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Erschienen in: Osteoporosis International 5/2019

21.01.2019 | Original Article

Gut microbiota composition and bone mineral loss—epidemiologic evidence from individuals in Wuhan, China

verfasst von: C. Li, Q. Huang, R. Yang, Y. Dai, Y. Zeng, L. Tao, X. Li, J. Zeng, Q. Wang

Erschienen in: Osteoporosis International | Ausgabe 5/2019

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Abstract

Summary

We explored the association between gut microbiota composition and bone mineral loss in Chinese elderly people by high-throughput 16S ribosomal RNA (rRNA) gene sequencing. Compared with controls, a smaller number of operational taxonomic units (OTUs), several taxa with altered abundance, and specific functional pathways were found in individuals with low-bone mineral density (BMD).

Introduction

Gut microbiota plays important roles in human health and associates with a number of diseases. However, few studies explored its association with bone mineral loss in human.

Methods

We collected 102 fecal samples from each eligible individual belonging to low-BMD and control groups for high-throughput 16S rRNA gene sequencing.

Results

The low-BMD individuals had a smaller number of OTUs and bacterial taxa at each level. At the phylum level, Bacteroidetes were more abundant in the low-BMD group; Firmicutes were enriched in the control group; Firmicutes and Actinobacteria positively correlated and Bacteroidetes negatively correlated with the BMD and T-score in all subjects. At the family level, the abundance of Lachnospiraceae in low-BMD individuals reduced and positively correlated with BMD and T-score; meanwhile, BMD increased with increasing Bifidobacteriaceae. At the genus level, low-BMD individuals had decreased proportions of Roseburia compared with control ones (P < 0.05). Roseburia, Bifidobacterium, and Lactobacillus positively correlated with BMD and T-score. Furthermore, BMD increased with rising abundance of Bifidobacterium. Functional prediction revealed that 93 metabolic pathways significantly differed between the two groups (FDR-corrected P < 0.05). Most pathways, especially pathways related to LPS biosynthesis, were more abundant in low-BMD individuals than in control ones.

