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Trabecular bone score in kidney transplant recipients

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Abstract

Summary

It is uncertain whether bone mineral density (BMD) can accurately predict fracture in kidney transplant recipients. Trabecular bone score (TBS) provides information independent of BMD. Kidney transplant recipients had abnormal bone texture as measured by lumbar spine TBS, and a lower TBS was associated with incident fractures in recipients.

Introduction

Trabecular bone score (TBS) is a texture measure derived from dual energy X-ray absorptiometry (DXA) lumbar spine images, providing information independent of bone mineral density. We assessed characteristics associated with TBS and fracture outcomes in kidney transplant recipients.

Methods

We included 327 kidney transplant recipients from Manitoba, Canada, who received a post-transplant DXA (median 106 days post-transplant). We matched each kidney transplant recipient (mean age 45 years, 39 % men) to three controls from the general population (matched on age, sex, and DXA date). Lumbar spine (L1-L4) DXA images were used to derive TBS. Non-traumatic incident fracture (excluding hand, foot, and craniofacial) (n = 31) was assessed during a mean follow-up of 6.6 years. We used multivariable linear regression models to test predictors of TBS, and multivariable Cox proportional hazard regression was used to estimate hazard ratios (HRs) per standard deviation decrease in TBS to express the gradient of risk.

Results

Compared to the general population, kidney transplant recipients had a significantly lower lumbar spine TBS (1.365 ± 0.129 versus 1.406 ± 0.125, P < 0.001). Multivariable linear regression revealed that receipt of a kidney transplant was associated with a significantly lower mean TBS compared to controls (−0.0369, 95 % confidence interval [95 % CI] −0.0537 to −0.0202). TBS was associated with fractures independent of the Fracture Risk Assessment score including BMD (adjusted HR per standard deviation decrease in TBS 1.64, 95 % CI 1.15–2.36).

Conclusion

Kidney transplant recipients had abnormal bone texture as assessed by TBS and a lower lumbar spine TBS was associated with fractures in recipients.

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References

  1. Abbott KC, Oglesby RJ, Hypolite IO, Kirk AD, Ko CW, Welch PG, Agodoa LY, Duncan WE (2001) Hospitalizations for fractures after renal transplantation in the United States. Ann Epidemiol 11:450–457

    Article  CAS  PubMed  Google Scholar 

  2. Conley E, Muth B, Samaniego M, Lotfi M, Voss B, Armbrust M, Pirsch J, Djamali A (2008) Bisphosphonates and bone fractures in long-term kidney transplant recipients. Transplantation 86:231–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kalker AJ, Pirsch JD, Heisey D, Sollinger HW, Beizer FO, Knechtle SJ, D'Alessandro AM (1996) Foot problems in the diabetic transplant recipient. Clin Transpl 10:503–510

    CAS  Google Scholar 

  4. Nikkel LE, Hollenbeak CS, Fox EJ, Uemura T, Ghahramani N (2009) Risk of fractures after renal transplantation in the United States. Transplantation 87:1846–1851

    Article  PubMed  Google Scholar 

  5. Ramsey-Goldman R, Dunn JE, Dunlop DD, Stuart FP, Abecassis MM, Kaufman DB, Langman CB, Salinger MH, Sprague SM (1999) Increased risk of fracture in patients receiving solid organ transplants. J Bone Miner Res 14:456–463

    Article  CAS  PubMed  Google Scholar 

  6. Vautour LM, Melton ILJ, Clarke BL, Achenbach SJ, Oberg AL, McCarthy JT (2004) Long-term fracture risk following renal transplantation: a population-based study. Osteoporos Int 15:160–167

    Article  PubMed  Google Scholar 

  7. Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, Kestenbaum BB, Stehman-Breen C (2002) Risk of hip fracture among dialysis and renal transplant recipients. J Am Med Assoc 288:3014–3018

    Article  Google Scholar 

  8. Rizzari MD, Suszynski TM, Gillingham KJ, Dunn TB, Ibrahim HN, Payne WD, Chinnakotla S, Finger EB, Sutherland DE, Kandaswamy R, Najarian JS, Pruett TL, Kukla A, Spong R, Matas AJ (2012) Ten-year outcome after rapid discontinuation of prednisone in adult primary kidney transplantation. Clin J Am Soc Nephrol 7:494–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Nikkel LE, Mohan S, Zhang A, McMahon DJ, Boutroy S, Dube G, Tanriover B, Cohen D, Ratner L, Hollenbeak CS, Leonard MB, Shane E, Nickolas TL (2012) Reduced fracture risk with early corticosteroid withdrawal after kidney transplant. Am J Transplant 12:649–659

