Skip to main content

Advertisement

SpringerLink
Log in

Age-related normative values of trabecular bone score (TBS) for Japanese women: the Japanese Population-based Osteoporosis (JPOS) study

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

A Correction to this article was published on 11 December 2018

This article has been updated

Abstract

Summary

Trabecular bone score (TBS), a surrogate measure of bone microarchitecture, represents fracture risk independently of bone density. We present normative TBS values from a representative population study of Japanese women. This database would enhance our understanding of trabecular bone microarchitecture and improve osteoporosis management.

Introduction

TBS is a texture parameter that quantifies local variation in gray level distribution within dual-energy X-ray absorptiometry (DXA) images of the lumbar spine. While TBS is associated with fracture risk independently of areal bone mineral density (aBMD), normative TBS values have only been reported for Caucasian women. This study provides age-specific normative values of TBS from a representative sample of Japanese women.

Methods

We randomly selected 4,550 women aged 15–79 years from 7 areas throughout Japan. Women younger than 20 years and those with any medical history which might affect bone metabolism were excluded, and the remaining 3,069 with at least two assessable vertebrae from the first to the fourth vertebrae were subjected to analysis. TBS values were calculated from spine DXA images using TBS iNsight software (Med-Imaps, France). Age-related models of TBS were constructed using piecewise linear regression analysis.

Results

Participant age, body mass index (BMI), spine aBMD, and TBS (mean ± SD) were 48.7 ± 16.8 years, 22.9 ± 3.4, 0.888 ± 0.169 g/cm2, and 1.187 ± 0.137, respectively. A three-piece linear regression model of TBS on age explained 70.7 % of the total variance in TBS and comprised very small age-related changes in the youngest segment of the regression line, rapid loss in the middle segment, and small loss in the oldest segment. TBS was lower in Japanese women than in Caucasian women across all age ranges, with the difference increasing with age up through 65 years.

Conclusions

The normative values of TBS for Japanese women presented here would enhance our understanding of trabecular bone microarchitecture and help improve the management of osteoporosis.

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

Change history

  • 11 December 2018

    I have, as the Principal Investigator of this study, identified an error in the computation of TBS values in the JPOS cohort, which resulted in the publication of incorrect TBS absolute values [1]. This error was linked to the calibration process for calculating standardized TBS values in the R&D TBS.

References

  1. Winzenrieth R, Michelet F, Hans D (2013) Three-dimensional (3D) microarchitecture correlations with 2D projection image gray-level variations assessed by trabecular bone score using high-resolution computed tomographic acquisitions: effects of resolution and noise. J Clin Densitomet 16:287–296

    Article  Google Scholar 

  2. Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14:302–312

    Article  PubMed  Google Scholar 

  3. Roux JP, Wegrzyn J, Boutroy S, Bouxsein ML, Hans D, Chapurlat R (2013) The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study. Osteoporos Int 24:2455–2460

    Article  CAS  PubMed  Google Scholar 

  4. Pothuaud L, Barthe N, Krieg MA, Mehsen N, Carceller P, Hans D (2009) Evaluation of the potential use of trabecular bone score to complement bone mineral density in the diagnosis of osteoporosis: a preliminary spine BMD-matched case–control study. J Clin Densitom 12:170–176

    Article  PubMed  Google Scholar 

  5. Winzenrieth R, Dufour R, Pothuaud L, Hans D (2010) A retrospective case–control study assessing the role of trabecular bone score in postmenopausal Caucasian women with osteopenia: analyzing the odds of vertebral fracture. Calcif Tissue Int 86:104–109

    Article  CAS  PubMed  Google Scholar 

  6. Rabier B, Heraud A, Grand-Lenoir C, Winzenrieth R, Hans D (2010) A multicentre, retrospective case–control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): analysing the odds of vertebral fracture. Bone 46:176–181

    Article  PubMed  Google Scholar 

  7. 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 26:2762–2769

    Article  PubMed  Google Scholar 

  8. Boutroy S, Hans D, Sornay-Rendu E, Vilayphiou N, Winzenrieth R, Chapurlat R (2013) Trabecular bone score improves fracture risk prediction in non-osteoporotic women: the OFELY study. Osteoporos Int 24:77–85

    Article  CAS  PubMed  Google Scholar 

  9. 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 29:399–407

    Article  PubMed  Google Scholar 

  10. Dufour R, Winzenrieth R, Heraud A, Hans D, Mehsen N (2013) Generation and validation of a normative, age-specific reference curve for lumbar spine trabecular bone score (TBS) in French women. Osteoporos Int 24:2837–2846

