Skip to main content

Advertisement

SpringerLink
Log in

Bone Mediated and Moderated the Associations Between Sarcopenic Obesity Indices and Cardiovascular Disease Risk Scores

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

To evaluate mediation and moderation of bone on the association of sarcopenic obesity (SO) indices using the metabolic load-capacity model with the 10-year cardiovascular disease risk scores (CVDR). In 2905 men and 3622 women (age ≥ 30 years), dual-energy X-ray absorptiometry was used to measure bone indicators [total bone mineral content percentage(TBM%), bone mineral density of femur neck (BMD_FN) and lumbar spines(BMD_LS)], total muscle (TMM) and fat mass (TFM), appendicular skeletal muscle mass (ASM), and truncal fat mass (TrFM). Two SO indices were TMM/TFM and ASM/TrFM. The Framingham model was used to calculate CVDR. Sex-specific mediation and moderation effects of bone indicators in the associations between the SO indices and the CVDR were analyzed. After adjusting for age, education, income, alcohol use, and physical activity, the SO indices inversely associated with the CVDR and TBM% inversely mediated those associations in both sexes. BMD inversely mediated those associations in men, while the mediation effects of BMD in women were non-significant or positive. In those aged ≥ 60, the mediation effects were found in TBM% and BMD_LS , but not in BMD_FN. The moderation analysis shows stronger inverse associations between the SO indices and the CVDR in those with low bone indicators in women and in men (for the relationship between ASM/TrFM and TBM%), while bone indicators did not moderate these associations in those aged ≥ 60. Bone mass mediated the associations between the SO indices and the CVDR in Korean men and women and moderated these associations in women.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

Korea Centers for Disease Control and Prevention. The 4th and 5th Korea National Health and Nutrition Examination Survey. Korea Centers for Disease Control and Prevention. Access site: https://knhanes.cdc.go.kr/knhanes/main.do.

References

  1. Bauer JM, Cruz-Jentoft AJ, Fielding RA, Kanis JA, Reginster JY, Bruyere O, Cesari M, Chapurlat R, Al-Daghri N, Dennison E, Kaufman JM, Landi F, Laslop A, Locquet M, Maggi S, McCloskey E, Perna S, Rizzoli R, Rolland Y, Rondanelli M, Szulc P, Vellas B, Vlaskovska M, Cooper C (2019) Is there enough evidence for osteosarcopenic obesity as a distinct entity? A critical literature review. Calcif Tissue Int 105:109–124

    Article  CAS  Google Scholar 

  2. Kelly OJ, Gilman JC, Boschiero D, Ilich JZ (2019) Osteosarcopenic obesity: current knowledge, revised identification criteria and treatment principles. Nutrients. https://doi.org/10.3390/nu11040747

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ilich JZ, Kelly OJ, Inglis JE (2016) Osteosarcopenic Obesity syndrome: what is it and how can it be identified and diagnosed? Curr Gerontol Geriatr Res 2016:7325973

    Article  Google Scholar 

  4. Ilich JZ, Inglis JE, Kelly OJ, McGee DL (2015) Osteosarcopenic obesity is associated with reduced handgrip strength, walking abilities, and balance in postmenopausal women. Osteoporos Int 26:2587–2595

    Article  CAS  Google Scholar 

  5. Szlejf C, Parra-Rodriguez L, Rosas-Carrasco O (2017) Osteosarcopenic obesity: prevalence and relation with frailty and physical performance in middle-aged and older women. J Am Med Dir Assoc 18:733.e1-733.e5

    Article  Google Scholar 

  6. Ma Y, Zhang W, Han P, Kohzuki M, Guo Q (2020) Osteosarcopenic obesity associated with poor physical performance in the elderly chinese community. Clin Interv Aging 15:1343–1352

    Article  Google Scholar 

  7. Mo D, Hsieh P, Yu H, Zhou L, Gong J, Xu L, Liu P, Chen G, Chen Z, Deng Q (2018) Osteosarcopenic obesity and its relationship with dyslipidemia in women from different ethnic groups of China. Arch Osteoporos 13:65

    Article  Google Scholar 

  8. Chen X, Kong C, Yu H, Gong J, Lan L, Zhou L, Gong J, Liu P, Xu L, Deng Q (2019) Association between osteosarcopenic obesity and hypertension among four minority populations in China: a cross-sectional study. BMJ Open 9(e026818):2018–026818

    Google Scholar 

  9. Lee K (2020) Association of osteosarcopenic obesity and its components: osteoporosis, sarcopenia and obesity with insulin resistance. J Bone Miner Metab 38:695–701

    Article  CAS  Google Scholar 

  10. Fukuda T, Bouchi R, Takeuchi T, Tsujimoto K, Minami I, Yoshimoto T, Ogawa Y (2018) Sarcopenic obesity assessed using dual energy X-ray absorptiometry (DXA) can predict cardiovascular disease in patients with type 2 diabetes: a retrospective observational study. Cardiovasc Diabetol 17:55

    Article  CAS  Google Scholar 

  11. Kim JH, Cho JJ, Park YS (2015) Relationship between sarcopenic obesity and cardiovascular disease risk as estimated by the Framingham risk score. J Korean Med Sci 30:264–271

    Article  CAS  Google Scholar 

  12. Atkins JL, Whincup PH, Morris RW, Lennon LT, Papacosta O, Wannamethee SG (2014) Sarcopenic obesity and risk of cardiovascular disease and mortality: a population-based cohort study of older men. J Am Geriatr Soc 62:253–260

    Article  Google Scholar 

  13. Woo J, Leung J (2018) Sarcopenic obesity revisited: insights from the Mr and Ms Os cohort. J Am Med Dir Assoc 19(679):684.e2

