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Body mass index inversely associated with bone microarchitecture quality: a systematic review and meta-analysis

  • Kevin Kusuman ,
  • Kadek Adit Wiryadana ,
  • I Made Buddy Setiawan ,
  • Su Djie To Rante ,

Abstract

Introduction: The rising prevalence of obesity forces the orthopedist to consider it in fracture risk assessment. Multiple studies have consistently demonstrated that people with obesity have increased bone mineral density (BMD). Although it appears other factors in bone strength may influence the fracture risk, including bone microarchitecture, which recently can be measured by trabecular bone score (TBS). The complex associations between TBS and BMI remain unclear, and some studies show inconsistent findings. This systematic review and meta-analysis aimed to understand whether increased BMI is associated with lower TBS by indirectly pooling all the available evidence from the published literature.

Methods: A literature search was carried out using PubMed, Cochrane Library, Google Scholar and other popular journal databases using the terms "trabecular bone score", "body mass index" and the possible synonyms. We extracted the total sample, mean and standard deviation of TBS for patients within each BMI category from the selected literature. A meta-analysis was conducted using a random-effects model and inverse variant methods to synthesize the pooled effect size (mean difference) for each gender subgroup.

Results: After an initial search and screening of 2399 studies, seven reports published between 2016-2019 were included (five cross-sectional, one cohort, and one randomized clinical trial). These include 2872 samples which were mostly women (2286). One thousand thirty-one samples were with normal BMI, 1124 samples were with overweight BMI, and 717 samples were with obesity. The included studies varied by age group and gender. The between-study heterogeneity with I2 index ranging 0%-76% studies in man showed higher heterogeneity. Compared with normal individuals, those with overweight and obesity had lower TBS with a mean difference of -0.02 (95% CI -0.03 to -0.01) and -0.07 (95% CI, -0.09 to -0.05), respectively. The differences were consistent across gender, although larger differences were found in men.

Conclusion: Individuals with higher BMI have a lower TBS than individuals with normal BMI in a stepwise manner. It suggests that the inclusion of TBS can improve the assessment of fracture risk in obese individuals.