    Article  CAS  PubMed  Google Scholar 

  10. Kidney Disease Imrpoving Global Outcomes (KDIGO) Work Group (2009) KDIGO clinical practice guidelines for the prevention, diagnosis, evaluation, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl 113:S1–130

    Google Scholar 

  11. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM (1993) Bone density at various sites for prediction of hip fractures. The study of osteoporotic fractures research group. Lancet 341:72–75

    Article  CAS  PubMed  Google Scholar 

  12. Schott AM, Cormier C, Hans D et al (1998) How hip and whole-body bone mineral density predict hip fracture in elderly women: the EPIDOS prospective study. Osteoporos Int 8:247–254

    Article  CAS  PubMed  Google Scholar 

  13. Mussolino ME, Gillum RF (2008) Low bone mineral density and mortality in men and women: the third national health and nutrition examination survey linked mortality file. Ann Epidemiol 18:847–850

    Article  PubMed  PubMed Central  Google Scholar 

  14. Qu X, Huang X, Jin F, Wang H, Hao Y, Tang T, Dai K (2013) Bone mineral density and all-cause, cardiovascular and stroke mortality: a meta-analysis of prospective cohort studies. Int J Cardiol 166:385–393

    Article  PubMed  Google Scholar 

  15. Akaberi S, Simonsen O, Lindergard B, Nyberg G (2008) Can DXA predict fractures in renal transplant patients? Am J Transplant 8:2647–2651

    Article  CAS  PubMed  Google Scholar 

  16. Grotz WH, Mundinger FA, Gugel B, Exner V, Kirste G, Schollmeyer PJ (1994) Bone fracture and osteodensitometry with dual energy X-ray absorptiometry in kidney transplant recipients. Transplantation 58:912–915

    Article  CAS  PubMed  Google Scholar 

  17. Durieux S, Mercadal L, Orcel P et al (2002) Bone mineral density and fracture prevalence in long-term kidney graft recipients. Transplantation 74:496–500

    Article  CAS  PubMed  Google Scholar 

  18. Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29:518–530

    Article  PubMed  Google Scholar 

  19. 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 

  20. 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 

  21. 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 

  22. 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 

  23. 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 

  24. Popp AW, Meer S, Krieg MA, Perrelet R, Hans D, Lippuner K (2015) Bone mineral density (BMD) and vertebral trabecular bone score (TBS) for the identification of elderly women at high risk for fracture: the SEMOF cohort study. Eur Spine J. Epub 2015 May 27.

  25. Leslie WD, Aubry-Rozier B, Lamy O, Hans D (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98:602–609

    Article  CAS  PubMed  Google Scholar 

  26. Breban S, Briot K, Kolta S, Paternotte S, Ghazi M, Fechtenbaum J, Roux C (2012) Identification of rheumatoid arthritis patients with vertebral fractures using bone mineral density and trabecular bone score. J Clin Densitom 15:260–266

    Article  PubMed  Google Scholar 

  27. Ulivieri FM, Silva BC, Sardanelli F, Hans D, Bilezikian JP, Caudarella R (2014) Utility of the trabecular bone score (TBS) in secondary osteoporosis. Endocrine 47:435–448

    Article  CAS  PubMed  Google Scholar 

  28. Paggiosi MA, Peel NF, Eastell R (2015) The impact of glucocorticoid therapy on trabecular bone score in older women. Osteoporos Int 26:1773–1780

    Article  CAS  PubMed  Google Scholar 

  29. Manitoba Health (2012) Part Two Manitoba Health Population Report. http://www.gov.mb.ca/health/population/parttwo.pdf. Accessed 27 June 2015.