Conclusions

Several taxa with altered abundance and specific functional pathways were discovered in low-BMD individuals. Our findings provide novel epidemiologic evidence to elucidate the underlying microbiota-relevant mechanism in bone mineral loss and osteoporosis.
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Literatur
1.
Zurück zum Zitat Park JS, Choi SB, Rhee Y, Chung JW, Choi EY, Kim DW (2015) Parathyroid hormone, calcium, and sodium bridging between osteoporosis and hypertension in postmenopausal Korean women. Calcified Tissue Int 96:417–429CrossRef Park JS, Choi SB, Rhee Y, Chung JW, Choi EY, Kim DW (2015) Parathyroid hormone, calcium, and sodium bridging between osteoporosis and hypertension in postmenopausal Korean women. Calcified Tissue Int 96:417–429CrossRef
2.
Zurück zum Zitat Gass M, Dawson-Hughes B (2006) Preventing osteoporosis-related fractures: an overview. Am J Med 119:S3–s11CrossRefPubMed Gass M, Dawson-Hughes B (2006) Preventing osteoporosis-related fractures: an overview. Am J Med 119:S3–s11CrossRefPubMed
3.
Zurück zum Zitat Ilic K, Obradovic N, Vujasinovic-Stupar N (2013) The relationship among hypertension, antihypertensive medications, and osteoporosis: a narrative review. Calcified Tissue Int 92:217–227CrossRef Ilic K, Obradovic N, Vujasinovic-Stupar N (2013) The relationship among hypertension, antihypertensive medications, and osteoporosis: a narrative review. Calcified Tissue Int 92:217–227CrossRef
4.
Zurück zum Zitat Chung HJ, Cho L, Shin JS, Lee J, Ha IH, Park HJ, Lee SK (2014) Effects of JSOG-6 on protection against bone loss in ovariectomized mice through regulation of osteoblast differentiation and osteoclast formation. BMC Complem Altern M 14:184CrossRef Chung HJ, Cho L, Shin JS, Lee J, Ha IH, Park HJ, Lee SK (2014) Effects of JSOG-6 on protection against bone loss in ovariectomized mice through regulation of osteoblast differentiation and osteoclast formation. BMC Complem Altern M 14:184CrossRef
5.
Zurück zum Zitat Harada S, Rodan GA (2003) Control of osteoblast function and regulation of bone mass. Nature 423:349–355CrossRefPubMed Harada S, Rodan GA (2003) Control of osteoblast function and regulation of bone mass. Nature 423:349–355CrossRefPubMed
6.
Zurück zum Zitat Nieves JW, Barrett-Connor E, Siris ES, Zion M, Barlas S, Chen YT (2008) Calcium and vitamin D intake influence bone mass, but not short-term fracture risk, in Caucasian postmenopausal women from the National Osteoporosis Risk Assessment (NORA) study. Osteoporos Int 19:673–679CrossRefPubMed Nieves JW, Barrett-Connor E, Siris ES, Zion M, Barlas S, Chen YT (2008) Calcium and vitamin D intake influence bone mass, but not short-term fracture risk, in Caucasian postmenopausal women from the National Osteoporosis Risk Assessment (NORA) study. Osteoporos Int 19:673–679CrossRefPubMed
7.
Zurück zum Zitat Warensjo E, Byberg L, Melhus H, Gedeborg R, Mallmin H, Wolk A, Michaelsson K (2011) Dietary calcium intake and risk of fracture and osteoporosis: prospective longitudinal cohort study. Bmj 342:d1473CrossRefPubMedPubMedCentral Warensjo E, Byberg L, Melhus H, Gedeborg R, Mallmin H, Wolk A, Michaelsson K (2011) Dietary calcium intake and risk of fracture and osteoporosis: prospective longitudinal cohort study. Bmj 342:d1473CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Pollitzer WS, Anderson JJ (1989) Ethnic and genetic differences in bone mass: a review with a hereditary vs environmental perspective. Am J Clin Nutr 50:1244–1259CrossRefPubMed Pollitzer WS, Anderson JJ (1989) Ethnic and genetic differences in bone mass: a review with a hereditary vs environmental perspective. Am J Clin Nutr 50:1244–1259CrossRefPubMed
9.
Zurück zum Zitat Boudin E, Fijalkowski I, Hendrickx G, Van Hul W (2016) Genetic control of bone mass. Mol Cell Endocrinol 432:3–13CrossRefPubMed Boudin E, Fijalkowski I, Hendrickx G, Van Hul W (2016) Genetic control of bone mass. Mol Cell Endocrinol 432:3–13CrossRefPubMed
10.
Zurück zum Zitat Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Backhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367CrossRefPubMed Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Backhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367CrossRefPubMed
11.
Zurück zum Zitat Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651CrossRefPubMedPubMedCentral Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Nagpal R, Yadav H, Marotta F (2014) Gut microbiota: the next-gen frontier in preventive and therapeutic medicine? Front Med 1:15CrossRef Nagpal R, Yadav H, Marotta F (2014) Gut microbiota: the next-gen frontier in preventive and therapeutic medicine? Front Med 1:15CrossRef
15.
Zurück zum Zitat Hernandez CJ, Guss JD, Luna M, Goldring SR (2016) Links between the microbiome and bone. J Bone Miner Res 31:1638–1646CrossRefPubMed Hernandez CJ, Guss JD, Luna M, Goldring SR (2016) Links between the microbiome and bone. J Bone Miner Res 31:1638–1646CrossRefPubMed
16.
