Multiple micronutrient supplementation transiently ameliorates environmental enteropathy in Malawian children aged 12-35 months in a randomized controlled clinical trial

Journal of Nutrition

Volumn 144, Issue 12, 2014, Pages 2059-2065

  Smith, Hannah E ^a   Ryan, Kelsey N ^a   Stephenson, Kevin B ^a   Westcott, Claire ^a   Thakwalakwa, Chrissie ^b   Maleta, Ken ^b   Cheng, Jacqueline Y ^c   Brenna, J Thomas ^c   Shulman, Robert J ^d   Trehan, Indi ^a,b   Manary, Mark J ^a,b,d  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF MALAWI   (Malawi)

^c Department of Obstetrics Gynecology   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Enteropathy; Environmental enteropathy; Fish oil; Malawi; Micronutrients

Indexed keywords

DOCOSAHEXAENOIC ACID; FISH OIL; ICOSAPENTAENOIC ACID; LACTULOSE; MANNITOL; MINERAL; PLACEBO; TRACE ELEMENT; VITAMIN; RETINOL; UNSATURATED FATTY ACID;

ADOLESCENT; ADULT; ARTICLE; CHILD; CONTROLLED STUDY; COUGHING; DIARRHEA; DIET SUPPLEMENTATION; DIETARY INTAKE; ENTEROPATHY; ENVIRONMENTAL ENTEROPATHY; FEMALE; FEVER; FOLLOW UP; HUMAN; MAJOR CLINICAL STUDY; MALAWIAN; MALE; MORBIDITY; OUTCOME ASSESSMENT; RANDOMIZED CONTROLLED TRIAL; SCHOOL CHILD; URINALYSIS; VOMITING; BLOOD; CALORIC INTAKE; CLINICAL TRIAL; CLUSTER ANALYSIS; DEFICIENCY; DIETARY REFERENCE INTAKE; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; INFANT; INTESTINAL DISEASES; INTESTINE MUCOSA; MALAWI; METABOLISM; MULTICENTER STUDY; NUTRITIONAL ASSESSMENT; PATIENT COMPLIANCE; PRESCHOOL CHILD; URINE;

CHILD, PRESCHOOL; CLUSTER ANALYSIS; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOUBLE-BLIND METHOD; EICOSAPENTAENOIC ACID; ENERGY INTAKE; FATTY ACIDS, UNSATURATED; FEMALE; FISH OILS; FOLLOW-UP STUDIES; HUMANS; INFANT; INTESTINAL DISEASES; INTESTINAL MUCOSA; LACTULOSE; MALAWI; MALE; MANNITOL; MICRONUTRIENTS; NUTRITION ASSESSMENT; PATIENT COMPLIANCE; RECOMMENDED DIETARY ALLOWANCES; VITAMIN A;

EID: 84912051005     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.114.201673     Document Type: Article

References (40)

