{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T18:11:19Z","timestamp":1788372679308,"version":"build-2803163510"},"reference-count":57,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2024,8,6]],"date-time":"2024-08-06T00:00:00Z","timestamp":1722902400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Increasing evidence has shown that gut microbiota (GM) was involved in the pathophysiology of musculoskeletal disorders through multiple pathways such as protein anabolism, chronic inflammation and immunity, and imbalanced metabolism. We performed a systematic review and meta-analysis of human studies to evaluate GM diversity differences between individuals with and without sarcopenia, and explore bacteria with potential to become biomarkers. PubMed, Embase and Cochrane library were systematically searched from inception to February 16, 2024. Studies were included if they (1) sampled adults with sarcopenia, and (2) performed GM analysis and reported \u03b1-diversity, \u03b2-diversity or relative abundance. The methodological quality of included studies and the certainty of evidence were assessed through the Joanna Briggs Institute critical appraisal checklist for analytical cross-sectional studies and the Grades of Recommendation, Assessment, Development and Evaluation (GRADE) Working Group system, respectively. Weighted standardized mean differences (SMDs) and corresponding 95% confidence intervals (CIs) were estimated for \u03b1-diversity indices using a fixed-effects and a random-effects model. Beta diversity and the relative abundance of GM were summarized qualitatively. A total of 19 studies involving 6,565 participants were included in this study. Compared with controls, significantly moderate decrease in microbial richness in participants with sarcopenia were found (Chao1: SMD = -0.44; 95%CI, -0.64 to -0.23, <jats:italic>I<\/jats:italic><jats:sup><jats:italic>2<\/jats:italic><\/jats:sup> = 57.23%, 13 studies; observed species: SMD = -0.68; 95%CI, -1.00 to -0.37, <jats:italic>I<\/jats:italic><jats:sup><jats:italic>2<\/jats:italic><\/jats:sup> = 66.07%, 5 studies; ACE index: SMD = -0.30; 95%CI, -0.56 to -0.04, <jats:italic>I<\/jats:italic><jats:sup><jats:italic>2<\/jats:italic><\/jats:sup> = 8.12%, 4 studies), with very low certainty of evidence. Differences in <jats:italic>\u03b2<\/jats:italic>-diversity were consistently observed in 84.6% of studies and 97.3% of participants. The detailed analysis of the gut microbial differential abundance identified a loss of <jats:italic>Prevotellaceae<\/jats:italic>, <jats:italic>Prevotella<\/jats:italic>, and <jats:italic>Megamonas<\/jats:italic> in sarcopenia compared with non-sarcopenia. In conclusion, sarcopenia was found to be associated with reduced richness of GM, and supplementing intestinal bacteria described above may contribute to preventing and treating this muscle disease. The research protocol was registered and approved in PROSPERO (CRD42023412849).<\/jats:p>","DOI":"10.1371\/journal.pone.0308360","type":"journal-article","created":{"date-parts":[[2024,8,6]],"date-time":"2024-08-06T17:23:25Z","timestamp":1722965005000},"page":"e0308360","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":10,"title":["Gut microbial composition is altered in sarcopenia: A systematic review and meta-analysis of clinical studies"],"prefix":"10.1371","volume":"19","author":[{"given":"Xiaohong","family":"Mai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuyi","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qifeng","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3782-4831","authenticated-orcid":true,"given":"Kangkang","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,8,6]]},"reference":[{"issue":"3","key":"pone.0308360.ref001","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/j.jamda.2019.12.012","article-title":"Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment","volume":"21","author":"LK Chen","year":"2020","journal-title":"Journal of the American Medical Directors Association"},{"issue":"1","key":"pone.0308360.ref002","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1093\/ageing\/afy169","article-title":"Sarcopenia: revised European consensus on definition and diagnosis","volume":"48","author":"AJ Cruz-Jentoft","year":"2019","journal-title":"Age and ageing"},{"issue":"3","key":"pone.0308360.ref003","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1002\/jcsm.12411","article-title":"Sarcopenia and its