Maternal-Child Microbiome and Impact on Growth and Neurodevelopment in Infants and Children: A Scoping Review

Abstract

Background

Pathologic changes in the microbiome (dysbiosis) have been implicated in affecting the growth and neurodevelopment of infants and children. There is evidence to suggest that prenatal and postnatal stressors may be a factor in dysbiosis and there is also a growing body of evidence to suggest that interventions may reduce this negative impact. A scoping review was undertaken to identify association between maternal and/or child microbiome with child growth and neurodevelopment. Additionally, intervention studies such as use of nutritional supplementation and its impact on the microbiome, growth and neurodevelopment were reviewed.

Methods

An exhaustive literature search identified 654 relevant citations. After review of abstracts, 557 were eliminated, and 97 remained for full text review. We identified and reported on 42 articles which met inclusion criteria.

Results

Seven studies examined associations between microbiome and neurodevelopment and 36 studies evaluated anthropometric measurements, most commonly weight, and microbiota relationships. One study evaluated both growth and neurodevelopment and microbiota. Fourteen studies evaluated supplemental nutrients. Preterm, low birth weight (LBW), and very low birth weight (VLBW) infants were most studied. Findings were inconclusive for consistent associations between microbiota and growth and neurodevelopment. Further, there were no consistent conclusive changes with prescribed treatment interventions.

Discussion

There is a need for high-quality longitudinal studies evaluating repeated developmental assessment measures using consistent microbial analysis techniques to inform conclusions regarding the association between microbiome and infant and child growth and neurodevelopment. Additional intervention studies that may mitigate dysbiosis are warranted.

Keywords

microbiome anthropometric changes maternal-child neurodevelopment

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References

Aatsinki

A.-K.

Kataja

E.-L.

Munukka

Lahti

Keskitalo

Korja

Nolvi

Häikiö

Tarro

Karlsson

(2020). Infant fecal microbiota composition and attention to emotional faces. Emotion, https://doi.org/10.1037/emo0000924.

Aatsinki

A.-K.

Lahti

Uusitupa

H.-M.

Munukka

Keskitalo

Nolvi

O’Mahony

Pietilä

Elo

L. L.

Eerola

Karlsson

(2019). Gut microbiota composition is associated with temperament traits in infants. Brain, Behavior, and Immunity, 80(Aug), 849–858. https://doi.org/10.1016/j.bbi.2019.05.035.

Alderete

T. L.

Jones

R. B.

Shaffer

J. P.

Holzhausen

E. A.

Patterson

W. B.

Kazemian

Chatzi

Knight

Plows

J. F.

Berger

P. K.

Goran

M. I.

(2021). Early life gut microbiota is associated with rapid infant growth in Hispanics from Southern California. Gut Microbes, 13(1), 1961203. https://doi.org/10.1080/19490976.2021.1961203

Aly

Said

R. N.

Wali

I. E.

Elwakkad

Soliman

Awad

A. R.

Shawky

M. A.

Alam

M. S. A.

Mohamed

M. A.

(2017). Medically graded honey supplementation formula to preterm infants as a prebiotic: A randomized controlled trial. Journal of Pediatric Gastroenterology and Nutrition, 64(6), 966–970. https://doi.org/10.1097/mpg.0000000000001597

Baldassarre

M. E.

Di Mauro

Tafuri

Rizzo

Gallone

M. S.

Mastromarino

Capobianco

Laghi

Zhu

Capozza

Laforgia

(2018). Effectiveness and safety of a probiotic-mixture for the treatment of infantile colic: A double-blind, randomized, placebo-controlled clinical trial with fecal real-time PCR and NMR-based metabolomics analysis. Nutrients, 10(2), 195. https://doi.org/10.3390/nu10020195

Baqui

A. H.

Lee

A. C.

Koffi

A. K.

Khanam

Mitra

D. K.

Dasgupta

S. K.

Uddin

Ahmed

Rafiqullah

Rahman

Quaiyum

Koumans

E. H.

Christian

Saha

S. K.

Mullany

L. C.

Labrique

the MIST Study Team of the Projahnmo Study Group in Bangladesh (2019). Prevalence of and risk factors for abnormal vaginal flora and its association with adverse pregnancy outcomes in a rural district in North-East Bangladesh. Acta Obstetricia et Gynecologica Scandinavica, 98(3), 309–319. https://doi.org/10.1111/aogs.13492