    Google Scholar 

  14. Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR (2005) Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone Miner Res 20:1912–1920

    Article  Google Scholar 

  15. Veronese N, Stubbs B, Crepaldi G, Solmi M, Cooper C, Harvey NC, Reginster JY, Rizzoli R, Civitelli R, Schofield P, Maggi S, Lamb SE (2017) Relationship between low bone mineral density and fractures with incident cardiovascular disease: a systematic review and meta-analysis. J Bone Miner Res 32:1126–1135

    Article  Google Scholar 

  16. Ye C, Xu M, Wang S, Jiang S, Chen X, Zhou X, He R (2016) Decreased bone mineral density is an independent predictor for the development of atherosclerosis: a systematic review and meta-analysis. PLoS ONE 11:e0154740

    Article  Google Scholar 

  17. Siervo M, Prado CM, Mire E, Broyles S, Wells JC, Heymsfield S, Katzmarzyk PT (2015) Body composition indices of a load-capacity model: gender- and BMI-specific reference curves. Public Health Nutr 18:1245–1254

    Article  Google Scholar 

  18. Prado CM, Wells JC, Smith SR, Stephan BC, Siervo M (2012) Sarcopenic obesity: a critical appraisal of the current evidence. Clin Nutr 31:583–601

    Article  CAS  Google Scholar 

  19. Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, Chun C, Khang YH, Oh K (2014) Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 43:69–77

    Article  Google Scholar 

  20. Korea Centers for Disease Control and Prevention. Guidelines for using the Fifth National Healthy and Nutition Examination Survey (KNHANES V-3), 2012. Korea Centers for Disease Control and Prevention, Osong

  21. Oh H (2010) Education and quality control of bone mineral density test in the Fourth National Health and Nutrition Examination Survey (KNHANES IV-3), 2009. Korea Centers for Disease Control and Prevention, Osong

  22. Shafiee G, Ostovar A, Heshmat R, Keshtkar AA, Sharifi F, Shadman Z, Nabipour I, Soltani A, Larijani A (2018) Appendicular skeletal muscle mass reference values and the peak muscle mass to identify saropenia among Iranian healthy populaion. J Prev Med 9:25

    Google Scholar 

  23. American Diabetes Association (2018) 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2018. Diabetes Care 41:S13-27

    Article  Google Scholar 

  24. Korea Centers for Disease Control and Prevention (2013) Procedural manual. The Sixth Korea National Health and Nutrition Examination Survey (KNHANES VI-1). Korea Centers for Disease Control and Prevention, Osong

  25. D’Agostino RBS, Vasan RS, Pencina MJ, Wolf PA, Cobain M, Massaro JM, Kannel WB (2008) General cardiovascular risk profile for use in primary care: the Framingham Heart Study. Circulation 117:743–753

    Article  Google Scholar 

  26. Hayes AF (2013) Introduction to mediation, moderation, and conditional process analysis: a regression-based approach. The Guilford Press, New York

    Google Scholar 

  27. Hayes AF, Rockwood NJ (2017) Regression-based statistical mediation and moderation analysis in clinical research: observations, recommendations, and implementation. Behav Res Ther 98:39–57

    Article  Google Scholar 

  28. van Strien T, Winkens L, Toft MB, Pedersen S, Brouwer I, Visser M, Lahteenmaki L (2016) The mediation effect of emotional eating between depression and body mass index in the two European countries Denmark and Spain. Appetite 105:500–508

    Article  Google Scholar 

  29. Kirk B, Feehan J, Lombardi G, Duque G (2020) Muscle, bone, and fat crosstalk: the biological role of myokines, osteokines, and adipokines. Curr Osteoporos Rep 18:388–400

    Article  Google Scholar 

  30. Lello S, Capozzi A, Scambia G (2015) Osteoporosis and cardiovascular disease: an update. Gynecol Endocrinol 31:590–594

    Article  CAS  Google Scholar 

  31. Schorr M, Dichtel LE, Gerweck AV, Valera RD, Torriani M, Miller KK, Bredella MA (2018) Sex differences in body composition and association with cardiometabolic risk. Biol Sex Differ 9:28

    Article  Google Scholar 

Download references

Funding

This work was supported by 2021 Inje University Busan Paik Hospital research grant and the Ministry of Education of the Republic of Korea and the National Research Foundation of Korea (NRF-2020S1A5C2A02092454).

Author information

Authors and Affiliations

  1. Department of Family Medicine, Busan Paik Hospital, College of Medicine, Inje University, 75, Bokji-ro, Busanjin-gu, Busan, 47392, Republic of Korea

    Kayoung Lee

Authors
  1. Kayoung Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kayoung Lee.

Ethics declarations

Disclosure

Kayoung Lee declares that she has no conflict of interest.

Ethical Approval

It was performed in accordance with the ethical standards as laid down in the 1964 declaration of Helsinki and its later amendments. The Korea National Health and Nutrition Examination Survey protocol was approved by the institutional review board of Korea Centers for Disease Control and Prevention (IRB Approval Number: 2008-04EXP-01-C, 2009-01CON-03-2C, 2010-02CON-21-C, and 2011-02CON-06-C). The current study was categorized as an exemption category of ethical review.

Consent to Participate

The consent was obtained in the original survey.

Consent for Publication

The consent for publication was stated in the original consent form.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, K. Bone Mediated and Moderated the Associations Between Sarcopenic Obesity Indices and Cardiovascular Disease Risk Scores. Calcif Tissue Int 109, 490–498 (2021). https://doi.org/10.1007/s00223-021-00861-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-021-00861-0

Keywords

Search

Navigation