Intestinal permeability and inflammation mediate the association between nutrient density of complementary foods and biochemical measures of micronutrient status in young children: results from the MAL-ED study
Author:
McCormick Benjamin J J1ORCID, Murray-Kolb Laura E2ORCID, Lee Gwenyth O3ORCID, Schulze Kerry J3ORCID, Ross A Catharine2ORCID, Bauck Aubrey3ORCID, Lima Aldo A M4, Maciel Bruna L L5ORCID, Kosek Margaret N3, Seidman Jessica C1, Ambikapathi Ramya1, Bose Anuradha6, John Sushil6, Kang Gagandeep6ORCID, Turab Ali7, Mduma Estomih8ORCID, Bessong Pascal9, Shrestra Sanjaya K10, Ahmed Tahmeed11ORCID, Mahfuz Mustafa11ORCID, Olortegui Maribel Paredes12, Bhutta Zulfiqar7, Caulfield Laura E3ORCID, Acosta Angel Mendez12, Burga Rosa Rios de12, Chavez Cesar Banda12, Flores Julian Torres12, Olotegui Maribel Paredes12, Pinedo Silvia Rengifo12, Salas Mery Siguas12, Trigoso Dixner Rengifo12, Vasquez Angel Orbe12, Ahmed Imran13, Alam Didar13, Ali Asad13, Bhutta Zulfiqar A13, Qureshi Shahida13, Rasheed Muneera13, Soofi Sajid13, Turab Ali13, Zaidi Anita K M13, Bodhidatta Ladaporn14, Mason Carl J14, Babji Sudhir15, Bose Anuradha15, George Ajila T15, Hariraju Dinesh15, Jennifer M Steffi15, John Sushil15, Kaki Shiny15, Kang Gagandeep15, Karunakaran Priyadarshani15, Koshy Beena15, Lazarus Robin P15, Muliyil Jayaprakash15, Raghava Mohan Venkata15, Raju Sophy15, Ramachandran Anup15, Ramadas Rakhi15, Ramanujam Karthikeyan15, Bose Anuradha15, Roshan Reeba15, Sharma Srujan L15, Sundaram E Shanmuga15, Thomas Rahul J15, Pan William K116, Ambikapathi Ramya1, Carreon J Daniel1, Charu Vivek1, Doan Viyada1, Graham Jhanelle1, Hoest Christel1, Knobler Stacey1, Lang Dennis R117, McCormick Benjamin J J1, McGrath Monica1, Miller Mark A1, Mohale Archana1, Nayyar Gaurvika1, Psaki Stephanie1, Rasmussen Zeba1, Richard Stephanie A1, Seidman Jessica C1, Wang Vivian1, Blank Rebecca17, Gottlieb Michael17, Tountas Karen H17, Amour Caroline8, Bayyo Eliwaza8, Mduma Estomih R8, Mvungi Regisiana8, Nshama Rosemary8, Pascal John8, Swema Buliga Mujaga8, Yarrot Ladislaus8, Ahmed Tahmeed18, Ahmed A M Shamsir18, Haque Rashidul18, Hossain Iqbal18, Islam Munirul18, Mahfuz Mustafa18, Mondal Dinesh18, Tofail Fahmida18, Chandyo Ram Krishna19, Shrestha Prakash Sunder19, Shrestha Rita19, Ulak Manjeswori19, Bauck Aubrey20, Black Robert E20, Caulfield Laura E20, Checkley William120, Kosek Margaret N20, Lee Gwenyth20, Schulze Kerry20, Yori Pablo Peñataro20, Murray-Kolb Laura E21, Ross A Catharine21, Schaefer Barbara121, Simons Suzanne21, Pendergast Laura22, Abreu Cláudia B23, Costa Hilda23, Moura Alessandra Di23, Filho José Quirino123, Havt Alexandre23, Leite Álvaro M23, Lima Aldo A M23, Lima Noélia L23, Lima Ila F23, Maciel Bruna L L23, Medeiros Pedro H Q S23, Moraes Milena23, Mota Francisco S23, Oriá Reinaldo B23, Quetz Josiane23, Soares Alberto M23, Mota Rosa M S23, Patil Crystal L24, Bessong Pascal9, Mahopo Cloupas9, Maphula Angelina9, Nyathi Emanuel9, Samie Amidou9, Barrett Leah25, Dillingham Rebecca25, Gratz Jean25, Guerrant Richard L25, Houpt Eric25, Petri William A25, Platts-Mills James25, Scharf Rebecca25, Shrestha Binob26, Shrestha Sanjaya Kumar26, Strand Tor27, Svensen Erling828,
Affiliation:
1. Fogarty International Center, NIH, Bethesda, MD, USA 2. Department of Nutritional Sciences, The Pennsylvania State University, University Park, PA, USA 3. Department of International Health, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA 4. Universidade Federal do Ceará, INCT—Instituto de Biomedicina do Semiárido Brasileiro, Fortaleza, Brazil 5. Department of Nutrition, Federal University of Rio Grande do Norte, Natal, Rio Negro, Brazil 6. Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India 7. Centre of Excellence in Women and Child Health, Aga Khan University, Karachi, Pakistan 8. Haydom Lutheran Hospital, Haydom, Tanzania 9. University of Venda, Thohoyandou, South Africa 10. Walter Reed, Armed Forces Research Institute of Medical Sciences (AFRIMS) Research Unit, Nepal (WARUN), Kathmandu, Nepal 11. Division of Nutrition and Clinical Services, icddr,b, Dhaka, Bangladesh 12. AB Prisma, Iquitos, Peru 13. Aga Khan University, Karachi, Pakistan 14. Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand 15. Christian Medical College, Vellore, India 16. Duke University, Durham, NC, USA 17. Foundation for the NIH, Bethesda, MD, USA 18. icddr, b, Dhaka, Bangladesh 19. Institute of Medicine, Tribhuvan University, Kathmandu, Nepal 20. Johns Hopkins University, Baltimore, MD, USA 21. The Pennsylvania State University, University Park, PA, USA 22. Temple University, Philadelphia, PA, USA 23. Universidade Federal do Ceara, Fortaleza, Brazil 24. University of Illinois, Chicago, IL, USA 25. University of Virginia, Charlottesville, VA, USA 26. Walter Reed/AFRIMS Research Unit, Kathmandu, Nepal 27. University of Bergen, Norway 28. Haukeland University Hospital, Bergen, Norway
Abstract
ABSTRACTBackgroundEnvironmental enteric dysfunction (EED) is thought to increase the risk of micronutrient deficiencies, but few studies adjust for dietary intakes and systemic inflammation.ObjectiveWe tested whether EED is associated with micronutrient deficiency risk independent of diet and systemic inflammation, and whether it mediates the relation between intake and micronutrient status.MethodsUsing data from 1283 children in the MAL-ED (Etiology, Risk Factors, and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health) birth cohort we evaluated the risk of anemia, low retinol, zinc, and ferritin, and high transferrin receptor (TfR) at 15 mo. We characterized gut inflammation and permeability by myeloperoxidase (MPO), neopterin (NEO), and α-1-antitrypsin (AAT) concentrations from asymptomatic fecal samples averaged from 9 to 15 mo, and averaged the lactulose:mannitol ratio z-score (LMZ) at 9 and 15 mo. Nutrient intakes from complementary foods were quantified monthly from 9 to 15 mo and densities were averaged for analyses. α-1-Acid glycoprotein at 15 mo characterized systemic inflammation. Relations between variables were modeled using a Bayesian network.ResultsA greater risk of anemia was associated with LMZ [1.15 (95% CI: 1.01, 1.31)] and MPO [1.16 (1.01, 1.34)]. A greater risk of low ferritin was associated with AAT [1.19 (1.03, 1.37)] and NEO [1.22 (1.04, 1.44)]. A greater risk of low retinol was associated with LMZ [1.24 (1.08, 1.45)]. However, MPO was associated with a lower risk of high transferrin receptor [0.86 (0.74, 0.98)], NEO with a lower risk of low retinol [0.75 (0.62, 0.89)], and AAT with a lower risk of low plasma zinc [0.83 (0.70, 0.99)]. Greater nutrient intake densities (vitamins A and B6, calcium, protein, and zinc) were negatively associated with EED. Inverse associations between nutrient densities and micronutrient deficiency largely disappeared after adjustment for EED, suggesting that EED mediates these associations.ConclusionsEED is independently associated with an increased risk of low ferritin, low retinol, and anemia. Greater nutrient density from complementary foods may reduce EED, and the control of micronutrient deficiencies may require control of EED.
Funder
Christian Medical College, Vellore Duke University Fogarty International Center National Institutes of Health Foundation for the NIH Johns Hopkins University Pennsylvania State University Temple University University of Illinois University of Venda University of Virginia University of Bergen Haukeland University Hospital
Publisher
Oxford University Press (OUP)
Subject
Nutrition and Dietetics,Medicine (miscellaneous)
Cited by
28 articles.
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