1921
Volume 93, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

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.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.14-0694
2015-08-05
2017-09-26
Loading full text...

Full text loading...

/deliver/fulltext/14761645/93/2/269.html?itemId=/content/journals/10.4269/ajtmh.14-0694&mimeType=html&fmt=ahah

References

  1. de Onis M, Blossner M, Borghi E, , 2012. Prevalence and trends of stunting among pre-school children, 1990–2020. Public Health Nutr 15: 142148.[Crossref]
  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: 193198.
  3. Victora CG, de Onis M, Hallal PC, Blossner M, Shrimpton R, , 2010. Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 125: e473e480.[Crossref]
  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: 520529.[Crossref]
  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: 390396.[Crossref]
  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.[Crossref]
  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: 13321338.
  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: 153157.[Crossref]
  9. Lunn PG, Northrop-Clewes CA, Downes RM, , 1991. Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. Lancet 338: 907910.[Crossref]
  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: 747750.[Crossref]
  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: 15091516.[Crossref]
  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: 185192.[Crossref]
  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: 558567.[Crossref]
  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: 203208.[Crossref]
  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: 130137.[Crossref]
  16. Humphrey JH, , 2009. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374: 10321035.[Crossref]
  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: 483489.[Crossref]
  18. Thomas G, Clain DJ, Wicks AC, , 1976. Tropical enteropathy in Rhodesia. Gut 17: 888894.[Crossref]
  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: 156163.[Crossref]
  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.[Crossref]
  21. Haghighi P, Wolf PL, , 1997. Tropical sprue and subclinical enteropathy: a vision for the nineties. Crit Rev Clin Lab Sci 34: 313341.[Crossref]
  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: 282290.[Crossref]
  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.[Crossref]
  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: 547553.[Crossref]
  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: 467470.[Crossref]
  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: 23722377.[Crossref]
  27. Laine L, Garcia F, McGilligan K, Malinko A, Sinatra FR, Thomas DW, , 1993. Protein-losing enteropathy and hypoalbuminemia in AIDS. AIDS 7: 837840.[Crossref]
  28. Saiki T, , 1998. Myeloperoxidase concentrations in the stool as a new parameter of inflammatory bowel disease. Kurume Med J 45: 6973.[Crossref]
  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: 146149.[Crossref]
  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.[Crossref]
  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: 10981104.[Crossref]
  35. Trevena WB, Willshaw GA, Cheasty T, Domingue G, Wray C, , 1999. Transmission of Vero cytotoxin producing Escherichia coli O157 infection from farm animals to humans in Cornwall and west Devon. Commun Dis Public Health 2: 263268.
  36. Chapman PA, Cornell J, Green C, , 2000. Infection with verocytotoxin-producing Escherichia coli O157 during a visit to an inner city open farm. Epidemiol Infect 125: 531536.[Crossref]
  37. Bender JB, Shulman SA, , 2004. Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings. J Am Vet Med Assoc 224: 11051109.[Crossref]
  38. Oberhelman RA, Gilman RH, Sheen P, Cordova J, Zimic M, Cabrera L, Meza R, Perez J, , 2006. An intervention-control study of corralling of free-ranging chickens to control Campylobacter infections among children in a Peruvian periurban shantytown. Am J Trop Med Hyg 74: 10541059.
  39. Grados O, Bravo N, Black RE, Butzler JP, , 1988. Paediatric Campylobacter diarrhoea from household exposure to live chickens in Lima, Peru. Bull World Health Organ 66: 369374.
  40. Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, Colford JM, Jr, 2005. Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis 5: 4252.[Crossref]
  41. Curtis V, Cairncross S, , 2003. Effect of washing hands with soap on diarrhoea risk in the community: a systematic review. Lancet Infect Dis 3: 275281.[Crossref]
  42. Pickering AJ, Julian TR, Mamuya S, Boehm AB, Davis J, , 2011. Bacterial hand contamination among Tanzanian mothers varies temporally and following household activities. Trop Med Int Health 16: 233239.[Crossref]
  43. Langford R, Lunn P, Panter-Brick C, , 2011. Hand-washing, subclinical infections, and growth: a longitudinal evaluation of an intervention in Nepali slums. Am J Hum Biol 23: 621629.[Crossref]
  44. Tagoe E, Makinwa P, An-Magritt J, , 1995. Maternal education and infant/child morbidity in Ghana: the case of diarrhoea. Evidence from the Ghana DHS. , eds. Women's Position and Demographic Change in Sub-Saharan Africa. Liege, Belgium: International Union for the Scientific Study of Population (IUSSP), 169200.
  45. Woldemicael G, , 2001. Diarrhoeal morbidity among young children in Eritrea: environmental and socioeconomic determinants. J Health Popul Nutr 19: 8390.
  46. 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: 787795.[Crossref]
  47. 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: 711.[Crossref]
  48. 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: 169174.[Crossref]
  49. 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: 220227.[Crossref]
  50. 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: 57365743.[Crossref]
  51. George CM, Oldja L, Biswas S, Perin J, Lee GO, Kosek M, Sack RB, Ahmed S, Haque R, Parvin T, Azmi IJ, Bhuyian SI, Talukder KA, Mohammad S, Faruque AG, , 2015. Geophagy is associated with environmental enteropathy and stunting in children in rural Bangladesh. Am J Trop Med Hyg 92: 11171124.[Crossref]
  52. Shivoga WA, Moturi WN, , 2009. Geophagia as a risk factor for diarrhoea. J Infect Dev Ctries 3: 9498.
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.14-0694
Loading
/content/journals/10.4269/ajtmh.14-0694
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

Erratum

  • Received : 03 Nov 2014
  • Accepted : 20 Apr 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error