Bhattarai

Muniz Pedrogo

D. A.

Kashyap

P. C.

(2017). Irritable bowel syndrome: A gut microbiota-related disorder? American Journal of Physiology-Gastrointestinal and Liver Physiology, 312(1), G52–G62. https://doi.org/10.1152/ajpgi.00338.2016

Bierut

Duckworth

Grabowsky

Ordiz

M. I.

Laury

M. L.

Callaghan-Gillespie

Maleta

Manary

M. J.

(2021). The effect of bovine colostrum/egg supplementation compared with corn/soy flour in young Malawian children: A randomized, controlled clinical trial. The American Journal of Clinical Nutrition, 113(2), 420–427. https://doi.org/10.1093/ajcn/nqaa325

Bisanz

J. E.

Enos

M. K.

PrayGod

Seney

Macklaim

J. M.

Chilton

Willner

Knight

Fusch

Gloor

G. B.

Burton

J. P.

Reid

(2015). Microbiota at multiple body sites during pregnancy in a rural Tanzanian population and effects of Moringa-supplemented probiotic yogurt. Applied and Environmental Microbiology, 81(15), 4965–4975. https://doi.org/10.1128/aem.00780-15

10.

Blakstad

E. W.

Korpela

Lee

Nakstad

Moltu

S. J.

Strømmen

Rønnestad

A. E.

Brække

Iversen

P. O.

de Vos

W. M.

Drevon

C. A.

(2019). Enhanced nutrient supply and intestinal microbiota development in very low birth weight infants. Pediatric Research, 86(3), 323–332. https://doi.org/10.1038/s41390-019-0412-x

11.

Carney

M. C.

Zhan

Rangnekar

Chroneos

M. Z.

Craig

S. J.

Makova

K. D.

Paul

I. M.

Hicks

S. D.

(2021). Associations between stool micro-transcriptome, gut microbiota, and infant growth. Journal of Developmental Origins of Health and Disease, 12(6), 876–882. https://doi.org/10.1017/s2040174420001324

12.

Codagnone

M. G.

Stanton

O’Mahony

S. M.

Dinan

T. G.

Cryan

J. F.

(2019). Microbiota and neurodevelopmental trajectories: Role of maternal and early-life nutrition. Annals of Nutrition & Metabolism, 74(2), 16–27. https://doi.org/10.1159/000499144

13.

Cryan

J. F.

Dinan

T. G.

(2012). Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience, 13(10), 701–712. https://doi.org/10.1038/nrn3346

14.

Daudt

H. M.

van Mossel

Scott

S. J.

(2013). Enhancing the scoping study methodology: A large, inter-professional team’s experience with Arksey and O’Malley’s framework. BMC Medical Research Methodology, 13(1), 1–9. https://doi.org/10.1186/1471-2288-13-48

15.

Dinh

D. M.

Ramadass

Kattula

Sarkar

Braunstein

Tai

Wanke

C. A.

Hassoun

Kane

A. V.

Naumova

E. N.

Kang

Ward

H. D.

(2016). Longitudinal analysis of the intestinal microbiota in persistently stunted young children in South India. Plos One, 11(5), Article e0155405. https://doi.org/10.1371/journal.pone.0155405

16.

Doyle

R. M.

Harris

Kamiza

Harjunmaa

Ashorn

Nkhoma

Dewey

K. G.

Maleta

Ashorn

Klein

(2017). Bacterial communities found in placental tissues are associated with severe chorioamnionitis and adverse birth outcomes. Plos One, 12(7), Article e0180167. https://doi.org/10.1371/journal.pone.0180167

17.

Hayden

H. S.

Eng

Pope

C. E.

Brittnacher

M. J.

A. T.

Weiss

E. J.

Hager

K. R.

Martin

B. D.

Leung

D. H.

Heltshe

S. L.

Borenstein

Miller

S. I.

Hoffman

L. R.

(2020). Fecal dysbiosis in infants with cystic fibrosis is associated with early linear growth failure. Nature Medicine, 26(2), 215–221. https://doi.org/10.1038/s41591-019-0714-x

18.

Heida

F. H.

Kooi

E. M.

Wagner

Nguyen

T.-Y.