Section

References

  1. Hou J, He C, He W, Yang M, Luo X, Li C. Obesity and Bone Health: A Complex Link. Front Cell Dev Biol. 2020;8:600181.
  2. Komatsu N, Takayanagi H. T Cells in The Regulation of Bone Metabolism. In: Zaidi M, editor. Encyclopedia of Bone Biology. Oxford: Academic Press; 2020. p. 12–9. Available from: https://www.sciencedirect.com/science/article/pii/B9780128012383622274
  3. Body-mass index and all-cause mortality: individual-participant-data meta-analysis of 239 prospective studies in four continents - The Lancet [Internet]. Available from: https://www.thelancet.com/journals/lancet/article/PIIS0140-6736(16)30175-1/fulltext
  4. Fawzy T, Muttappallymyalil J, Sreedharan J, Ahmed A, Alshamsi SOS, Al Ali MSSHBB, et al. Association between Body Mass Index and Bone Mineral Density in Patients Referred for Dual-Energy X-Ray Absorptiometry Scan in Ajman, UAE. J Osteoporos. 2011;2011:876309.
  5. Wu S-F, Du X-J. Body Mass Index May Positively Correlate with Bone Mineral Density of Lumbar Vertebra and Femoral Neck in Postmenopausal Females. Med Sci Monit Int Med J Exp Clin Res. 2016;22:145–51.
  6. Goldman AL, Donlon CM, Cook NR, Manson JE, Buring JE, Copeland T, et al. VITamin D and OmegA-3 TriaL (VITAL) bone health ancillary study: clinical factors associated with trabecular bone score in women and men. Osteoporos Int. 2018;29(11):2505–15.
  7. JMedLife-08-462.pdf.
  8. Berro A-J, Ayoub M-L, Pinti A, Ahmaidi S, El Khoury G, El Khoury C, et al. Trabecular Bone Score in Overweight and Normal-Weight Young Women. In: Rojas I, Ortuño F, editors. Bioinformatics and Biomedical Engineering. Cham: Springer International Publishing; 2018. p. 59–68. (Lecture Notes in Computer Science; vol. 10814). Available from: http://link.springer.com/10.1007/978-3-319-78759-6_6
  9. Romagnoli E, Lubrano C, Carnevale V, Costantini D, Nieddu L, Morano S, et al. Assessment of trabecular bone score (TBS) in overweight/obese men: effect of metabolic and anthropometric factors. Endocrine. 2016;54(2):342–7.
  10. Shevroja E, Aubry-Rozier B, Hans G, Gonzalez- Rodriguez E, Stoll D, Lamy O, et al. Clinical Performance of the Updated Trabecular Bone Score (TBS) Algorithm, Which Accounts for the Soft Tissue Thickness: The OsteoLaus Study. J Bone Miner Res Off J Am Soc Bone Miner Res. 2019;34(12):2229–37.
  11. Rajaei A, Amiri A, Farsad F, Dehghan P. The Correlation between Trabecular Bone Score and Lumbar Spine Bone Mineral Density in Patients with Normal and High Body Mass Index. Iran J Med Sci. 2019;44(5):374–81.
  12. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
  13. Higgins J, Thomas J, Chandler J, Cumpston M, Li T, Page M, et al. Chapter 6: Choosing effect measures and computing estimates of effect [Internet]. Cochrane Handbook for Systematic Reviews of Interventions. Available from: https://training.cochrane.org/handbook/current/chapter-06
  14. R Core Team. R: A language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2021. Available from: https://www.R-project.org/.
  15. Rstudio Team. RStudio: Integrated Development for R [Internet]. Boston: Rstudio PBC; 2021. Available from: http://www.rstudio.com/
  16. Balduzzi S, Rücker G, Schwarzer G. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health. 2019;22(4):153–60.
  17. PRISMA2020: an R package and Shiny app for producing PRISMA 2020-compliant flow diagrams, with interactivity for optimised digital transparency and Open Synthesis | medRxiv [Internet]. Available from: https://www.medrxiv.org/content/10.1101/2021.07.14.21260492v1
  18. Ayoub M-L, El Khoury G, Zakhem E, El Khoury C, Cortet B, El Hage R. Trabecular Bone Score in obese, overweight and normal-weight young men. Sci Sports. 2017;32(1):33–8.
  19. Rajaei A, Amiri A, Farsad F, Dehghan P. The Correlation between Trabecular Bone Score and Lumbar Spine Bone Mineral Density in Patients with Normal and High Body Mass Index. Iran J Med Sci. 2019;44(5). Available from: https://doi.org/10.30476/ijms.2019.45413
  20. Messina C, Buonomenna C, Menon G, Magnani S, Albano D, Gitto S, et al. Fat Mass Does Not Increase the Precision Error of Trabecular Bone Score Measurements. J Clin Densitom. 2019;22(3):359–66.
  21. Shevroja E, Aubry‐Rozier B, Hans G, Gonzalez‐Rodriguez E, Stoll D, Lamy O, et al. Clinical Performance of the Updated Trabecular Bone Score (TBS) Algorithm, Which Accounts for the Soft Tissue Thickness: The OsteoLaus Study. J Bone Miner Res. 2019;34(12):2229–37.
  22. Morgan SL, Prater GL. Quality in dual-energy X-ray absorptiometry scans. Bone. 2017;104:13–28.
  23. Ho-Pham LT, Tran B, Do AT, Nguyen TV. Association between pre-diabetes, type 2 diabetes and trabecular bone score: The Vietnam Osteoporosis Study. Diabetes Res Clin Pract. 2019;155:107790.
  24. Leslie WD, Aubry-Rozier B, Lamy O, Hans D, for the Manitoba Bone Density Program. TBS (Trabecular Bone Score) and Diabetes-Related Fracture Risk. J Clin Endocrinol Metab. 2013;98(2):602–9.
  25. Ho-Pham LT, Nguyen TV. Association between trabecular bone score and type 2 diabetes: a quantitative update of evidence. Osteoporos Int. 2019;30(10):2079–85.
  26. McCloskey EV, Odén A, Harvey NC, Leslie WD, Hans D, Johansson H, et al. A Meta-Analysis of Trabecular Bone Score in Fracture Risk Prediction and Its Relationship to FRAX: TBS IN FRACTURE RISK PREDICTION AND RELATIONSHIP TO FRAX. J Bone Miner Res. 2016;31(5):940–8.
  27. Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg. 2011;6(1):30.
  28. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose Expression of Tumor Necrosis Factor-α: Direct Role in Obesity-Linked Insulin Resistance. Science. 1993;259(5091):87–91.
  29. Pfeilschifter J, Köditz R, Pfohl M, Schatz H. Changes in proinflammatory cytokine activity after menopause. Endocr Rev. 2002;23(1):90–119.
  30. Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology. 2001;142(12):5050–5.
  31. Oshima K, Nampei A, Matsuda M, Iwaki M, Fukuhara A, Hashimoto J, et al. Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun. 2005;331(2):520–6.
  32. van Dielen FM, van’t Veer C, Schols AM, Soeters PB, Buurman WA, Greve JW. Increased leptin concentrations correlate with increased concentrations of inflammatory markers in morbidly obese individuals. Int J Obes Relat Metab Disord J Int Assoc Study Obes. 2001;25(12):1759–66.
  33. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999;257(1):79–83.
  34. Nelson SE, Frantz JA, Ziegler EE. Absorption of fat and calcium by infants fed a milk-based formula containing palm olein. J Am Coll Nutr. 1998;17(4):327–32.
  35. Carnielli VP, Luijendijk IH, Van Goudoever JB, Sulkers EJ, Boerlage AA, Degenhart HJ, et al. Structural position and amount of palmitic acid in infant formulas: effects on fat, fatty acid, and mineral balance. J Pediatr Gastroenterol Nutr. 1996;23(5):553–60.
  36. Lucas A, Quinlan P, Abrams S, Ryan S, Meah S, Lucas PJ. Randomised controlled trial of a synthetic triglyceride milk formula for preterm infants. Arch Dis Child Fetal Neonatal Ed. 1997;77(3):F178-184.

How to Cite

Kusuman, K., Wiryadana, K. A., Setiawan, I. M. B., & Rante, S. D. T. (2022). Body mass index inversely associated with bone microarchitecture quality: a systematic review and meta-analysis. Indonesia Journal of Biomedical Science, 16(1), 28–33. https://doi.org/10.15562/ijbs.v16i1.383

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Kevin Kusuman
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Pubmed
IJBS Journal


Kadek Adit Wiryadana
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IJBS Journal


I Made Buddy Setiawan
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IJBS Journal


Su Djie To Rante
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IJBS Journal