Systematic review of associations between gut microbiome composition and stunting in under-five children.
Journal
NPJ biofilms and microbiomes
ISSN: 2055-5008
Titre abrégé: NPJ Biofilms Microbiomes
Pays: United States
ID NLM: 101666944
Informations de publication
Date de publication:
23 May 2024
23 May 2024
Historique:
received:
16
11
2023
accepted:
29
04
2024
medline:
24
5
2024
pubmed:
24
5
2024
entrez:
23
5
2024
Statut:
epublish
Résumé
Childhood stunting is associated with impaired cognitive development and increased risk of infections, morbidity, and mortality. The composition of the enteric microbiota may contribute to the pathogenesis of stunting. We systematically reviewed and synthesized data from studies using high-throughput genomic sequencing methods to characterize the gut microbiome in stunted versus non-stunted children under 5 years in LMICs. We included 14 studies from Asia, Africa, and South America. Most studies did not report any significant differences in the alpha diversity, while a significantly higher beta diversity was observed in stunted children in four out of seven studies that reported beta diversity. At the phylum level, inconsistent associations with stunting were observed for Bacillota, Pseudomonadota, and Bacteroidota phyla. No single genus was associated with stunted children across all 14 studies, and some associations were incongruent by specific genera. Nonetheless, stunting was associated with an abundance of pathobionts that could drive inflammation, such as Escherichia/Shigella and Campylobacter, and a reduction of butyrate producers, including Faecalibacterium, Megasphera, Blautia, and increased Ruminoccoccus. An abundance of taxa thought to originate in the oropharynx was also reported in duodenal and fecal samples of stunted children, while metabolic pathways, including purine and pyrimidine biosynthesis, vitamin B biosynthesis, and carbohydrate and amino acid degradation pathways, predicted linear growth. Current studies show that stunted children can have distinct microbial patterns compared to non-stunted children, which could contribute to the pathogenesis of stunting.
Identifiants
pubmed: 38782939
doi: 10.1038/s41522-024-00517-5
pii: 10.1038/s41522-024-00517-5
doi:
Types de publication
Journal Article
Systematic Review
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
46Subventions
Organisme : Wellcome Trust (Wellcome)
ID : 219829/Z/19/Z
Organisme : Wellcome Trust (Wellcome)
ID : 219829/Z/19/Z
Organisme : Wellcome Trust (Wellcome)
ID : 219829/Z/19/Z
Organisme : Wellcome Trust (Wellcome)
ID : 219829/Z/19/Z
Informations de copyright
© 2024. The Author(s).
Références
UNICEF, WHO. World Bank. Levels and Trends in Child Malnutrition: UNICEF-WHO-World Bank Joint Child Malnutrition Estimates [Internet]. Available from: https://www.who.int/publications/i/item/9789240073791 . (2023).
WHO MULTICENTRE GROWTH REFERENCE STUDY GROUP. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-forheight and body mass index-for-age: methods and development. Geneva, Switzerland. Acta Paediatr. 450, 76–85 (2006).
Kossmann, J., Nestel, P., Herrera, M. G., el Amin, A. & Fawzi, W. W. Undernutrition in relation to childhood infections: a prospective study in the Sudan. Eur. J. Clin. Nutr. 54, 463–472 (2000).
pubmed: 10878647
doi: 10.1038/sj.ejcn.1600998
Caulfield, L. E., de Onis, M., Blössner, M. & Black, R. E. Undernutrition as an underlying cause of child deaths associated with diarrhea, pneumonia, malaria, and measles. Am. J. Clin. Nutr. 80, 193–198 (2004).
pubmed: 15213048
doi: 10.1093/ajcn/80.1.193
Dewey, K. G. & Begum, K. Long-term consequences of stunting in early life. Matern Child Nutr. 7, 5–18 (2011).
pubmed: 21929633
pmcid: 6860846
doi: 10.1111/j.1740-8709.2011.00349.x
Danaei, G. et al. Risk factors for childhood stunting in 137 developing countries: a comparative risk assessment analysis at global, regional, and Country levels. PLoS Med. 13, e1002164 (2016).
