Polydextrose with and without Bifidobacterium animalis ssp. lactis 420 drives the prevalence of Akkermansia and improves liver health in a multi-compartmental obesogenic mice study

Christian Clement Yde; Henrik Max Jensen; Niels Christensen; Florence Servant; Benjamin Lelouvier; Sampo Lahtinen; Lotta K. Stenman; Kaisa Airaksinen; Henna-Maria Kailanto

doi:10.1371/journal.pone.0260765

Polydextrose with and without Bifidobacterium animalis ssp. lactis 420 drives the prevalence of Akkermansia and improves liver health in a multi-compartmental obesogenic mice study

Christian Clement Yde^*
, Henrik Max Jensen
, Niels Christensen
, Florence Servant
, Benjamin Lelouvier
, Sampo Lahtinen
, Lotta K. Stenman
, Kaisa Airaksinen
, Henna-Maria Kailanto

^*Corresponding author for this work

Department of Food Science

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

17 Citations (Scopus)

Abstract

The past two decades of research have raised gut microbiota composition as a contributing factor to the development of obesity, and higher abundance of certain bacterial species has been linked to the lean phenotype, such as Akkermansia muciniphila. The ability of pre- and probiotics to affect metabolic health could be via microbial community alterations and subsequently changes in metabolite profiles, modulating for example host energy balance via complex signaling pathways. The aim of this mice study was to determine how administration of a prebiotic fiber, polydextrose (PDX) and a probiotic Bifidobacterium animalis ssp. lactis 420 (B420), during high fat diet (HFD; 60 kcal% fat) affects microbiota composition in the gastrointestinal tract and adipose tissue, and metabolite levels in gut and liver. In this study C57Bl/6J mice (N = 200) were split in five treatments and daily gavaged: 1) Normal control (NC); 2) HFD; 3) HFD + PDX; 4) HFD + B420 or 5) HFD + PDX + B420 (HFD+S). At six weeks of treatment intraperitoneal glucose-tolerance test (IPGTT) was performed, and feces were collected at weeks 0, 3, 6 and 9. At end of the intervention, ileum and colon mucosa, adipose tissue and liver samples were collected. The microbiota composition in fecal, ileum, colon and adipose tissue was analyzed using 16S rDNA sequencing, fecal and liver metabolomics were performed by nuclear magnetic resonance (NMR) spectroscopy. It was found that HFD+PDX intervention reduced body weight gain and hepatic fat compared to HFD. Sequencing the mice adipose tissue (MAT) identified Akkermansia and its prevalence was increased in HFD+S group. Furthermore, by the inclusion of PDX, fecal, lleum and colon levels of Akkermansia were increased and liver health was improved as the detoxification capacity and levels of methyl-donors were increased. These new results demonstrate how PDX and B420 can affect the interactions between gut, liver and adipose tissue.

Original language	English
Article number	e0260765
Journal	PLoS One
Volume	16
Issue	12
Number of pages	20
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0260765
Publication status	Published - Dec 2021

Keywords

BETAINE
CONSENSUS STATEMENT
DOUBLE-BLIND
GUT MICROBIOME
IMPACT
INTERNATIONAL SCIENTIFIC ASSOCIATION
OBESITY
OVERWEIGHT
SERUM METABOLOME
WEIGHT

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Yde, C. C., Jensen, H. M., Christensen, N., Servant, F., Lelouvier, B., Lahtinen, S., Stenman, L. K., Airaksinen, K., & Kailanto, H.-M. (2021). Polydextrose with and without Bifidobacterium animalis ssp. lactis 420 drives the prevalence of Akkermansia and improves liver health in a multi-compartmental obesogenic mice study. PLoS One, 16(12), Article e0260765. https://doi.org/10.1371/journal.pone.0260765

