About the Authors:
Zhaowei Teng
Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing
Affiliations The Sixth Affiliated Hospital of Kunming Medical University, Yuxi, China, Yunnan Key Laboratory of Digital Orthopedics, The First People’s Hospital of Yunnan Province, Kunming, China
ORCID logo https://orcid.org/0000-0002-4843-8277
Yun Zhu
Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Software, Validation, Visualization, Writing – original draft
Affiliation: The Sixth Affiliated Hospital of Kunming Medical University, Yuxi, China
Xiaochao Yu
Roles Investigation, Methodology, Resources, Software, Validation, Visualization, Writing – original draft
Affiliation: The Sixth Affiliated Hospital of Kunming Medical University, Yuxi, China
Jie Liu
Roles Investigation, Methodology, Resources, Software, Validation, Visualization, Writing – original draft
Affiliation: Yunnan Key Laboratory of Digital Orthopedics, The First People’s Hospital of Yunnan Province, Kunming, China
Qing Long
Roles Investigation, Methodology, Resources, Software, Validation, Visualization, Writing – original draft
Affiliation: The Sixth Affiliated Hospital of Kunming Medical University, Yuxi, China
ORCID logo https://orcid.org/0000-0002-0034-8934
Yong Zeng
Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing
* E-mail: [email protected] (YZ); [email protected] (SL)
Affiliation: The Sixth Affiliated Hospital of Kunming Medical University, Yuxi, China
Sheng Lu
Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing
* E-mail: [email protected] (YZ); [email protected] (SL)
Affiliation: Yunnan Key Laboratory of Digital Orthopedics, The First People’s Hospital of Yunnan Province, Kunming, China
Introduction
Sarcopenia is a muscle disorder involving depletion of skeletal muscle mass with a risk of adverse outcomes, such as physical disability and poor quality of life [1], is associated with many clinical conditions, such as cancer, diabetes, rheumatoid arthritis, and osteopenia [2–4]. Osteopenia, defined by the World Health Organization that is a t-score between -1 to -2.5, is a clinical term used to describe a decrease in bone mineral density [5]. Projections estimate that over 47 million Americans will be afflicted with osteopenia [5, 6]. Thus osteopenia is one of the major public health problems globally, and the burden is extremely heavy.
Some studies have indicated that osteopenia is associated with an increased risk of sarcopenia [4, 7–16]. However, others have shown no significant association exists between sarcopenia and osteopenia [17–19]. Therefore, we performed a pooled analysis to assess the relationship between sarcopenia and osteopenia risk.
Methods
This analysis was conducted in accordance with the Meta-analysis of Observational Studies in Epidemiology guidelines and the Preferred Reporting Items for Systematic Reviews and Meta-analyses standards [20, 21].
Search strategy and selection of eligible studies
We systematically searched PubMed and Embase (from their inception to October 1, 2020) for studies conducted on the association between sarcopenia and osteopenia. Our core search keywords are as follows: “sarcopenia”, “osteopenia”, and “low bone mineral density”. Two researchers (TZW and ZY) independently reviewed the titles and abstracts of the studies retrieved from the databases. We included studies that reported sufficient data on sarcopenia increasing osteopenia risk, such as risk estimates (relative risks [RRs], odds ratios [ORs]) with 95% confidence intervals (CIs). The studies were assessed based on the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement [20]. All disagreements were resolved by discussion with the corresponding authors.
Data extraction and analysis
The data extraction and analysis were similar as our previous studies [22]. The following variables were recorded as: name of the first author, year of publication, region in which the study was performed, type of study design, sample size, participant gender and age, risk estimates with 95% CIs, adjustment factors. When one study included more than one trial, we pooled the trials and considered each trial an independent study. We computed a pooled OR and 95% CI. The Cochrane Q and I2 statistics were used to evaluate the statistical heterogeneity [23]. When the P value was < 0.1 and the I2 value was > 50%, the data were considered to be heterogeneous, and a random-effects model [24] was applied. To further explore the origin of heterogeneity and the stability of conclusion, we also performed subgroup analyses by sex, study design, study region, and criteria of sarcopenia. A sensitivity analysis was conducted to estimate the influence of each individual study on the pooled result. Begg’s test and Egger’s test were used to assess the potential publication bias [25, 26]. STATA version 12.0 (College Station, TX, USA) was used to analyze the data.
