Skip to main content
Log in

Effects of metabolic syndrome on bone health in older adults: the Bushehr Elderly Health (BEH) program

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

Based on the clinical, BMD, and TBS data of 2380 participants aged ≥ 60 which was gathered during the BEH program, stage II, we showed that MetS was positively associated with BMD, while a negative or no association was observed between MetS and TBS depending on the sex and the adjustment model.

Introduction

The results of previous reports in regard to the effect of metabolic syndrome (MetS) on bone health are not conclusive. This study aimed to evaluate the association between MetS with bone mineral density (BMD) and trabecular bone score (TBS) as an indicator of bone quantity and quality, respectively.

Methods

Using a cross-sectional design, this study was carried out based on the data collected during the BEH Program, stage II. MetS was defined according to NCEP-ATP III criteria. BMD (at the lumbar spine and the hip) and lumbar spine TBS were assessed by dual-energy X-ray absorptiometry device.

Results

The data of 2380 participants (women = 1228, men = 1152) aged ≥ 60 were analyzed. In the fully adjusted regression models (including BMI), significant associations between MetS and mean BMD were observed across all locations in men (P values ≤ 0.001) and in the lumbar spine in women (P value = 0.003). In addition, the prevalence of osteoporosis (based on BMD) was significantly lower in those with MetS than those without MetS in both sexes, even after full adjustments (women, OR = 0.707, P value = 0.013; men, OR = 0.563, P value = 0.001). In contrast, in age-adjusted regression analyses, the prevalence of degraded bone microarchitecture (TBS ≤ 1.2) was significantly increased in those with MetS than those without, irrespective of the participants’ sex (P values < 0.05). The mean TBS was also negatively associated with MetS in women (β = − 0.075, P value = 0.007) but not in men (β = − 0.052, P value = 0.077), in age-adjusted regression models. However, after including BMI in the adjusted models, all significant associations between TBS values and MetS disappeared.

Conclusion

It seems that a positive association exists between MetS and BMD, while MetS is either not associated or negatively correlated with bone quality as measured by TBS.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Pisani P, Renna MD, Conversano F, Casciaro E, Di Paola M, Quarta E, Muratore M, Casciaro S (2016) Major osteoporotic fragility fractures: risk factor updates and societal impact. World J Orthopedics 7(3):171–181

    Article  Google Scholar 

  2. Iki M, Tamaki J, Kadowaki E, Sato Y, Dongmei N, Winzenrieth R, Kagamimori S, Kagawa Y, Yoneshima H (2014) Trabecular bone score (TBS) predicts vertebral fractures in Japanese women over 10 years independently of bone density and prevalent vertebral deformity: the Japanese Population-based Osteoporosis (JPOS) cohort study. J Bone Miner Res 29(2):399–407

    Article  PubMed  Google Scholar 

  3. Leslie W, Aubry-Rozier B, Lix L, Morin S, Majumdar S, Hans D (2014) Spine bone texture assessed by trabecular bone score (TBS) predicts osteoporotic fractures in men: the Manitoba Bone Density Program. Bone 67:10–14

    Article  CAS  PubMed  Google Scholar 

  4. Briot K, Paternotte S, Kolta S, Eastell R, Reid DM, Felsenberg D, Glüer CC, Roux C (2013) Added value of trabecular bone score to bone mineral density for prediction of osteoporotic fractures in postmenopausal women: the OPUS study. Bone 57(1):232–236

    Article  PubMed  Google Scholar 

  5. Griffith JF, Engelke K, Genant HK (2010) Looking beyond bone mineral density. Ann N Y Acad Sci 1192(1):45–56

    Article  PubMed  Google Scholar 

  6. Link TM (2012) Osteoporosis imaging: state of the art and advanced imaging. Radiology 263(1):3–17

    Article  PubMed  PubMed Central  Google Scholar 

  7. Link TM, Heilmeier U (2016) Bone quality-beyond bone mineral density. Semin Musculoskelet Radiol 20(3):269–278

  8. Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26(11):2762–2769

    Article  PubMed  Google Scholar 

  9. Pucci G, Alcidi R, Tap L, Battista F, Mattace-Raso F, Schillaci G (2017) Sex-and gender-related prevalence, cardiovascular risk and therapeutic approach in metabolic syndrome: a review of the literature. Pharmacol Res 120:34–42

    Article  PubMed  Google Scholar 

  10. Xue P, Gao P, Li Y (2012) The association between metabolic syndrome and bone mineral density: a meta-analysis. Endocr 42(3):546–554

  11. Zhou J, Zhang Q, Yuan X, Wang J, Li C, Sheng H, Qu S, Li H (2013) Association between metabolic syndrome and osteoporosis: a meta-analysis. Bone 57(1):30–35

    Article  PubMed  Google Scholar 

  12. Yang S, Nguyen ND, Center JR, Eisman JA, Nguyen TV (2013) Association between abdominal obesity and fracture risk: a prospective study. J Clin Endocrinol Metabol 98(6):2478–2483

