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Role of the microbiome in regulating bone metabolism and susceptibility to osteoporosis

Role of the microbiome in regulating bone metabolism and susceptibility to osteoporosis
Role of the microbiome in regulating bone metabolism and susceptibility to osteoporosis

The human microbiota functions at the interface between diet, medication-use, lifestyle, host immune development and health. It is therefore closely aligned with many of the recognised modifiable factors that influence bone mass accrual in the young, and bone maintenance and skeletal decline in older populations. While understanding of the relationship between micro-organisms and bone health is still in its infancy, two decades of broader microbiome research and discovery supports a role of the human gut microbiome in the regulation of bone metabolism and pathogenesis of osteoporosis as well as its prevention and treatment. Pre-clinical research has demonstrated biological interactions between the microbiome and bone metabolism. Furthermore, observational studies and randomized clinical trials have indicated that therapeutic manipulation of the microbiota by oral administration of probiotics may influence bone turnover and prevent bone loss in humans. In this paper, we summarize the content, discussion and conclusions of a workshop held by the Osteoporosis and Bone Research Academy of the Royal Osteoporosis Society in October, 2020. We provide a detailed review of the literature examining the relationship between the microbiota and bone health in animal models and in humans, as well as formulating the agenda for key research priorities required to advance this field. We also underscore the potential pitfalls in this research field that should be avoided and provide methodological recommendations to facilitate bridging the gap from promising concept to a potential cause and intervention target for osteoporosis.

Immunology, Microbiome, Osteoporosis, Probiotics
0171-967X
Cronin, Owen
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Lanham-New, Susan
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Corfe, Bernard M.
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Gregson, Celia L.
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Darling, Andrea L.
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Ahmadi, Kourosh R
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Gibson, Philippa S.
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Tobias, Jonathan H.
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Ward, Kate
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Traka, Maria H.
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Rossi, Megan
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Williams, Claire
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Harvey, Nicholas
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Cooper, Cyrus
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Whelan, Kevin
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Uitterlinden, André G.
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O'Toole, Paul W.
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Ohlsson, Claes
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Compston, Juliet E.
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Ralston, Stuart H.
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Cronin, Owen
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Lanham-New, Susan
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Corfe, Bernard M.
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Gregson, Celia L.
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Darling, Andrea L.
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Ahmadi, Kourosh R
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Gibson, Philippa S.
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Tobias, Jonathan H.
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Ward, Kate
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Traka, Maria H.
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Rossi, Megan
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Williams, Claire
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Harvey, Nicholas
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Cooper, Cyrus
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Whelan, Kevin
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Uitterlinden, André G.
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O'Toole, Paul W.
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Ohlsson, Claes
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Compston, Juliet E.
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Ralston, Stuart H.
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Cronin, Owen, Lanham-New, Susan, Corfe, Bernard M., Gregson, Celia L., Darling, Andrea L., Ahmadi, Kourosh R, Gibson, Philippa S., Tobias, Jonathan H., Ward, Kate, Traka, Maria H., Rossi, Megan, Williams, Claire, Harvey, Nicholas, Cooper, Cyrus, Whelan, Kevin, Uitterlinden, André G., O'Toole, Paul W., Ohlsson, Claes, Compston, Juliet E. and Ralston, Stuart H. (2021) Role of the microbiome in regulating bone metabolism and susceptibility to osteoporosis. Calcified Tissue International. (doi:10.1007/s00223-021-00924-2).

Record type: Article

Abstract

The human microbiota functions at the interface between diet, medication-use, lifestyle, host immune development and health. It is therefore closely aligned with many of the recognised modifiable factors that influence bone mass accrual in the young, and bone maintenance and skeletal decline in older populations. While understanding of the relationship between micro-organisms and bone health is still in its infancy, two decades of broader microbiome research and discovery supports a role of the human gut microbiome in the regulation of bone metabolism and pathogenesis of osteoporosis as well as its prevention and treatment. Pre-clinical research has demonstrated biological interactions between the microbiome and bone metabolism. Furthermore, observational studies and randomized clinical trials have indicated that therapeutic manipulation of the microbiota by oral administration of probiotics may influence bone turnover and prevent bone loss in humans. In this paper, we summarize the content, discussion and conclusions of a workshop held by the Osteoporosis and Bone Research Academy of the Royal Osteoporosis Society in October, 2020. We provide a detailed review of the literature examining the relationship between the microbiota and bone health in animal models and in humans, as well as formulating the agenda for key research priorities required to advance this field. We also underscore the potential pitfalls in this research field that should be avoided and provide methodological recommendations to facilitate bridging the gap from promising concept to a potential cause and intervention target for osteoporosis.

