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Traditional and Non-traditional Risk Factors for Osteoporosis in CKD

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Abstract

Osteoporosis is a state of bone fragility with reduced skeletal resistance to trauma, and consequently increased risk of fracture. A wide range of conditions, including traditional risk factors, lifestyle choices, diseases and their treatments may contribute to bone fragility. It is therefore not surprising that the multi-morbid patient with chronic kidney disease (CKD) is at a particularly high risk. CKD is associated with reduced bone quantity, as well as impaired bone quality. Bone fragility in CKD is a composite of primary osteoporosis, accumulation of traditional and uremia-related risk factors, assaults brought on by systemic disease, and detrimental effects of drugs. Some risk factors are modifiable and represent potential targets for intervention. This review provides an overview of the heterogeneity of bone fragility in CKD.

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References

  1. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis and T (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA J Am Med Assoc 285:785–795. https://doi.org/10.1001/jama.285.6.785

    Article  Google Scholar 

  2. Jadoul M, Albert JM, Akiba T et al (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. https://doi.org/10.1038/sj.ki.5001754

    Article  CAS  PubMed  Google Scholar 

  3. Tentori F, McCullough K, Kilpatrick RD et al (2014) High rates of death and hospitalization follow bone fracture among hemodialysis patients. Kidney Int 85:166–173. https://doi.org/10.1038/ki.2013.279;10.1038/ki.2013.279

    Article  PubMed  Google Scholar 

  4. Yusuf AA, Hu Y, Chandler D et al (2020) Predictors of imminent risk of fracture in Medicare-enrolled men and women. Arch Osteoporos 15:120. https://doi.org/10.1007/s11657-020-00784-7

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bowling CB, Bromfield SG, Colantonio LD et al (2016) Association of reduced eGFR and albuminuria with serious fall injuries among older adults. Clin J Am Soc Nephrol 11:1236–1243. https://doi.org/10.2215/CJN.11111015

    Article  PubMed  PubMed Central  Google Scholar 

  6. Rossier A, Pruijm M, Hannane D et al (2012) Incidence, complications and risk factors for severe falls in patients on maintenance haemodialysis. Nephrol Dial Transplant 27:352–357. https://doi.org/10.1093/ndt/gfr326

    Article  PubMed  Google Scholar 

  7. Wang AY, Sherrington C, Toyama T et al (2017) Muscle strength, mobility, quality of life and falls in patients on maintenance haemodialysis: a prospective study. Nephrology (Carlton) 22:220–227. https://doi.org/10.1111/nep.12749

    Article  CAS  Google Scholar 

  8. Evenepoel P, Claes K, Meijers B et al (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 

  9. Mortensen SJ, Mohamadi A, Wright CL et al (2020) Medications as a risk factor for fragility hip fractures: a systematic review and meta-analysis. Calcif Tissue Int 107:1–9. https://doi.org/10.1007/s00223-020-00688-1

    Article  CAS  PubMed  Google Scholar 

  10. Moe S, Drüeke T, Cunningham J et al (2006) Definition, evaluation, and classification of renal osteodystrophy: a position statement from kidney disease: improving global outcomes (KDIGO). Kidney Int 69:1945–1953. https://doi.org/10.1038/sj.ki.5000414

    Article  CAS  PubMed  Google Scholar 

  11. Taal MW, Masud T, Green D, Cassidy MJ (1999) Risk factors for reduced bone density in haemodialysis patients. Nephrol Dial Transplant 14:1922–1928. https://doi.org/10.1093/ndt/14.8.1922

    Article  CAS  PubMed  Google Scholar 

  12. Weisinger JR, Gonzalez L, Alvarez H et al (2000) Role of persistent amenorrhea in bone mineral metabolism of young hemodialyzed women. Kidney Int 58:331–335. https://doi.org/10.1046/j.1523-1755.2000.00170.x

    Article  CAS  PubMed  Google Scholar 

  13. Weaver CM, Gordon CM, Janz KF et al (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27:1281–1386. https://doi.org/10.1007/s00198-015-3440-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Brockstedt H, Kassem M, Eriksen EF et al (1993) Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone 14:681–91. https://doi.org/10.1016/8756-3282(93)90092-o

    Article  CAS  PubMed  Google Scholar 

  15. Boros K, Freemont T (2017) Physiology of ageing of the musculoskeletal system. Best Pract Res Clin Rheumatol 31:203–217. https://doi.org/10.1016/j.berh.2017.09.003

    Article  PubMed  Google Scholar 

  16. Gosman JH, Stout SD, Larsen CS (2011) Skeletal biology over the life span: a view from the surfaces. Am J Phys Anthropol 146:86–98. https://doi.org/10.1002/ajpa.21612

    Article  PubMed  Google Scholar 

  17. Bailey AJ, Sims TJ, Ebbesen EN et al (1999) Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int 65:203–210. https://doi.org/10.1007/s002239900683

    Article  CAS  PubMed  Google Scholar 

  18. Kooman JP, Kotanko P, Schols AMWJ et al (2014) Chronic kidney disease and premature ageing. Nat Rev Nephrol 10:732–742. https://doi.org/10.1038/nrneph.2014.185

    Article  CAS  PubMed  Google Scholar 

  19. Rix M, Andreassen H, Eskildsen P et al (1999) Bone mineral density and biochemical markers of bone turnover in patients with predialysis chronic renal failure. Kidney Int 56:1084–1093. https://doi.org/10.1046/j.1523-1755.1999.00617.x

    Article  CAS  PubMed  Google Scholar 

  20. Hansen D, Olesen JB, Gislason GH et al (2016) Risk of fracture in adults on renal replacement therapy: a Danish national cohort study. Nephrol Dial Transplant 31:1654–1662. https://doi.org/10.1093/ndt/gfw073

    Article  PubMed  Google Scholar 

  21. Kramer HM, Curhan G, Singh A (2003) Hemodialysis and estrogen levels in postmenopausal (HELP) patients: the multicenter HELP study. Am J Kidney Dis 41:1240–1246. https://doi.org/10.1016/S0272-6386(03)00357-3

    Article  CAS  PubMed  Google Scholar 

  22. Khurana KK, Navaneethan SD, Arrigain S et al (2014) Serum testosterone levels and mortality in men with CKD stages 3–4. Am J Kidney Dis 64:367–374. https://doi.org/10.1053/j.ajkd.2014.03.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Carrero JJ, Qureshi AR, Nakashima A et al (2011) Prevalence and clinical implications of testosterone deficiency in men with end-stage renal disease. Nephrol Dial Transplant 26:184–190. https://doi.org/10.1093/ndt/gfq397