  30. Roos NP, Shapiro E (1999) Revisiting the manitoba centre for health policy and evaluation and its population-based health information system. Med Care 37:JS10–14

    CAS  PubMed  Google Scholar 

  31. Kozyrskyj AL, Mustard CA (1998) Validation of an electronic, population-based prescription database. Ann Pharmacother 32:1152–1157

    Article  CAS  PubMed  Google Scholar 

  32. Jeffery JR, Leslie WD, Karpinski ME, Nickerson PW, Rush DN (2003) Prevalence and treatment of decreased bone density in renal transplant recipients: a randomized prospective trial of calcitriol versus alendronate. Transplantation 76:1498–1502

    Article  PubMed  Google Scholar 

  33. Looker AC, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP, Johnston CC Jr, Lindsay R (1998) Updated data on proximal femur bone mineral levels of US adults. Osteoporos Int 8:468–489

    Article  CAS  PubMed  Google Scholar 

  34. World Health Organization (2011) FRAX World Health Organization Fracture Risk Assessment Tool. http:// www.shef.ac.uk/FRAX/index.aspx. Accessed 29 June 2015.

  35. Lix LM, Azimaee M, Osman BA, Caetano P, Morin S, Metge C, Goltzman D, Kreiger N, Prior J, Leslie WD (2012) Osteoporosis-related fracture case definitions for population-based administrative data. BMC Public Health 12:301

    Article  PubMed  PubMed Central  Google Scholar 

  36. Tamblyn R, Reid T, Mayo N, McLeod P, Churchill-Smith M (2000) Using medical services claims to assess injuries in the elderly: sensitivity of diagnostic and procedure codes for injury ascertainment. J Clin Epidemiol 53:183–194

    Article  CAS  PubMed  Google Scholar 

  37. Naylor KL, Garg AX, Hodsman AB, Rush DN, Leslie WD (2014) Long-term changes in bone mineral density in kidney transplant recipients. Transplantation 98:1279–85

    Article  PubMed  Google Scholar 

  38. Weisinger JR, Carlini RG, Rojas E, Bellorin-Font E (2006) Bone disease after renal transplantation. Clin J Am Soc Nephrol 1:1300–1313

    Article  CAS  PubMed  Google Scholar 

  39. Keaveny TM, Bouxsein ML (2008) Theoretical implications of the biomechanical fracture threshold. J Bone Miner Res 23:1541–1547

    Article  PubMed  PubMed Central  Google Scholar 

  40. Chesnut C, Majumdar S, Gardner J, Shields A, Newitt DC, Erickson E, Glott M, Kriegman A, Mindeholm L (2001) Assessment of bone quality, quantity, and turnover with multiple methodologies at multiple skeletal sites. Adv Exp Med Biol 496:95–97

    Article  CAS  PubMed  Google Scholar 

  41. Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515

    Article  CAS  PubMed  Google Scholar 

  42. Leslie WD, Johansson H, Kanis JA, Lamy O, Oden A, McCloskey EV, Hans D (2014) Lumbar spine texture enhances 10-year fracture probability assessment. Osteoporos Int 25:2271–2277

    Article  CAS  PubMed  Google Scholar 

  43. McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H, Kanis JA (2015) Adjusting fracture probability by trabecular bone score. Calcif Tissue Int 96:500–509

    Article  CAS  PubMed  Google Scholar 

  44. Carlini RG, Rojas E, Weisinger JR, Lopez M, Martinis R, Arminio A, Bellorin-Font E (2000) Bone disease in patients with long-term renal transplantation and normal renal function. Am J Kidney Dis 36:160–166

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Dr. Naylor is supported by the Canadian Institutes of Health Research Fellowship and the Canadian National Transplant Research Program Astellas Training Award. The authors are indebted to Manitoba Health for the provision of data (HIPC File No. 2011/2012–31). The results and conclusions are those of the authors, and no official endorsement by Manitoba Health is intended or should be inferred. This article has been reviewed and approved by the members of the Manitoba Bone Density Program Committee.

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Correspondence to W. D. Leslie.

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Conflicts of interest

Didier Hans: Co-ownership in the TBS patent. Stock options or royalties: Med-Imaps. William Leslie: Speaker bureau (paid to facility): Amgen, Eli Lily, Novartis. Research grants (paid to facility): Amgen, Genzyme. Amit Garg: Investigator-initiated grant from Astellas and Roche for a Canadian Institutes of Health Research study in living kidney donors and his institution received unrestricted research funding from Pfizer. David Rush: Advisory board member, Astellas; Grant investigator, Astellas; Speaker: Astellas, STA Communications, Pfizer. Kyla Naylor, Lisa M Lix, and Anthony B. Hodsman declare that they have no conflict of interest.

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Naylor, K.L., Lix, L.M., Hans, D. et al. Trabecular bone score in kidney transplant recipients. Osteoporos Int 27, 1115–1121 (2016). https://doi.org/10.1007/s00198-015-3424-3

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