Hulscher

J. B.

van Zoonen

A. G.

Bos

A. F.

Harmsen

H. J.

de Goffau

M. C.

(2021). Weight shapes the intestinal microbiome in preterm infants: Results of a prospective observational study. BMC Microbiology, 21(1), 1–12. https://doi.org/10.1186/s12866-021-02279-y

19.

T. T.

Groer

M. W.

Kane

Yee

A. L.

Torres

B. A.

Gilbert

J. A.

Maheshwari

(2019). Enteric dysbiosis and fecal calprotectin expression in premature infants. Pediatric Research, 85(3), 361–368. https://doi.org/10.1038/s41390-018-0254-y

20.

Benny

Wang

Lambertini

Peter

Lee

M.-J.

(2021). Intrauterine growth restriction is associated with unique features of the reproductive microbiome. Reproductive Sciences, 28(3), 828–837. https://doi.org/10.1007/s43032-020-00374-5

21.

Huet

Abrahamse-Berkeveld

Tims

Simeoni

Beley

Savagner

Vandenplas

Hourihane

J. O. B.

(2016). Partly fermented infant formulae with specific oligosaccharides support adequate infant growth and are well-tolerated. Journal of Pediatric Gastroenterology and Nutrition, 63(4), e43-e53. https://doi.org/10.1097/mpg.0000000000001360

22.

Jacquot

Neveu

Aujoulat

Mercier

Marchandin

Jumas-Bilak

Picaud

J.-C.

(2011). Dynamics and clinical evolution of bacterial gut microflora in extremely premature patients. The Journal of Pediatrics, 158(3), 390–396. https://doi.org/10.1016/j.jpeds.2010.09.007

23.

Jiang

N. M.

Cowan

Moonah

S. N.

Petri

W. A.

Jr (2018). The impact of systemic inflammation on neurodevelopment. Trends in Molecular Medicine, 24(9), 794–804. https://doi.org/10.1016/j.molmed.2018.06.008

24.

Kapiki

Costalos

Oikonomidou

Triantafyllidou

Loukatou

Pertrohilou

(2007). The effect of a fructo-oligosaccharide supplemented formula on gut flora of preterm infants. Early Human Development, 83(5), 335–339. https://doi.org/10.1016/j.earlhumdev.2006.07.003

25.

Kim

C. S.

Grady

Derrick

Oliphant

Claud

E. C.

(2021). Effect of antibiotic use within first 48 hours of life on the preterm infant microbiome: A randomized clinical trial. JAMA Pediatrics, 175(3), 303–305. https://doi.org/10.1001/jamapediatrics.2020.4916

26.

Laforest-Lapointe

Becker

A. B.

Mandhane

P. J.

Turvey

S. E.

Moraes

T. J.

Sears

M. R.

Subbarao

Sycuro

L. K.

Azad

M. B.

Arrieta

M.-C.

(2021). Maternal consumption of artificially sweetened beverages during pregnancy is associated with infant gut microbiota and metabolic modifications and increased infant body mass index. Gut Microbes, 13(1), 1857513–1857515. https://doi.org/10.1080/19490976.2020.1857513

27.

Laue

H. E.

Coker

M. O.

Madan

J. C.

(2022). The developing microbiome from birth to 3 years: The gut-brain axis and neurodevelopmental outcomes. Frontiers in Pediatrics, 10(Mar 7), 815885. https://doi.org/10.3389/fped.2022.815885.

28.

Lei

W.-T.

Huang

K.-Y.

Jhong

J.-H.

Chen

C.-H.

Weng

S.-L.

(2021). Metagenomic analysis of the gut microbiome composition associated with vitamin D supplementation in Taiwanese infants. Scientific Reports, 11(1), 1–15. https://doi.org/10.1038/s41598-021-82584-8

29.

Gao

Zhou

Xiao

Huang

(2019). Characteristics of the intestinal microbiota in very low birth weight infants with extrauterine growth restriction. Frontiers in Pediatrics, 7(March), 99. https://doi.org/10.3389/fped.2019.00099.

30.

Zhao

Wang

Chen

Tao

Tian

Liu

Cui

Geng

Zhang

Weldon

Auguste

Yang

Liu

Chen

Yang

Zhu

Cai

(2017). Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome, 5(1), 1–19. https://doi.org/10.1186/s40168-016-0222-x

31.