    Article  CAS  PubMed  Google Scholar 

  24. Ahmed SB, Ramesh S (2016) Sex hormones in women with kidney disease. Nephrol Dial Transplant 31:1787–1795. https://doi.org/10.1093/ndt/gfw084

    Article  CAS  PubMed  Google Scholar 

  25. Carrero JJ, Stenvinkel P (2012) The vulnerable man: impact of testosterone deficiency on the uraemic phenotype. Nephrol Dial Transplant 27:4030–4041. https://doi.org/10.1093/ndt/gfs383

    Article  CAS  PubMed  Google Scholar 

  26. Ji M-X, Yu Q (2015) Primary osteoporosis in postmenopausal women. Chronic Dis Transl Med 1:9–13. https://doi.org/10.1016/j.cdtm.2015.02.006

    Article  PubMed  PubMed Central  Google Scholar 

  27. Zhu L, Jiang X, Sun Y, Shu W (2016) Effect of hormone therapy on the risk of bone fractures: a systematic review and meta-analysis of randomized controlled trials. Menopause 23:461–470. https://doi.org/10.1097/GME.0000000000000519

    Article  PubMed  Google Scholar 

  28. Khosla S, Melton LJ, Riggs BL (2011) The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Miner Res 26:441–451. https://doi.org/10.1002/jbmr.262

    Article  CAS  PubMed  Google Scholar 

  29. LeBlanc ES, Nielson CM, Marshall LM et al (2009) The effects of serum testosterone, estradiol, and sex hormone binding globulin levels on fracture risk in older men. J Clin Endocrinol Metab 94:3337–3346. https://doi.org/10.1210/jc.2009-0206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shahinian VB, Kuo Y-F, Freeman JL, Goodwin JS (2005) Risk of fracture after androgen deprivation for prostate cancer. N Engl J Med 352:154–164. https://doi.org/10.1056/NEJMoa041943

    Article  CAS  PubMed  Google Scholar 

  31. Sugiya N, Nakashima A, Takasugi N et al (2011) Endogenous estrogen may prevent bone loss in postmenopausal hemodialysis patients throughout life. Osteoporos Int 22:1573–1579. https://doi.org/10.1007/s00198-010-1350-y

    Article  CAS  PubMed  Google Scholar 

  32. Jørgensen HS, Winther S, Bøttcher M et al (2018) Bioavailable testosterone is positively associated with bone mineral density in male kidney transplantation candidates. Kidney Int Rep 3:661–670. https://doi.org/10.1016/j.ekir.2018.01.009

    Article  PubMed  PubMed Central  Google Scholar 

  33. Aleksova J, Wong P, McLachlan R et al (2018) Sex hormone–binding globulin is a biomarker associated with nonvertebral fracture in men on dialysis therapy. Kidney Int 94:372–380. https://doi.org/10.1016/j.kint.2018.02.021

    Article  CAS  PubMed  Google Scholar 

  34. Mirfakhraee S, Sakhaee K, Zerwekh J et al (2012) Risk factors for diminished bone mineral density among male hemodialysis patients–a cross-sectional study. Arch Osteoporos 7:283–290. https://doi.org/10.1007/s11657-012-0110-3

    Article  PubMed  Google Scholar 

  35. Adami S, Palacios S, Rizzoli R et al (2014) The efficacy and safety of bazedoxifene in postmenopausal women by baseline kidney function status. Climacteric 17:273–284. https://doi.org/10.3109/13697137.2013.830605

    Article  CAS  PubMed  Google Scholar 

  36. Aleksova J, Rodriguez AJ, McLachlan R et al (2018) Gonadal hormones in the pathogenesis and treatment of bone health in patients with chronic kidney disease: a systematic review and meta-analysis. Curr Osteoporos Rep 16:674–692. https://doi.org/10.1007/s11914-018-0483-3

    Article  PubMed  Google Scholar 

  37. Matuszkiewicz-Rowinska J, Skorzewska K, Radowicki S et al (1999) The benefits of hormone replacement therapy in pre-menopausal women with oestrogen deficiency on haemodialysis. Nephrol Dial Transplant 14:1238–1243

    Article  CAS  PubMed  Google Scholar 

  38. Brockenbrough AT, Dittrich MO, Page ST et al (2006) Transdermal androgen therapy to augment EPO in the treatment of anemia of chronic renal disease. Am J Kidney Dis 47:251–262. https://doi.org/10.1053/j.ajkd.2005.10.022

    Article  CAS  PubMed  Google Scholar 

  39. Vellanki K, Hou S (2018) Menopause in CKD. Am J Kidney Dis 71:710–719. https://doi.org/10.1053/j.ajkd.2017.12.019

    Article  PubMed  Google Scholar 

  40. Zhu K, Prince RL (2015) Lifestyle and osteoporosis. Curr Osteoporos Rep 13:52–59. https://doi.org/10.1007/s11914-014-0248-6

    Article  PubMed  Google Scholar 

  41. De Laet C, Kanis JA, Odén A et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338. https://doi.org/10.1007/s00198-005-1863-y

    Article  PubMed  Google Scholar 

  42. Karsenty G, Ferron M (2012) The contribution of bone to whole-organism physiology. Nature 481:314–320. https://doi.org/10.1038/nature10763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Compston J (2015) Obesity and fractures in postmenopausal women. Curr Opin Rheumatol 27:414–419. https://doi.org/10.1097/BOR.0000000000000182

    Article  PubMed  Google Scholar 

  44. Barbour KE, Zmuda JM, Boudreau R et al (2011) Adipokines and the risk of fracture in older adults. J Bone Miner Res 26:1568–1576. https://doi.org/10.1002/jbmr.361

    Article  CAS  PubMed  Google Scholar 

  45. Kittiskulnam P, Johansen KL (2019) The obesity paradox: a further consideration in dialysis patients. Semin Dial 32:485–489. https://doi.org/10.1111/sdi.12834

    Article  PubMed  PubMed Central  Google Scholar 

  46. Stehman-Breen CO, Sherrard DJ, Alem AM et al (2000) Risk factors for hip fracture among patients with end-stage renal disease. Kidney Int 58:2200–2205. https://doi.org/10.1111/j.1523-1755.2000.00394.x

    Article  CAS  PubMed  Google Scholar 

  47. Bolam KA, van Uffelen JGZ, Taaffe DR (2013) The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporos Int 24:2749–2762. https://doi.org/10.1007/s00198-013-2346-1

    Article  CAS  PubMed  Google Scholar 

  48. Zehnacker CH, Bemis-Dougherty A (2007) Effect of weighted exercises on bone mineral density in post menopausal women. A systematic review. J Geriatr Phys Ther 30:79–88. https://doi.org/10.1519/00139143-200708000-00007