    Article  CAS  Google Scholar 

  13. Yang L, Lv X, Wei D, Yue F, Guo J, Zhang T (2016) Metabolic syndrome and the risk of bone fractures: a meta-analysis of prospective cohort studies. Bone 84:52–56

    Article  PubMed  Google Scholar 

  14. Kinjo M, Setoguchi S, Solomon DH (2007) Bone mineral density in adults with the metabolic syndrome: analysis in a population-based US sample. J Clin Endocrinol Metabol 92(11):4161–4164

    Article  CAS  Google Scholar 

  15. Freitas P, Rosa MG, Gomes A, Wahrlich V, Di Luca D, da Cruz FR, da Silva CD, Faria C, Yokoo E (2016) Central and peripheral fat body mass have a protective effect on osteopenia or osteoporosis in adults and elderly? Osteoporos Int 27(4):1659–1663

    Article  CAS  PubMed  Google Scholar 

  16. Hwang D-K, Choi H-J (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21(3):425–431

    Article  PubMed  Google Scholar 

  17. Hsu Y-H, Venners SA, Terwedow HA, Feng Y, Niu T, Li Z, Laird N, Brain JD, Cummings SR, Bouxsein ML (2006) Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 83(1):146–154

    Article  CAS  PubMed  Google Scholar 

  18. Qin L, Yang Z, Zhang W, Gu H, Li X, Zhu L, Lu S, Xing Y, Zhang H, Niu Y (2016) Metabolic syndrome and osteoporotic fracture: a population-based study in China. BMC Endocr Disord 16(1):27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, Müller R, Zhao B, Guo X, Lang T (2013) Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metabol 98(6):2562–2572

    Article  CAS  Google Scholar 

  20. Gonnelli S, Caffarelli C, Nuti R (2014) Obesity and fracture risk. Clin Cases Min Bone Metabol 11(1):9–14

    Google Scholar 

  21. Muka T, Trajanoska K, Kiefte-de Jong JC, Oei L, Uitterlinden AG, Hofman A, Dehghan A, Zillikens MC, Franco OH, Rivadeneira F (2015) The association between metabolic syndrome, bone mineral density, hip bone geometry and fracture risk: the Rotterdam Study. PLoS One 10(6):e0129116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Ostovar A, Nabipour I, Larijani B, Heshmat R, Darabi H, Vahdat K, Ravanipour M, Mehrdad N, Raeisi A, Heidari G (2015) Bushehr elderly health (BEH) Programme, phase I (cardiovascular system). BMJ Open 5(12):e009597

    Article  PubMed  PubMed Central  Google Scholar 

  23. Shafiee G, Ostovar A, Heshmat R, Darabi H, Sharifi F, Raeisi A, Mehrdad N, Shadman Z, Razi F, Amini MR (2017) Bushehr Elderly Health (BEH) programme: study protocol and design of musculoskeletal system and cognitive function (stage II). BMJ Open 7(8):e013606

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ervin RB (2009) Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003-2006. Natl Health Stat Report (13):1–7

  25. Aadahl M, Jørgensen T (2003) Validation of a new self-report instrument for measuring physical activity. Med Sci Sports Exerc 35(7):1196–1202

    Article  PubMed  Google Scholar 

  26. Shuhart CR, Yeap SS, Anderson PA, Jankowski LG, Lewiecki EM, Morse LR, Rosen HN, Weber DR, Zemel BS, Shepherd JA (2019) Executive summary of the 2019 ISCD position development conference on monitoring treatment, DXA cross-calibration and least significant change, spinal cord injury, peri-prosthetic and orthopedic bone health, transgender medicine and pediatrics. J Clin Densitom 22(4):453–471

  27. Kim B-J, Kwak MK, Ahn SH, Kim H, Lee SH, Koh J-M (2017) Lower trabecular bone score in patients with primary aldosteronism: human skeletal deterioration by aldosterone excess. J Clin Endocrinol Metabol 103(2):615–621

    Article  Google Scholar 

  28. Langsetmo L, Vo TN, Ensrud KE, Taylor BC, Cawthon PM, Schwartz AV, Bauer DC, Orwoll ES, Lane NE, Barrett-Connor E (2016) The association between trabecular bone score and lumbar spine volumetric BMD is attenuated among older men with high body mass index. J Bone Miner Res 31(10):1820–1826

    Article  PubMed  Google Scholar 

  29. Tay Y-KD, Cusano NE, Rubin MR, Williams J, Omeragic B, Bilezikian JP (2018) Trabecular bone score in obese and nonobese subjects with primary hyperparathyroidism before and after parathyroidectomy. J Clin Endocrinol Metabol 103(4):1512–1521