Results
Selected studies
A total of 1727 studies were retrieved from PubMed and Embase, after removing duplicates, 1475 were identified. After screening the title and abstract, 288 necessitated reading of the full article. Ultimately, 20 studies [4, 7–19, 27–32] involving 47,744 participants were included (Fig 1). The study characteristics are listed in Table 1. The quality of the studies access by the STROBE statement (S1 Table).
[Figure omitted. See PDF.]
Fig 1. Flow diagram of the steps for study inclusion.
https://doi.org/10.1371/journal.pone.0250437.g001
[Figure omitted. See PDF.]
Table 1. Characteristics of the 20 eligible studies.
https://doi.org/10.1371/journal.pone.0250437.t001
Main analysis
A pooled analysis of 20 studies involving 25 researches showed that sarcopenia significantly increased osteopenia risk (OR, 2.08 [95% CI, 1.66–2.60]; Pheterogeneity = 0.000, I2 = 86.1%) (Fig 2). Substantial heterogeneity was observed (P<0.10, I2 >50%) (Fig 2); however, the analysis revealed that exclusion of any single study did not alter the overall combined results, which indicated that the outcome was stable (Fig 3). Subgroup pooled analyses performed according to gender, study design type, different criteria of sarcopenia, and region also indicated that sarcopenia significantly increased osteopenia risk in each subgroup (Table 2). The Begg and Egger test indicated no evidence of publication bias among the studies [Begg, P > |z| = 0.168; Egger, P = 0.058, 95% CI -0.055–3.098] (Fig 4).
[Figure omitted. See PDF.]
Fig 2. Forest plot of the estimated effects of sarcopenia on osteopenia risk.
https://doi.org/10.1371/journal.pone.0250437.g002
[Figure omitted. See PDF.]
Fig 3. Sensitivity analysis for the estimated effects of sarcopenia on osteopenia risk.
The analysis was performed via recalculation of the pooled results of the primary analysis after exclusion of one study per iteration.
https://doi.org/10.1371/journal.pone.0250437.g003
[Figure omitted. See PDF.]
Fig 4. Publication bias plot.
A, Begg’s funnel plot. B, Egger’s publication bias plot.
https://doi.org/10.1371/journal.pone.0250437.g004
[Figure omitted. See PDF.]
Table 2. Subgroup analysis for sarcopenia and risk of osteopaenia using random-effects model.
https://doi.org/10.1371/journal.pone.0250437.t002
Discussion
Osteopenia is characterized by loss of bone mass, reduced bone mineral density, which will develop into osteoporosis, may further lead to heavy economic and social burdens. Sarcopenia is one of the most important contributing factors related to osteopenia. Muscle and bone are interconnected biochemically and biomechanically, and they can mutually influence each other [33, 34]. Sarcopaenia and osteopaenia are two musculoskeletal pathologies mutually influencing each other, both associated with aging, lifestyle factors, falls and fractures [1, 3]. Thus, sarcopenia and osteopaenia frequently occur concomitantly, which leads to osteosarcopenia, and all of these conditions are critically associated with bone fragility, increased fall risk, fractures [35]. And osteosarcopaenia should be consciously incorporated into daily life and therapeutic strategies. This pooled analysis indicated that sarcopenia significantly increased osteopenia risk. Although heterogeneity was substantial, sensitivity analysis did not alter the overall combined results, subgroup analyses showed that sarcopenia significantly increased the risk of osteopenia in each pooled subgroup, which all demonstrated the credibility of the results. This pooled analysis has strengthened previous findings, for example, one study showed that older women with sarcopenia exhibited lower bone mineral density than those without sarcopenia [35]. Therefore, it may be possible to prevent osteopenia and related adverse events by the treatment of sarcopenia.
This study has several limitations. First, the study design included cross-sectional studies, case-control studies, and others, which might have led to substantial heterogeneity. Second, some trials did not provide the data as estimates with 95% CIs, so we had to calculate these values according to specific numbers of participants, which might have influenced the accuracy of the results. Third, different studies used different diagnostic criteria for sarcopenia, which might have slightly affected the results. Therefore, the results should be interpreted with caution.