    Article  PubMed  Google Scholar 

  49. Cardoso DF, Marques EA, Leal DV et al (2020) Impact of physical activity and exercise on bone health in patients with chronic kidney disease: a systematic review of observational and experimental studies. BMC Nephrol 21:334. https://doi.org/10.1186/s12882-020-01999-z

    Article  PubMed  PubMed Central  Google Scholar 

  50. Yeung SSY, Reijnierse EM, Pham VK et al (2019) Sarcopenia and its association with falls and fractures in older adults: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 10:485–500. https://doi.org/10.1002/jcsm.12411

    Article  PubMed  PubMed Central  Google Scholar 

  51. Bonewald L (2019) Use it or lose it to age: a review of bone and muscle communication. Bone 120:212–218. https://doi.org/10.1016/j.bone.2018.11.002

    Article  PubMed  Google Scholar 

  52. Kirk B, Miller S, Zanker J, Duque G (2020) A clinical guide to the pathophysiology, diagnosis and treatment of osteosarcopenia. Maturitas 140:27–33. https://doi.org/10.1016/j.maturitas.2020.05.012

    Article  CAS  PubMed  Google Scholar 

  53. Delgado C, Shieh S, Grimes B et al (2015) Association of self-reported frailty with falls and fractures among patients new to dialysis. Am J Nephrol 42:134–140. https://doi.org/10.1159/000439000

    Article  PubMed  Google Scholar 

  54. Jamal SA, Leiter RE, Jassal V et al (2006) Impaired muscle strength is associated with fractures in hemodialysis patients. Osteoporos Int 17:1390–1397. https://doi.org/10.1007/s00198-006-0133-y

    Article  CAS  PubMed  Google Scholar 

  55. West SL, Jamal SA, Lok CE (2012) Tests of neuromuscular function are associated with fractures in patients with chronic kidney disease. Nephrol Dial Transplant 27:2384–2388. https://doi.org/10.1093/ndt/gfr620

    Article  PubMed  Google Scholar 

  56. Kalkwarf HJ, Khoury JC, Lanphear BP (2003) Milk intake during childhood and adolescence, adult bone density, and osteoporotic fractures in US women. Am J Clin Nutr 77:257–265. https://doi.org/10.1093/ajcn/77.1.257

    Article  CAS  PubMed  Google Scholar 

  57. Lips P (2001) Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implications. Endocr Rev 22:477–501. https://doi.org/10.1210/edrv.22.4.0437

    Article  CAS  PubMed  Google Scholar 

  58. Priemel M, von Domarus C, Klatte TO et al (2010) Bone mineralization defects and vitamin D deficiency: histomorphometric analysis of iliac crest bone biopsies and circulating 25-hydroxyvitamin D in 675 patients. J Bone Miner Res 25:305–312. https://doi.org/10.1359/jbmr.090728

    Article  CAS  PubMed  Google Scholar 

  59. Reid IR, Bolland MJ, Grey A (2014) Effects of vitamin D supplements on bone mineral density: a systematic review and meta-analysis. Lancet (London, England) 383:146–155. https://doi.org/10.1016/S0140-6736(13)61647-5

    Article  CAS  Google Scholar 

  60. Bischoff-Ferrari HA, Willett WC, Orav EJ et al (2012) A pooled analysis of vitamin D dose requirements for fracture prevention. N Engl J Med 367:40–49. https://doi.org/10.1056/NEJMoa1109617

    Article  CAS  PubMed  Google Scholar 

  61. Pfeifer M, Begerow B, Minne HW et al (2001) Vitamin D status, trunk muscle strength, body sway, falls, and fractures among 237 postmenopausal women with osteoporosis. Exp Clin Endocrinol Diabetes 109:87–92. https://doi.org/10.1055/s-2001-14831

    Article  CAS  PubMed  Google Scholar 

  62. European Food Safety Authority (EFSA) (2015) Scientific opinion on dietary reference values for calcium. EFSA J. https://doi.org/10.2903/j.efsa.2015.4101

    Article  Google Scholar 

  63. Bouillon R (2017) Comparative analysis of nutritional guidelines for vitamin D. Nat Rev Endocrinol 13:466–479. https://doi.org/10.1038/nrendo.2017.31

    Article  CAS  PubMed  Google Scholar 

  64. Block GA, Wheeler DC, Persky MS et al (2012) Effects of phosphate binders in moderate CKD. J Am Soc Nephrol 23:1407–1415. https://doi.org/10.1681/ASN.2012030223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Spiegel DM, Brady K (2012) Calcium balance in normal individuals and in patients with chronic kidney disease on low- and high-calcium diets. Kidney Int 81:1116–1122. https://doi.org/10.1038/ki.2011.490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Evenepoel P, Cunningham J, Ferrari S et al (2020) European Consensus Statement on the diagnosis and management of osteoporosis in chronic kidney disease stages G4–G5D. Nephrol Dial Transplant. https://doi.org/10.1093/ndt/gfaa192

    Article  PubMed  PubMed Central  Google Scholar 

  67. Metzger M, Houillier P, Gauci C et al (2013) Relation between circulating levels of 25(OH) vitamin D and parathyroid hormone in chronic kidney disease: quest for a threshold. J Clin Endocrinol Metab 98:2922–2928. https://doi.org/10.1210/jc.2013-1294

    Article  CAS  PubMed  Google Scholar 

  68. Ambrus C, Almasi C, Berta K et al (2011) Vitamin D insufficiency and bone fractures in patients on maintenance hemodialysis. Int Urol Nephrol 43:475–482. https://doi.org/10.1007/s11255-010-9723-x

    Article  CAS  PubMed  Google Scholar 

  69. Wolf M, Shah A, Gutierrez O et al (2007) Vitamin D levels and early mortality among incident hemodialysis patients. Kidney Int 72:1004–1013. https://doi.org/10.1038/sj.ki.5002451

    Article  CAS  PubMed  Google Scholar 

  70. Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Update Work Group (2017) KDIGO 2017 clinical practice guideline update for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl 7:1–59. https://doi.org/10.1016/j.kisu.2017.04.001

    Article  Google Scholar 

  71. Fusaro M, Gallieni M, Porta C et al (2020) Vitamin K effects in human health: new insights beyond bone and cardiovascular health. J Nephrol 33:239–249. https://doi.org/10.1007/s40620-019-00685-0

    Article  PubMed  Google Scholar 

  72. Evenepoel P, Claes K, Meijers B et al (2019) Poor vitamin K status is associated with low bone mineral density and increased fracture risk in end-stage renal disease. J Bone Miner Res 34:262–269. https://doi.org/10.1002/jbmr.3608

