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.


Journal

The American journal of clinical nutrition
ISSN: 1938-3207
Titre abrégé: Am J Clin Nutr
Pays: United States
ID NLM: 0376027

Informations de publication

Date de publication:
01 10 2019
Historique:
received: 03 12 2018
accepted: 24 06 2019
entrez: 1 10 2019
pubmed: 1 10 2019
medline: 24 3 2020
Statut: ppublish

Résumé

Environmental enteric dysfunction (EED) is thought to increase the risk of micronutrient deficiencies, but few studies adjust for dietary intakes and systemic inflammation. We 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. Using 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. A 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. EED 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.

Sections du résumé

BACKGROUND
Environmental enteric dysfunction (EED) is thought to increase the risk of micronutrient deficiencies, but few studies adjust for dietary intakes and systemic inflammation.
OBJECTIVE
We 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.
METHODS
Using 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.
RESULTS
A 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.
CONCLUSIONS
EED 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.

Identifiants

pubmed: 31565748
pii: S0002-9165(22)01276-X
doi: 10.1093/ajcn/nqz151
pmc: PMC6766446
doi:

Substances chimiques

Biomarkers 0
Micronutrients 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1015-1025

Subventions

Organisme : NICHD NIH HHS
ID : R01 HD066982
Pays : United States

Investigateurs

Angel Mendez Acosta (AM)
Rosa Rios de Burga (RR)
Cesar Banda Chavez (CB)
Julian Torres Flores (JT)
Maribel Paredes Olotegui (MP)
Silvia Rengifo Pinedo (SR)
Mery Siguas Salas (MS)
Dixner Rengifo Trigoso (DR)
Angel Orbe Vasquez (AO)
Imran Ahmed (I)
Didar Alam (D)
Asad Ali (A)
Zulfiqar A Bhutta (ZA)
Shahida Qureshi (S)
Muneera Rasheed (M)
Sajid Soofi (S)
Ali Turab (A)
Anita K M Zaidi (AKM)
Ladaporn Bodhidatta (L)
Carl J Mason (CJ)
Sudhir Babji (S)
Anuradha Bose (A)
Ajila T George (AT)
Dinesh Hariraju (D)
M Steffi Jennifer (MS)
Sushil John (S)
Shiny Kaki (S)
Gagandeep Kang (G)
Priyadarshani Karunakaran (P)
Beena Koshy (B)
Robin P Lazarus (RP)
Jayaprakash Muliyil (J)
Mohan Venkata Raghava (MV)
Sophy Raju (S)
Anup Ramachandran (A)
Rakhi Ramadas (R)
Karthikeyan Ramanujam (K)
Anuradha Bose (A)
Reeba Roshan (R)
Srujan L Sharma (SL)
Shanmuga Sundaram E (S)
Rahul J Thomas (RJ)
William K Pan (WK)
Ramya Ambikapathi (R)
J Daniel Carreon (JD)
Vivek Charu (V)
Viyada Doan (V)
Jhanelle Graham (J)
Christel Hoest (C)
Stacey Knobler (S)
Dennis R Lang (DR)
Benjamin J J McCormick (BJJ)
Monica McGrath (M)
Mark A Miller (MA)
Archana Mohale (A)
Gaurvika Nayyar (G)
Stephanie Psaki (S)
Zeba Rasmussen (Z)
Stephanie A Richard (SA)
Jessica C Seidman (JC)
Vivian Wang (V)
Rebecca Blank (R)
Michael Gottlieb (M)
Karen H Tountas (KH)
Caroline Amour (C)
Eliwaza Bayyo (E)
Estomih R Mduma (ER)
Regisiana Mvungi (R)
Rosemary Nshama (R)
John Pascal (J)
Buliga Mujaga Swema (BM)
Ladislaus Yarrot (L)
Tahmeed Ahmed (T)
A M Shamsir Ahmed (AMS)
Rashidul Haque (R)
Iqbal Hossain (I)
Munirul Islam (M)
Mustafa Mahfuz (M)
Dinesh Mondal (D)
Fahmida Tofail (F)
Ram Krishna Chandyo (RK)
Prakash Sunder Shrestha (PS)
Rita Shrestha (R)
Manjeswori Ulak (M)
Aubrey Bauck (A)
Robert E Black (RE)
Laura E Caulfield (LE)
William Checkley (W)
Margaret N Kosek (MN)
Gwenyth Lee (G)
Kerry Schulze (K)
Pablo Peñataro Yori (PP)
Laura E Murray-Kolb (LE)
A Catharine Ross (AC)
Barbara Schaefer (B)
Suzanne Simons (S)
Laura Pendergast (L)
Cláudia B Abreu (CB)
Hilda Costa (H)
Alessandra Di Moura (AD)
José Quirino Filho (JQ)
Alexandre Havt (A)
Álvaro M Leite (ÁM)
Aldo A M Lima (AAM)
Noélia L Lima (NL)
Ila F Lima (IF)
Bruna L L Maciel (BLL)
Pedro H Q S Medeiros (PHQS)
Milena Moraes (M)
Francisco S Mota (FS)
Reinaldo B Oriá (RB)
Josiane Quetz (J)
Alberto M Soares (AM)
Rosa M S Mota (RMS)
Crystal L Patil (CL)
Pascal Bessong (P)
Cloupas Mahopo (C)
Angelina Maphula (A)
Emanuel Nyathi (E)
Amidou Samie (A)
Leah Barrett (L)
Rebecca Dillingham (R)
Jean Gratz (J)
Richard L Guerrant (RL)
Eric Houpt (E)
William A Petri (WA)
James Platts-Mills (J)
Rebecca Scharf (R)
Binob Shrestha (B)
Sanjaya Kumar Shrestha (SK)
Tor Strand (T)
Erling Svensen (E)