Conclusion
In this study, our findings showed that sarcopenia significantly increases osteopenia risk. However, care should be taken when interpreting the findings, and large randomized controlled trials are still needed to further specify the association between osteopenia and sarcopenia.
Supporting information
S1 Table. Methodological quality of studies included in the final analysis based on STROBE statement checklists.
https://doi.org/10.1371/journal.pone.0250437.s001
(PDF)
S1 Checklist. PRISMA 2009 checklist.
https://doi.org/10.1371/journal.pone.0250437.s002
(PDF)
Acknowledgments
We appreciate the contribution of all patients, their families, the investigator and the medical staff.
Citation: Teng Z, Zhu Y, Yu X, Liu J, Long Q, Zeng Y, et al. (2021) An analysis and systematic review of sarcopenia increasing osteopenia risk. PLoS ONE 16(4): e0250437. https://doi.org/10.1371/journal.pone.0250437
1. Cruz-Jentoft AJ, Sayer AA. Sarcopenia. Lancet. 2019;393(10191):2636–46. Epub 2019/06/07. pmid:31171417.
2. Kanis JA, Cooper C, Rizzoli R, Reginster JY, Scientific Advisory Board of the European Society for Clinical and Economic Aspects of Osteoporosis (ESCEO), The Committees of Scientific Advisors and National Societies of the International Osteoporosis Foundation (IOF). European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int. 2019;30(1):3–44. pmid:30324412.
3. Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet (London, England). 2019;393(10169):364–76. Epub 2019/01/31. pmid:30696576.
4. Bieliuniene E, Brondum Frokjaer J, Pockevicius A, Kemesiene J, Lukosevicius S, Basevicius A, et al. CT- and MRI-Based Assessment of Body Composition and Pancreatic Fibrosis Reveals High Incidence of Clinically Significant Metabolic Changes That Affect the Quality of Life and Treatment Outcomes of Patients with Chronic Pancreatitis and Pancreatic Cancer. Medicina (Kaunas, Lithuania). 2019;55(10). Epub 2019/10/02. pmid:31569661.
5. Varacallo M, Seaman TJ, Jandu JS, Pizzutillo P. Osteopenia. StatPearls. Treasure Island (FL): StatPearls Publishing Copyright © 2020, StatPearls Publishing LLC.; 2020.
6. Varacallo MA, Fox EJ, Paul EM, Hassenbein SE, Warlow PM. Patients’ response toward an automated orthopedic osteoporosis intervention program. Geriatric orthopaedic surgery & rehabilitation. 2013;4(3):89–98. Epub 2013/12/10. pmid:24319621.
7. Santos VRD, Christofaro DGD, Gomes IC, Junior IFF, Gobbo LA. Relationship between obesity, sarcopenia, sarcopenic obesity, and bone mineral density in elderly subjects aged 80 years and over. Revista brasileira de ortopedia. 2018;53(3):300–5. Epub 2018/06/13. pmid:29892580.
8. Schneider S, Al-Jaouni R, Filippi J, Wiroth JB, Zeanandin G, Arab K, et al. Sarcopenia is prevalent in patients with Crohn’s disease in clinical remission. Inflammatory bowel diseases. 2008;14(11):1562–8. pmid:18478564
9. Falutz J, Rosenthall L, Guaraldi G. Association of osteoporosis and sarcopenia in treated HIV patients. Antiviral Therapy. 2013;18:A17.
10. Lee SG, Lee YH, Kim KJ, Lee W, Kwon OH, Kim JH. Additive association of vitamin D insufficiency and sarcopenia with low femoral bone mineral density in noninstitutionalized elderly population: the Korea National Health and Nutrition Examination Surveys 2009–2010. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2013;24(11):2789–99. Epub 2013/05/09. pmid:23652463.
11. Wu CH, Yang KC, Chang HH, Yen JF, Tsai KS, Huang KC. Sarcopenia is related to increased risk for low bone mineral density. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry. 2013;16(1):98–103. Epub 2012/09/15. pmid:22975297.
12. Bryant RV, Ooi S, Schultz CG, Goess C, Grafton R, Hughes J, et al. Low muscle mass and sarcopenia: common and predictive of osteopenia in inflammatory bowel disease. Alimentary pharmacology & therapeutics. 2015;41(9):895–906. Epub 2015/03/11. pmid:25753216.
