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Clinical predictors of incipient vertebral fractures and bone mineral density in kidney transplant patients

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Abstract

Purpose

Kidney transplant recipients are prone to metabolic bone diseases and consequent fractures. This study aimed to evaluate the incidence of incipient vertebral fractures, osteopenia, osteoporosis, and the clinical factors associated with incipient vertebral fractures in a group of kidney transplant patients.

Methods

Two hundred sixty-four patients (F/M 124/140, 45.3 ± 13 years) who had undergone kidney transplantation in tertiary care centers were included. Vertebral fractures were assessed semiquantitatively using conventional thoracolumbar lateral radiography in 202 of the patients.

Results

Vertebral fractures were observed in 56.4% (n = 114) of the study group. The frequency of osteoporosis was 20.0% (53 of 264 patients), and osteopenia was 35.6% (94 of 264 patients). Bone mineral density (BMD) levels were in the normal range in 40.3% (n = 46) of the subjects with vertebral fractures. It was in the osteoporotic range in 20.1% (n = 23) and the osteopenic range in 40.3% (n = 46). Vertebral fractures were associated with age, duration of hemodialysis, BMI, and femoral neck Z score (R2 37.8%, p = 0.027).

Conclusion

As incipient vertebral fractures can be observed in patients with normal BMD levels in kidney transplant recipients, conventional X-ray screening for vertebral fractures may be beneficial for a proper therapy decision of metabolic bone disease in kidney transplant recipients.

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References

  1. Park WY, Han S, Choi BS, Park CW, Yang CW, Kim YS, Kim JI, Moon IS, Chung BH (2017) Progression of osteoporosis after kidney transplantation in patients with end-stage renal disease. Transplant Proc 49:1033–1037. https://doi.org/10.1016/j.transproceed.2017.03.038

    Article  CAS  PubMed  Google Scholar 

  2. Unal A, Kocyigit I, Sipahioglu MH, Tokgoz B, Kavuncuoglu F, Oymak O, Utas C (2010) Loss of bone mineral density in renal transplantation recipients. Transplant Proc 42:3550–3553. https://doi.org/10.1016/j.transproceed.2010.07.106

    Article  CAS  PubMed  Google Scholar 

  3. Techawathanawanna N, Avihingsanon Y, Praditpornsilpa K, Kingpetch K, Suwanwalaikorn S, Kanjanabuch T, Eiam-Ong S, Tungsanga K (2005) The prevalence and risk factors of osteoporosis in Thai renal-transplant patients. J Med Assoc Thai 88(Suppl 4):S103-109

    PubMed  Google Scholar 

  4. Durieux S, Mercadal L, Orcel P, Dao H, Rioux C, Bernard M, Rozenberg S, Barrou B, Bourgeois P, Deray G, Bagnis CI (2002) Bone mineral density and fracture prevalence in long-term kidney graft recipients. Transplantation 74:496–500. https://doi.org/10.1097/00007890-200208270-00011

    Article  CAS  PubMed  Google Scholar 

  5. Akaberi S, Simonsen O, Lindergard B, Nyberg G (2008) Can DXA predict fractures in renal transplant patients? Am J Transplant 8:2647–2651. https://doi.org/10.1111/j.1600-6143.2008.02423.x

    Article  CAS  PubMed  Google Scholar 

  6. Marcen R, Caballero C, Uriol O, Fernandez A, Villafruela JJ, Pascual J, Martins J, Rodriguez N, Burgos FJ, Ortuno J (2007) Prevalence of osteoporosis, osteopenia, and vertebral fractures in long-term renal transplant recipients. Transplant Proc 39:2256–2258. https://doi.org/10.1016/j.transproceed.2007.07.073

    Article  CAS  PubMed  Google Scholar 

  7. Pereira S, Pedroso S, Martins L, Santos P, Almeida M, Freitas C, Dias L, Dores J, Almeida R, Castro Henriques A, Teixeira M (2010) Bone mineral density after simultaneous kidney-pancreas transplantation: four years follow-up of 57 recipients. Transplant Proc 42:555–557. https://doi.org/10.1016/j.transproceed.2010.01.046