association with falls and fractures in older adults: A systematic review and meta-analysis","volume":"10","author":"SSY Yeung","year":"2019","journal-title":"Journal of cachexia, sarcopenia and muscle"},{"key":"pone.0308360.ref004","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.exger.2017.06.008","article-title":"Is sarcopenia associated with an increased risk of all-cause mortality and functional disability?","volume":"96","author":"GA Kelley","year":"2017","journal-title":"Experimental gerontology"},{"issue":"2","key":"pone.0308360.ref005","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1002\/jcsm.12149","article-title":"Validation of the SarQoL\u00ae, a specific health-related quality of life questionnaire for Sarcopenia","volume":"8","author":"C Beaudart","year":"2017","journal-title":"Journal of cachexia, sarcopenia and muscle"},{"issue":"6","key":"pone.0308360.ref006","article-title":"Pathogenesis, Intervention, and Current Status of Drug Development for Sarcopenia: A Review","volume":"11","author":"JY Jang","year":"2023","journal-title":"Biomedicines"},{"issue":"8","key":"pone.0308360.ref007","doi-asserted-by":"crossref","DOI":"10.3390\/nu14081537","article-title":"Prevalence of Undernutrition, Frailty and Sarcopenia in Community-Dwelling People Aged 50 Years and Above: Systematic Review and Meta-Analysis","volume":"14","author":"N Almohaisen","year":"2022","journal-title":"Nutrients"},{"key":"pone.0308360.ref008","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1146\/annurev-nutr-072610-145146","article-title":"Interaction between obesity and the gut microbiota: relevance in nutrition","volume":"31","author":"NM Delzenne","year":"2011","journal-title":"Annual review of nutrition"},{"issue":"4","key":"pone.0308360.ref009","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1007\/s11154-019-09512-0","article-title":"Dietary lipids, gut microbiota and lipid metabolism","volume":"20","author":"M Schoeler","year":"2019","journal-title":"Reviews in endocrine & metabolic disorders"},{"issue":"7\u20138","key":"pone.0308360.ref010","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1016\/j.nut.2015.02.011","article-title":"The aromatic amino acid tryptophan stimulates skeletal muscle IGF1\/p70s6k\/mTor signaling in vivo and the expression of myogenic genes in vitro","volume":"31","author":"A Dukes","year":"2015","journal-title":"Nutrition (Burbank, Los Angeles County, Calif)"},{"issue":"502","key":"pone.0308360.ref011","doi-asserted-by":"crossref","DOI":"10.1126\/scitranslmed.aan5662","article-title":"The gut microbiota influences skeletal muscle mass and function in mice","volume":"11","author":"S Lahiri","year":"2019","journal-title":"Science translational medicine"},{"key":"pone.0308360.ref012","doi-asserted-by":"crossref","first-page":"101739","DOI":"10.1016\/j.arr.2022.101739","article-title":"Gut microbiota as a promising therapeutic target for age-related sarcopenia","volume":"81","author":"T Zhang","year":"2022","journal-title":"Ageing research reviews"},{"key":"pone.0308360.ref013","doi-asserted-by":"crossref","first-page":"j5145","DOI":"10.1136\/bmj.j5145","article-title":"The role of the gut microbiome in systemic inflammatory disease","volume":"360","author":"JC Clemente","year":"2018","journal-title":"BMJ (Clinical research ed)"},{"issue":"1","key":"pone.0308360.ref014","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1038\/s41579-020-0433-9","article-title":"Gut microbiota in human metabolic health and disease","volume":"19","author":"Y Fan","year":"2021","journal-title":"Nature reviews Microbiology"},{"issue":"4","key":"pone.0308360.ref015","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1007\/s00223-017-0345-5","article-title":"Gut Microbiota Contribute to Age-Related Changes in Skeletal Muscle Size, Composition, and Function: Biological Basis for a Gut-Muscle Axis","volume":"102","author":"GJ Grosicki","year":"2018","journal-title":"Calcified tissue international"},{"issue":"8","key":"pone.0308360.ref016","doi-asserted-by":"crossref","DOI":"10.3390\/nu11081765","article-title":"Age-Associated Changes in Gut Microbiota and Dietary Components Related with the Immune System in Adulthood and Old Age: A Cross-Sectional Study","volume":"11","author":"N Salazar","year":"2019","journal-title":"Nutrients"},{"issue":"12","key":"pone.0308360.ref017","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1007\/s00284-023-03480-0","article-title":"A Sedentary