    Article  CAS  PubMed  Google Scholar 

  73. Fusaro M, Noale M, Viola V et al (2012) Vitamin K, vertebral fractures, vascular calcifications, and mortality: VItamin K Italian (VIKI) dialysis study. J Bone Miner Res 27:2271–2278. https://doi.org/10.1002/jbmr.1677

    Article  CAS  PubMed  Google Scholar 

  74. Apalset EM, Gjesdal CG, Eide GE, Tell GS (2011) Intake of vitamin K1 and K2 and risk of hip fractures: the Hordaland Health Study. Bone 49:990–995. https://doi.org/10.1016/j.bone.2011.07.035

    Article  CAS  PubMed  Google Scholar 

  75. Urena P, Bernard-Poenaru O, Ostertag A et al (2003) Bone mineral density, biochemical markers and skeletal fractures in haemodialysis patients. Nephrol Dial Transplant 18:2325–2331

    Article  CAS  PubMed  Google Scholar 

  76. Vervloet MG, Sezer S, Massy ZA et al (2017) The role of phosphate in kidney disease. Nat Rev Nephrol 13:27–38. https://doi.org/10.1038/nrneph.2016.164

    Article  CAS  PubMed  Google Scholar 

  77. Evenepoel P, Rodriguez M, Ketteler M (2014) Laboratory abnormalities in CKD-MBD: markers, predictors, or mediators of disease? Semin Nephrol 34:151–163. https://doi.org/10.1016/j.semnephrol.2014.02.007

    Article  CAS  PubMed  Google Scholar 

  78. Lacativa PGS, Franco FM, Pimentel JR et al (2009) Prevalence of radiological findings among cases of severe secondary hyperparathyroidism. Sao Paulo Med J 127:71–77. https://doi.org/10.1590/s1516-31802009000200004

    Article  PubMed  Google Scholar 

  79. Appelman-Dijkstra NM, Navas Cañete A, Soonawala D (2016) The rugger-jersey spine. Kidney Int 90:454. https://doi.org/10.1016/j.kint.2016.04.006

    Article  PubMed  Google Scholar 

  80. Abdelhadi M, Nordenström J (1998) Bone mineral recovery after parathyroidectomy in patients with primary and renal hyperparathyroidism. J Clin Endocrinol Metab 83:3845–3851. https://doi.org/10.1210/jcem.83.11.5249

    Article  CAS  PubMed  Google Scholar 

  81. Lu KC, Ma WY, Yu JC et al (2012) Bone turnover markers predict changes in bone mineral density after parathyroidectomy in patients with renal hyperparathyroidism. Clin Endocrinol (Oxf) 76:634–642. https://doi.org/10.1111/j.1365-2265.2011.04265.x

    Article  CAS  Google Scholar 

  82. Nickolas TL, Stein EM, Dworakowski E et al (2013) Rapid cortical bone loss in patients with chronic kidney disease. J Bone Miner Res 28:1811–1820. https://doi.org/10.1002/jbmr.1916

    Article  CAS  PubMed  Google Scholar 

  83. Iimori S, Mori Y, Akita W et al (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. https://doi.org/10.1093/ndt/gfr317

    Article  CAS  PubMed  Google Scholar 

  84. Geng S, Kuang Z, Peissig PL et al (2019) Parathyroid hormone independently predicts fracture, vascular events, and death in patients with stage 3 and 4 chronic kidney disease. Osteoporos Int 30:2019–2025. https://doi.org/10.1007/s00198-019-05033-3

    Article  CAS  PubMed  Google Scholar 

  85. Atsumi K, Kushida K, Yamazaki K et al (1999) Risk factors for vertebral fractures in renal osteodystrophy. Am J Kidney Dis 33:287

    Article  CAS  PubMed  Google Scholar 

  86. Dukkipati R, Kovesdy CP, Colman S et al (2010) Association of relatively low serum parathyroid hormone with malnutrition-inflammation complex and survival in maintenance hemodialysis patients. J Ren Nutr 20:243–254. https://doi.org/10.1053/j.jrn.2009.10.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Kalantar-Zadeh K, Kuwae N, Regidor DL et al (2006) Survival predictability of time-varying indicators of bone disease in maintenance hemodialysis patients. Kidney Int 70:771–780. https://doi.org/10.1038/sj.ki.5001514

    Article  CAS  PubMed  Google Scholar 

  88. Bhadada SK, Rao SD (2020) Role of phosphate in biomineralization. Calcif Tissue Int. https://doi.org/10.1007/s00223-020-00729-9

    Article  PubMed  Google Scholar 

  89. Block GA (2004) Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol 15:2208–2218. https://doi.org/10.1097/01.ASN.0000133041.27682.A2

    Article  CAS  PubMed  Google Scholar 

  90. Vorland CJ, Stremke ER, Moorthi RN, Hill Gallant KM (2017) Effects of excessive dietary phosphorus intake on bone health. Curr Osteoporos Rep 15:473–482. https://doi.org/10.1007/s11914-017-0398-4

    Article  PubMed  PubMed Central  Google Scholar 

  91. Campos-Obando N, Koek WNH, Hooker ER et al (2017) Serum phosphate is associated with fracture risk: the Rotterdam Study and MrOS. J Bone Miner Res 32:1182–1193. https://doi.org/10.1002/jbmr.3094

    Article  CAS  PubMed  Google Scholar 

  92. Bushinsky DA (1995) Stimulated osteoclastic and suppressed osteoblastic activity in metabolic but not respiratory acidosis. Am J Physiol 268:C80–C88. https://doi.org/10.1152/ajpcell.1995.268.1.C80

    Article  CAS  PubMed  Google Scholar 

  93. Chen W, Melamed ML, Abramowitz MK (2015) Serum bicarbonate and bone mineral density in US adults. Am J Kidney Dis 65:240–248. https://doi.org/10.1053/j.ajkd.2014.07.007

    Article  CAS  PubMed  Google Scholar 

  94. Schulte K, Püchel J, Schüssel K et al (2019) Effect of sodium bicarbonate in kidney transplant recipients with chronic metabolic acidosis. Transplant Direct 5:e464. https://doi.org/10.1097/TXD.0000000000000910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sebastian A, Harris ST, Ottaway JH et al (1994) Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate. N Engl J Med 330:1776–1781. https://doi.org/10.1056/NEJM199406233302502

