1921
Volume 95, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

Environmental enteropathy (EE), a subclinical intestinal disorder characterized by mucosal inflammation, reduced barrier integrity, and malabsorption, appears to be associated with increased risk of stunting in children in low- and middle-income countries. Fecal biomarkers indicative of EE (neopterin [NEO], myeloperoxidase [MPO], and alpha-1-antitrypsin [AAT]) have been negatively associated with 6-month linear growth. Associations between fecal markers (NEO, MPO, and AAT) and short-term linear growth were examined in a birth cohort of 246 children in Bangladesh. Marker concentrations were categorized in stool samples based on their distribution (< first quartile, interquartile range, > third quartile), and a 10-point composite EE score was calculated. Piecewise linear mixed-effects models were used to examine the association between markers measured quarterly (in months 3–21, 3–9, and 12–21) and 3-month change in length-for-age z-score (ΔLAZ). Children with high MPO levels at quarterly time points lost significantly more LAZ per 3-month period during the second year of life than those with low MPO (ΔLAZ = −0.100; 95% confidence interval = −0.167 to −0.032). AAT and NEO were not associated with growth; however, composite EE score was negatively associated with subsequent 3-month growth. In this cohort of children from an urban setting in Bangladesh, elevated MPO levels, but not NEO or AAT levels, were associated with decreases in short-term linear growth during the second year of life, supporting previous data suggesting the relevance of MPO as a marker of EE.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.16-0098
2016-09-07
2017-09-23
Loading full text...

Full text loading...

/deliver/fulltext/14761645/95/3/694.html?itemId=/content/journals/10.4269/ajtmh.16-0098&mimeType=html&fmt=ahah

