264.
37. Juberg DR, Alfano K, Coughlin RJ, Thompson KM, 2001. An observational study of object mouthing behavior by young children. Pediatrics 107:135-142.
38. Ruff HA, 1984. Infants' manipulative exploration of objects: effects of age and object characteristics. Dev Psychol 20:9.
39. Ruff HA, Dubiner K, 1987. Stability of individual differences in infants' manipulation and exploration of objects. Percept Mot Skills 64:1095-1101.
40. Groot ME, Lekkerkerk M, Steenbekkers L, 1998. Mouthing Behaviour of Young Children: An Observational Study. Wageningen, The Netherlands: Wageningen Agricultural University.
41. Hunter JM, 1973. Geophagy in Africa and in the United States: a culture-nutrition hypothesis. Geogr Rev 63:170-195.
42. Pickering AJ, Julian TR, Marks SJ, Mattioli MC, Boehm AB, Schwab KJ, Davis J, 2012. Fecal contamination and diarrheal pathogens on surfaces and in soils among Tanzanian households with and without improved sanitation. Environ Sci Technol 46:5736-5743.
43. Kaper JB, Nataro JP, Mobley HL, 2004. Pathogenic Escherichia coli. Nat Rev Microbiol 2:123-140.
44. Ngure FM, Reid BM, Humphrey JH, Mbuya MN, Pelto G, Stoltzfus RJ, 2014. Water, sanitation, and hygiene (WASH), environmental enteropathy, nutrition, and early child development: making the links. Ann N Y Acad Sci 1308:118-128.
45. Young SL, Sherman PW, Lucks JB, Pelto GH, 2011. Why on earth? Evaluating hypotheses about the physiological functions of human geophagy. Q Rev Biol 86:97-120.
46. Young SL, Khalfan SS, Farag TH, Kavle JA, Ali SM, Hajji H, Rasmussen KM, Pelto GH, Tielsch JM, Stoltzfus RJ, 2010. Association of pica with anemia and gastrointestinal distress among pregnant women in Zanzibar, Tanzania. Am J Trop Med Hyg 83:144-151.
47. Gutelius MF, Millican FK, Layman EM, Cohen GJ, Dublin CC, 1962. Nutritional studies of children with pica. I Controlled study evaluating nutritional status. Pediatrics 29:1012-1023.
48. Nchito M, Geissler PW, Mubila L, Friis H, Olsen A, 2004. Effects of iron and multimicronutrient supplementation on geophagy: a two-by-two factorial study among Zambian schoolchildren in Lusaka. Trans R Soc Trop Med Hyg 98:218-227.
49. Chen P, Soares AM, Lima AA, Gamble MV, Schorling JB, Conway M, Conway M, Barrett LJ, Blaner WS, Guerrant RL, 2003. Association of vitamin A and zinc status with altered intestinal permeability: analyses of cohort data from northeastern Brazil. J Health Popul Nutr 21:309-315.
50. Alam AN, Sarker SA, Wahed MA, Khatun M, Rahaman MM, 1994. Enteric protein loss and intestinal permeability changes in children during acute shigellosis and after recovery: effect of zinc supplementation. Gut 35:1707-1711.
51. Ryan KN, Stephenson KB, Trehan I, Shulman RJ, Thakwalakwa C, Murray E, Maleta K, Manary MJ. Zinc or albendazole attenuates the progression of environmental enteropathy: a randomized controlled trial. Clin Gastroenterol Hepatol 12:1507-1513.e1.
52. Nchito M, Friis H, Michaelsen KF, Mubila L, Olsen A, 2006. Iron supplementation increases small intestine permeability in primary schoolchildren in Lusaka, Zambia. Trans R Soc Trop Med Hyg 100:791-794.