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Chronic kidney disease is associated with low BMD at the hip but not at the spine

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Abstract

Summary

Although chronic kidney disease is associated with other bone disorders, osteoporosis can be found in this context, and it is defined based on bone mineral density (BMD), measured by dual-energy X-ray absorptiometry. As CKD progresses, the percentage of normal BMD decreases, whereas that of osteopenia/osteoporosis increases, mostly due to hip involvement, particularly in patients with reduced renal function.

Introduction

Osteoporosis is a highly prevalent disease in patients with chronic kidney disease (CKD). We investigated the features of bone mineral density (BMD) in patients with assorted kidney diseases and hypothesized that low BMD, as measured by dual-energy X-ray absorptiometry (DXA), would be more prevalent as kidney function decreased and would correlate with biomarkers of mineral and bone disease.

Methods

DXA obtained from January 1, 2008, to December 31, 2017, clinical, demographic, and biochemical data at the time of image acquisition were recorded. Data from 1172 patients were included in this study (81.3% women, 79.9% white, and 8.1% diabetic).

Results

Osteopenia and osteoporosis in at least one site (total hip or spine) were found in 32.7% and 20.0% of patients, respectively. As CKD progressed, the percentage of patients with normal BMD decreased, whereas the percentage of osteopenia and osteoporosis increased, which was mostly due to the total hip involvement, particularly in patients with estimated glomerular filtration rate (eGFR) < 60 ml/min/1.73 m2. Older age and hyperparathyroidism were independent risk factors for osteopenia/osteoporosis at the total hip; female gender, older age, and higher iCa were independently associated with the risk of osteopenia/osteoporosis at the spine. With eGFR > 90 ml/min as reference, the odds ratios for osteoporosis/osteopenia at the hip were 1.51 (95% CI 1.01–2.24) and 1.91 (95% CI 1.13–3.20) for patients with eGFR 30–60 and 15–30 ml/min/1.73 m2, respectively. No CKD stage was significantly associated with the risk of osteoporosis/osteopenia at the spine.

Conclusion

Our results highlighted that low BMD in patients with CKD is associated with age and hyperparathyroidism, and affects predominantly the hip.

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References

  1. Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359:1929–1936

    Article  PubMed  Google Scholar 

  2. Levey AS, Eckardt KU, Tsukamoto Y, Levin A, Coresh J, Rossert J, De Zeeuw D, Hostetter TH, Lameire N, Eknoyan G (2005) Definition and classification of chronic kidney disease: a position statement from kidney disease: improving global outcomes (KDIGO). Kidney Int 67:2089–2100

    Article  PubMed  Google Scholar 

  3. Denburg MR, Kumar J, Jemielita T, Brooks ER, Skversky A, Portale AA, Salusky IB, Warady BA, Furth SL, Leonard MB (2016) Fracture burden and risk factors in childhood CKD: results from the CKiD cohort study. J Am Soc Nephrol 27:543–550

    Article  CAS  PubMed  Google Scholar 

  4. Weisinger JR, Bellorin-Font E (2004) Outcomes associated with hypogonadism in women with chronic kidney disease. Adv Chronic Kidney Dis 11:361–370

    Article  PubMed  Google Scholar 

  5. Naylor KL, McArthur E, Leslie WD, Fraser LA, Jamal SA, Cadarette SM, Pouget JG, Lok CE, Hodsman AB, Adachi JD, Garg AX (2014) The three-year incidence of fracture in chronic kidney disease. Kidney Int 86:810–818

    Article  PubMed  Google Scholar 

  6. Avin KG, Moorthi RN (2015) Bone is not alone: the effects of skeletal muscle dysfunction in chronic kidney disease. Curr Osteoporos Rep 13:173–179

    Article  PubMed  PubMed Central  Google Scholar 

  7. Alem AM, Sherrard DJ, Gillen DL, Weiss NS, Beresford SA, Heckbert SR, Wong C, Stehman-Breen C (2000) Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int 58:396–399

    Article  CAS  PubMed  Google Scholar 

  8. Nickolas TL, McMahon DJ, Shane E (2006) Relationship between moderate to severe kidney disease and hip fracture in the United States. J Am Soc Nephrol 17:3223–3232

    Article  PubMed  Google Scholar 

  9. Khairallah P, Nickolas TL (2018) Management of osteoporosis in CKD. Clin J Am Soc Nephrol 13:962–969

    Article  PubMed  PubMed Central  Google Scholar 

  10. Kim SM, Long J, Montez-Rath M, Leonard M, Chertow GM (2016) Hip fracture in patients with non-dialysis-requiring chronic kidney disease. J Bone Miner Res 31:1803–1809

    Article  PubMed  Google Scholar 

  11. Klawansky S, Komaroff E, Cavanaugh PF Jr, Mitchell DY, Gordon MJ, Connelly JE, Ross SD (2003) Relationship between age, renal function and bone mineral density in the US population. Osteoporos Int 14:570–576