    Article  Google Scholar 

  30. Hernández J, Olmos J, González-Macías J (2011) Metabolic syndrome, fractures and gender. Maturitas 68(3):217–223

    Article  PubMed  Google Scholar 

  31. Jeon YK, Lee JG, Kim SS, Kim BH, Kim S-J, Kim YK, Kim IJ (2011) Association between bone mineral density and metabolic syndrome in pre-and postmenopausal women. Endocr J 58(2):87–93

  32. Von Muhlen D, Safii S, Jassal S, Svartberg J, Barrett-Connor E (2007) Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos Int 18(10):1337–1344

    Article  Google Scholar 

  33. Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R (2010) Men with metabolic syndrome have lower bone mineral density but lower fracture risk—the MINOS study. J Bone Miner Res 25(6):1446–1454

    Article  PubMed  Google Scholar 

  34. Hernández JL, Olmos JM, Pariente E, Martínez J, Valero C, García-Velasco P, Nan D, Llorca J, González-Macías J (2010) Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 17(5):955–961

    Article  PubMed  Google Scholar 

  35. Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res 8(5):567–573

    Article  CAS  PubMed  Google Scholar 

  36. Povoroznyuk V, Martynyuk L, Shved M, Dzerovych N, Vayda V, Martyntyuk L (2008) Associations between the metabolic syndrome and bone mineral density in Ukrainian women in postmenopausal period. Bone 43(1):S84

    Article  CAS  Google Scholar 

  37. Liu CT, Broe KE, Zhou Y, Boyd SK, Cupples LA, Hannan MT, Lim E, McLean RR, Samelson EJ, Bouxsein ML (2017) Visceral adipose tissue is associated with bone microarchitecture in the Framingham Osteoporosis Study. J Bone Miner Res 32(1):143–150

    Article  CAS  PubMed  Google Scholar 

  38. Bredella MA, Lin E, Gerweck AV, Landa MG, Thomas BJ, Torriani M, Bouxsein ML, Miller KK (2012) Determinants of bone microarchitecture and mechanical properties in obese men. J Clin Endocrinol Metabol 97(11):4115–4122

    Article  CAS  Google Scholar 

  39. Lv S, Zhang A, Di W, Sheng Y, Cheng P, Qi H, Liu J, Yu J, Ding G, Cai J (2016) Assessment of fat distribution and bone quality with trabecular bone score (TBS) in healthy Chinese men. Sci Rep 6(1):1–8

    Article  CAS  Google Scholar 

  40. Kim B-J, Ahn S, Bae S, Kim E, Kim T-H, Lee S, Kim H-K, Choe J, Kim S-Y, Koh J-M (2013) Association between metabolic syndrome and bone loss at various skeletal sites in postmenopausal women: a 3-year retrospective longitudinal study. Osteoporos Int 24(8):2243–2252

    Article  CAS  PubMed  Google Scholar 

  41. Greco EA, Lenzi A, Migliaccio S (2015) The obesity of bone. Ther Adv Endocrinol Metabol 6(6):273–286

    Article  CAS  Google Scholar 

  42. De Fusco C, Messina A, Monda V, Viggiano E, Moscatelli F, Valenzano A, Esposito T, Sergio C, Cibelli G, Monda M, Messina G (2017) Osteopontin: Relation between Adipose Tissue and Bone Homeostasis. Stem Cells Int. https://doi.org/10.1155/2017/4045238

  43. Knight JA (2012) Physical inactivity: associated diseases and disorders. Ann Clin Lab Sci 42(3):320–337

    PubMed  Google Scholar 

  44. Esposito K, Chiodini P, Capuano A, Colao A, Giugliano D (2013) Fracture risk and bone mineral density in metabolic syndrome: a meta-analysis. J Clin Endocrinol Metabol 98(8):3306–3314

    Article  CAS  Google Scholar 

  45. Kolta S, Briot K, Fechtenbaum J, Paternotte S, Armbrecht G, Felsenberg D, Glüer C, Eastell R, Roux C (2014) TBS result is not affected by lumbar spine osteoarthritis. Osteoporos Int 25(6):1759–1764

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to express their gratefulness to the staff and researchers of the Bushehr Elderly Health program for their thoughtful contribution.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. Larijani.

Ethics declarations

Conflicts of interest

None.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was approved by the Ethical Research Committee (ERC) of Endocrinology and Metabolism Research Institute, which is affiliated to Tehran University of Medical Sciences and the ERC of Bushehr University of Medical Sciences.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 34 kb)

ESM 2

(DOCX 28 kb)

ESM 3

(DOCX 25 kb)

ESM 4

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bagherzadeh, M., Sajjadi-Jazi, S.M., Sharifi, F. et al. Effects of metabolic syndrome on bone health in older adults: the Bushehr Elderly Health (BEH) program. Osteoporos Int 31, 1975–1984 (2020). https://doi.org/10.1007/s00198-020-05455-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-020-05455-4

Keywords

Navigation