Lifestyle Changes the Composition and Predicted Functions of the Gut Bacterial and Fungal Microbiota of Subjects from the Same Company","volume":"80","author":"L Xu","year":"2023","journal-title":"Current microbiology"},{"key":"pone.0308360.ref018","doi-asserted-by":"crossref","first-page":"2407","DOI":"10.3389\/fmicb.2019.02407","article-title":"Rarefaction, Alpha Diversity, and Statistics","volume":"10","author":"AD Willis","year":"2019","journal-title":"Frontiers in microbiology"},{"issue":"2","key":"pone.0308360.ref019","doi-asserted-by":"crossref","DOI":"10.1093\/ageing\/afad018","article-title":"Higher dietary protein intake is associated with sarcopenia in older British twins","volume":"52","author":"M Ni Lochlainn","year":"2023","journal-title":"Age and ageing"},{"issue":"7","key":"pone.0308360.ref020","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1016\/j.clnu.2022.05.008","article-title":"Differences in the gut microbiome and reduced fecal butyrate in elders with low skeletal muscle mass","volume":"41","author":"DS Han","year":"2022","journal-title":"Clinical nutrition (Edinburgh, Scotland)"},{"issue":"10","key":"pone.0308360.ref021","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1016\/j.jclinepi.2009.06.006","article-title":"The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration","volume":"62","author":"A Liberati","year":"2009","journal-title":"J Clin Epidemiol"},{"issue":"7454","key":"pone.0308360.ref022","doi-asserted-by":"crossref","first-page":"1490","DOI":"10.1136\/bmj.328.7454.1490","article-title":"Grading quality of evidence and strength of recommendations","volume":"328","author":"D Atkins","year":"2004","journal-title":"BMJ (Clinical research ed)"},{"key":"pone.0308360.ref023","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1186\/1471-2288-14-135","article-title":"Estimating the sample mean and standard deviation from the sample size, median, range and\/or interquartile range","volume":"14","author":"X Wan","year":"2014","journal-title":"BMC medical research methodology"},{"issue":"1","key":"pone.0308360.ref024","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1111\/bdi.12682","article-title":"A step ahead: Exploring the gut microbiota in inpatients with bipolar disorder during a depressive episode","volume":"21","author":"A Painold","year":"2019","journal-title":"Bipolar disorders"},{"issue":"23","key":"pone.0308360.ref025","doi-asserted-by":"crossref","DOI":"10.3390\/ijms21238946","article-title":"The Gut-Muscle Axis in Older Subjects with Low Muscle Mass and Performance: A Proof of Concept Study Exploring Fecal Microbiota Composition and Function with Shotgun Metagenomics Sequencing","volume":"21","author":"A Ticinesi","year":"2020","journal-title":"Int J Mol Sci"},{"issue":"1","key":"pone.0308360.ref026","doi-asserted-by":"crossref","DOI":"10.3390\/nu12010065","article-title":"Gut Microbial, Inflammatory and Metabolic Signatures in Older People with Physical Frailty and Sarcopenia: Results from the BIOSPHERE Study","volume":"12","author":"A Picca","year":"2019","journal-title":"Nutrients"},{"key":"pone.0308360.ref027","doi-asserted-by":"crossref","first-page":"111927","DOI":"10.1016\/j.exger.2022.111927","article-title":"Sarcopenia in community-dwelling older adults is associated with the diversity and composition of the gut microbiota","volume":"167","author":"YA Lee","year":"2022","journal-title":"Experimental gerontology"},{"issue":"5","key":"pone.0308360.ref028","doi-asserted-by":"crossref","first-page":"2340","DOI":"10.1002\/jcsm.13037","article-title":"Population-based metagenomics analysis reveals altered gut microbiome in sarcopenia: data from the Xiangya Sarcopenia Study","volume":"13","author":"Y Wang","year":"2022","journal-title":"Journal of cachexia, sarcopenia and muscle"},{"issue":"1","key":"pone.0308360.ref029","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1007\/s12603-022-1875-8","article-title":"Association of Dental Caries with Muscle Mass, Muscle Strength, and Sarcopenia: A Community-Based Study","volume":"27","author":"Y Yang","year":"2023","journal-title":"The journal of nutrition, health & aging"},{"issue":"5","key":"pone.0308360.ref030","doi-asserted-by":"crossref","DOI":"10.3390\/nu15051266","article-title":"Bifidobacterium as a Potential Biomarker of Sarcopenia in Elderly Women","volume":"15","author":"Z