Zurück zum Zitat Yan J, Herzog JW, Tsang K, Brennan CA, Bower MA, Garrett WS, Sartor BR, Aliprantis AO, Charles JF (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. P Natl Acad Sci USA 113:E7554–E7563CrossRef Yan J, Herzog JW, Tsang K, Brennan CA, Bower MA, Garrett WS, Sartor BR, Aliprantis AO, Charles JF (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. P Natl Acad Sci USA 113:E7554–E7563CrossRef
17.
Zurück zum Zitat McCabe L, Britton RA, Parameswaran N (2015) Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr Osteoporos Rep 13:363–371CrossRefPubMedPubMedCentral McCabe L, Britton RA, Parameswaran N (2015) Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr Osteoporos Rep 13:363–371CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Wang J, Wang Y, Gao W, Wang B, Zhao H, Zeng Y, Ji Y, Hao D (2017) Diversity analysis of gut microbiota in osteoporosis and osteopenia patients. PeerJ 5:e3450CrossRefPubMedPubMedCentral Wang J, Wang Y, Gao W, Wang B, Zhao H, Zeng Y, Ji Y, Hao D (2017) Diversity analysis of gut microbiota in osteoporosis and osteopenia patients. PeerJ 5:e3450CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Expert Panel on Musculoskeletal I, Ward RJ, Roberts CC et al (2017) ACR Appropriateness Criteria® osteoporosis and bone mineral density. J Am Coll Radiol 14:S189–S202CrossRef Expert Panel on Musculoskeletal I, Ward RJ, Roberts CC et al (2017) ACR Appropriateness Criteria® osteoporosis and bone mineral density. J Am Coll Radiol 14:S189–S202CrossRef
20.
Zurück zum Zitat Qian J, Cai M, Gao J, Tang S, Xu L, Critchley JA (2010) Trends in smoking and quitting in China from 1993 to 2003: National Health Service Survey data. B World Health Organ 88:769–776CrossRef Qian J, Cai M, Gao J, Tang S, Xu L, Critchley JA (2010) Trends in smoking and quitting in China from 1993 to 2003: National Health Service Survey data. B World Health Organ 88:769–776CrossRef
21.
Zurück zum Zitat Fugmann M, Breier M, Rottenkolber M, Banning F, Ferrari U, Sacco V, Grallert H, Parhofer KG, Seissler J, Clavel T, Lechner A (2015) The stool microbiota of insulin resistant women with recent gestational diabetes, a high risk group for type 2 diabetes. Sci Rep 5:13212CrossRefPubMedPubMedCentral Fugmann M, Breier M, Rottenkolber M, Banning F, Ferrari U, Sacco V, Grallert H, Parhofer KG, Seissler J, Clavel T, Lechner A (2015) The stool microbiota of insulin resistant women with recent gestational diabetes, a high risk group for type 2 diabetes. Sci Rep 5:13212CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Mejia-Leon ME, Petrosino JF, Ajami NJ, Dominguez-Bello MG, de la Barca AM (2014) Fecal microbiota imbalance in Mexican children with type 1 diabetes. Sci Rep 4:3814CrossRefPubMedPubMedCentral Mejia-Leon ME, Petrosino JF, Ajami NJ, Dominguez-Bello MG, de la Barca AM (2014) Fecal microbiota imbalance in Mexican children with type 1 diabetes. Sci Rep 4:3814CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat de Vlaming R, Groenen PJ (2015) The current and future use of ridge regression for prediction in quantitative genetics. Biomed Res Int 2015:143712CrossRefPubMedPubMedCentral de Vlaming R, Groenen PJ (2015) The current and future use of ridge regression for prediction in quantitative genetics. Biomed Res Int 2015:143712CrossRefPubMedPubMedCentral
24.
25.
Zurück zum Zitat Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK (2014) Specialized metabolites from the microbiome in health and disease. Cell Metab 20:719–730CrossRefPubMedPubMedCentral Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK (2014) Specialized metabolites from the microbiome in health and disease. Cell Metab 20:719–730CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573CrossRefPubMed Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573CrossRefPubMed
27.
Zurück zum Zitat Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504:451–455CrossRefPubMedPubMedCentral Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504:451–455CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450CrossRefPubMed Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450CrossRefPubMed
29.
Zurück zum Zitat Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, Thangaraju M, Prasad PD, Manicassamy S, Munn DH, Lee JR, Offermanns S, Ganapathy V (2014) Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40:128–139CrossRefPubMedPubMedCentral Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, Thangaraju M, Prasad PD, Manicassamy S, Munn DH, Lee JR, Offermanns S, Ganapathy V (2014) Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40:128–139CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Aurigemma NC, Koltun KJ, VanEvery H, Rogers CJ, De Souza MJ (2018) Linking the gut microbiota to bone health in anorexia nervosa. Curr Osteoporos Rep 16:65–75CrossRefPubMed Aurigemma NC, Koltun KJ, VanEvery H, Rogers CJ, De Souza MJ (2018) Linking the gut microbiota to bone health in anorexia nervosa. Curr Osteoporos Rep 16:65–75CrossRefPubMed
31.