    Article  CAS  PubMed  Google Scholar 

  12. Moe SM (2017) Renal osteodystrophy or kidney-induced osteoporosis? Curr Osteoporos Rep 15:194–197

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yenchek RH, Ix JH, Shlipak MG, Bauer DC, Rianon NJ, Kritchevsky SB, Harris TB, Newman AB, Cauley JA, Fried LF, for the Health, Aging, and Body Composition Study (2012) Bone mineral density and fracture risk in older individuals with CKD. Clin J Am Soc Nephrol 7:1130–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. West SL, Lok CE, Langsetmo L, Cheung AM, Szabo E, Pearce D, Fusaro M, Wald R, Weinstein J, Jamal SA (2015) Bone mineral density predicts fractures in chronic kidney disease. J Bone Miner Res 30:913–919

    Article  PubMed  Google Scholar 

  15. Iimori S, Mori Y, Akita W, Kuyama T, Takada S, Asai T, Kuwahara M, Sasaki S, Tsukamoto Y (2012) Diagnostic usefulness of bone mineral density and biochemical markers of bone turnover in predicting fracture in CKD stage 5D patients—a single-center cohort study. Nephrol Dial Transplant 27:345–351

    Article  CAS  PubMed  Google Scholar 

  16. Isakova T, Nickolas TL, Denburg M, Yarlagadda S, Weiner DE, Gutiérrez OM, Bansal V, Rosas SE, Nigwekar S, Yee J, Kramer H (2017) KDOQI US commentary on the 2017 KDIGO clinical practice guideline update for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Am J Kidney Dis 70:737–751

    Article  PubMed  Google Scholar 

  17. Levey AS, Stevens LA, Schmid CH, Zhang Y(L), Castro AF III, Feldman HI, Kusek JW, Eggers P, van Lente F, Greene T, Coresh J, for the CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration) (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612

    Article  PubMed  PubMed Central  Google Scholar 

  18. 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 

  19. 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 

  20. Bianchi ML, Baim S, Bishop NJ, Gordon CM, Hans DB, Langman CB, Leonard MB, Kalkwarf HJ (2010) Official positions of the International Society for Clinical Densitometry (ISCD) on DXA evaluation in children and adolescents. Pediatr Nephrol 25:37–47

    Article  PubMed  Google Scholar 

  21. Babayev R, Nickolas TL (2015) Bone disorders in chronic kidney disease: an update in diagnosis and management. Semin Dial 28:645–653

    Article  PubMed  Google Scholar 

  22. Torres PU, Bover J, Mazzaferro S, de Vernejoul MC, Cohen-Solal M (2014) When, how, and why a bone biopsy should be performed in patients with chronic kidney disease. Semin Nephrol 34:612–625

    Article  PubMed  Google Scholar 

  23. Nickolas TL, Stein EM, Dworakowski E, Nishiyama KK, Komandah-Kosseh M, Zhang CA, McMahon DJ, Liu XS, Boutroy S, Cremers S, Shane E (2013) Rapid cortical bone loss in patients with chronic kidney disease. J Bone Miner Res 28:1811–1820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chen H, Lips P, Vervloet MG, van Schoor NM, de Jongh RT (2018) Association of renal function with bone mineral density and fracture risk in the longitudinal aging study Amsterdam. Osteoporos Int 29:2129–2138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jadoul M, Albert JM, Akiba T, Akizawa T, Arab L, Bragg-Gresham JL, Mason N, Prutz KG, Young EW, Pisoni RL (2006) Incidence and risk factors for hip or other bone fractures among hemodialysis patients in the dialysis outcomes and practice patterns study. Kidney Int 70:1358–1366

    Article  CAS  PubMed  Google Scholar 

  26. Maravic M, Ostertag A, Torres PU, Cohen-Solal M (2014) Incidence and risk factors for hip fractures in dialysis patients. Osteoporos Int 25:159–165

    Article  CAS  PubMed  Google Scholar 

  27. Wakasugi M, Kazama JJ, Taniguchi M, Wada A, Iseki K, Tsubakihara Y, Narita I (2013) Increased risk of hip fracture among Japanese hemodialysis patients. J Bone Miner Metab 31:315–321

    Article  PubMed  Google Scholar 

  28. Przedlacki J, Buczynska-Chyl J, Kozminski P et al (2018) The utility of FRAX(R) in predicting bone fractures in patients with chronic kidney disease on hemodialysis: a two-year prospective multicenter cohort study. Osteoporos Int 29:1105–1115

    Article  CAS  PubMed  Google Scholar 

  29. Marques ID, Araujo MJ, Graciolli FG, Reis LM, Pereira RM, Custodio MR, Jorgetti V, Elias RM, David-Neto E, Moyses RM (2017) Biopsy vs. peripheral computed tomography to assess bone disease in CKD patients on dialysis: differences and similarities. Osteoporos Int 28:1675–1683