pubmed: 27802277
pmcid: 5089547
doi: 10.1371/journal.pmed.1002164
Checkley, W. et al. Multi-country analysis of the effects of diarrhoea on childhood stunting. Int J. Epidemiol. 37, 816–830 (2008).
pubmed: 18567626
pmcid: 2734063
doi: 10.1093/ije/dyn099
Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).
pubmed: 22699611
pmcid: 3376388
doi: 10.1038/nature11053
Robertson, R. C., Manges, A. R., Finlay, B. B. & Prendergast, A. J. The Human Microbiome and Child Growth – First 1000 Days and Beyond. Trends Microbiol. p. 131–147. https://doi.org/10.1016/j.tim.2018.09.008 (2019).
Million, M., Diallo, A. & Raoult, D. Gut microbiota and malnutrition. Microb. Pathogen. 106, 127–138 (2017).
doi: 10.1016/j.micpath.2016.02.003
Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).
pubmed: 17183312
doi: 10.1038/nature05414
Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: Human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).
pubmed: 17183309
doi: 10.1038/4441022a
Chambers, E. S., Morrison, D. J. & Frost, G. Control of appetite and energy intake by SCFA: What are the potential underlying mechanisms? Proc. Nutr. Soc. 74, 328–336 (2015).
pubmed: 25497601
doi: 10.1017/S0029665114001657
Schroeder, B. O. & Bäckhed, F. Signals from the gut microbiota to distant organs in physiology and disease. Nat. Med [Internet] 22, 1079–1089 (2016).
pubmed: 27711063
doi: 10.1038/nm.4185
Strand, T. A. et al. Vitamin B-12, folic acid, and growth in 6- to 30-month-old children: a randomized controlled trial. Pediatrics [Internet] 135, e918–e926 (2015).
pubmed: 25802345
doi: 10.1542/peds.2014-1848
Baümler, A. J. & Sperandio, V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535, 85–93 (2016).
pubmed: 27383983
pmcid: 5114849
doi: 10.1038/nature18849
Gensollen, T., Iyer, S. S., Kasper, D. L. & Blumberg, R. S. How colonization by microbiota in early life shapes the immune system. Sci. (1979). 352, 539–544 (2016).
Kane, A. V., Dinh, D. M. & Ward, H. D. Childhood malnutrition and the intestinal microbiome. Pediatr. Res. 77, 256–262 (2015).
pubmed: 25356748
doi: 10.1038/pr.2014.179
Arrieta, M. C. et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 7, 307ra152 (2015).
pubmed: 26424567
doi: 10.1126/scitranslmed.aab2271
de Onis, M. & Branca, F. Childhood stunting: a global perspective. Matern Child Nutr. 12, 12–26 (2016).
pubmed: 27187907
pmcid: 5084763
doi: 10.1111/mcn.12231
Mameli, C., Mazzantini, S. & Zuccotti, G. V. Nutrition in the first 1000 days: the origin of childhood obesity. Int. J. Environ. Res. Public Health 13, 838 (2016).
pubmed: 27563917
pmcid: 5036671
doi: 10.3390/ijerph13090838
Chen, R. Y. et al. Duodenal microbiota in stunted undernourished children with enteropathy. N. Engl. J. Med. 383, 321–333 (2020).
pubmed: 32706533
pmcid: 7289524
doi: 10.1056/NEJMoa1916004
Khan Mirzaei, M. et al. Bacteriophages isolated from stunted children can regulate gut bacterial communities in an age-specific manner. Cell Host Microbe 27, 199–212.e5 (2020).
pubmed: 32053789
pmcid: 7013830
doi: 10.1016/j.chom.2020.01.004
Perin, J. et al. A retrospective case-control study of the relationship between the gut microbiota, enteropathy, and child growth. Am. J. Tropical Med. Hyg. 103, 520–527 (2020).
doi: 10.4269/ajtmh.19-0761
Gough, E. K. et al. Linear growth faltering in infants is associated with Acidaminococcus sp. and community-level changes in the gut microbiota. Microbiome 3, 24 (2015).
