Interplay Between Helminth Infections, Malnutrition, and Gut Microbiota in Children and Mothers from Pemba, Tanzania: Potential of Microbiota-Directed Interventions

Overview

Journal Nutrients

Date 2024 Dec 17

PMID 39683417

Authors

Aristide Toussaint Nguele

Matteo Mozzicafreddo

Chiara Carrara

Angela Piersanti

Salum Seif Salum

Said M Ali

Cristina Miceli

Affiliations

Soon will be listed here.

Abstract

Background/objectives: Despite efforts within the framework of the Sustainable Development Goal to end malnutrition by 2030, malnutrition and soil-transmitted helminth infections persist in sub-Saharan Africa. A significant barrier to success is the inadequate understanding of effective intervention methods. Most research on the gut microbiota's role in health has been conducted in developed countries, leaving a critical gap in knowledge regarding low-income populations. This study addresses this gap by expanding research on the gut microbiota of underprivileged populations to help tackle these public health challenges.

Methods: We employed 16S rDNA sequencing to assess the bacterial gut microbiota composition of 60 children (mean age: 26.63 ± 6.36 months) and their 58 mothers (mean age: 30.03 ± 6.31 years) in Pemba, with a focus on helminth infection and nutritional status.

Results: Our differential abundance analysis identified bacterial taxa that were significantly negatively associated with both helminth infections and malnutrition, highlighting the potential for microbiota-directed interventions to address these health issues simultaneously. Notably, we identified , , , and as promising probiotic candidates for such interventions. In stunted children, positive co-occurrences were observed between , , and , while displayed negative co-abundance relationships with short-chain fatty acid (SCFA) producers in the gut microbiota. These findings suggest that administering and SCFA-producing probiotics to children may foster the growth of beneficial bacteria like and while reducing the relative abundance of , potentially enhancing overall health.

Conclusions: This study underscores the importance of microbiota-directed interventions in children and women of reproductive age as promising strategies, alongside established approaches, for combating helminth infections and malnutrition in vulnerable populations.

References

Jin X, Liu Y, Wang J, Wang X, Tang B, Liu M . β-Glucan-triggered Akkermansia muciniphila expansion facilitates the expulsion of intestinal helminth via TLR2 in mice. Carbohydr Polym. 2021; 275:118719. DOI: 10.1016/j.carbpol.2021.118719. View

Chen L, Collij V, Jaeger M, van den Munckhof I, Vich Vila A, Kurilshikov A . Gut microbial co-abundance networks show specificity in inflammatory bowel disease and obesity. Nat Commun. 2020; 11(1):4018. PMC: 7419557. DOI: 10.1038/s41467-020-17840-y. View

Blanton L, Charbonneau M, Salih T, Barratt M, Venkatesh S, Ilkaveya O . Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016; 351(6275). PMC: 4787260. DOI: 10.1126/science.aad3311. View

Mertens A, Benjamin-Chung J, Colford Jr J, Coyle J, van der Laan M, Hubbard A . Causes and consequences of child growth faltering in low-resource settings. Nature. 2023; 621(7979):568-576. PMC: 10511328. DOI: 10.1038/s41586-023-06501-x. View

Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P . Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science. 2016; 351(6275):854-7. DOI: 10.1126/science.aad8588. View

Bosch B, Moutaharrik S, Gazzaniga A, Hiippala K, Santos H, Maroni A . Development of a time-dependent oral colon delivery system of anaerobic Odoribacter splanchnicus for bacteriotherapy. Eur J Pharm Biopharm. 2023; 190:73-80. DOI: 10.1016/j.ejpb.2023.07.010. View

Morelli L, Garbagna N, Rizzello F, Zonenschain D, Grossi E . In vivo association to human colon of Lactobacillus paracasei B21060: map from biopsies. Dig Liver Dis. 2006; 38(12):894-8. DOI: 10.1016/j.dld.2006.07.010. View

Hayes K, Bancroft A, Goldrick M, Portsmouth C, Roberts I, Grencis R . Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science. 2010; 328(5984):1391-4. PMC: 3428897. DOI: 10.1126/science.1187703. View

Lu F, Li Y, Wang X, Hu X, Liao X, Zhang Y . Early-life polyphenol intake promotes Akkermansia growth and increase of host goblet cells in association with the potential synergistic effect of Lactobacillus. Food Res Int. 2021; 149:110648. DOI: 10.1016/j.foodres.2021.110648. View

10.