    Article  CAS  PubMed  Google Scholar 

  96. Jehle S, Zanetti A, Muser J et al (2006) Partial neutralization of the acidogenic Western diet with potassium citrate increases bone mass in postmenopausal women with osteopenia. J Am Soc Nephrol 17:3213–3222. https://doi.org/10.1681/ASN.2006030233

    Article  CAS  PubMed  Google Scholar 

  97. National Kidney Foundation (2002) K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 39:S1-266

    Google Scholar 

  98. Stenvinkel P, Alvestrand A (2002) Inflammation in end-stage renal disease: sources, consequences, and therapy. Semin Dial 15:329–37. https://doi.org/10.1046/j.1525-139x.2002.00083.x

    Article  PubMed  Google Scholar 

  99. Viaene L, Behets GJ, Heye S et al (2016) Inflammation and the bone-vascular axis in end-stage renal disease. Osteoporos Int 27:489–497. https://doi.org/10.1007/s00198-015-3233-8

    Article  CAS  PubMed  Google Scholar 

  100. Cafiero C, Gigante M, Brunetti G et al (2018) Inflammation induces osteoclast differentiation from peripheral mononuclear cells in chronic kidney disease patients: crosstalk between the immune and bone systems. Nephrol Dial Transplant 33:65–75. https://doi.org/10.1093/ndt/gfx222

    Article  CAS  PubMed  Google Scholar 

  101. Ferreira A, Saraiva M, Behets G, et al (2009) Evaluation of bone remodeling in hemodialysis patients: serum biochemistry, circulating cytokines and bone histomorphometry. J Nephrol 22:783–93

  102. Hofbauer LC, Lacey DL, Dunstan CR et al (1999) Interleukin-1beta and tumor necrosis factor-alpha, but not interleukin-6, stimulate osteoprotegerin ligand gene expression in human osteoblastic cells. Bone 25:255–259. https://doi.org/10.1016/s8756-3282(99)00162-3

    Article  CAS  PubMed  Google Scholar 

  103. Nakashima T, Kobayashi Y, Yamasaki S et al (2000) Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-kappaB ligand: modulation of the expression by osteotropic factors and cytokines. Biochem Biophys Res Commun 275:768–775. https://doi.org/10.1006/bbrc.2000.3379

    Article  CAS  PubMed  Google Scholar 

  104. Barreto FC, Barreto DV, Moyses RMA et al (2006) Osteoporosis in hemodialysis patients revisited by bone histomorphometry: a new insight into an old problem. Kidney Int 69:1852–1857. https://doi.org/10.1038/sj.ki.5000311

    Article  CAS  PubMed  Google Scholar 

  105. Steenkamp R, Rao A, Fraser S (2016) UK Renal Registry 18th Annual Report (December 2015) Chapter 5: survival and causes of death in UK adult patients on renal replacement therapy in 2014: national and centre-specific Analyses. Nephron 132 Suppl:111–44. https://doi.org/10.1159/000444819

  106. Wahl P, Xie H, Scialla J et al (2012) Earlier onset and greater severity of disordered mineral metabolism in diabetic patients with chronic kidney disease. Diabetes Care 35:994–1001. https://doi.org/10.2337/dc11-2235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Vestergaard P, Rejnmark L, Mosekilde L (2009) Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 84:45–55. https://doi.org/10.1007/s00223-008-9195-5

    Article  CAS  PubMed  Google Scholar 

  108. Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int 18:427–444. https://doi.org/10.1007/s00198-006-0253-4

    Article  CAS  PubMed  Google Scholar 

  109. Jørgensen HS, Winther S, Bøttcher M et al (2017) Bone turnover markers are associated with bone density, but not with fracture in end stage kidney disease: a cross-sectional study. BMC Nephrol 18:284. https://doi.org/10.1186/s12882-017-0692-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Napoli N, Chandran M, Pierroz DD et al (2016) Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol 13:208–219. https://doi.org/10.1038/nrendo.2016.153

    Article  CAS  PubMed  Google Scholar 

  111. Shanbhogue VV, Hansen S, Folkestad L et al (2015) Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR-pQCT in adult patients with hypophosphatemic rickets. J Bone Miner Res 30:176–183. https://doi.org/10.1002/jbmr.2310

    Article  PubMed  Google Scholar 

  112. Roe TF, Mora S, Costin G et al (1991) Vertebral bone density in insulin-dependent diabetic children. Metabolism 40:967–971. https://doi.org/10.1016/0026-0495(91)90074-7

    Article  CAS  PubMed  Google Scholar 

  113. Abdalrahaman N, McComb C, Foster JE et al (2015) Deficits in trabecular bone microarchitecture in young women with type 1 diabetes mellitus. J Bone Miner Res 30:1386–1393. https://doi.org/10.1002/jbmr.2465

    Article  CAS  PubMed  Google Scholar 

  114. Hunt HB, Torres AM, Palomino PM et al (2019) Altered tissue composition, microarchitecture, and mechanical performance in cancellous bone from men with type 2 diabetes mellitus. J Bone Miner Res 34:1191–1206. https://doi.org/10.1002/jbmr.3711

    Article  CAS  PubMed  Google Scholar 

  115. Andrade VFC, Chula DC, Sabbag FP et al (2020) Bone histomorphometry in young patients with type 2 diabetes is affected by disease control and chronic complications. J Clin Endocrinol Metab. https://doi.org/10.1210/clinem/dgz070

    Article  PubMed  Google Scholar 

  116. Hygum K, Starup-Linde J, Harsløf T et al (2017) Diabetes mellitus, a state of low bone turnover—a systematic review and meta-analysis. Eur J Endocrinol 176:R137–R157. https://doi.org/10.1530/EJE-16-0652

    Article  CAS  PubMed  Google Scholar 

  117. Sherrard DJ, Hercz G, Pei Y, Segre G (1996) The aplastic form of renal osteodystrophy. Nephrol Dial Transplant 11:29–31. https://doi.org/10.1093/ndt/11.supp3.29

    Article  PubMed  Google Scholar 

  118. de Oliveira RA, Barreto FC, Mendes M et al (2015) Peritoneal dialysis per se is a risk factor for sclerostin-associated adynamic bone disease. Kidney Int 87:1039–1045. https://doi.org/10.1038/ki.2014.372

    Article  CAS  PubMed  Google Scholar 

  119. Malluche HH, Mawad HW, Monier-Faugere M-C (2011) Renal osteodystrophy in the first decade of the new millennium: analysis of 630 bone biopsies in black and white patients. J Bone Miner Res 26:1368–1376. https://doi.org/10.1002/jbmr.309

    Article  PubMed  Google Scholar 

  120. Torres VE, Harris PC, Pirson Y (2007) Autosomal dominant polycystic kidney disease. Lancet (London, England) 369:1287–1301. https://doi.org/10.1016/S0140-6736(07)60601-1