pubmed: 26106478
pmcid: 4477476
doi: 10.1186/s40168-015-0089-2
Dinh, D. M. et al. Longitudinal analysis of the intestinal microbiota in persistently stunted young children in South India. PLoS ONE [Electron. Resour.] 11, e0155405 (2016).
pubmed: 27228122
doi: 10.1371/journal.pone.0155405
Shivakumar, N. et al. Gut microbiota profiles of young South Indian children: child sex-specific relations with growth. PLoS ONE [Electron. Resour.] 16, e0251803 (2021).
pubmed: 33989353
doi: 10.1371/journal.pone.0251803
Surono, I. S., Widiyanti, D., Kusumo, P. D. & Venema, K. Gut microbiota profile of Indonesian stunted children and children with normal nutritional status. PLoS ONE [Electron. Resour.] 16, e0245399 (2021).
pubmed: 33497390
doi: 10.1371/journal.pone.0245399
Masrul, M. et al. Microbiota profile with stunting children in west sumatera province, indonesia. Open Access Maced. J. Med Sci. 8, 334–340 (2020).
doi: 10.3889/oamjms.2020.4209
Desai, C. et al. Growth velocity in children with environmental enteric dysfunction is associated with specific bacterial and viral taxa of the gastrointestinal tract in malawian children. PLoS Negl. Trop. Dis. 14, e0008387 (2020).
pubmed: 32574158
pmcid: 7310680
doi: 10.1371/journal.pntd.0008387
Kamng’ona, A. W. et al. The association of gut microbiota characteristics in Malawian infants with growth and inflammation. Sci. Rep. 9, 12893 (2019).
pubmed: 31501455
pmcid: 6733848
doi: 10.1038/s41598-019-49274-y
Robertson, R. C. et al. The gut microbiome and early-life growth in a population with high prevalence of stunting. Nat. Commun. 14, 654 (2023).
pubmed: 36788215
pmcid: 9929340
doi: 10.1038/s41467-023-36135-6
Vonaesch, P. et al. Stunted childhood growth is associated with decompartmentalization of the gastrointestinal tract and overgrowth of oropharyngeal taxa. Proc. Natl Acad. Sci. USA 115, E8489–E8498 (2018).
pubmed: 30126990
pmcid: 6130352
doi: 10.1073/pnas.1806573115
Rouhani, S. et al. Gut microbiota features associated with campylobacter burden and postnatal linear growth deficits in a Peruvian birth cohort. Clin. Infect. Dis. 71, 1000–1007 (2020).
pubmed: 31773126
doi: 10.1093/cid/ciz906
Zambruni, M. et al. Stunting is preceded by intestinal mucosal damage and microbiome changes and is associated with systemic inflammation in a cohort of Peruvian infants. Am. J. Tropical Med. Hyg. 101, 1009–1017 (2019).
doi: 10.4269/ajtmh.18-0975
Shkoporov, A. N. et al. The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 26, 527–541 (2019).
pubmed: 31600503
doi: 10.1016/j.chom.2019.09.009
Stephenson, L. S., Latham, M. C. & Ottesen, E. A. Malnutrition and parasitic helminth infections. Parasitology [Internet]. 2001/06/15. Available from: https://www.cambridge.org/core/article/malnutrition-and-parasitic-helminth-infections/7B648AE4E9EBC6C006AC39272FFA7BE7 121, S23–S38 (2000).
Guerrant, R. L., Deboer, M. D., Moore, S. R., Scharf, R. J. & Lima, A. A. M. The impoverished gut - A triple burden of diarrhoea, stunting and chronic disease. Nat. Rev. Gastroenterol. Hepatol. 10, 220–229 (2013).
pubmed: 23229327
doi: 10.1038/nrgastro.2012.239
Prendergast, A. J. & Humphrey, J. H. The stunting syndrome in developing countries. Paediatr Int Child Health [Internet]. 2014. Nov;34:250–265. Available from: https://pubmed.ncbi.nlm.nih.gov/25310000 .
Smith, M. I. et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Sci. (1979). 339, 548–554 (2013).