Zurück zum Zitat Li JY, Chassaing B, Tyagi AM, Vaccaro C, Luo T, Adams J, Darby TM, Weitzmann MN, Mulle JG, Gewirtz AT, Jones RM, Pacifici R (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126:2049–2063CrossRefPubMedPubMedCentral Li JY, Chassaing B, Tyagi AM, Vaccaro C, Luo T, Adams J, Darby TM, Weitzmann MN, Mulle JG, Gewirtz AT, Jones RM, Pacifici R (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126:2049–2063CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Ohlsson C, Engdahl C, Fak F, Andersson A, Windahl SH, Farman HH, Moverare-Skrtic S, Islander U, Sjogren K (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9:e92368CrossRefPubMedPubMedCentral Ohlsson C, Engdahl C, Fak F, Andersson A, Windahl SH, Farman HH, Moverare-Skrtic S, Islander U, Sjogren K (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9:e92368CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229:1822–1830CrossRefPubMedPubMedCentral Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229:1822–1830CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Tilg H, Moschen AR, Kaser A, Pines A, Dotan I (2008) Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57:684–694CrossRefPubMed Tilg H, Moschen AR, Kaser A, Pines A, Dotan I (2008) Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57:684–694CrossRefPubMed
35.
Zurück zum Zitat Harris L, Senagore P, Young VB, McCabe LR (2009) Inflammatory bowel disease causes reversible suppression of osteoblast and chondrocyte function in mice. Am J Physiol- Gastr L 296:G1020–G1029CrossRef Harris L, Senagore P, Young VB, McCabe LR (2009) Inflammatory bowel disease causes reversible suppression of osteoblast and chondrocyte function in mice. Am J Physiol- Gastr L 296:G1020–G1029CrossRef
36.
Zurück zum Zitat McCabe LR, Irwin R, Schaefer L, Britton RA (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 228:1793–1798CrossRefPubMedPubMedCentral McCabe LR, Irwin R, Schaefer L, Britton RA (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 228:1793–1798CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat Kimble RB, Bain S, Pacifici R (1997) The functional block of TNF but not of IL-6 prevents bone loss in ovariectomized mice. J Bone Miner Res 12:935–941CrossRefPubMed Kimble RB, Bain S, Pacifici R (1997) The functional block of TNF but not of IL-6 prevents bone loss in ovariectomized mice. J Bone Miner Res 12:935–941CrossRefPubMed
38.
Zurück zum Zitat Charatcharoenwitthaya N, Khosla S, Atkinson EJ, McCready LK, Riggs BL (2007) Effect of blockade of TNF-alpha and interleukin-1 action on bone resorption in early postmenopausal women. J Bone Miner Res 22:724–729CrossRefPubMed Charatcharoenwitthaya N, Khosla S, Atkinson EJ, McCready LK, Riggs BL (2007) Effect of blockade of TNF-alpha and interleukin-1 action on bone resorption in early postmenopausal women. J Bone Miner Res 22:724–729CrossRefPubMed
39.
40.
Zurück zum Zitat Kohn FR, Kung AH (1995) Role of endotoxin in acute inflammation induced by gram-negative bacteria: specific inhibition of lipopolysaccharide-mediated responses with an amino-terminal fragment of bactericidal/permeability-increasing protein. Infect Immun 63:333–339PubMedPubMedCentral Kohn FR, Kung AH (1995) Role of endotoxin in acute inflammation induced by gram-negative bacteria: specific inhibition of lipopolysaccharide-mediated responses with an amino-terminal fragment of bactericidal/permeability-increasing protein. Infect Immun 63:333–339PubMedPubMedCentral
41.
Zurück zum Zitat Cybulsky MI, Chan MK, Movat HZ (1988) Acute inflammation and microthrombosis induced by endotoxin, interleukin-1, and tumor necrosis factor and their implication in gram-negative infection. Lab Investig 58:365–378PubMed Cybulsky MI, Chan MK, Movat HZ (1988) Acute inflammation and microthrombosis induced by endotoxin, interleukin-1, and tumor necrosis factor and their implication in gram-negative infection. Lab Investig 58:365–378PubMed
42.
Zurück zum Zitat Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, Martino ME, Balmand S, Hudcovic T, Heddi A, Rieusset J, Kozakova H, Vidal H, Leulier F (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351:854–857CrossRefPubMed Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, Martino ME, Balmand S, Hudcovic T, Heddi A, Rieusset J, Kozakova H, Vidal H, Leulier F (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351:854–857CrossRefPubMed
43.
Zurück zum Zitat von Martels JZH, Sadaghian Sadabad M, Bourgonje AR, Blokzijl T, Dijkstra G, Faber KN, Harmsen HJM (2017) The role of gut microbiota in health and disease: in vitro modeling of host-microbe interactions at the aerobe-anaerobe interphase of the human gut. Anaerobe 44:3–12CrossRef von Martels JZH, Sadaghian Sadabad M, Bourgonje AR, Blokzijl T, Dijkstra G, Faber KN, Harmsen HJM (2017) The role of gut microbiota in health and disease: in vitro modeling of host-microbe interactions at the aerobe-anaerobe interphase of the human gut. Anaerobe 44:3–12CrossRef
Metadaten
Titel
Gut microbiota composition and bone mineral loss—epidemiologic evidence from individuals in Wuhan, China
verfasst von
C. Li
Q. Huang
R. Yang
Y. Dai
Y. Zeng
L. Tao
X. Li
J. Zeng
Q. Wang
Publikationsdatum
21.01.2019
Verlag
Springer London
Erschienen in
Osteoporosis International / Ausgabe 5/2019
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-019-04855-5

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