{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T00:13:19Z","timestamp":1793923999658,"version":"4.8.0"},"reference-count":46,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T00:00:00Z","timestamp":1587427200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"DOI":"10.3389\/fcimb.2020.00160","type":"journal-article","created":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T00:21:55Z","timestamp":1587428515000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":149,"title":["Gut Microbiome Reveals Specific Dysbiosis in Primary Osteoporosis"],"prefix":"10.3389","volume":"10","author":[{"given":"Zhiming","family":"Xu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zheng","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianguang","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shilei","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yangyang","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chengxiang","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xing","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bicheng","family":"Xia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lingyang","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caijuan","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Feng","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guofu","family":"Pi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2020,4,21]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.maturitas.2017.06.025","article-title":"Estrogen-gut microbiome axis: physiological and clinical implications","volume":"103","author":"Baker","year":"2017","journal-title":"Maturitas"},{"key":"B2","doi-asserted-by":"publisher","first-page":"e00770","DOI":"10.1128\/mBio.00770-17","article-title":"Microbial metabolic networks at the mucus layer lead to diet-independent butyrate and Vitamin B12 production by intestinal symbionts","volume":"8","author":"Belzer","year":"2017","journal-title":"MBio"},{"key":"B3","doi-asserted-by":"publisher","first-page":"100946","DOI":"10.1016\/j.arr.2019.100946","article-title":"Gut microbiota and osteoarthritis management: an expert consensus of the European society for clinical and economic aspects of osteoporosis, osteoarthritis and musculoskeletal diseases (ESCEO)","volume":"55","author":"Biver","year":"2019","journal-title":"Ageing Res. Rev."},{"key":"B4","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1056\/NEJMcp1513724","article-title":"Clinical practice. Postmenopausal osteoporosis","volume":"374","author":"Black","year":"2016","journal-title":"N. Engl. J. Med."},{"key":"B5","doi-asserted-by":"publisher","first-page":"S15","DOI":"10.1038\/550S15a","article-title":"Osteoporosis: staying strong","volume":"550","author":"Brown","year":"2017","journal-title":"Nature"},{"key":"B6","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1007\/s40618-014-0236-9","article-title":"Perspectives on osteoporosis therapies","volume":"38","author":"Cairoli","year":"2015","journal-title":"J. Endocrinol. Invest."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1221","DOI":"10.1210\/me.2014-1108","article-title":"Minireview: gut microbiota: the neglected endocrine organ","volume":"28","author":"Clarke","year":"2014","journal-title":"Mol. Endocrinol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1077","DOI":"10.1023\/a:1010722314493","article-title":"Small intestine bacterial overgrowth and metabolic bone disease","volume":"46","author":"Di Stefano","year":"2001","journal-title":"Dig. Dis. Sci."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1635","DOI":"10.1126\/science.1110591","article-title":"Diversity of the human intestinal microbial flora","volume":"308","author":"Eckburg","year":"2005","journal-title":"Science"},{"key":"B10","doi-asserted-by":"publisher","first-page":"C17","DOI":"10.7326\/AITC201708010","article-title":"Osteoporosis","volume":"167","author":"Ensrud","year":"2017","journal-title":"Ann. Intern. Med."},{"key":"B11","doi-asserted-by":"publisher","first-page":"e145878","DOI":"10.1371\/journal.pone.0145878","article-title":"Intestinal microbiota in patients with spinal cord injury","volume":"11","author":"Gungor","year":"2016","journal-title":"PLoS ONE"},{"key":"B12","doi-asserted-by":"publisher","first-page":"10","DOI":"10.3109\/13697137.2015.1101256","article-title":"Role of biochemical markers in the management of osteoporosis","volume":"18","author":"Henriksen","year":"2015","journal-title":"Climacteric"},{"key":"B13","doi-asserted-by":"publisher","first-page":"1638","DOI":"10.1002\/jbmr.2887","article-title":"Links between the microbiome and bone","volume":"31","author":"Hernandez","year":"2016","journal-title":"J. Bone Miner. Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.jbspin.2018.02.008","article-title":"Gut microbiome and bone","volume":"86","author":"Ib\u00e1\u00f1ez","year":"2019","journal-title":"Joint Bone Spine"},{"key":"B15","doi-asserted-by":"publisher","first-page":"8787","DOI":"10.3748\/wjg.v21.i29.8787","article-title":"Role of the normal gut microbiota","volume":"21","author":"Jandhyala","year":"2015","journal-title":"World J. Gastroenterol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"2471","DOI":"10.1099\/ijs.0.63715-0","article-title":"Dialister micraerophilus sp. nov. and dialister propionicifaciens sp. nov., isolated from human clinical samples","volume":"55","author":"Jumas-Bilak","year":"2005","journal-title":"Int. J. Syst. Evol. Micr."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1934","DOI":"10.1248\/bpb.b17-00482","article-title":"Effects of the antiepileptic drugs phenytoin, gabapentin, and levetiracetam on bone strength, bone mass, and bone turnover in rats","volume":"40","author":"Kanda","year":"2017","journal-title":"Biol. Pharm. Bull."},{"key":"B18","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1016\/j.archoralbio.2008.02.016","article-title":"Sodium butyrate stimulates mineralized nodule formation and osteoprotegerin expression by human osteoblasts","volume":"53","author":"Katono","year":"2008","journal-title":"Arch. Oral Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1007\/978-3-319-56895-9_3","article-title":"Cell membrane transport mechanisms: ion channels and electrical properties of cell membranes","volume":"227","author":"Kulbacka","year":"2017","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1481","DOI":"10.1016\/j.cell.2017.11.024","article-title":"Our gut microbiome: the evolving inner self","volume":"171","author":"Kundu","year":"2017","journal-title":"Cell"},{"key":"B21","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1186\/s12934-017-0691-z","article-title":"Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria","volume":"16","author":"LeBlanc","year":"2017","journal-title":"Microb. Cell Fact."},{"key":"B22","doi-asserted-by":"publisher","first-page":"2432","DOI":"10.1210\/me.2006-0061","article-title":"Histone deacetylase 1-mediated histone modification regulates osteoblast differentiation","volume":"20","author":"Lee","year":"2006","journal-title":"Mol. Endocrinol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"748","DOI":"10.3390\/genes10100748","article-title":"Comparative analysis of fecal microbiota composition between rheumatoid arthritis and osteoarthritis patients","volume":"10","author":"Lee","year":"2019","journal-title":"Genes"},{"key":"B24","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1111\/joim.12369","article-title":"Osteoporosis: the evolution of a diagnosis","volume":"277","author":"Lorentzon","year":"2015","journal-title":"J. Intern. Med."},{"key":"B25","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1038\/s41467-017-02490-4","article-title":"Short-chain fatty acids regulate systemic bone mass and protect from pathologicalbone loss","volume":"9","author":"Lucas","year":"2018","journal-title":"Nat. Commun."},{"key":"B26","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/ismej.2012.104","article-title":"Gut microbiome composition is linked to whole grain-induced immunological improvements","volume":"7","author":"Mart\u00ednez","year":"2013","journal-title":"ISME J."},{"key":"B27","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.mib.2013.06.003","article-title":"Faecalibacterium prausnitzii and human intestinal health","volume":"16","author":"Miquel","year":"2013","journal-title":"Curr. Opin. Microbiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"4498","DOI":"10.1128\/AAC.00538-07","article-title":"Antimicrobial susceptibilities and clinical sources of dialister species","volume":"51","author":"Morio","year":"2007","journal-title":"Antimicrob. Agents Chemother."},{"key":"B29","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.tem.2014.11.004","article-title":"Effects of the gut microbiota on bone mass","volume":"26","author":"Ohlsson","year":"2015","journal-title":"Trends Endocrinol. Metab."},{"key":"B30","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/j.tem.2016.10.007","article-title":"GPCR signaling and trafficking: the long and short of it","volume":"28","author":"Pavlos","year":"2017","journal-title":"Trends Endocrinol. Metab."},{"key":"B31","doi-asserted-by":"publisher","first-page":"818","DOI":"10.7326\/M15-1361","article-title":"Treatment of low bone density or osteoporosis to prevent fractures in men andwomen: a clinical practice guideline update from the American college of physicians","volume":"166","author":"Qaseem","year":"2017","journal-title":"Ann. Intern. Med."