Wang","year":"2023","journal-title":"Nutrients"},{"key":"pone.0308360.ref031","doi-asserted-by":"crossref","first-page":"105063","DOI":"10.1016\/j.archger.2023.105063","article-title":"Relationships between sarcopenia, nutrient intake, and gut microbiota in Chinese community-dwelling older women","volume":"113","author":"X Yan","year":"2023","journal-title":"Archives of gerontology and geriatrics"},{"key":"pone.0308360.ref032","doi-asserted-by":"crossref","first-page":"112376","DOI":"10.1016\/j.exger.2024.112376","article-title":"Alterations in the diversity, composition and function of the gut microbiota in Uyghur individuals with sarcopenia","volume":"187","author":"Q Zhang","year":"2024","journal-title":"Experimental gerontology"},{"issue":"1","key":"pone.0308360.ref033","doi-asserted-by":"crossref","first-page":"4628","DOI":"10.1038\/s41598-021-84031-0","article-title":"Alterations in intestinal microbiota diversity, composition, and function in patients with sarcopenia","volume":"11","author":"L Kang","year":"2021","journal-title":"Sci Rep"},{"issue":"3","key":"pone.0308360.ref034","first-page":"327","article-title":"The composition of the gut microbiome in patients with sarcopenia","volume":"47","author":"Y Wu","year":"2022","journal-title":"Turkish Journal of Biochemistry"},{"issue":"1","key":"pone.0308360.ref035","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1111\/ggi.14661","article-title":"Changes and correlation analysis of intestinal microflora composition, inflammatory index, and skeletal muscle mass in elderly patients with sarcopenia","volume":"24","author":"J Lou","year":"2024","journal-title":"Geriatrics & gerontology international"},{"issue":"1","key":"pone.0308360.ref036","doi-asserted-by":"crossref","first-page":"e1097","DOI":"10.1002\/iid3.1097","article-title":"Analysis of intestinal flora in elderly Uygur patients with sarcopenia","volume":"12","author":"Meilibana","year":"2024","journal-title":"Immunity, inflammation and disease"},{"issue":"6","key":"pone.0308360.ref037","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.1111\/liv.14876","article-title":"Characterization of the gut-liver-muscle axis in cirrhotic patients with sarcopenia","volume":"41","author":"FR Ponziani","year":"2021","journal-title":"Liver Int"},{"issue":"1","key":"pone.0308360.ref038","article-title":"Sarcopenia-related gut microbial changes are associated with the risk of complications in people with cirrhosis","volume":"5","author":"PC Lee","year":"2023","journal-title":"JHEP Reports"},{"issue":"8","key":"pone.0308360.ref039","doi-asserted-by":"crossref","first-page":"1899","DOI":"10.1007\/s11255-021-03056-6","article-title":"Characterization of the gut microbiota in hemodialysis patients with sarcopenia","volume":"54","author":"Q Zhou","year":"2022","journal-title":"Int Urol Nephrol"},{"key":"pone.0308360.ref040","doi-asserted-by":"crossref","first-page":"1127041","DOI":"10.3389\/fcimb.2023.1127041","article-title":"Characteristics of the fecal microbiome and metabolome in older patients with heart failure and sarcopenia","volume":"13","author":"J Peng","year":"2023","journal-title":"Front Cell Infect Microbiol"},{"issue":"7","key":"pone.0308360.ref041","doi-asserted-by":"crossref","DOI":"10.3390\/toxins13070472","article-title":"Association of Sarcopenia and Gut Microbiota Composition in Older Patients with Advanced Chronic Kidney Disease, Investigation of the Interactions with Uremic Toxins, Inflammation and Oxidative Stress","volume":"13","author":"E Margiotta","year":"2021","journal-title":"Toxins"},{"key":"pone.0308360.ref042","doi-asserted-by":"crossref","first-page":"813289","DOI":"10.3389\/fmicb.2021.813289","article-title":"Alterations of the Gut Microbiota in Patients With Severe Chronic Heart Failure","volume":"12","author":"W Sun","year":"2021","journal-title":"Frontiers in microbiology"},{"issue":"10","key":"pone.0308360.ref043","article-title":"Pathobiological Relationship of Excessive Dietary Intake of Choline\/L-Carnitine: A TMAO Precursor-Associated Aggravation in Heart Failure in Sarcopenic Patients","volume":"13","author":"MN Bin-Jumah","year":"2021","journal-title":"Nutrients"},{"issue":"6","key":"pone.0308360.ref044","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1111\/acel.12387","article-title":"The histone deacetylase inhibitor butyrate improves metabolism and reduces muscle atrophy during aging","volume":"14","author":"ME Walsh","year":"2015","journal-title":"Aging cell"},{"issue":"12","key":"pone.0308360.ref045","doi-asserted-by":"crossref","first-page":"e007198","DOI":"10.1161\/CIRCHEARTFAILURE.120.007198","article-title":"Skeletal