1. Keusch GT, Rosenberg IH, Denno DM, Duggan C, Guerrant RL, Lavery JV, Tarr PI,Ward HD, Black RE, Nataro JP, et al. Implications of acquired environmental enteric dysfunction for growth and stunting in infants and children living in low-and middle-income countries. Food Nutr Bull 2013;34:357-64.
2. Lindenbaum J, Harmon JW, Gerson CD. Subclinical malabsorption in developing countries. Am J Clin Nutr 1972;25:1056-61.
3. Kelly P, Menzies I, Crane R, Zulu I, Nickols C, Feakins R, Mwamsa K, Mudenda V, Katubulushi M, Greenwald S, et al. Responses of small intestinal architecture and function over time to environmental factors in a tropical population. Am J Trop Med Hyg 2004;70:412-9.
4. Prendergast A, Kelly P. Review: enteropathies in the developing world: neglected effects on global health. Am J Trop Med Hyg 2012;86:756-63.
5. Korpe PS, Petri WA. Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol Med 2012;18:328-36.
6. Weisz AJ, Manary MJ, Stephenson K, Agapova S, Manary FG, Thakwalakwa C, Shulman RJ, Manary MJ. Abnormal gut integrity is associated with reduced linear growth in rural Malawian children. J Pediatr Gastroenterol Nutr 2012;55:747-50.
7. Menzies IS, Zuckerman MJ, Nukajam WS, Somasundaram SG, Murphy B, Jenkins AP, Crane RS, Gregory GG. Geography of intestinal permeability and absorption. Gut 1999;44:483-9.
8. Galpin L, Manary MJ, Fleming K, Ou CN, Ashorn P, Shulman RJ. Effect of Lactobacillus GG on intestinal integrity in Malawian children at risk of tropical enteropathy. Am J Clin Nutr 2005;82:1040-5.
9. Trehan I, Shulman RJ, Ou CN, Maleta K, Manary MJ. A randomized, double-blind, placebo-controlled trial of rifaximin, a nonabsorbable antibiotic, in the treatment of tropical enteropathy. Am J Gastroenterol 2009;104:2326-33.
10. 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. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013;382:427-51.
11. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 2008;371:243-60.
12. Ueno PM, Oria RB, Maier EA, Guedes M, de Azevedo OG, Wu D, Willson T, Hogan SP, Lima AA, Guerrant RL, et al. Alanyl-glutamine promotes intestinal epithelial cell homeostasis in vitro and in a murine model of weanling undernutrition. Am J Physiol Gastrointest Liver Physiol 2011;301:G612-22.
13. Calder PC. Polyunsaturated fatty acids, inflammation, and immunity. Lipids 2001;36:1007-24.
14. Kremer JM, Lawrence DA, Petrillo GF, Litts LL, Mullaly PM, Rynes RI, Stocker RP, Parhami N, Greenstein NS, Fuchs BR, et al. Effects of highdose fish oil on rheumatoid arthritis after stopping nonsteroidal antiinflammatory drugs. Clinical and immune correlates. Arthritis Rheum 1995;38:1107-14.
15. Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Miglioli M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 1996;334:1557-60.
16. Romano C, Cucchiara S, Barabino A, Annese V, Sferlazzas C. Usefulness of omega-3 fatty acid supplementation in addition to mesalazine in maintaining remission in pediatric Crohn's disease: a double-blind, randomized, placebo controlled study. World J Gastroenterol 2005;11: 7118-21.
17. Lev-Tzion R, Griffiths AM, Leder O, Turner D. Omega 3 fatty acids (fish oil) for maintenance of remission in Crohn's disease. Cochrane Database Syst Rev 2014; (2):CD006320 10.1002/14651858.CD006320.
18. McOmber ME, Ou CN, Shulman RJ. Effects of timing, sex, and age on site-specific gastrointestinal permeability testing in children and adults. J Pediatr Gastroenterol Nutr 2010;50:269-75.
19. Lunn PG, Northrop-Clewes CA, Downes RM. Intestinal permeability, mucosal injury and growth faltering in Gambian infants. Lancet 1991; 338:907-10.
20. Manary MJ, Sandige HL. Management of acute moderate and severe childhood malnutrition. BMJ 2008;337:1227-30.
21. Coates J, Swindale A, Bilinsky P. Household Food Insecurity Access Scale (HFIAS) for measurement of food access: indicator guide. Washington, DC: U.S. Agency for International Development, Food and Nutrition Technical Assistance; 2007
22. WHOWorld Health Organization (WHO),Food and Agricultural Organization. Vitamin and mineral requirements in human nutrition. Geneva: WHO; 2004.
23. World Health Organization (WHO). Trace elements in human nutrition and health. Geneva: WHO; 1996.
24. Thakwalakwa CM, Kuusipalo HM, Maleta KM, Phuka JC, Ashorn P, Cheung YB. The validity of a structured interactive 24-hour recall in estimating energy and nutrient intakes in 15-month-old rural Malawian children. Matern Child Nutr 2012;8:380-9.
25. Gibson RS, Ferguson EL. An interactive 24-hour recall for assessing the adequacy of iron and zinc intakes in developing countries [HarvestPlus Technical Monograph 8]. Washington, DC: International Food Policy Research Institute; 2008.
26. 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 2014;12:1507-13.
27. Shulman RJ, Schanler RJ, Lau C, Heitkemper M, Ou CN, Smith EO. Early feeding, antenatal glucocorticoids, and human milk decrease intestinal permeability in preterm infants. Pediatr Res 1998;44: 519-23.
28. Sheaff RC, Su HM, Keswick LA, Brenna JT. Conversion of alphalinolenate to docosahexaenoate is not depressed by high dietary levels of linoleate in young rats: tracer evidence using high precision mass spectrometry. J Lipid Res 1995;36:998-1008.
29. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911-7.
30. Turpeinen AM, Barlund S, Freese R, Lawrence P, Brenna JT. Effects of conjugated linoleic acid on linoleic and linolenic acid metabolism in man. Br J Nutr 2006;95:727-33.
31. Tumwine J, Thompson J, Katui-Katua M, Mujwahuzi M, Johnstone N, Porras I. Sanitation and hygiene in urban and rural households in East Africa. Int J Environ Health Res 2003;13:107-15.
32. Humphrey JH. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 2009;374:1032-5.
33. Hoffman D, Ziegler E, Mitmesser SH, Harris CL, Diersen-Schade DA. Soy-based infant formula supplemented with DHA and ARA supports growth and increases circulating levels of these fatty acids in infants. Lipids 2008;43:29-35.
34. Hoffman DR, Wheaton DKH, James KJ, Tuazon M, Diersen-Schade DA, Harris CL, Stolz S, Berseth CL. Docosahexaenoic acid in red blood cells of term infants receiving two levels of long-chain polyunsaturated fatty acids. J Pediatr Gastroenterol Nutr 2006;42:287-92.
35. Harris WS, Pottala JV, Varvel SA, Borowski JJ, Ward JN, McConnell JP. Erythrocyte omega-3 fatty acids increase and linoleic acid decreases with age: observations from 160,000 patients. Prostaglandins Leukot Essent Fatty Acids 2013;88:257-63.
36. Manno D, Kowa PK, Bwalya HK, Siame J, Grantham-McGregor S, Baisley K, De Stavola BL, Jaffar S, Filteau S. Rich micronutrient fortification of locally produced infant food does not improve mental and motor development of Zambian infants: a randomised controlled trial. Br J Nutr 2012;107:556-66.
37. Soofi S, Cousens S, Iqbal SP, Akhund T, Khan J, Ahmed I, Zaidi AKM, Bhutta ZA. Effect of provision of daily zinc and iron with several micronutrients on growth and morbidity among young children in Pakistan: a cluster-randomised trial. Lancet 2013;382:29-40.
38. Bhandari N, Bahl R, Taneja S. Effect of micronutrient supplementation on linear growth of children. Br J Nutr 2001;85:(Suppl 2): S131-7.
39. Louis-Auguste J, Greenwald S, Simuyandi M, Soko R, Banda R, Kelly P. High dose multiple micronutrient supplementation improves villous morphology in environmental enteropathy without HIV enteropathy: results from a double-blind randomised placebo controlled trial in Zambian adults. BMC Gastroenterol 2014;14:15.
40. van der Merwe LF, Moore SE, Fulford AJ, Halliday KE, Drammeh S, Young S, Prentice AM. Long-chain PUFA supplementation in rural African infants: a randomized controlled trial of effects on gut integrity, growth and cognitive development. Am J Clin Nutr 2013;97: 45-57.