    Article  Google Scholar 

  121. Evenepoel P, Claes K, Cavalier E et al (2019) A distinct bone phenotype in ADPKD patients with end-stage renal disease. Kidney Int 95:412–419. https://doi.org/10.1016/j.kint.2018.09.018

    Article  CAS  PubMed  Google Scholar 

  122. Gitomer B, Pereira R, Salusky IB et al (2020) Mineral bone disease in autosomal dominant polycystic kidney disease. Kidney Int. https://doi.org/10.1016/j.kint.2020.07.041

    Article  PubMed  PubMed Central  Google Scholar 

  123. Nguyen AM, Jacobs CR (2013) Emerging role of primary cilia as mechanosensors in osteocytes. Bone 54:196–204. https://doi.org/10.1016/j.bone.2012.11.016

    Article  CAS  PubMed  Google Scholar 

  124. Wakasugi M, Kazama JJ, Kikuchi K et al (2019) Hemodialysis product and hip fracture in hemodialysis patients: a nationwide cohort study in Japan. Ther Apher Dial 23:507–517. https://doi.org/10.1111/1744-9987.12807

    Article  CAS  PubMed  Google Scholar 

  125. Raggi P, James G, Burke SK et al (2005) Decrease in thoracic vertebral bone attenuation with calcium-based phosphate binders in hemodialysis. J Bone Miner Res 20:764–772. https://doi.org/10.1359/JBMR.041221

    Article  CAS  PubMed  Google Scholar 

  126. Evenepoel P, Opdebeeck B, David K, D’Haese PC (2019) Bone-vascular axis in chronic kidney disease. Adv Chronic Kidney Dis 26:472–483. https://doi.org/10.1053/j.ackd.2019.09.006

    Article  PubMed  Google Scholar 

  127. Bultink IEM (2018) Bone disease in connective tissue disease/systemic lupus erythematosus. Calcif Tissue Int 102:575–591. https://doi.org/10.1007/s00223-017-0322-z

    Article  CAS  PubMed  Google Scholar 

  128. Briot K, Geusens P, Em Bultink I et al (2017) Inflammatory diseases and bone fragility. Osteoporos Int 28:3301–3314. https://doi.org/10.1007/s00198-017-4189-7

    Article  CAS  PubMed  Google Scholar 

  129. Teichmann J, Lange U, Stracke H et al (1999) Bone metabolism and bone mineral density of systemic lupus erythematosus at the time of diagnosis. Rheumatol Int 18:137–140. https://doi.org/10.1007/s002960050072

    Article  CAS  PubMed  Google Scholar 

  130. Petri M (1995) Musculoskeletal complications of systemic lupus erythematosus in the Hopkins Lupus Cohort: an update. Arthritis Care Res 8:137–145. https://doi.org/10.1002/art.1790080305

    Article  CAS  PubMed  Google Scholar 

  131. Li EK, Tam LS, Griffith JF et al (2009) High prevalence of asymptomatic vertebral fractures in Chinese women with systemic lupus erythematosus. J Rheumatol 36:1646–1652. https://doi.org/10.3899/jrheum.081337

    Article  PubMed  Google Scholar 

  132. Lai E-L, Huang W-N, Chen H-H et al (2019) Ten-year fracture risk by FRAX and osteoporotic fractures in patients with systemic autoimmune diseases. Lupus 28:945–953. https://doi.org/10.1177/0961203319855122

    Article  PubMed  Google Scholar 

  133. Lai E-L, Huang W-N, Chen H-H et al (2020) Degraded microarchitecture by low trabecular bone score is associated with prevalent vertebral fractures in patients with systemic lupus erythematosus. Arch Osteoporos 15:54. https://doi.org/10.1007/s11657-020-00726-3

    Article  PubMed  Google Scholar 

  134. Peterkin-McCalman R, Waller JL, Le B et al (2020) Fractures in patients with rheumatoid arthritis and end-stage renal disease. Arch Osteoporos 15:146. https://doi.org/10.1007/s11657-020-00815-3

    Article  PubMed  Google Scholar 

  135. Le B, Waller JL, Radhakrishnan R et al (2018) Osteoporotic fractures in patients with systemic lupus erythematosus and end stage renal disease. Lupus 27:17–24. https://doi.org/10.1177/0961203317709953

    Article  CAS  PubMed  Google Scholar 

  136. Shoenfeld Y, Giacomelli R, Azrielant S et al (2018) Vitamin D and systemic lupus erythematosus—the hype and the hope. Autoimmun Rev 17:19–23. https://doi.org/10.1016/j.autrev.2017.11.004

    Article  CAS  PubMed  Google Scholar 

  137. Kristinsson SY, Tang M, Pfeiffer RM et al (2010) Monoclonal gammopathy of undetermined significance and risk of skeletal fractures: a population-based study. Blood 116:2651–2655. https://doi.org/10.1182/blood-2010-04-282848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Ng AC, Khosla S, Charatcharoenwitthaya N et al (2011) Bone microstructural changes revealed by high-resolution peripheral quantitative computed tomography imaging and elevated DKK1 and MIP-1α levels in patients with MGUS. Blood 118:6529–6534. https://doi.org/10.1182/blood-2011-04-351437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Drake MT (2014) Unveiling skeletal fragility in patients diagnosed with MGUS: no longer a condition of undetermined significance? J Bone Miner Res 29:2529–2533. https://doi.org/10.1002/jbmr.2387

    Article  PubMed  Google Scholar 

  140. Terpos E, Morgan G, Dimopoulos MA et al (2013) International myeloma working group recommendations for the treatment of multiple myeloma-related bone disease. J Clin Oncol 31:2347–2357. https://doi.org/10.1200/JCO.2012.47.7901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Lim LS, Fink HA, Kuskowski MA et al (2008) Loop diuretic use and increased rates of hip bone loss in older men: the Osteoporotic Fractures in Men Study. Arch Intern Med 168:735–740. https://doi.org/10.1001/archinte.168.7.735

    Article  PubMed  Google Scholar 

  142. Heidrich FE, Stergachis A, Gross KM (1991) Diuretic drug use and the risk for hip fracture. Ann Intern Med 115:1–6. https://doi.org/10.7326/0003-4819-115-1-1

    Article  CAS  PubMed  Google Scholar 

  143. van der Burgh AC, Oliai Araghi S, Zillikens MC et al (2020) The impact of thiazide diuretics on bone mineral density and the trabecular bone score: the Rotterdam Study. Bone 138:115475. https://doi.org/10.1016/j.bone.2020.115475