13. Pereira FB, Leite AF, de Paula AP. Relationship between pre-sarcopenia, sarcopenia and bone mineral density in elderly men. Archives of endocrinology and metabolism. 2015;59(1):59–65. Epub 2015/05/01. pmid:25926116.
14. Chung SM, Hyun MH, Lee E, Seo HS. Novel effects of sarcopenic osteoarthritis on metabolic syndrome, insulin resistance, osteoporosis, and bone fracture: the national survey. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2016;27(8):2447–57. Epub 2016/05/15. pmid:27177746.
15. He H, Liu Y, Tian Q, Papasian CJ, Hu T, Deng HW. Relationship of sarcopenia and body composition with osteoporosis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2016;27(2):473–82. Epub 2015/08/06. pmid:26243357.
16. Lee DW, Choi EY. Sarcopenia as an Independent Risk Factor for Decreased BMD in COPD Patients: Korean National Health and Nutrition Examination Surveys IV and V (2008–2011). PloS one. 2016;11(10):e0164303. Epub 2016/10/18. pmid:27749901.
17. Lee I, Cho J, Jin Y, Ha C, Kim T, Kang H. Body Fat and Physical Activity Modulate the Association Between Sarcopenia and Osteoporosis in Elderly Korean Women. Journal of sports science & medicine. 2016;15(3):477–82. Epub 2016/11/03. pmid:27803626.
18. Lee I, Ha C, Kang H. Association of sarcopenia and physical activity with femur bone mineral density in elderly women. Journal of exercise nutrition & biochemistry. 2016;20(1):23–8. Epub 2016/06/15. pmid:27298809.
19. Kim IJ, Kang KY. Low Skeletal Muscle Mass is Associated with the Risk of Low Bone Mineral Density in Urban Dwelling Pr emenopausal Women. Calcified tissue international. 2017;101(6):581–92. pmid:28828511.
20. Vandenbroucke JP, von Elm E, Altman DG, Gotzsche PC, Mulrow CD, Pocock SJ, et al. Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. PLoS Med. 2007;4(10):e297. pmid:17941715.
21. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. Jama. 2000;283(15):2008–12. pmid:10789670.
22. Teng Z, Zhu Y, Wu F, Zhu Y, Zhang X, Zhang C, et al. Opioids contribute to fracture risk: a meta-analysis of 8 cohort studies. PloS one. 2015;10(6):e0128232. Epub 2015/06/02. pmid:26030421.
23. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60. pmid:12958120.
24. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88. pmid:3802833.
25. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101. pmid:7786990.
26. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629–34. Epub 1997/10/06. pmid:9310563.
27. Choi CJ, Choi WS, Kim CM, Lee SY, Kim KS. Risk of Sarcopenia and Osteoporosis in Male Tuberculosis Survivors: Korea National Health and Nutrition Examination Survey. Scientific reports. 2017;7(1):13127. Epub 2017/10/17. pmid:29030560.
28. França NAG, Peters BSE, Lima MMS, Santos EA, Santos PC, Martini LA. Muscle mass as the main component of body composition associated with bone mineral density. Osteoporosis International. 2017;28:S210–S1.
29. Harris R, Chang Y, Beavers K, Laddu-Patel D, Bea J, Johnson K, et al. Risk of Fracture in Women with Sarcopenia, Low Bone Mass, or Both. Journal of the American Geriatrics Society. 2017;65(12):2673–8. Epub 2017/09/30. pmid:28960230.
30. Hwang JA, Kim YS, Leem AY, Park MS, Kim SK, Chang J, et al. Clinical Implications of Sarcopenia on Decreased Bone Density in Men With COPD. Chest. 2017;151(5):1018–27. Epub 2016/12/26. pmid:28012805.
31. Krajewska-Wlodarczyk M, Owczarczyk-Saczonek A, Placek W. Changes in body composition and bone mineral density in postmenopausal women with psoriatic arthritis. Reumatologia. 2017;55(5):215–21. pmid:29332959
32. Lee DW, Jin HJ, Shin KC, Chung JH, Lee HW, Lee KH. Presence of sarcopenia in asthma-COPD overlap syndrome may be a risk factor for decreased bone-mineral density, unlike asthma: Korean National Health and Nutrition Examination Survey (KNHANES) IV and V (2008–2011). International journal of chronic obstructive pulmonary disease. 2017;12:2355–62. Epub 2017/08/30. pmid:28848336.