    Article  CAS  PubMed  Google Scholar 

  11. Simonelli C, Leib E, Mossman N, Winzenrieth R, Hans D, McClung M (2014) Creation of an age-adjusted, dual-energy X-ray absorptiometry-derived trabecular bone score curve for the lumbar spine in non-Hispanic US white women. J Clin Densitom 17:314–319

    Article  PubMed  Google Scholar 

  12. Cheng SY, Levy AR, Lefaivre KA, Guy P, Kuramoto L, Sobolev B (2011) Geographic trends in incidence of hip fractures: a comprehensive literature review. Osteoporos Int 22:2575–2586

    Article  CAS  PubMed  Google Scholar 

  13. Ross PD, Fujiwara S, Huang C, Davis JW, Epstein RS, Wasnich RD, Kodama K, Melton LJ 3rd (1995) Vertebral fracture prevalence in women in Hiroshima compared to Caucasians or Japanese in the US. Int J Epidemiol 24:1171–1177

  14. Iki M, Tamaki J, Sato Y, Morita A, Ikeda Y, Kajita E, Nishino H, Akiba T, Matsumoto T, Kagamimori S, Kagawa Y, Yoneshima H, Matsukura T, Yamagami T, Kitagawa J, the JPOS Study Group (2014) Cohort profile: the Japanese Population-based Osteoporosis (JPOS) cohort study. Intern J Epidemiol. doi:10.1093/ije/dyu084

    Google Scholar 

  15. Iki M, Kagamimori S, Kagawa Y, Matsuzaki T, Yoneshima H, Marumo F (2001) Bone mineral density of the spine, hip and distal forearm in representative samples of the Japanese female population: Japanese Population-based Osteoporosis (JPOS) Study. Osteoporos Int 12:529–537

    Article  CAS  PubMed  Google Scholar 

  16. Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S (2008) International Society for Clinical Densitometry 2007 adult and pediatric official positions. Bone 43:1115–1121

    Article  PubMed  Google Scholar 

  17. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Proceedings of the second international symposium on information theory. Akademiai Kiado, Budapest, pp 267–281

  18. Marquardt DW (1963) An algorithm for least-squares estimation of nonlinear parameters. J Soc Ind Appl Math 11:431–441

    Article  Google Scholar 

  19. SAS Institute Inc (2008) Chapter 60. The NLIN Procedure. SAS/STAT®9.2 User’s Guide. SAS Institute Inc, Cary, NC

  20. Kanis JA, Melton LJ 3rd, Christiansen C, Johnston CC, Khaltaev N (1994) The diagnosis of osteoporosis. J Bone Miner Res 9:1137–1141

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  22. Hanson J (1997) Standardization of femur BMD. J Bone Miner Res 12:1316–1317

    Article  CAS  PubMed  Google Scholar 

  23. Kiebzak GM, Binkley N, Lewiecki EM, Miller PD (2007) Diagnostic agreement at the total hip using different DXA systems and the NHANES III database. J Clin Densitom 10:132–137

    Article  PubMed  Google Scholar 

  24. Cleary MP, Grossmann ME (2009) Minireview: obesity and breast cancer: the estrogen connection. Endocrinology 150(6):2537–2542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Bezemer ID, Rinaldi S, Dossus L, Gils CH, Peeters PH, Noord PA, Bueno-de-Mesquita HB, Johnsen SP, Overvad K, Olsen A, Tjønneland A, Boeing H, Lahmann PH, Linseisen J, Nagel G, Allen N, Roddam A, Bingham S, Khaw KT, Kesse E, Téhard B, Clavel-Chapelon F, Agudo A, Ardanaz E, Quiros JR, Amiano P, Martínez-Garcia C, Tormo MJ, Pala V, Panico S, Vineis P, Palli D, Tumino R, Trichopoulou A, Baibas N, Zilis D, Hémon B, Norat T, Riboli E, Kaaks R (2005) C-peptide, IGF-I, sex-steroid hormones and adiposity: a cross-sectional study in healthy women within the European Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Causes Control 16:561–572

    Article  PubMed  Google Scholar 

  26. Lundberg V, Tolonen H, Stegmayr B, Kuulasmaa K, Asplund K, WHO MONICA Project (2004) Use of oral contraceptives and hormone replacement therapy in the WHO MONICA project. Maturitas 48:39–49