References

  1. de Onis M, Blössner M, Borghi E, , 2012. Prevalence and trends of stunting among pre-school children, 1990–2020. Public Health Nutr 15: 142148.[Crossref]
  2. Olofin I, McDonald CM, Ezzati M, Flaxman S, Black RE, Fawzi WW, Caulfield LE, Danaei G, Nutrition Impact Model Study (anthropometry cohort pooling); , 2013. Associations of suboptimal growth with all-cause and cause-specific mortality in children under five years: a pooled analysis of ten prospective studies. PLoS One 8: e64636.[Crossref]
  3. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE, Child Health Epidemiology Reference Group of WHO and UNICEF; , 2012. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 379: 21512161.[Crossref]
  4. Bhutta ZA, Ahmed T, Black RE, Cousens S, Dewey K, Giugliani E, Haider BA, Kirkwood B, Morris SS, Sachdev HP, Shekar M, Maternal and Child Undernutrition Study Group; , 2008. What works? Interventions for maternal and child undernutrition and survival. Lancet 371: 417440.[Crossref]
  5. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L, Sachdev HS, Maternal and Child Undernutrition Study Group; , 2008. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 371: 340357.[Crossref]
  6. Black RE, Victora CG, Walker SP, Bhutta ZA, Christian P, de Onis M, Ezzati M, Grantham-McGregor S, Katz J, Martorell R, Uauy R, Maternal and Child Nutrition Study Group; , 2013. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382: 427451.[Crossref]
  7. Berkman D, Lescano A, Gilman R, Lopez S, Black M, , 2002. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359: 564571.[Crossref]
  8. Mendez M, Adair L, , 1999. Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. J Nutr 129: 15551562.
  9. Powell C, Walker S, Himes J, Fletcher P, Grantham-McGregor S, , 1995. Relationships between physical growth, mental development and nutritional supplementation in stunted children: the Jamaican study. Acta Paediatr 84: 2229.[Crossref]
  10. Dewey K, Begum K, , 2011. Long-term consequences of stunting in early life. Matern Child Nutr 7 (Suppl 3): 518.[Crossref]
  11. Ozaltin E, Hill K, Subramanian S, , 2010. Association of maternal stature with offspring mortality, underweight, and stunting in low- to middle-income countries. JAMA 303: 15071516.[Crossref]
  12. Keusch GT, Denno DM, Black RE, Duggan C, Guerrant RL, Lavery JV, Nataro JP, Rosenberg IH, Ryan ET, Tarr PI, Ward H, Bhutta ZA, Coovadia H, Lima A, Ramakrishna B, Zaidi AKM, Hay Burgess DC, Brewer T, , 2014. Environmental enteric dysfunction: pathogenesis, diagnosis, and clinical consequences. Clin Infect Dis 59: S207S212.[Crossref]
  13. Humphrey JH, , 2009. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374: 10321035.[Crossref]
  14. Korpe PS, Petri WA, , 2012. Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol Med 18: 328336.[Crossref]
  15. Guerrant RL, Oriá RB, Moore SR, Oriá MO, Lima AA, , 2008. Malnutrition as an enteric infectious disease with long-term effects on child development. Nutr Rev 66: 487505.[Crossref]
  16. Denno DM, VanBuskirk K, Nelson ZC, Musser CA, Hay Burgess DC, Tarr PI, , 2014. Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review. Clin Infect Dis 59: S213S219.[Crossref]
  17. Kosek M, Guerrant RL, Kang G, Bhutta Z, Yori PP, Gratz J, Gottlieb M, Lang D, Lee G, Haque R, Mason CJ, Ahmed T, Lima A, Petri WA, Houpt E, Olortegui MP, Seidman JC, Mduma E, Samie A, Babji S, MAL-ED Network Investigators; , 2014. Assessment of environmental enteropathy in the MAL-ED cohort study: theoretical and analytic framework. Clin Infect Dis 59: S239S247.[Crossref]
  18. 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]
  19. Peterson KM, Buss J, Easley R, Yang Z, Korpe PS, Niu F, Ma JZ, Olortegui MP, Haque R, Kosek MN, Petri WA, , 2013. REG1B as a predictor of childhood stunting in Bangladesh and Peru. Am J Clin Nutr 97: 11291133.[Crossref]
  20. Widner B, Wirleitner B, Baier-Bitterlich G, Weiss G, Fuchs D, , 2000. Cellular immune activation, neopterin production, tryptophan degradation and the development of immunodeficiency. Arch Immunol Ther Exp (Warsz) 48: 251258.
  21. Wagner M, Peterson CG, Ridefelt P, Sangfelt P, Carlson M, , 2008. Fecal markers of inflammation used as surrogate markers for treatment outcome in relapsing inflammatory bowel disease. World J Gastroenterol 14: 55845589, discussion 5588.[Crossref]
  22. Peterson CG, Eklund E, Taha Y, Raab Y, Carlson M, , 2002. A new method for the quantification of neutrophil and eosinophil cationic proteins in feces: establishment of normal levels and clinical application in patients with inflammatory bowel disease. Am J Gastroenterol 97: 17551762.[Crossref]
  23. Hill RE, Hercz A, Corey ML, Gilday DL, Hamilton JR, , 1981. Fecal clearance of alpha 1-antitrypsin: a reliable measure of enteric protein loss in children. J Pediatr 99: 416418.[Crossref]
  24. Bernier JJ, Florent C, Desmazures C, Aymes C, L'Hirondel C, , 1978. Diagnosis of protein-losing enteropathy by gastrointestinal clearance of alpha1-antitrypsin. Lancet 2: 763764.[Crossref]
  25. Karbach U, Ewe K, Bodenstein H, , 1983. Alpha 1-antitrypsin, a reliable endogenous marker for intestinal protein loss and its application in patients with Crohn's disease. Gut 24: 718723.[Crossref]
  26. Wiria AE, Prasetyani MA, Hamid F, Wammes LJ, Lell B, Ariawan I, Uh HW, Wibowo H, Djuardi Y, Wahyuni S, Sutanto I, May L, Luty AJ, Verweij JJ, Sartono E, Yazdanbakhsh M, Supali T, , 2010. Does treatment of intestinal helminth infections influence malaria? Background and methodology of a longitudinal study of clinical, parasitological and immunological parameters in Nangapanda, Flores, Indonesia (ImmunoSPIN Study). BMC Infect Dis 10: 77.[Crossref]
  27. Ahmed T, Mahfuz M, Islam MM, Mondal D, Hossain MI, Ahmed AS, Tofail F, Gaffar SA, Haque R, Guerrant RL, Petri WA, , 2014. The MAL-ED cohort study in Mirpur, Bangladesh. Clin Infect Dis 59: S280S286.[Crossref]
  28. Investigators TM-EN, 2014. 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 59: S193S206.[Crossref]
  29. Richard SA, McCormick BJJ, Miller MA, Caulfield LE, Checkley W, , 2014. Modeling environmental influences on child growth in the MAL-ED cohort study: opportunities and challenges. Clin Infect Dis 59: S255S260.[Crossref]
  30. Saiki T, , 1998. Myeloperoxidase concentrations in the stool as a new parameter of inflammatory bowel disease. Kurume Med J 45: 6973.[Crossref]
  31. Beckmann GT, Rüffer A, , 2000. Mikroökologie des Darmes: Grundlagen, Diagnostik, Therapie [Microbiology of the Intestines: Basics, Diagnostics, Therapy]. Hannover, Germany: Schlütersche.
  32. Ledjeff E, Artner-Dworzak E, Witasek A, Fuchs D, Hausen A, , 2001. Neopterin concentrations in colon dialysate. Pteridines 12: 155160.[Crossref]
  33. Naylor C, Lu M, Haque R, Mondal D, Buonomo E, Nayak U, Mychaleckyj JC, Kirkpatrick B, Colgate R, Carmolli M, Dickson D, van der Klis F, Weldon W, Steven Oberste M, Ma JZ, Petri WA, Jr, 2015. Environmental enteropathy, oral vaccine failure and growth faltering in infants in Bangladesh. EBioMedicine 2: 17591766.[Crossref]
  34. Wardlaw TM, , 2004. Low Birthweight: Country, Regional and Global Estimates. New York, NY: UNICEF.
  35. Victora C, Onis M, Hallal P, Blössner M, Shrimpton R, , 2010. Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 125: e473e480.[Crossref]
  36. Dewey K, Adu-Afarwuah S, , 2008. Systematic review of the efficacy and effectiveness of complementary feeding interventions in developing countries. Matern Child Nutr 4 (Suppl 1): 2485.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.16-0098
Loading
/content/journals/10.4269/ajtmh.16-0098
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 08 Feb 2016
  • Accepted : 06 May 2016

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