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Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load
BACKGROUND: Infants are at a high risk of acquiring fatal infections, and their treatment relies on functioning antibiotics. Antibiotic resistance genes (ARGs) are present in high numbers in antibiotic-naive infants’ gut microbiomes, and infant mortality caused by resistant infections is high. The r...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8827105/ https://www.ncbi.nlm.nih.gov/pubmed/34677583 http://dx.doi.org/10.1093/ajcn/nqab353 |
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author | Pärnänen, Katariina M M Hultman, Jenni Markkanen, Melina Satokari, Reetta Rautava, Samuli Lamendella, Regina Wright, Justin McLimans, Christopher J Kelleher, Shannon L Virta, Marko P |
author_facet | Pärnänen, Katariina M M Hultman, Jenni Markkanen, Melina Satokari, Reetta Rautava, Samuli Lamendella, Regina Wright, Justin McLimans, Christopher J Kelleher, Shannon L Virta, Marko P |
author_sort | Pärnänen, Katariina M M |
collection | PubMed |
description | BACKGROUND: Infants are at a high risk of acquiring fatal infections, and their treatment relies on functioning antibiotics. Antibiotic resistance genes (ARGs) are present in high numbers in antibiotic-naive infants’ gut microbiomes, and infant mortality caused by resistant infections is high. The role of antibiotics in shaping the infant resistome has been studied, but there is limited knowledge on other factors that affect the antibiotic resistance burden of the infant gut. OBJECTIVES: Our objectives were to determine the impact of early exposure to formula on the ARG load in neonates and infants born either preterm or full term. Our hypotheses were that diet causes a selective pressure that influences the microbial community of the infant gut, and formula exposure would increase the abundance of taxa that carry ARGs. METHODS: Cross-sectionally sampled gut metagenomes of 46 neonates were used to build a generalized linear model to determine the impact of diet on ARG loads in neonates. The model was cross-validated using neonate metagenomes gathered from public databases using our custom statistical pipeline for cross-validation. RESULTS: Formula-fed neonates had higher relative abundances of opportunistic pathogens such as Staphylococcus aureus, Staphylococcus epidermidis, Klebsiella pneumoniae, Klebsiella oxytoca, and Clostridioides difficile. The relative abundance of ARGs carried by gut bacteria was 69% higher in the formula-receiving group (fold change, 1.69; 95% CI: 1.12–2.55; P = 0.013; n = 180) compared to exclusively human milk–fed infants. The formula-fed infants also had significantly less typical infant bacteria, such as Bifidobacteria, that have potential health benefits. CONCLUSIONS: The novel finding that formula exposure is correlated with a higher neonatal ARG burden lays the foundation that clinicians should consider feeding mode in addition to antibiotic use during the first months of life to minimize the proliferation of antibiotic-resistant gut bacteria in infants. |
format | Online Article Text |
id | pubmed-8827105 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-88271052022-02-10 Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load Pärnänen, Katariina M M Hultman, Jenni Markkanen, Melina Satokari, Reetta Rautava, Samuli Lamendella, Regina Wright, Justin McLimans, Christopher J Kelleher, Shannon L Virta, Marko P Am J Clin Nutr Original Research Communications BACKGROUND: Infants are at a high risk of acquiring fatal infections, and their treatment relies on functioning antibiotics. Antibiotic resistance genes (ARGs) are present in high numbers in antibiotic-naive infants’ gut microbiomes, and infant mortality caused by resistant infections is high. The role of antibiotics in shaping the infant resistome has been studied, but there is limited knowledge on other factors that affect the antibiotic resistance burden of the infant gut. OBJECTIVES: Our objectives were to determine the impact of early exposure to formula on the ARG load in neonates and infants born either preterm or full term. Our hypotheses were that diet causes a selective pressure that influences the microbial community of the infant gut, and formula exposure would increase the abundance of taxa that carry ARGs. METHODS: Cross-sectionally sampled gut metagenomes of 46 neonates were used to build a generalized linear model to determine the impact of diet on ARG loads in neonates. The model was cross-validated using neonate metagenomes gathered from public databases using our custom statistical pipeline for cross-validation. RESULTS: Formula-fed neonates had higher relative abundances of opportunistic pathogens such as Staphylococcus aureus, Staphylococcus epidermidis, Klebsiella pneumoniae, Klebsiella oxytoca, and Clostridioides difficile. The relative abundance of ARGs carried by gut bacteria was 69% higher in the formula-receiving group (fold change, 1.69; 95% CI: 1.12–2.55; P = 0.013; n = 180) compared to exclusively human milk–fed infants. The formula-fed infants also had significantly less typical infant bacteria, such as Bifidobacteria, that have potential health benefits. CONCLUSIONS: The novel finding that formula exposure is correlated with a higher neonatal ARG burden lays the foundation that clinicians should consider feeding mode in addition to antibiotic use during the first months of life to minimize the proliferation of antibiotic-resistant gut bacteria in infants. Oxford University Press 2021-10-22 /pmc/articles/PMC8827105/ /pubmed/34677583 http://dx.doi.org/10.1093/ajcn/nqab353 Text en © The Author(s) 2021. Published by Oxford University Press https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Original Research Communications Pärnänen, Katariina M M Hultman, Jenni Markkanen, Melina Satokari, Reetta Rautava, Samuli Lamendella, Regina Wright, Justin McLimans, Christopher J Kelleher, Shannon L Virta, Marko P Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
title | Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
title_full | Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
title_fullStr | Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
title_full_unstemmed | Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
title_short | Early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
title_sort | early-life formula feeding is associated with infant gut microbiota alterations and an increased antibiotic resistance load |
topic | Original Research Communications |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8827105/ https://www.ncbi.nlm.nih.gov/pubmed/34677583 http://dx.doi.org/10.1093/ajcn/nqab353 |
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