Ghosh, T. S. et al. Gut microbiomes of Indian children of varying nutritional status. PLoS ONE [Electron. Resour.] 9, e95547 (2014).
pubmed: 24763225
doi: 10.1371/journal.pone.0095547
Raman, A. S. et al. A sparse covarying unit that describes healthy and impaired human gut microbiota development. Sci. (1979) [Internet]. 365, eaau4735 (2019).
Blanton, L. V. et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016 Feb;351: https://doi.org/10.1126/science.aad3311 .
Subramanian, S. et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510, 417–421 (2014).
pubmed: 24896187
pmcid: 4189846
doi: 10.1038/nature13421
Michielan, A. & D’Incà, R. Intestinal permeability in inflammatory bowel disease: pathogenesis, clinical evaluation, and therapy of leaky gut. Neuwirt H., editor. Mediators Inflamm [Internet] 2015, 628157 (2015).
Bischoff, S. C. et al. Intestinal permeability – a new target for disease prevention and therapy. BMC Gastroenterol. [Internet] 14, 189 (2014).
pubmed: 25407511
doi: 10.1186/s12876-014-0189-7
Strober, W. Impact of the gut microbiome on mucosal inflammation. Trends Immunol [Internet] 34, 423–430. Available from: https://www.sciencedirect.com/science/article/pii/S1471490613001087 (2013).
Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121–141 (2014).
pubmed: 24679531
pmcid: 4056765
doi: 10.1016/j.cell.2014.03.011
Pham, T. P. et al. Gut microbiota alteration is characterized by a proteobacteria and Fusobacteria bloom in Kwashiorkor and a bacteroidetes paucity in Marasmus. Sci. Rep. 9, 9084 (2019).
pubmed: 31235833
pmcid: 6591176
doi: 10.1038/s41598-019-45611-3
Lupp, C. et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2, 119–129 (2007).
pubmed: 18005726
doi: 10.1016/j.chom.2007.06.010
Monira, S. et al. Gut microbiota of healthy and malnourished children in Bangladesh. Front Microbiol. 2, 228 (2011).
pubmed: 22125551
pmcid: 3221396
doi: 10.3389/fmicb.2011.00228
Million, M. & Raoult, D. Linking gut redox to human microbiome. Hum. Micro. J. 10, 27–32 (2018).
doi: 10.1016/j.humic.2018.07.002
Nabwera, H. M. et al. Interactions between fecal gut microbiome, enteric pathogens, and energy regulating hormones among acutely malnourished rural Gambian children. EBioMedicine 73, 103644 (2021).
pubmed: 34695658
pmcid: 8550991
doi: 10.1016/j.ebiom.2021.103644
Yu, L. C. H. Microbiota dysbiosis and barrier dysfunction in inflammatory bowel disease and colorectal cancers: exploring a common ground hypothesis. J. Biomed. Sci. 25, 79 (2018).
pubmed: 30413188
pmcid: 6234774
doi: 10.1186/s12929-018-0483-8
Carbonero, F., Benefiel, A., Alizadeh-Ghamsari, A. & Gaskins, H. R. Microbial pathways in colonic sulfur metabolism and links with health and disease. Front. Physiol. 3. Available from: https://www.frontiersin.org/articles/10.3389/fphys.2012.00448 (2012).
Croxen, M. A. & Finlay, B. B. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol. 8, 26–38 (2010).
pubmed: 19966814
doi: 10.1038/nrmicro2265
Phalipon, A. & Sansonetti, P. J. Shigella’s ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival? Immunol. Cell Biol. 85, 119–129 (2007).
pubmed: 17213832
doi: 10.1038/sj.icb7100025
Rouhani, S. et al. Diarrhea as a potential cause and consequence of reduced gut microbial diversity among undernourished children in peru. Clin. Infect. Dis. 71, 989–999 (2020).
pubmed: 31773127
doi: 10.1093/cid/ciz905
Canani, R. B. et al. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 17, 1519–1528 (2011).