},{"key":"B32","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1038\/nature08821","article-title":"A human gut microbial gene catalogue established by metagenomic sequencing","volume":"464","author":"Qin","year":"2010","journal-title":"Nature"},{"key":"B33","doi-asserted-by":"publisher","first-page":"4502","DOI":"10.3390\/ijms20184502","article-title":"The endocrine function of osteocalcin regulated by bone resorption: a lesson from reduced and increased bone mass diseases","volume":"20","author":"Rossi","year":"2019","journal-title":"Int. J. Mol. Sci."},{"key":"B34","doi-asserted-by":"publisher","first-page":"859","DOI":"10.1152\/physrev.00045.2009","article-title":"Gut microbiota in health and disease","volume":"90","author":"Sekirov","year":"2010","journal-title":"Physiol. Rev."},{"key":"B35","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1080\/19490976.2017.1349041","article-title":"Gut microbiome in multiple sclerosis: the players involved and the roles they play","volume":"8","author":"Shahi","year":"2017","journal-title":"Gut Microbes"},{"key":"B36","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1034\/j.1399-302x.2002.170606.x","article-title":"Cytomegalovirus periodontal presence is associated with subgingival dialister pneumosintes and alveolar bone loss","volume":"17","author":"Slots","year":"2002","journal-title":"Oral Microbiol. Immunol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1007\/s12275-018-8238-5","article-title":"Progress of analytical tools and techniques for human gut microbiome research","volume":"56","author":"Song","year":"2018","journal-title":"J. Microbiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1021\/jo051687e","article-title":"Bone mineral density in patients with small intestinal bacterial overgrowth","volume":"50","author":"Stotzer","year":"2003","journal-title":"Hepatogastroenterology"},{"key":"B39","doi-asserted-by":"publisher","first-page":"8153","DOI":"10.1007\/s00253-018-9239-3","article-title":"Bacterial steroid hydroxylases: enzyme classes, their functions and comparison of their catalytic mechanisms","volume":"102","author":"Szaleniec","year":"2018","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1183","DOI":"10.1161\/CIRCRESAHA.117.309715","article-title":"Gut microbiota in cardiovascular health and disease","volume":"120","author":"Tang","year":"2017","journal-title":"Circ. Res."},{"key":"B41","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1002\/art.39802","article-title":"Brief report: dialister as a microbial marker of disease activity in spondyloarthritis","volume":"69","author":"Tito","year":"2017","journal-title":"Arthritis Rheumatol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1116","DOI":"10.1016\/j.immuni.2018.10.013","article-title":"The microbial metabolite butyrate stimulates bone formation via T regulatory cell-mediated regulation of WNT10B expression","volume":"49","author":"Tyagi","year":"2018","journal-title":"Immunity"},{"key":"B43","doi-asserted-by":"publisher","first-page":"4764","DOI":"10.1039\/c6fo01103a","article-title":"Sialoglycoprotein isolated from the eggs of Carassius auratus prevents bone loss:an effect associated with the regulation of gut microbiota in ovariectomizedrats","volume":"7","author":"Wang","year":"2016","journal-title":"Food Funct."},{"key":"B44","doi-asserted-by":"publisher","first-page":"e3450","DOI":"10.7717\/peerj.3450","article-title":"Diversity analysis of gut microbiota in osteoporosis and osteopenia patients","volume":"5","author":"Wang","year":"2017","journal-title":"Peer J."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1651","DOI":"10.1007\/s00198-009-0925-y","article-title":"Osteoporosis in china","volume":"20","author":"Wang","year":"2009","journal-title":"Osteoporosis Int."},{"key":"B46","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1007\/s11914-017-0382-z","article-title":"Gut microbiome and bone: to build, destroy, or both?","volume":"15","author":"Yan","year":"2017","journal-title":"Curr. Osteoporos. Rep."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fcimb.2020.00160\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T00:21:57Z","timestamp":1587428517000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fcimb.2020.00160\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,21]]},"references-count":46,"alternative-id":["10.3389\/fcimb.2020.00160"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2020.00160","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,21]]},"article-number":"160"}}