    Article  CAS  PubMed  Google Scholar 

  8. Falkiewicz K, Boratynska M, Zmonarski SC, Milewicz A, Patrzalek D, Biecek P, Klinger M (2009) Evolution of bone disease at 2 years after transplantation: a single-center study. Transplant Proc 41:3063–3066. https://doi.org/10.1016/j.transproceed.2009.09.041

    Article  CAS  PubMed  Google Scholar 

  9. Mikuls TR, Julian BA, Bartolucci A, Saag KG (2003) Bone mineral density changes within six months of renal transplantation. Transplantation 75:49–54. https://doi.org/10.1097/00007890-200301150-00009

    Article  CAS  PubMed  Google Scholar 

  10. van der Jagt-Willems HC, van Munster BC, Lems WF (2013) Vertebral fractures in elderly adults: atypical presentation rather than asymptomatic. J Am Geriatr Soc 61:2047–2048. https://doi.org/10.1111/jgs.12520

    Article  PubMed  Google Scholar 

  11. Nevitt MC, Ettinger B, Black DM, Stone K, Jamal SA, Ensrud K, Segal M, Genant HK, Cummings SR (1998) The association of radiographically detected vertebral fractures with back pain and function: a prospective study. Ann Intern Med 128:793–800. https://doi.org/10.7326/0003-4819-128-10-199805150-00001

    Article  CAS  PubMed  Google Scholar 

  12. Oleksik A, Lips P, Dawson A, Minshall ME, Shen W, Cooper C, Kanis J (2000) Health-related quality of life in postmenopausal women with low BMD with or without prevalent vertebral fractures. J Bone Miner Res 15:1384–1392. https://doi.org/10.1359/jbmr.2000.15.7.1384

    Article  CAS  PubMed  Google Scholar 

  13. Kado DM, Browner WS, Palermo L, Nevitt MC, Genant HK, Cummings SR (1999) Vertebral fractures and mortality in older women: a prospective study. Study of Osteoporotic Fractures Research Group. Arch Intern Med 159:1215–1220. https://doi.org/10.1001/archinte.159.11.1215

    Article  CAS  PubMed  Google Scholar 

  14. Rajapakse CS, Leonard MB, Bhagat YA, Sun W, Magland JF, Wehrli FW (2012) Micro-MR imaging-based computational biomechanics demonstrates reduction in cortical and trabecular bone strength after renal transplantation. Radiology 262:912–920. https://doi.org/10.1148/radiol.11111044

    Article  PubMed  PubMed Central  Google Scholar 

  15. Julian BA, Laskow DA, Dubovsky J, Dubovsky EV, Curtis JJ, Quarles LD (1991) Rapid loss of vertebral mineral density after renal transplantation. N Engl J Med 325:544–550. https://doi.org/10.1056/NEJM199108223250804

    Article  CAS  PubMed  Google Scholar 

  16. Horber FF, Casez JP, Steiger U, Czerniak A, Montandon A, Jaeger P (1994) Changes in bone mass early after kidney transplantation. J Bone Miner Res 9:1–9. https://doi.org/10.1002/jbmr.5650090102

    Article  CAS  PubMed  Google Scholar 

  17. Pichette V, Bonnardeaux A, Prudhomme L, Gagne M, Cardinal J, Ouimet D (1996) Long-term bone loss in kidney transplant recipients: a cross-sectional and longitudinal study. Am J Kidney Dis 28:105–114. https://doi.org/10.1016/s0272-6386(96)90138-9

    Article  CAS  PubMed  Google Scholar 

  18. Patel S, Kwan JT, McCloskey E, McGee G, Thomas G, Johnson D, Wills R, Ogunremi L, Barron J (2001) Prevalence and causes of low bone density and fractures in kidney transplant patients. J Bone Miner Res 16:1863–1870. https://doi.org/10.1359/jbmr.2001.16.10.1863

    Article  CAS  PubMed  Google Scholar 

  19. Giannini S, D’Angelo A, Carraro G, Antonello A, Di Landro D, Marchini F, Plebani M, Zaninotto M, Rigotti P, Sartori L, Crepaldi G (2001) Persistently increased bone turnover and low bone density in long-term survivors to kidney transplantation. Clin Nephrol 56:353–363