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Accepted/In Press date: 1 October 2021
e-pub ahead of print date: 6 December 2021
Published date: 6 December 2021
Additional Information: Funding Information: The workshop was supported by the Royal Osteoporosis Society’s (ROS). The authors would like to thank Dr. Kaumal Baig Mirza who assisted with drawing of the illustrations. Funding Information: Stuart H. Ralston reports non-personal fees from UCB, Pfizer, Abbvie, Cellgene, Kyowa-Kirin, Alexion, Amgen, Cellgene, Bristol Myers Squibb, Janssen-Cilag, Novartis, Eli Lilly, Thornton & Ross, Sanofi-Genzyme, Roche and Sandoz and grants from Kyowa Kirin and Astra Zeneca, outside the submitted work. NCH reports personal fees, consultancy, lecture fees and honoraria from Alliance for Better Bone Health, AMGEN, MSD, Eli Lilly, Servier, Shire, UCB, Consilient Healthcare, Kyowa Kirin and Internis Pharma, outside the submitted work. Cyrus Cooper reports consultancy, lecture fees and honoraria from AMGEN, GSK, Alliance for Better Bone Health, MSD, Eli Lilly, Pfizer, Novartis, Servier, Medtronic and Roche outside the scope of the submitted work. Kate A. Ward reports honoraria from Abbot Nutrition, Pfizer Healthcare outside the submitted work. Juliet E. Compston reports honoraria from Amgen and UCB outside the scope of the submitted work. CO is inventor of a patent concerning the use of probiotic strains for use in treatment or prevention of osteoporosis (EPA EP2981274A4). Owen Cronin, Susan A. Lanham‑New, Bernard M. Corfe, Celia L. Gregson, Andrea L. Darling, Kourosh R. Ahmadi, Philippa S. Gibson, Jon H. Tobias, Maria H. Traka, Megan Rossi, Claire Williams, Nicholas C. Harvey, Kevin Whelan, André G. Uitterlinden, and Paul W. O’Toole have no conflicts of interest to declare. Publisher Copyright: © 2021, The Author(s).
Keywords: Immunology, Microbiome, Osteoporosis, Probiotics

Identifiers

Local EPrints ID: 452081
URI: http://eprints.soton.ac.uk/id/eprint/452081
ISSN: 0171-967X
PURE UUID: b436d87e-e4fd-4193-a910-84234d7fc193
ORCID for Kate Ward: ORCID iD orcid.org/0000-0001-7034-6750
ORCID for Nicholas Harvey: ORCID iD orcid.org/0000-0002-8194-2512
ORCID for Cyrus Cooper: ORCID iD orcid.org/0000-0003-3510-0709

Catalogue record

Date deposited: 11 Nov 2021 17:32
Last modified: 29 Feb 2024 05:04

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Contributors

Author: Owen Cronin
Author: Susan Lanham-New
Author: Bernard M. Corfe
Author: Celia L. Gregson
Author: Andrea L. Darling
Author: Kourosh R Ahmadi
Author: Philippa S. Gibson
Author: Jonathan H. Tobias
Author: Kate Ward ORCID iD
Author: Maria H. Traka
Author: Megan Rossi
Author: Claire Williams
Author: Nicholas Harvey ORCID iD
Author: Cyrus Cooper ORCID iD
Author: Kevin Whelan
Author: André G. Uitterlinden
Author: Paul W. O'Toole
Author: Claes Ohlsson
Author: Juliet E. Compston
Author: Stuart H. Ralston

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