Walker S, Chang S, Wright A, Osmond C, Grantham-McGregor S . Early childhood stunting is associated with lower developmental levels in the subsequent generation of children. J Nutr. 2015; 145(4):823-8. DOI: 10.3945/jn.114.200261. View

11.

Jaswal K, Todd O, Behnsen J . Neglected gut microbiome: interactions of the non-bacterial gut microbiota with enteric pathogens. Gut Microbes. 2023; 15(1):2226916. PMC: 10305517. DOI: 10.1080/19490976.2023.2226916. View

12.

Mrimi E, Palmeirim M, Minja E, Long K, Keiser J . Malnutrition, anemia, micronutrient deficiency and parasitic infections among schoolchildren in rural Tanzania. PLoS Negl Trop Dis. 2022; 16(3):e0010261. PMC: 8926280. DOI: 10.1371/journal.pntd.0010261. View

13.

Kupritz J, Angelova A, Nutman T, Gazzinelli-Guimaraes P . Helminth-Induced Human Gastrointestinal Dysbiosis: a Systematic Review and Meta-Analysis Reveals Insights into Altered Taxon Diversity and Microbial Gradient Collapse. mBio. 2021; 12(6):e0289021. PMC: 8689561. DOI: 10.1128/mBio.02890-21. View

14.

Knopp S, Mohammed K, Rollinson D, Stothard J, Khamis I, Utzinger J . Changing patterns of soil-transmitted helminthiases in Zanzibar in the context of national helminth control programs. Am J Trop Med Hyg. 2009; 81(6):1071-8. DOI: 10.4269/ajtmh.2009.09-0377. View

15.

Du Toit A . Microbiome: Restoring healthy growth in infants. Nat Rev Microbiol. 2016; 14(4):191. DOI: 10.1038/nrmicro.2016.31. View

16.

Geleto G, Kassa T, Erko B . Epidemiology of soil-transmitted helminthiasis and associated malnutrition among under-fives in conflict affected areas in southern Ethiopia. Trop Med Health. 2022; 50(1):44. PMC: 9275057. DOI: 10.1186/s41182-022-00436-1. View

17.

Companys J, Gosalbes M, Pla-Paga L, Calderon-Perez L, Llaurado E, Pedret A . Gut Microbiota Profile and Its Association with Clinical Variables and Dietary Intake in Overweight/Obese and Lean Subjects: A Cross-Sectional Study. Nutrients. 2021; 13(6). PMC: 8231825. DOI: 10.3390/nu13062032. View

18.

Henriques A, Teixeira V, Cardoso H, Azevedo A . The influence of stunting on obesity in adulthood: results from the EPIPorto cohort. Public Health Nutr. 2018; 21(10):1819-1826. PMC: 10260921. DOI: 10.1017/S1368980018000460. View

19.

Lawson M, Roberts I, Grencis R . The interplay between and the microbiota. Parasitology. 2021; :1-8. PMC: 8660641. DOI: 10.1017/S0031182021000834. View

20.

Toussaint Nguele A, Carrara C, Mozzicafreddo M, Chen H, Piersanti A, Salum S . Association between Food or Nutrients and Gut Microbiota in Healthy and Helminth-Infected Women of Reproductive Age from Zanzibar, Tanzania. Nutrients. 2024; 16(9). PMC: 11085056. DOI: 10.3390/nu16091266. View