33. Di Monaco M, Castiglioni C, Bardesono F, Milano E, Massazza G. Sarcopenia, osteoporosis and the burden of prevalent vertebral fractures: a cross-sectional study of 350 women with hip fracture. European journal of physical and rehabilitation medicine [Internet]. February 12, 2020 Feb 12. https://www.ncbi.nlm.nih.gov/pubmed/32052946. pmid:32052946
34. Maurel DB, Jahn K, Lara-Castillo N. Muscle-bone crosstalk: emerging opportunities for novel therapeutic approaches to treat musculoskeletal pathologies. Biomedicines. 2017;5(4):E62. pmid:29064421.
35. Lima RM, de Oliveira RJ, Raposo R, Neri SGR, Gadelha AB. Stages of sarcopenia, bone mineral density, and the prevalence of osteoporosis in older women. Archives of osteoporosis. 2019;14(1):38. Epub 2019/03/15. pmid:30868338.
You have requested "on-the-fly" machine translation of selected content from our databases. This functionality is provided solely for your convenience and is in no way intended to replace human translation. Show full disclaimer
Neither ProQuest nor its licensors make any representations or warranties with respect to the translations. The translations are automatically generated "AS IS" and "AS AVAILABLE" and are not retained in our systems. PROQUEST AND ITS LICENSORS SPECIFICALLY DISCLAIM ANY AND ALL EXPRESS OR IMPLIED WARRANTIES, INCLUDING WITHOUT LIMITATION, ANY WARRANTIES FOR AVAILABILITY, ACCURACY, TIMELINESS, COMPLETENESS, NON-INFRINGMENT, MERCHANTABILITY OR FITNESS FOR A PARTICULAR PURPOSE. Your use of the translations is subject to all use restrictions contained in your Electronic Products License Agreement and by using the translation functionality you agree to forgo any and all claims against ProQuest or its licensors for your use of the translation functionality and any output derived there from. Hide full disclaimer
© 2021 Teng et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Abstract
Sarcopenia is a progressive generalized skeletal muscle disorder, which may increase the risk of osteopenia. The aim of this study was to systematically review studies on the association between sarcopenia and osteopenia by pooled analysis. The PubMed and Embase databases were searched from inception to October 2020 for studies focusing on the association between sarcopenia and osteopenia. Two reviewers independently extracted data and assessed study quality. A pooled analysis was performed to calculate odds ratios (ORs) and 95% confidence intervals (CIs) using random-effects models. Subgroup analysis was conducted to explore the source of heterogeneity and the stability of outcome. A total of 25 independent studies involving 47,744 participants fulfilled the inclusion criteria. Sarcopenia significantly increased the risk of osteopenia (OR, 2.08; 95% CI, 1.66–2.60); Sensitivity analyses indicated the outcome was stable. Subgroup analyses showed that sarcopenia significantly increased osteopenia risk in each subgroup. No evidence of publication bias among the studies existed. In this study, our findings showed that sarcopenia significantly increased the risk of osteopenia. Thus, we suggest that sarcopenia can be a predictor of osteopenia risk.
You have requested "on-the-fly" machine translation of selected content from our databases. This functionality is provided solely for your convenience and is in no way intended to replace human translation. Show full disclaimer
Neither ProQuest nor its licensors make any representations or warranties with respect to the translations. The translations are automatically generated "AS IS" and "AS AVAILABLE" and are not retained in our systems. PROQUEST AND ITS LICENSORS SPECIFICALLY DISCLAIM ANY AND ALL EXPRESS OR IMPLIED WARRANTIES, INCLUDING WITHOUT LIMITATION, ANY WARRANTIES FOR AVAILABILITY, ACCURACY, TIMELINESS, COMPLETENESS, NON-INFRINGMENT, MERCHANTABILITY OR FITNESS FOR A PARTICULAR PURPOSE. Your use of the translations is subject to all use restrictions contained in your Electronic Products License Agreement and by using the translation functionality you agree to forgo any and all claims against ProQuest or its licensors for your use of the translation functionality and any output derived there from. Hide full disclaimer