    CAS  PubMed  Google Scholar 

  20. Braga Junior JW, Neves RM, Pinheiro MM, Frisoli Junior A, Castro CH, Szejnfeld VL, Carvalho AB (2006) Prevalence of low trauma fractures in long-term kidney transplant patients with preserved renal function. Braz J Med Biol Res 39:137–147. https://doi.org/10.1590/s0100-879x2006000100016

    Article  CAS  PubMed  Google Scholar 

  21. Elmstedt E, Svahn T (1981) Skeletal complications following renal transplantation. Acta Orthop Scand 52:279–286. https://doi.org/10.3109/17453678109050104

    Article  CAS  PubMed  Google Scholar 

  22. 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. https://doi.org/10.1097/TP.0b013e3181a6bbda

    Article  PubMed  Google Scholar 

  23. Nam JH, Moon JI, Chung SS, Kim SI, Park KI, Song YD, Kim KR, Lee HC, Huh K, Lim SK (2000) Prevalence and risk factors for vertebral fractures in renal transplants. Transplant Proc 32:1877. https://doi.org/10.1016/s0041-1345(00)01472-x

    Article  CAS  PubMed  Google Scholar 

  24. Vautour LM, Melton LJ 3rd, 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. https://doi.org/10.1007/s00198-003-1532-y

    Article  PubMed  Google Scholar 

  25. O’Shaughnessy EA, Dahl DC, Smith CL, Kasiske BL (2002) Risk factors for fractures in kidney transplantation. Transplantation 74:362–366. https://doi.org/10.1097/00007890-200208150-00012

    Article  PubMed  Google Scholar 

  26. Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8:1137–1148. https://doi.org/10.1002/jbmr.5650080915

    Article  CAS  PubMed  Google Scholar 

  27. Van der Klift M, De Laet CE, McCloskey EV, Hofman A, Pols HA (2002) The incidence of vertebral fractures in men and women: the Rotterdam Study. J Bone Miner Res 17:1051–1056. https://doi.org/10.1359/jbmr.2002.17.6.1051

    Article  PubMed  Google Scholar 

  28. Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, Kestenbaum BR, Stehman-Breen C (2002) Risk of hip fracture among dialysis and renal transplant recipients. JAMA 288:3014–3018. https://doi.org/10.1001/jama.288.23.3014

    Article  PubMed  Google Scholar 

  29. 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. https://doi.org/10.1097/00007890-199410270-00009

    Article  CAS  PubMed  Google Scholar 

  30. Braga Júnior JW, Neves RM, Pinheiro MM, Frisoli Júnior A, Castro CH, Szejnfeld VL, Carvalho AB (2006) Prevalence of low trauma fractures in long-term kidney transplant patients with preserved renal function. Braz J Med Biol Res 39:137–147. https://doi.org/10.1590/s0100-879x2006000100016

    Article  PubMed  Google Scholar 

  31. Evenepoel P, Claes K, Meijers B, Laurent MR, Bammens B, Naesens M, Sprangers B, Pottel H, Cavalier E, Kuypers D (2019) Bone mineral density, bone turnover markers, and incident fractures in de novo kidney transplant recipients. Kidney Int 95:1461–1470. https://doi.org/10.1016/j.kint.2018.12.024

    Article  PubMed  Google Scholar 

  32. Schreiber PW, Bischoff-Ferrari HA, Boggian K, Bonani M, van Delden C, Enriquez N, Fehr T, Garzoni C, Hirsch HH, Hirzel C, Manuel O, Meylan P, Saleh L, Weisser M, Mueller NJ, Swiss Transplant Cohort S (2018) Bone metabolism dynamics in the early post-transplant period following kidney and liver transplantation. PLoS ONE 13:e0191167. https://doi.org/10.1371/journal.pone.0191167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nisbeth U, Lindh E, Ljunghall S, Backman U, Fellstrom B (1999) Increased fracture rate in diabetes mellitus and females after renal transplantation. Transplantation 67:1218–1222. https://doi.org/10.1097/00007890-199905150-00004