Jia

Lin

Fan

Huang

Wang

Liu

(2021). The diversity of the intestinal flora disturbed after feeding intolerance recovery in preterm twins. Frontiers in Pediatrics, 9(March 10), 648979. https://doi.org/10.3389/fped.2021.648979.

32.

Claud

E. C.

(2019). Connection between gut microbiome and brain development in preterm infants. Developmental Psychobiology, 61(5), 739–751. https://doi.org/10.1002/dev.21806

33.

Cluette-Brown

Martin

C. R.

Claud

E. C.

(2018). Effects of intestinal microbiota on brain development in humanized gnotobiotic mice. Scientific Reports, 8(1), 1–16. https://doi.org/10.1038/s41598-018-23692-w

34.

Lu-Culligan

Iwasaki

(2020). The role of immune factors in shaping fetal neurodevelopment. Annual Review of Cell and Developmental Biology, 36(1), 441–468. https://doi.org/10.1146/annurev-cellbio-021120-033518

35.

Mandal

Van Treuren

White

R. A.

Eggesbø

Knight

Peddada

S. D.

(2015). Analysis of composition of microbiomes: A novel method for studying microbial composition. Microbial Ecology in Health and Disease, 26(1), 27663. https://doi.org/10.3402/mehd.v26.27663

36.

Mirzaei

M. K.

Khan

M. A. A.

Ghosh

Taranu

Z. E.

Taguer

Chowdhury

Kabir

M. M.

Deng

Mondal

Maurice

C. F.

(2020). Bacteriophages isolated from stunted children can regulate gut bacterial communities in an age-specific manner. Cell Host & Microbe, 27(2), 199–212.e195. https://doi.org/10.1016/j.chom.2020.01.004

37.

Morais

L. H.

Schreiber

H. L.

Mazmanian

S. K.

(2021). The gut microbiota–brain axis in behaviour and brain disorders. Nature Reviews Microbiology, 19(4), 241–255. https://doi.org/10.1038/s41579-020-00460-0

38.

Neumer

Urraca

Alonso

Palencia

Varea

Theis

Rodriguez-Palmero

Moreno-Muñoz

J. A.

Guarner

Veereman

Vandenplas

Campoy

(2021). Long-term safety and efficacy of prebiotic enriched infant formula—a randomized controlled trial. Nutrients, 13(4), 1276. https://doi.org/10.3390/nu13041276

39.

Nguyen

Holdbrooks

Mishra

Abrantes

M. A.

Eskew

Garma

Oca

C.-G.

McGuckin

Hein

C. B.

Mitchell

R. D.

Kazi

Chew

Casaburi

Brown

H. K.

Frese

S. A.

Henrick

B. M.

(2021). Impact of probiotic B. infantis EVC001 feeding in premature infants on the gut microbiome, nosocomially acquired antibiotic resistance, and enteric inflammation. Frontiers in Pediatrics, 24(Feb 16), 618009. https://doi.org/10.3389/fped.2021.618009.

40.

Önning

Palm

Linninge

Larsson

(2021). New Lactiplantibacillus plantarum and Lacticaseibacillus rhamnosus strains: Well tolerated and improve infant microbiota. Pediatric Research, 91(7), 1–9. https://doi.org/10.1038/s41390-021-01678-1

41.

Ordiz

M. I.

Janssen

Humphrey

Ackermann

Stephenson

Agapova

Divala

Kaimila

Maleta

Zhong

Knight

Trehan

Tarr

P. I.

Rusconi

Manary

M. J.

(2020). The effect of legume supplementation on the gut microbiota in rural Malawian infants aged 6 to 12 months. American Journal of Clinical Nutrition, 111(4), 884–892. https://doi.org/10.1093/ajcn/nqaa011

42.

Peters

M. D.

Marnie

Tricco

A. C.

Pollock

Munn

Alexander

McInerney

Godfrey

C. M.

Khalil

(2020). Updated methodological guidance for the conduct of scoping reviews. JBI Evidence Synthesis, 18(10), 2119–2126. https://doi.org/10.11124/jbies-20-00167

43.

Pfister

K. M.

Ramel

S. E.

(2014). Linear growth and neurodevelopmental outcomes. Clinics in Perinatology, 41(2), 309–321. https://doi.org/10.1016/j.clp.2014.02.004

44.