Informations de copyright

Copyright © American Society for Nutrition 2019.

Références

Vaccine. 2019 Jan 7;37(2):352-365
pubmed: 30442479
BMC Gastroenterol. 2010 Jul 06;10:72
pubmed: 20604937
Emerg Themes Epidemiol. 2013 May 17;10(1):4
pubmed: 23683753
Trans R Soc Trop Med Hyg. 2006 Aug;100(8):791-4
pubmed: 16540136
Clin Chem. 1979 Aug;25(8):1487-91
pubmed: 455691
Clin Infect Dis. 2014 Nov 1;59 Suppl 4:S248-54
pubmed: 25305294
EBioMedicine. 2016 Aug;10:25-32
pubmed: 27495791
EBioMedicine. 2017 Apr;18:109-117
pubmed: 28396264
Curr Opin Infect Dis. 2016 Jun;29(3):229-36
pubmed: 26967147
J Pediatr Gastroenterol Nutr. 2017 Jan;64(1):8-14
pubmed: 27632432
Am J Trop Med Hyg. 2018 Mar;98(3):904-912
pubmed: 29380724
Epidemiology. 1999 Jan;10(1):37-48
pubmed: 9888278
Clin Infect Dis. 2014 Nov 1;59 Suppl 4:S220-4
pubmed: 25305290
Eur J Med Res. 1998 Feb 21;3(1-2):65-70
pubmed: 9512970
J Pediatr Gastroenterol Nutr. 1999 Mar;28(3):282-90
pubmed: 10067729
Nat Rev Immunol. 2015 Aug;15(8):500-10
pubmed: 26160612
Lancet. 2013 Aug 3;382(9890):427-451
pubmed: 23746772
Clin Infect Dis. 2014 Nov 1;59 Suppl 4:S207-12
pubmed: 25305288
BMJ Glob Health. 2018 Jul 23;3(4):e000752
pubmed: 30058645
Clin Infect Dis. 2014 Nov 1;59 Suppl 4:S239-47
pubmed: 25305293
Trends Mol Med. 2012 Jun;18(6):328-36
pubmed: 22633998
BMC Clin Pathol. 2011 Apr 21;11:5
pubmed: 21510885
Clin Infect Dis. 2014 Nov 1;59 Suppl 4:S193-206
pubmed: 25305287
Am J Clin Nutr. 2017 Dec;106(Suppl 6):1688S-1693S
pubmed: 29070552
J Nutr. 2014 Jun;144(6):979-87
pubmed: 24744314
BMJ Glob Health. 2017 Dec 28;2(4):e000370
pubmed: 29333282
Pediatr Res. 2010 Jun;67(6):671-5
pubmed: 20496476
Am J Clin Nutr. 2017 Jul;106(Suppl 1):372S-382S
pubmed: 28615256
Br J Nutr. 1993 Jan;69(1):243-55
pubmed: 8457531
PLoS One. 2016 Dec 6;11(12):e0167458
pubmed: 27923057
J Pediatr. 1981 Sep;99(3):416-8
pubmed: 6973619
Lancet Glob Health. 2015 Sep;3(9):e564-75
pubmed: 26202075
Am J Clin Nutr. 2002 May;75(5):789-808
pubmed: 11976152
Am J Clin Nutr. 2017 Jul;106(Suppl 1):333S-347S
pubmed: 28615254
Eur J Clin Nutr. 2004 Nov;58(11):1498-504
pubmed: 15162133
Am J Trop Med Hyg. 2017 Feb 8;96(2):465-472
pubmed: 27994110
Ann Nutr Metab. 2015;66 Suppl 2:22-33
pubmed: 26045325
Gut. 1994 Dec;35(12):1707-11
pubmed: 7829006
Biosci Rep. 1989 Apr;9(2):129-38
pubmed: 2669992
Nutr Rev. 2002 May;60(5 Pt 2):S46-52
pubmed: 12035858
Public Health Nutr. 2014 Aug;17(8):1689-96
pubmed: 23941862
Am J Trop Med Hyg. 2017 Jul;97(1):281-290
pubmed: 28719336
Eur Ann Allergy Clin Immunol. 2007 Jan;39(1):20-2
pubmed: 17375737
Environ Int. 2017 May;102:30-41
pubmed: 27988137
Gut. 2015 May;64(5):731-42
pubmed: 25143342
Pediatr Res. 1987 Sep;22(3):268-70
pubmed: 3498927
Eur J Clin Nutr. 2001 Apr;55(4):252-9
pubmed: 11360129
J Pediatr Gastroenterol Nutr. 2017 Jul;65(1):31-39
pubmed: 28644347