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title = "Polydextrose with and without Bifidobacterium animalis ssp. lactis 420 drives the prevalence of Akkermansia and improves liver health in a multi-compartmental obesogenic mice study",

abstract = "The past two decades of research have raised gut microbiota composition as a contributing factor to the development of obesity, and higher abundance of certain bacterial species has been linked to the lean phenotype, such as Akkermansia muciniphila. The ability of pre- and probiotics to affect metabolic health could be via microbial community alterations and subsequently changes in metabolite profiles, modulating for example host energy balance via complex signaling pathways. The aim of this mice study was to determine how administration of a prebiotic fiber, polydextrose (PDX) and a probiotic Bifidobacterium animalis ssp. lactis 420 (B420), during high fat diet (HFD; 60 kcal\% fat) affects microbiota composition in the gastrointestinal tract and adipose tissue, and metabolite levels in gut and liver. In this study C57Bl/6J mice (N = 200) were split in five treatments and daily gavaged: 1) Normal control (NC); 2) HFD; 3) HFD + PDX; 4) HFD + B420 or 5) HFD + PDX + B420 (HFD+S). At six weeks of treatment intraperitoneal glucose-tolerance test (IPGTT) was performed, and feces were collected at weeks 0, 3, 6 and 9. At end of the intervention, ileum and colon mucosa, adipose tissue and liver samples were collected. The microbiota composition in fecal, ileum, colon and adipose tissue was analyzed using 16S rDNA sequencing, fecal and liver metabolomics were performed by nuclear magnetic resonance (NMR) spectroscopy. It was found that HFD+PDX intervention reduced body weight gain and hepatic fat compared to HFD. Sequencing the mice adipose tissue (MAT) identified Akkermansia and its prevalence was increased in HFD+S group. Furthermore, by the inclusion of PDX, fecal, lleum and colon levels of Akkermansia were increased and liver health was improved as the detoxification capacity and levels of methyl-donors were increased. These new results demonstrate how PDX and B420 can affect the interactions between gut, liver and adipose tissue.",

keywords = "BETAINE, CONSENSUS STATEMENT, DOUBLE-BLIND, GUT MICROBIOME, IMPACT, INTERNATIONAL SCIENTIFIC ASSOCIATION, OBESITY, OVERWEIGHT, SERUM METABOLOME, WEIGHT",

author = "Yde, \{Christian Clement\} and Jensen, \{Henrik Max\} and Niels Christensen and Florence Servant and Benjamin Lelouvier and Sampo Lahtinen and Stenman, \{Lotta K.\} and Kaisa Airaksinen and Henna-Maria Kailanto",

year = "2021",

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doi = "10.1371/journal.pone.0260765",

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Yde, CC, Jensen, HM, Christensen, N, Servant, F, Lelouvier, B, Lahtinen, S, Stenman, LK, Airaksinen, K & Kailanto, H-M 2021, 'Polydextrose with and without Bifidobacterium animalis ssp. lactis 420 drives the prevalence of Akkermansia and improves liver health in a multi-compartmental obesogenic mice study', PLoS One, vol. 16, no. 12, e0260765. https://doi.org/10.1371/journal.pone.0260765

Polydextrose with and without Bifidobacterium animalis ssp. lactis 420 drives the prevalence of Akkermansia and improves liver health in a multi-compartmental obesogenic mice study. / Yde, Christian Clement; Jensen, Henrik Max; Christensen, Niels et al.
In: PLoS One, Vol. 16, No. 12, e0260765, 12.2021.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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AU - Yde, Christian Clement

AU - Jensen, Henrik Max

AU - Christensen, Niels

AU - Servant, Florence

AU - Lelouvier, Benjamin

AU - Lahtinen, Sampo

AU - Stenman, Lotta K.