Piper

H. G.

Fan

Coughlin

L. A.

E. X.

McDaniel

M. M.

Channabasappa

Kim

Zhan

Xie

Koh

A. Y.

(2017). Severe gut microbiota dysbiosis is associated with poor growth in patients with short bowel syndrome. JPEN. Journal of Parenteral and Enteral Nutrition, 41(7), 1202–1212. https://doi.org/10.1177/0148607116658762

45.

Pronovost

G. N.

Hsiao

E. Y.

(2019). Perinatal interactions between the microbiome, immunity, and neurodevelopment. Immunity, 50(1), 18–36. https://doi.org/10.1016/j.immuni.2018.11.016

46.

Radke

Picaud

J.-C.

Loui

Cambonie

Faas

Lafeber

H. N.

de Groot

Pecquet

S. S.

Steenhout

P. G.

Hascoet

J.-M.

(2017). Starter formula enriched in prebiotics and probiotics ensures normal growth of infants and promotes gut health: A randomized clinical trial. Pediatrics Research, 81(4), 622–631. https://doi.org/10.1038/pr.2016.270

47.

Rhee

S. H.

Pothoulakis

Mayer

E. A.

(2009). Principles and clinical implications of the brain–gut–enteric microbiota axis. Nature Reviews Gastroenterology & Hepatology, 6(5), 306–314. https://doi.org/10.1038/nrgastro.2009.35

48.

Rhoades

N. S.

Cinco

I. R.

Hendrickson

S. M.

Slifka

M. K.

Messaoudi

(2022). Taxonomic and functional shifts in the perinatal gut microbiome of rhesus macaques. bioRxiv.

49.

Sanctuary

M. R.

Kain

J. N.

Chen

S. Y.

Kalanetra

Lemay

D. G.

Rose

D. R.

Yang

H. T.

Tancredi

D. J.

German

J. B.

Slupsky

C. M.

Ashwood

Mills

D. A.

Smilowitz

J. T.

Angkustsiri

(2019). Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms. Plos One, 14(1), Article e0210064. https://doi.org/10.1371/journal.pone.0210064

50.

Segata

Izard

Waldron

Gevers

Miropolsky

Garrett

W. S.

Huttenhower

(2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12(6), 1–18. https://doi.org/10.1186/gb-2011-12-6-r60

51.

Sordillo

J. E.

Korrick

Laranjo

Carey

Weinstock

G. M.

Gold

D. R.

O’Connor

Sandel

Bacharier

L. B.

Beigelman

Zeiger

Litonjua

A. A.

Weiss

S. T.

(2019). Association of the infant gut microbiome with early childhood neurodevelopmental outcomes: An ancillary study to the VDAART randomized clinical trial. JAMA Network Open, 2(3), Article e190905. https://doi.org/10.1001/jamanetworkopen.2019.0905

52.

Spies

Geyer

Raab

Brandt

Meyer

Günther

Hoffmann

Hauner

(2022). Child anthropometrics and neurodevelopment at 2 and 3 years of age following an antenatal lifestyle intervention in routine care—a secondary analysis from the cluster-randomised gelis trial. Journal of Clinical Medicine, 11(6), 1688. https://doi.org/10.3390/jcm11061688

53.

Streit

Prandovszky

Send

Zillich

Frank

Sabunciyan

Foo

Sirignano

Lange

Bardtke

Hatfield

Witt

S. H.

Gilles

Rietschel

Deuschle

Yolken

(2021). Microbiome profiles are associated with cognitive functioning in 45-month-old children. Brain, Behavior, and Immunity, 98(Nov), 151–160. https://doi.org/10.1016/j.bbi.2021.08.001.

54.

Swift

Cresswell

Johnson

Stilianoudakis

Wei

(2022). A review of normalization and differential abundance methods for microbiome counts data. Wiley Interdisciplinary Reviews: Computational Statistics, e1586. https://doi.org/10.1002/wics.1586

55.

Tamana

S. K.

Tun

H. M.

Konya

Chari

R. S.

Field

C. J.

Guttman

D. S.

Becker

A. B.

Moraes

T. J.

Turvey

S. E.

Subbarao

Sears

M. R.

Pei

Scott

J. A.

Mandhane

P. J.

Kozyrskyj

A. L.

(2021). Bacteroides-dominant gut microbiome of late infancy is associated with enhanced neurodevelopment. Gut Microbes, 13(1), 1930875. https://doi.org/10.1080/19490976.2021.1930875

56.