    Article  CAS  PubMed  Google Scholar 

  144. Bolland MJ, Ames RW, Horne AM et al (2007) The effect of treatment with a thiazide diuretic for 4 years on bone density in normal postmenopausal women. Osteoporos Int 18:479–486. https://doi.org/10.1007/s00198-006-0259-y

    Article  CAS  PubMed  Google Scholar 

  145. Bokrantz T, Schiöler L, Boström KB et al (2020) Antihypertensive drug classes and the risk of hip fracture: results from the Swedish primary care cardiovascular database. J Hypertens 38:167–175. https://doi.org/10.1097/HJH.0000000000002245

    Article  CAS  PubMed  Google Scholar 

  146. Yang L-J, Wu P-H, Huang T-H et al (2018) Thiazide-associated hyponatremia attenuates the fracture-protective effect of thiazide: a population-based study. PLoS ONE 13:e0208712. https://doi.org/10.1371/journal.pone.0208712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Ghebre YT (2020) Proton pump inhibitors and osteoporosis: is collagen a direct target? Front Endocrinol (Lausanne). https://doi.org/10.3389/fendo.2020.00473

    Article  Google Scholar 

  148. Lyu B, Jorgenson M, Hansen KE et al (2020) Proton pump inhibitors, but not H2 receptor antagonists, are associated with incident fractures among kidney transplant recipients. Transplantation. https://doi.org/10.1097/TP.0000000000003178

    Article  PubMed  Google Scholar 

  149. Barbour LA, Kick SD, Steiner JF et al (1994) A prospective study of heparin-induced osteoporosis in pregnancy using bone densitometry. Am J Obstet Gynecol 170:862–869. https://doi.org/10.1016/s0002-9378(94)70299-3

    Article  CAS  PubMed  Google Scholar 

  150. Gajic-Veljanoski O, Phua CW, Shah PS, Cheung AM (2016) Effects of long-term low-molecular-weight heparin on fractures and bone density in non-pregnant adults: a systematic review with meta-analysis. J Gen Intern Med 31:947–957. https://doi.org/10.1007/s11606-016-3603-8

    Article  PubMed  PubMed Central  Google Scholar 

  151. Veronese N, Bano G, Bertozzo G et al (2015) Vitamin K antagonists’ use and fracture risk: results from a systematic review and meta-analysis. J Thromb Haemost 13:1665–1675. https://doi.org/10.1111/jth.13052

    Article  CAS  PubMed  Google Scholar 

  152. Lutsey PL, Norby FL, Ensrud KE et al (2020) Association of anticoagulant therapy with risk of fracture among patients with atrial fibrillation. JAMA Intern Med 180:245–253. https://doi.org/10.1001/jamainternmed.2019.5679

    Article  CAS  PubMed  Google Scholar 

  153. Namba S, Yamaoka-Tojo M, Kakizaki R et al (2017) Effects on bone metabolism markers and arterial stiffness by switching to rivaroxaban from warfarin in patients with atrial fibrillation. Heart Vessels 32:977–982. https://doi.org/10.1007/s00380-017-0950-2

    Article  PubMed  Google Scholar 

  154. Fusaro M, Tripepi G, Noale M et al (2015) Prevalence of vertebral fractures, vascular calcifications, and mortality in warfarin treated hemodialysis patients. Curr Vasc Pharmacol 13:248–258. https://doi.org/10.2174/15701611113119990146

    Article  CAS  PubMed  Google Scholar 

  155. Ravera M, Bussalino E, Fusaro M et al (2020) Systematic DOACs oral anticoagulation in patients with atrial fibrillation and chronic kidney disease: the nephrologist’s perspective. J Nephrol 33:483–495. https://doi.org/10.1007/s40620-020-00720-5

    Article  PubMed  Google Scholar 

  156. Ponticelli C, Locatelli F (2018) Glucocorticoids in the treatment of glomerular diseases: pitfalls and pearls. Clin J Am Soc Nephrol 13:815–822. https://doi.org/10.2215/CJN.12991117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Kadmiel M, Cidlowski JA (2013) Glucocorticoid receptor signaling in health and disease. Trends Pharmacol Sci 34:518–530. https://doi.org/10.1016/j.tips.2013.07.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Van Staa TP, Leufkens HGM, Cooper C (2002) The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int 13:777–787. https://doi.org/10.1007/s001980200108

    Article  PubMed  Google Scholar 

  159. Weinstein RS, Jilka RL, Michael Parfitt A, Manolagas SC (1998) Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts end osteocytes by glucocorticoids potential mechanisms of their deleterious effects on bone. J Clin Invest 102:274–282. https://doi.org/10.1172/JCI2799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Ton FN, Gunawardene SC, Lee H, Neer RM (2005) Effects of low-dose prednisone on bone metabolism. J Bone Miner Res 20:464–470. https://doi.org/10.1359/JBMR.041125

    Article  CAS  PubMed  Google Scholar 

  161. Yao W, Cheng Z, Busse C et al (2008) Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum 58:1674–1686. https://doi.org/10.1002/art.23454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. De Vries F, Bracke M, Leufkens HGM et al (2007) Fracture risk with intermittent high-dose oral glucocorticoid therapy. Arthritis Rheum 56:208–214. https://doi.org/10.1002/art.22294

    Article  CAS  PubMed  Google Scholar 

  163. Nikkel LE, Hollenbeak CS, Fox EJ et al (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 

  164. Nikkel LE, Mohan S, Zhang A et al (2012) Reduced fracture risk with early corticosteroid withdrawal after kidney transplant. Am J Transplant 12:649–659. https://doi.org/10.1111/j.1600-6143.2011.03872.x

    Article  CAS  PubMed  Google Scholar 

  165. Iyer SP, Nikkel LE, Nishiyama KK et al (2014) Kidney transplantation with early corticosteroid withdrawal: paradoxical effects at the central and peripheral skeleton. J Am Soc Nephrol 25:1331–1341. https://doi.org/10.1681/ASN.2013080851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Mann GN, Jacobs TW, Buchinsky FJ et al (1994) Interferon-gamma causes loss of bone volume in vivo and fails to ameliorate cyclosporin A-induced osteopenia. Endocrinology 135:1077–1083. https://doi.org/10.1210/endo.135.3.8070349

    Article  CAS  PubMed  Google Scholar 

  167. Guañabens N, Parés A, Navasa M et al (1994) Cyclosporin A increases the biochemical markers of bone remodeling in primary biliary cirrhosis. J Hepatol 21:24–28. https://doi.org/10.1016/s0168-8278(94)80132-0