AU - Airaksinen, Kaisa

AU - Kailanto, Henna-Maria

PY - 2021/12

Y1 - 2021/12

N2 - The past two decades of research have raised gut microbiota composition as a contributing factor to the development of obesity, and higher abundance of certain bacterial species has been linked to the lean phenotype, such as Akkermansia muciniphila. The ability of pre- and probiotics to affect metabolic health could be via microbial community alterations and subsequently changes in metabolite profiles, modulating for example host energy balance via complex signaling pathways. The aim of this mice study was to determine how administration of a prebiotic fiber, polydextrose (PDX) and a probiotic Bifidobacterium animalis ssp. lactis 420 (B420), during high fat diet (HFD; 60 kcal% fat) affects microbiota composition in the gastrointestinal tract and adipose tissue, and metabolite levels in gut and liver. In this study C57Bl/6J mice (N = 200) were split in five treatments and daily gavaged: 1) Normal control (NC); 2) HFD; 3) HFD + PDX; 4) HFD + B420 or 5) HFD + PDX + B420 (HFD+S). At six weeks of treatment intraperitoneal glucose-tolerance test (IPGTT) was performed, and feces were collected at weeks 0, 3, 6 and 9. At end of the intervention, ileum and colon mucosa, adipose tissue and liver samples were collected. The microbiota composition in fecal, ileum, colon and adipose tissue was analyzed using 16S rDNA sequencing, fecal and liver metabolomics were performed by nuclear magnetic resonance (NMR) spectroscopy. It was found that HFD+PDX intervention reduced body weight gain and hepatic fat compared to HFD. Sequencing the mice adipose tissue (MAT) identified Akkermansia and its prevalence was increased in HFD+S group. Furthermore, by the inclusion of PDX, fecal, lleum and colon levels of Akkermansia were increased and liver health was improved as the detoxification capacity and levels of methyl-donors were increased. These new results demonstrate how PDX and B420 can affect the interactions between gut, liver and adipose tissue.

AB - The past two decades of research have raised gut microbiota composition as a contributing factor to the development of obesity, and higher abundance of certain bacterial species has been linked to the lean phenotype, such as Akkermansia muciniphila. The ability of pre- and probiotics to affect metabolic health could be via microbial community alterations and subsequently changes in metabolite profiles, modulating for example host energy balance via complex signaling pathways. The aim of this mice study was to determine how administration of a prebiotic fiber, polydextrose (PDX) and a probiotic Bifidobacterium animalis ssp. lactis 420 (B420), during high fat diet (HFD; 60 kcal% fat) affects microbiota composition in the gastrointestinal tract and adipose tissue, and metabolite levels in gut and liver. In this study C57Bl/6J mice (N = 200) were split in five treatments and daily gavaged: 1) Normal control (NC); 2) HFD; 3) HFD + PDX; 4) HFD + B420 or 5) HFD + PDX + B420 (HFD+S). At six weeks of treatment intraperitoneal glucose-tolerance test (IPGTT) was performed, and feces were collected at weeks 0, 3, 6 and 9. At end of the intervention, ileum and colon mucosa, adipose tissue and liver samples were collected. The microbiota composition in fecal, ileum, colon and adipose tissue was analyzed using 16S rDNA sequencing, fecal and liver metabolomics were performed by nuclear magnetic resonance (NMR) spectroscopy. It was found that HFD+PDX intervention reduced body weight gain and hepatic fat compared to HFD. Sequencing the mice adipose tissue (MAT) identified Akkermansia and its prevalence was increased in HFD+S group. Furthermore, by the inclusion of PDX, fecal, lleum and colon levels of Akkermansia were increased and liver health was improved as the detoxification capacity and levels of methyl-donors were increased. These new results demonstrate how PDX and B420 can affect the interactions between gut, liver and adipose tissue.

KW - BETAINE

KW - CONSENSUS STATEMENT

KW - DOUBLE-BLIND

KW - GUT MICROBIOME

KW - IMPACT

KW - INTERNATIONAL SCIENTIFIC ASSOCIATION

KW - OBESITY

KW - OVERWEIGHT

KW - SERUM METABOLOME

KW - WEIGHT

U2 - 10.1371/journal.pone.0260765

DO - 10.1371/journal.pone.0260765

M3 - Journal article

C2 - 34855861

SN - 1932-6203

VL - 16

JO - PLoS One

JF - PLoS One

IS - 12

M1 - e0260765

ER -