Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets

ABSTRACT The impact of human milk (HM) feeding compared with cow’s milk formula (MF) feeding on small intestinal and circulatory metabolome patterns has not been fully investigated. Therefore, 2-day-old male piglets were fed HM or MF (n = 26/group) from postnatal day 2 (PND 2) through 21 and were we...

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Autores principales: Fernanda Rosa, Katelin S. Matazel, Ahmed A. Elolimy, Sean H. Adams, Anne Bowlin, Keith D. Williams, Lars Bode, Laxmi Yeruva
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Publicado: American Society for Microbiology 2021
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Acceso en línea:https://doaj.org/article/bef707eb921f4a9caa76ef4988caac93
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spelling oai:doaj.org-article:bef707eb921f4a9caa76ef4988caac932021-12-02T18:20:19ZHuman Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets10.1128/mSystems.01376-202379-5077https://doaj.org/article/bef707eb921f4a9caa76ef4988caac932021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01376-20https://doaj.org/toc/2379-5077ABSTRACT The impact of human milk (HM) feeding compared with cow’s milk formula (MF) feeding on small intestinal and circulatory metabolome patterns has not been fully investigated. Therefore, 2-day-old male piglets were fed HM or MF (n = 26/group) from postnatal day 2 (PND 2) through 21 and were weaned to a solid diet until PND 51. The small intestine (gastrointestinal [GI]) contents, serum, and urine were collected from subsets of piglets at PND 21 and PND 51. Samples were subjected to primary metabolomics analyses at the West Coast Metabolomics Center, UC Davis. The metabolome data assessment and the statistical analyses were performed with MetaboAnalyst software. Compared with MF feeding, at PND 21, HM feeding resulted in a higher abundance of fucose in the jejunum and urine and a greater concentration of myo-inositol in serum. In HM-fed piglets, 1,5-anhydroglucitol was higher in the duodenum, serum, and urine at PND 21. Additionally, the HM group had higher levels of urinary kynurenic acid at PND 21. Correlations between bacterial genera and altered metabolites in ileum revealed that Turicibacter sp. and Campylobacter sp. were positively correlated with maltotriose and panose at PND 21, while ileal Campylobacter sp. was negatively correlated with fumaric acid. At PND 51, no significant metabolites were identified between HM and MF diet groups. The metabolites associated with the neonatal diets may serve as the substrates and signals that contribute to the physiological effects in HM and MF during infancy, with a subset reflecting diet-associated differences in microbial metabolism and ecology. IMPORTANCE Exclusive HM feeding for newborns is recommended at least for the first 6 months of life. However, when breastfeeding is not possible, MF is recommended as a substitute. Due to the challenges associated with sample collection from infants fed HM or MF, their gut metabolism is poorly understood. Thus, an established piglet model from our team was used to determine the metabolite profile in relation to host, diet, and microbiota. The current study is the first to provide novel insights across the small intestine metabolism and its association with circulatory metabolites in the HM group relative to the MF group at the weaning and postweaning period. Data also demonstrate that during the neonatal period, diet, host, and microbial metabolism contribute to the lumen and circulatory metabolite profile. Furthermore, small intestinal lumen metabolome can be tracked in the urine as a biomarker of dietary differences, which would be a useful tool for clinical interventions.Fernanda RosaKatelin S. MatazelAhmed A. ElolimySean H. AdamsAnne BowlinKeith D. WilliamsLars BodeLaxmi YeruvaAmerican Society for Microbiologyarticleformula milkguthuman milkmetabolomeserumurineMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution DOAJ
collection DOAJ
language EN
topic formula milk
gut
human milk
metabolome
serum
urine
Microbiology
QR1-502
spellingShingle formula milk
gut
human milk
metabolome
serum
urine
Microbiology
QR1-502
Fernanda Rosa
Katelin S. Matazel
Ahmed A. Elolimy
Sean H. Adams
Anne Bowlin
Keith D. Williams
Lars Bode
Laxmi Yeruva
Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets
description ABSTRACT The impact of human milk (HM) feeding compared with cow’s milk formula (MF) feeding on small intestinal and circulatory metabolome patterns has not been fully investigated. Therefore, 2-day-old male piglets were fed HM or MF (n = 26/group) from postnatal day 2 (PND 2) through 21 and were weaned to a solid diet until PND 51. The small intestine (gastrointestinal [GI]) contents, serum, and urine were collected from subsets of piglets at PND 21 and PND 51. Samples were subjected to primary metabolomics analyses at the West Coast Metabolomics Center, UC Davis. The metabolome data assessment and the statistical analyses were performed with MetaboAnalyst software. Compared with MF feeding, at PND 21, HM feeding resulted in a higher abundance of fucose in the jejunum and urine and a greater concentration of myo-inositol in serum. In HM-fed piglets, 1,5-anhydroglucitol was higher in the duodenum, serum, and urine at PND 21. Additionally, the HM group had higher levels of urinary kynurenic acid at PND 21. Correlations between bacterial genera and altered metabolites in ileum revealed that Turicibacter sp. and Campylobacter sp. were positively correlated with maltotriose and panose at PND 21, while ileal Campylobacter sp. was negatively correlated with fumaric acid. At PND 51, no significant metabolites were identified between HM and MF diet groups. The metabolites associated with the neonatal diets may serve as the substrates and signals that contribute to the physiological effects in HM and MF during infancy, with a subset reflecting diet-associated differences in microbial metabolism and ecology. IMPORTANCE Exclusive HM feeding for newborns is recommended at least for the first 6 months of life. However, when breastfeeding is not possible, MF is recommended as a substitute. Due to the challenges associated with sample collection from infants fed HM or MF, their gut metabolism is poorly understood. Thus, an established piglet model from our team was used to determine the metabolite profile in relation to host, diet, and microbiota. The current study is the first to provide novel insights across the small intestine metabolism and its association with circulatory metabolites in the HM group relative to the MF group at the weaning and postweaning period. Data also demonstrate that during the neonatal period, diet, host, and microbial metabolism contribute to the lumen and circulatory metabolite profile. Furthermore, small intestinal lumen metabolome can be tracked in the urine as a biomarker of dietary differences, which would be a useful tool for clinical interventions.
format article
author Fernanda Rosa
Katelin S. Matazel
Ahmed A. Elolimy
Sean H. Adams
Anne Bowlin
Keith D. Williams
Lars Bode
Laxmi Yeruva
author_facet Fernanda Rosa
Katelin S. Matazel
Ahmed A. Elolimy
Sean H. Adams
Anne Bowlin
Keith D. Williams
Lars Bode
Laxmi Yeruva
author_sort Fernanda Rosa
title Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets
title_short Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets
title_full Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets
title_fullStr Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets
title_full_unstemmed Human Milk-Fed Piglets Have a Distinct Small Intestine and Circulatory Metabolome Profile Relative to That of Milk Formula-Fed Piglets
title_sort human milk-fed piglets have a distinct small intestine and circulatory metabolome profile relative to that of milk formula-fed piglets
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/bef707eb921f4a9caa76ef4988caac93
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