    Article  CAS  PubMed  Google Scholar 

  30. Hall RK, Sloane R, Pieper C, Van Houtven C, LaFleur J, Adler R, Colon-Emeric C (2018) Competing risks of fracture and death in older adults with chronic kidney disease. J Am Geriatr Soc 66:532–538

    Article  PubMed  PubMed Central  Google Scholar 

  31. Hansen D, Olesen JB, Gislason GH, Abrahamsen B, Hommel K (2016) Risk of fracture in adults on renal replacement therapy: a Danish national cohort study. Nephrol Dial Transplant 31:1654–1662

    Article  PubMed  Google Scholar 

  32. Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22:465–475

    Article  PubMed  Google Scholar 

  33. Nickolas TL, Cremers S, Zhang A, Thomas V, Stein E, Cohen A, Chauncey R, Nikkel L, Yin MT, Liu XS, Boutroy S, Staron RB, Leonard MB, McMahon DJ, Dworakowski E, Shane E (2011) Discriminants of prevalent fractures in chronic kidney disease. J Am Soc Nephrol 22:1560–1572

    Article  PubMed  PubMed Central  Google Scholar 

  34. Coco M, Rush H (2000) Increased incidence of hip fractures in dialysis patients with low serum parathyroid hormone. Am J Kidney Dis 36:1115–1121

    Article  CAS  PubMed  Google Scholar 

  35. Atsumi K, Kushida K, Yamazaki K, Shimizu S, Ohmura A, Inoue T (1999) Risk factors for vertebral fractures in renal osteodystrophy. Am J Kidney Dis 33:287–293

    Article  CAS  PubMed  Google Scholar 

  36. Ambrus C, Almasi C, Berta K, Deak G, Marton A, Molnar MZ, Nemeth Z, Horvath C, Lakatos P, Szathmari M, Mucsi I (2011) Vitamin D insufficiency and bone fractures in patients on maintenance hemodialysis. Int Urol Nephrol 43:475–482

    Article  CAS  PubMed  Google Scholar 

  37. Bucur RC, Panjwani DD, Turner L, Rader T, West SL, Jamal SA (2015) Low bone mineral density and fractures in stages 3-5 CKD: an updated systematic review and meta-analysis. Osteoporos Int 26:449–458

    Article  CAS  PubMed  Google Scholar 

  38. Pimentel A, Urena-Torres P, Zillikens MC, Bover J, Cohen-Solal M (2017) Fractures in patients with CKD-diagnosis, treatment, and prevention: a review by members of the European Calcified Tissue Society and the European Renal Association of Nephrology Dialysis and Transplantation. Kidney Int 92:1343–1355

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Fatima Libânio for her assistance in collecting the electronic data.

Author information

Authors and Affiliations

  1. Nephrology Service, Hospital das Clinicas HCFMUSP, Universidade de Sao Paulo, Rua Dr. Enéas de Carvalho Aguiar 255, 7° andar, São Paulo, SP, 05403-000, Brazil

    K. S. Bezerra de Carvalho, R.F.V. Vasco, M.R. Custodio, V. Jorgetti, R.M.A. Moysés & R.M. Elias

  2. Hospital Samaritano, São Paulo, Brazil

    V. Jorgetti

  3. Universidade Nove de Julho, UNINOVE, São Paulo, Brazil

    R.M.A. Moysés & R.M. Elias

Authors
  1. K. S. Bezerra de Carvalho
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  2. R.F.V. Vasco
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  3. M.R. Custodio
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  4. V. Jorgetti
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  5. R.M.A. Moysés
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  6. R.M. Elias
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Contributions

Authors’ roles: Study design: KSBC, and RME. Study conduct: KSBC, RFVV, MRC, VJ, RMAM, and RME. Data collection: KSBC, RFVV, and RME. Data analysis: KSBC, RMAM, and RME. Data interpretation: KSBC, MRC, VJ, RMAM, and RME. Drafting manuscript: KSBC, RMAM and RME. Revising manuscript content: KSBC, MRC, VJ, RMAM, and RME. Approving final version of manuscript: KSBC, RFVV, MRC, VJ, RMAM, and RME. RME takes responsibility for the integrity of the data analysis.

Corresponding author

Correspondence to R.M. Elias.

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Conflicts of interest

KSBC, MRC, and RME have nothing to declare. VJ and RMAM are financially supported by CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant numbers 303684/2013-5 and 304249/2013-0, respectively). This financial support had no role in study design; collection, analysis, and interpretation of data; writing the report; and the decision to submit the report for publication.

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Bezerra de Carvalho, K.S., Vasco, R., Custodio, M. et al. Chronic kidney disease is associated with low BMD at the hip but not at the spine. Osteoporos Int 30, 1015–1023 (2019). https://doi.org/10.1007/s00198-019-04864-4

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