Terrazzan Nutricionist

A. C.

Procianoy

R. S.

Roesch

L. F. W.

Corso

A. L.

Dobbler

P. T.

Silveira

R. C.

(2020). Meconium microbiome and its relation to neonatal growth and head circumference catch-up in preterm infants. Plos One, 15(9), Article e0238632. https://doi.org/10.1371/journal.pone.0238632

57.

Underwood

M. A.

Salzman

N. H.

Bennett

S. H.

Barman

Mills

Marcobal

Tancredi

D. J.

Bevins

C. L.

Sherman

M. P.

(2009). A randomized placebo-controlled comparison of two prebiotic/probiotic combinations in preterm infants: Impact on weight gain, intestinal microbiota, and fecal short chain fatty acids. Journal of Pediatric Gastroenterology and Nutrition, 48(2), 216–225. https://doi.org/10.1097/mpg.0b013e31818de195

58.

Ursell

L. K.

Metcalf

J. L.

Parfrey

L. W.

Knight

(2012). Defining the human microbiome. Nutrition Reviews, 70(suppl_1), S38–S44. https://doi.org/10.1111/j.1753-4887.2012.00493.x

59.

Uzan-Yulzari

Turta

Belogolovski

Ziv

Kunz

Perschbacher

Neuman

Pasolli

Ben-Amram

Kumar

Ollila

Kaljonen

Isolauri

Salminen

Lagstrom

Segata

Sharon

Louzoun

Koren

(2021). Neonatal antibiotic exposure impairs child growth during the first six years of life by perturbing intestinal microbial colonization. Nature Communications, 12(1), 1–12. https://doi.org/10.1038/s41467-020-20495-4

60.

Vettore

Leão

Leal

M. d. C.

Feres

Sheiham

(2008). The relationship between periodontal disease and preterm low birthweight: Clinical and microbiological results. Journal of Periodontal Research, 43(6), 615–626. https://doi.org/10.1111/j.1600-0765.2007.01027.x

61.

Vivatvakin

Mahayosnond

Theamboonlers

Steenhout

P. G.

Conus

N. J.

(2010). Effect of a whey-predominant starter formula containing LCPUFAs and oligosaccharides (FOS/GOS) on gastrointestinal comfort in infants. Asia Pacific Journal of Clinical Nutrition, 19(4), 473–480.

62.

Wall

Ross

Ryan

Hussey

Murphy

Fitzgerald

Stanton

(2009). Role of gut microbiota in early infant development. Clinical Medicine. Pediatrics, 3, 45. https://doi.org/10.4137/cmped.s2008.

63.

Warner

B. B.

(2019). The contribution of the gut microbiome to neurodevelopment and neuropsychiatric disorders. Pediatric Research, 85(2), 216–224. https://doi.org/10.1038/s41390-018-0191-9.

64.

Willis

A. D.

(2019). Rarefaction, alpha diversity, and statistics. Frontiers in Microbiology, 10(Oct), 2407. https://doi.org/10.3389/fmicb.2019.02407.

65.

Zhao

Liu

W.-H.

H.-W.

Zhang

Y.-M.

(2021). Neurodevelopmental outcomes and gut bifidobacteria in term infants fed an infant formula containing high sn-2 palmitate: A cluster randomized clinical trial. , 13(2), 693. https://doi.org/10.3390/nu13020693

66.

Yang

Corwin

E. J.

Brennan

P. A.

Jordan

Murphy

J. R.

Dunlop

(2016). The infant microbiome: Implications for infant health and neurocognitive development. Nursing Research, 65(1), 76–88. https://doi.org/10.1097/nnr.0000000000000133

67.

Zambruni

Ochoa

T. J.

Somasunderam

Cabada

M. M.

Morales

M. L.

Mitreva

Rosa

B. A.

Acosta

G. J.

Vigo

N. I.

Riveros

Arango

Durand

Berends

M. N.

Melby

Utay

N. S.

(2019). Stunting is preceded by intestinal mucosal damage and microbiome changes and is associated with systemic inflammation in a cohort of Peruvian infants. The American Journal of Tropical Medicine and Hygiene, 101(5), 1009–1017. https://doi.org/10.4269/ajtmh.18-0975

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