    Article  CAS  PubMed  Google Scholar 

  34. Giannini S, Sella S, Silva Netto F, Cattelan C, Dalle Carbonare L, Lazzarin R, Marchini F, Rigotti P, Marcocci C, Cetani F, Pardi E, D’Angelo A, Realdi G, Bonfante L (2010) Persistent secondary hyperparathyroidism and vertebral fractures in kidney transplantation: role of calcium-sensing receptor polymorphisms and vitamin D deficiency. J Bone Miner Res 25:841–848. https://doi.org/10.1359/jbmr.091025

    Article  CAS  PubMed  Google Scholar 

  35. Rolla D, Ballanti P, Marsano L, Bianchi G, Messa P, Paoletti E, Cannella G (2006) Bone disease in long-term renal transplant recipients with severe osteopenia: a cross-sectional study. Transplantation 81:915–921. https://doi.org/10.1097/01.tp.0000178376.02130.ca

    Article  PubMed  Google Scholar 

  36. Mazzaferro S, Diacinti D, Proietti E, Barresi G, Baldinelli M, Pisani D, D’Erasmo E, Pugliese F (2006) Morphometric X-ray absorptiometry in the assessment of vertebral fractures in renal transplant patients. Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association—European Renal Association 21:466–471. https://doi.org/10.1093/ndt/gfi206

    Article  Google Scholar 

  37. Heaf J, Tvedegaard E, Kanstrup IL, Fogh-Andersen N (2003) Hyperparathyroidism and long-term bone loss after renal transplantation. Clin Transplant 17:268–274. https://doi.org/10.1034/j.1399-0012.2003.00047.x

    Article  PubMed  Google Scholar 

  38. Vestergaard P, Mollerup CL, Frøkjaer VG, Christiansen P, Blichert-Toft M, Mosekilde L (2000) Cohort study of risk of fracture before and after surgery for primary hyperparathyroidism. BMJ (Clinical Research Ed) 321:598–602. https://doi.org/10.1136/bmj.321.7261.598

    Article  CAS  Google Scholar 

  39. De Geronimo S, Romagnoli E, Diacinti D, D’Erasmo E, Minisola S (2006) The risk of fractures in postmenopausal women with primary hyperparathyroidism. Eur J Endocrinol 155:415–420. https://doi.org/10.1530/eje.1.02225

    Article  CAS  PubMed  Google Scholar 

  40. Molnar MZ, Naser MS, Rhee CM, Kalantar-Zadeh K, Bunnapradist S (2014) Bone and mineral disorders after kidney transplantation: therapeutic strategies. Transplant Rev (Orlando) 28:56–62. https://doi.org/10.1016/j.trre.2013.12.003

    Article  Google Scholar 

  41. Kidney Disease: Improving Global Outcomes Transplant Work G (2009) KDIGO clinical practice guideline for the care of kidney transplant recipients. Am J Transplant 9(Suppl 3):S1-155. https://doi.org/10.1111/j.1600-6143.2009.02834.x

    Article  Google Scholar 

  42. Maalouf NM, Shane E (2005) Osteoporosis after solid organ transplantation. J Clin Endocrinol Metab 90:2456–2465. https://doi.org/10.1210/jc.2004-1978

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study did not receive any specific grants from any funding agencies in public, commercial, or not-for-profit sector.

Funding

This study did not receive specific grants from any funding agencies in the public, commercial, or not-for-profit sectors.

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Correspondence to Tugce Apaydin.

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All authors made substantial contributions to conception and design, and/or acquisition of data, analysis and interpretation of data participated in drafting the article or revising it critically for important intellectual content, and gave final approval of the version to be submitted.

Conflict of interest

Dilek Gogas Yavuz, Kadriye Aydin, Tugce Apaydın, Arzu Velioglu, Meral Mert, Zafer Pekkolay, Ergun Parmaksiz, Meral Mese, Ayse Esen Pazir, Emre Aydın, Onur Bugdayci, Serhan Tuglular declare that they have no conflict of interest.

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Gogas Yavuz, D., Aydin, K., Apaydin, T. et al. Clinical predictors of incipient vertebral fractures and bone mineral density in kidney transplant patients. Eur Spine J 31, 2423–2430 (2022). https://doi.org/10.1007/s00586-022-07162-6

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