pubmed: 21472114
pmcid: 3070119
doi: 10.3748/wjg.v17.i12.1519
Fluitman, K. S. et al. The intestinal microbiota, energy balance, and malnutrition: emphasis on the role of short-chain fatty acids. Expert Rev. Endocrinol. Metab. 12, 215–226 (2017).
pubmed: 30063458
doi: 10.1080/17446651.2017.1318060
Mowat, A. M. & Agace, W. W. Regional specialization within the intestinal immune system. Nat. Rev. Immunol. [Internet] 14, 667–685 (2014).
pubmed: 25234148
doi: 10.1038/nri3738
Mendez-Salazar, E. O., Ortiz-Lopez, M. G., Granados-Silvestre, M. D. L. A., Palacios-Gonzalez, B. & Menjivar, M. Altered gut microbiota and compositional changes in firmicutes and proteobacteria in mexican undernourished and obese children. Front Microbiol. 9, 2494 (2018).
pubmed: 30386323
pmcid: 6198253
doi: 10.3389/fmicb.2018.02494
Iddrisu, I. et al. Malnutrition and gut microbiota in children. Nutrients 13, 8 (2021).
doi: 10.3390/nu13082727
Lkhagva, E. et al. The regional diversity of gut microbiome along the GI tract of male C57BL/6 mice. BMC Microbiol. 21, 44 (2021).
pubmed: 33579191
pmcid: 7881553
doi: 10.1186/s12866-021-02099-0
Hillman, E. T., Lu, H., Yao, T. & Nakatsu, C. H. Microbial ecology along the gastrointestinal tract. Microbes Environ. 32, 300–313 (2017).
pubmed: 29129876
pmcid: 5745014
doi: 10.1264/jsme2.ME17017
Leite, G. G. S. et al. Mapping the segmental microbiomes in the human small bowel in comparison with stool: a REIMAGINE study. Dig. Dis. Sci. 65, 2595–2604 (2020).
pubmed: 32140945
pmcid: 7419378
doi: 10.1007/s10620-020-06173-x
Shalon, D. et al. Profiling the human intestinal environment under physiological conditions. Nature 617, 581–591 (2023).
pubmed: 37165188
pmcid: 10191855
doi: 10.1038/s41586-023-05989-7
Guetterman, H. M. et al. Vitamin B-12 and the gastrointestinal microbiome: a systematic review. 13, Advances in Nutrition. Oxford University Press, p. 530–558 (2022).
Chen, R. Y. et al. A microbiota-directed food intervention for undernourished children. N. Engl. J. Med. 384, 1517–1528 (2021).
pubmed: 33826814
pmcid: 7993600
doi: 10.1056/NEJMoa2023294
Gehrig, J. L. et al. Effects of microbiota-directed foods in gnotobiotic animals and undernourished children. Sci. (1979). 365, 12 (2019).
Hopkins, M. J., Sharp, R. & Macfarlane, G. T. Variation in human intestinal microbiota with age. Digestive Liver Dis. 34, S12–S18 (2002).
doi: 10.1016/S1590-8658(02)80157-8
Poretsky, R., Rodriguez-R, L. M., Luo, C., Tsementzi, D. & Konstantinidis, K. T. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE 9, e93827 (2014).
pubmed: 24714158
pmcid: 3979728
doi: 10.1371/journal.pone.0093827
Methley, A. M., Campbell, S., Chew-Graham, C., McNally, R. & Cheraghi-Sohi, S. P. I. C. O. PICOS and SPIDER: a comparison study of specificity and sensitivity in three search tools for qualitative systematic reviews. BMC Health Serv. Res. 14, 579 (2014).
pubmed: 25413154
pmcid: 4310146
doi: 10.1186/s12913-014-0579-0
Liberati A. et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ [Internet]. Available from: https://www.bmj.com/content/339/bmj.b2700 (2009).
Porritt, K., Gomersall, J. & Lockwood, C. JBI’s systematic reviews: study selection and critical appraisal. AJN Am. J. Nurs. 114, 47–52 (2014).
pubmed: 24869584
doi: 10.1097/01.NAJ.0000450430.97383.64