    Article  CAS  PubMed  Google Scholar 

  27. Arima M (2009) The social situation of usage of hormone therapy among Japanese working women with quality of life: comparison of menopausal situation with other countries. Health Care Menopaus Elder Women (Kounenki to karei no herusukea) 8:60–66 (in Japanese)

    Google Scholar 

  28. Wu XP, Liao EY, Huang G, Dai RC, Zhang H (2003) A comparison study of the reference curves of bone mineral density at different skeletal sites in native Chinese, Japanese, and American Caucasian women. Calcif Tissue Int 73:122–132

    Article  CAS  PubMed  Google Scholar 

  29. Park EJ, Joo IW, Jang MJ, Kim YT, Oh K, Oh HJ (2014) Prevalence of osteoporosis in the Korean population based on Korea National Health and Nutrition Examination Survey (KNHANES), 2008–2011. Yonsei Med J 55:1049–1057

    Article  PubMed Central  PubMed  Google Scholar 

  30. Ho-Pham LT, Nguyen UD, Pham HN, Nguyen ND, Nguyen TV (2011) Reference ranges for bone mineral density and prevalence of osteoporosis in Vietnamese men and women. BMC Musculoskelet Disord 12:182

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank the personnel at the health departments of municipalities studied (Miyakojima, Sanuki, Nishi-aizu, Memuro, Joetsu, Iwate, and Kousa) for their excellent support and Toyo Medic Co., Osaka, Japan, and Toyukai Medical Corporation, Tokyo, Japan, for their technical assistance.

This study represents a part of the research conducted by the JPOS study group (Chairman Hideo Yoneshima, MD, PhD, President, Shuwa General Hospital) comprising Fumiaki Marumo (former chairman, Professor Emeritus, Tokyo Medical and Dental University), Toshihisa Matsuzaki (former co-chairman, Professor Emeritus, University of the Ryukyus), Takashi Akiba (Tokyo Women’s Medical University), Etsuko Kajita (Nagoya University School of Health Sciences), Harumi Nishino (Toyama Pharmaceutical Association), Tomoharu Matsukura (Toyama Prefectural Government), Toshio Matsumoto (University of Tokushima Graduate School of Medical Sciences), and Takashi Yamagami (Hokuriku Health Service Association), in addition to the authors.

Financial support for the JPOS baseline study was provided by the Japanese Ministry of Agriculture, Forestries and Fisheries, the Japan Milk Promotion Board, and the Japan Dairy Council. TBS-related studies were financially supported by Grants-in-Aid for Exploratory Research (No. 25670326, 2013–2014) from the Japanese Society for the Promotion of Science.

Conflicts of interest

Renaud Winzenrieth is a senior scientist at Med-Imaps. Masayuki Iki, Junko Tamaki, Yuho Sato, Sadanobu Kagamimori, Yoshiko Kagawa, and Hideo Yoneshima declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Public Health, Kinki University Faculty of Medicine, 377-2 Oono-higashi, Osaka-Sayama, Osaka, 589-8511, Japan

    M. Iki

  2. Department of Hygiene and Public Health, Osaka Medical College, 2-7 Daigaku-machi, Takatsuki, Osaka, 569-8686, Japan

    J. Tamaki

  3. Department of Human Life, Jin-ai University, 3-1-1 Otemachi, Echizen, Fukui, 915-8586, Japan

    Y. Sato

  4. Med-Imaps, Hôpital Xavier Arnozan, Avenue du Haut Lévèque, Pessac, 33600, Bordeaux , France

    R. Winzenrieth

  5. University of Toyama, 2630 Sugitani, Toyama, Toyama, 930-0194, Japan

    S. Kagamimori

  6. Kagawa Nutrition University, 3-9-21 Chiyoda, Sakado, Saitama, 350-0288, Japan

    Y. Kagawa

  7. Shuwa General Hospital, 1200 Tanihara-shinden, Kasukabe, Saitama, 344-0035, Japan

    H. Yoneshima

Authors
  1. M. Iki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Tamaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Winzenrieth
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Kagamimori
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Y. Kagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Yoneshima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Iki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iki, M., Tamaki, J., Sato, Y. et al. Age-related normative values of trabecular bone score (TBS) for Japanese women: the Japanese Population-based Osteoporosis (JPOS) study. Osteoporos Int 26, 245–252 (2015). https://doi.org/10.1007/s00198-014-2856-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-014-2856-5

Keywords

Search

Navigation