Auteurs

Benjamin J J McCormick (BJJ)

Fogarty International Center, NIH, Bethesda, MD, USA.

Laura E Murray-Kolb (LE)

Department of Nutritional Sciences, The Pennsylvania State University, University Park, PA, USA.

Gwenyth O Lee (GO)

Department of International Health, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.

Kerry J Schulze (KJ)

Department of International Health, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.

A Catharine Ross (AC)

Department of Nutritional Sciences, The Pennsylvania State University, University Park, PA, USA.

Aubrey Bauck (A)

Department of International Health, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.

Aldo A M Lima (AAM)

Universidade Federal do Ceará, INCT-Instituto de Biomedicina do Semiárido Brasileiro, Fortaleza, Brazil.

Bruna L L Maciel (BLL)

Department of Nutrition, Federal University of Rio Grande do Norte, Natal, Rio Negro, Brazil.

Margaret N Kosek (MN)

Department of International Health, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.

Jessica C Seidman (JC)

Fogarty International Center, NIH, Bethesda, MD, USA.

Ramya Ambikapathi (R)

Fogarty International Center, NIH, Bethesda, MD, USA.

Anuradha Bose (A)

Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Sushil John (S)

Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Gagandeep Kang (G)

Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Ali Turab (A)

Centre of Excellence in Women and Child Health, Aga Khan University, Karachi, Pakistan.

Estomih Mduma (E)

Haydom Lutheran Hospital, Haydom, Tanzania.

Pascal Bessong (P)

University of Venda, Thohoyandou, South Africa.

Sanjaya K Shrestra (SK)

Walter Reed, Armed Forces Research Institute of Medical Sciences (AFRIMS) Research Unit, Nepal (WARUN), Kathmandu, Nepal.

Tahmeed Ahmed (T)

Division of Nutrition and Clinical Services, icddr,b, Dhaka, Bangladesh.

Mustafa Mahfuz (M)

Division of Nutrition and Clinical Services, icddr,b, Dhaka, Bangladesh.

Maribel Paredes Olortegui (MP)

AB Prisma, Iquitos, Peru.

Zulfiqar Bhutta (Z)

Centre of Excellence in Women and Child Health, Aga Khan University, Karachi, Pakistan.

Laura E Caulfield (LE)

Department of International Health, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.

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