Muscle Function, Structure, and Metabolism in Patients With Heart Failure With Reduced Ejection Fraction and Heart Failure With Preserved Ejection Fraction","volume":"13","author":"T Bekfani","year":"2020","journal-title":"Circ Heart Fail"},{"key":"pone.0308360.ref046","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.anaerobe.2018.10.009","article-title":"The gut microbiome of Mexican children affected by obesity","volume":"55","author":"O Maya-Lucas","year":"2019","journal-title":"Anaerobe"},{"key":"pone.0308360.ref047","doi-asserted-by":"crossref","first-page":"e10946","DOI":"10.7717\/peerj.10946","article-title":"Comparison of gut microbiota between adults with autism spectrum disorder and obese adults","volume":"9","author":"Q Zhang","year":"2021","journal-title":"PeerJ"},{"issue":"4","key":"pone.0308360.ref048","first-page":"308","article-title":"The human gut microbiota: Metabolism and perspective in obesity","volume":"9","author":"AC Gomes","year":"2018","journal-title":"Gut Microbes"},{"issue":"1","key":"pone.0308360.ref049","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1093\/ageing\/afy169","article-title":"Sarcopenia: revised European consensus on definition and diagnosis","volume":"48","author":"AJ Cruz-Jentoft","year":"2019","journal-title":"Age and ageing"},{"key":"pone.0308360.ref050","doi-asserted-by":"crossref","first-page":"696186","DOI":"10.3389\/fcimb.2021.696186","article-title":"Altered Fecal Microbiota Composition in Older Adults With Frailty","volume":"11","author":"Y Xu","year":"2021","journal-title":"Frontiers in cellular and infection microbiology"},{"key":"pone.0308360.ref051","doi-asserted-by":"crossref","first-page":"101744","DOI":"10.1016\/j.arr.2022.101744","article-title":"Differential gut microbiota and intestinal permeability between frail and healthy older adults: A systematic review","volume":"82","author":"NH Rashidah","year":"2022","journal-title":"Ageing research reviews"},{"issue":"1","key":"pone.0308360.ref052","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.1038\/s41598-017-17851-8","article-title":"Comparative analyses of fecal microbiota in Chinese isolated Yao population, minority Zhuang and rural Han by 16sRNA sequencing","volume":"8","author":"M Liao","year":"2018","journal-title":"Scientific reports"},{"issue":"6","key":"pone.0308360.ref053","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1038\/s41591-019-0458-7","article-title":"Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer","volume":"25","author":"S Yachida","year":"2019","journal-title":"Nature medicine"},{"key":"pone.0308360.ref054","doi-asserted-by":"crossref","first-page":"e01202","DOI":"10.7554\/eLife.01202","article-title":"Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis","volume":"2","author":"JU Scher","year":"2013","journal-title":"eLife"},{"issue":"1","key":"pone.0308360.ref055","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/mi.2015.33","article-title":"Gut dendritic cell activation links an altered colonic microbiome to mucosal and systemic T-cell activation in untreated HIV-1 infection","volume":"9","author":"SM Dillon","year":"2016","journal-title":"Mucosal immunology"},{"key":"pone.0308360.ref056","doi-asserted-by":"crossref","first-page":"110722","DOI":"10.1016\/j.exger.2019.110722","article-title":"Muscle strength is increased in mice that are colonized with microbiota from high-functioning older adults","volume":"127","author":"RA Fielding","year":"2019","journal-title":"Experimental gerontology"},{"issue":"12","key":"pone.0308360.ref057","doi-asserted-by":"crossref","first-page":"1913","DOI":"10.1136\/gutjnl-2013-306541","article-title":"Exercise and associated dietary extremes impact on gut microbial diversity","volume":"63","author":"SF Clarke","year":"2014","journal-title":"Gut"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0308360","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,6]],"date-time":"2024-08-06T17:23:54Z","timestamp":1722965034000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0308360"}},"subtitle":[],"editor":[{"given":"Masoud","family":"Rahmati","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,8,6]]},"references-count":57,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2024,8,6]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0308360","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,6]]}}}