    Article  PubMed  Google Scholar 

  168. Julian BA, Laskow DA, Dubovsky J et al (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 

  169. Sprague SM, Bellorin-Font E, Jorgetti V et al (2016) Diagnostic accuracy of bone turnover markers and bone histology in patients with CKD treated by dialysis. Am J Kidney Dis 67:559–566. https://doi.org/10.1053/j.ajkd.2015.06.023

    Article  PubMed  Google Scholar 

  170. Malluche HH, Monier-Faugere MC (2006) Renal osteodystrophy: what’s in a name? Presentation of a clinically useful new model to interpret bone histologic findings. Clin Nephrol 65:235–242. https://doi.org/10.5414/cnp65235

    Article  CAS  PubMed  Google Scholar 

  171. Eastell R, Barton I, Hannon RA et al (2003) Relationship of early changes in bone resorption to the reduction in fracture risk with risedronate. J Bone Miner Res 18:1051–1056. https://doi.org/10.1359/jbmr.2003.18.6.1051

    Article  CAS  PubMed  Google Scholar 

  172. Monier-Faugere MC, Malluche HH (1996) Trends in renal osteodystrophy: a survey from 1983 to 1995 in a total of 2248 patients. Nephrol Dial Transplant 11(Suppl 3):111–120. https://doi.org/10.1093/ndt/11.supp3.111

    Article  PubMed  Google Scholar 

  173. Ng AH, Omelon S, Variola F et al (2016) Adynamic bone decreases bone toughness during aging by affecting mineral and matrix. J Bone Miner Res 31:369–379. https://doi.org/10.1002/jbmr.2702

    Article  CAS  PubMed  Google Scholar 

  174. Malluche HH, Porter DS, Monier-Faugere M-C et al (2012) Differences in bone quality in low- and high-turnover renal osteodystrophy. J Am Soc Nephrol 23:525–532. https://doi.org/10.1681/ASN.2010121253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Heaf JG, Løkkegård H (1998) Parathyroid hormone during maintenance dialysis: influence of low calcium dialysate, plasma albumin and age. J Nephrol 11:203–10

  176. Cannata Andía JB (1996) Aluminium toxicity: its relationship with bone and iron metabolism. Nephrol Dial Transplant 11(Suppl 3):69–73. https://doi.org/10.1093/ndt/11.supp3.69

    Article  PubMed  Google Scholar 

  177. Daugirdas JT, Chertow GM, Larive B et al (2012) Effects of frequent hemodialysis on measures of CKD mineral and bone disorder. J Am Soc Nephrol 23:727–738. https://doi.org/10.1681/ASN.2011070688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Hanudel MR, Froch L, Gales B et al (2017) Fractures and osteomalacia in a patient treated with frequent home hemodialysis. Am J Kidney Dis 70:445–448. https://doi.org/10.1053/j.ajkd.2017.03.015

    Article  PubMed  PubMed Central  Google Scholar 

  179. Evenepoel P, Claes K, Kuypers D et al (2004) Natural history of parathyroid function and calcium metabolism after kidney transplantation: a single-centre study. Nephrol Dial Transplant 19:1281–1287. https://doi.org/10.1093/ndt/gfh128

    Article  PubMed  Google Scholar 

  180. Neves CL, Dos Reis LM, Batista DG et al (2013) Persistence of bone and mineral disorders 2 years after successful kidney transplantation. Transplantation 96:290–296. https://doi.org/10.1097/TP.0b013e3182985468

    Article  CAS  PubMed  Google Scholar 

  181. Araújo SMHA, Ambrosoni P, Lobão RRS et al (2003) The renal osteodystrophy pattern in Brazil and Uruguay: an overview. Kidney Int Suppl 63:S54–S56. https://doi.org/10.1046/j.1523-1755.63.s85.13.x

    Article  Google Scholar 

  182. Piraino B, Chen T, Cooperstein L et al (1988) Fractures and vertebral bone mineral density in patients with renal osteodystrophy. Clin Nephrol 30:57–62

    CAS  PubMed  Google Scholar 

  183. Carbonara CEM, Reis LM Dos, Quadros KR da S et al (2020) Renal osteodystrophy and clinical outcomes: data from the Brazilian Registry of Bone Biopsies—REBRABO. J Bras Nefrol 42:138–146. https://doi.org/10.1590/2175-8239-JBN-2019-0045

    Article  Google Scholar 

  184. Evenepoel P, D’Haese P, Bacchetta J et al (2017) Bone biopsy practice patterns across Europe: the European renal osteodystrophy initiative-a position paper. Nephrol Dial Transplant 32:1608–1613. https://doi.org/10.1093/ndt/gfw468

    Article  PubMed  Google Scholar 

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Acknowledgements

EUROD is supported by an unrestricted grant from Amgen inc. HSJ is supported by an ERA-EDTA long-term fellowship. KD receives funding from the Research Foundation Flanders.

Funding

EUROD is supported by an unrestricted grant from Amgen inc. HSJ is supported by an ERA-EDTA long-term fellowship. KD receives funding from the Research Foundation Flanders (FWO, Grant 1196520N). SS received research funding from Kidney Research UK and Immuno Diagnostic Systems.

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Authors and Affiliations

  1. Nephrology and Renal Transplantation Research Group, Department of Microbiology, Immunology and Transplantation, KU Leuven, Leuven, Belgium

    Hanne Skou Jørgensen, Karel David & Pieter Evenepoel

  2. Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark

    Hanne Skou Jørgensen

  3. Laboratory of Clinical and Experimental Endocrinology, Department of Chronic Diseases and Metabolism, KU Leuven, Leuven, Belgium

    Karel David

  4. Sheffield Kidney Institute, Sheffield Teaching Hospitals National Health Service Foundation Trust, Sheffield, UK

    Syazrah Salam

  5. Academic Unit of Bone Metabolism and 3 Mellanby Centre for Bone Research, Medical School, University of Sheffield, Sheffield, UK

    Syazrah Salam

  6. Department of Nephrology and Renal Transplantation, University Hospitals Leuven, Leuven, Belgium

    Pieter Evenepoel

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the European Renal Osteodystrophy (EUROD) workgroup, an initiative of the CKD-MBD working group of the ERA-EDTA

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HSJ reports grants from ERA-EDTA, KD reports grants from Flemish Fund for Scientific Research, SS reports grants from Kidney Research UK and Immuno Diagnostic Systems, and PE reports personal fees and non-financial support from Amgen, and personal fees from Vifor FMC, outside the submitted work.

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Jørgensen, H.S., David, K., Salam, S. et al. Traditional and Non-traditional Risk Factors for Osteoporosis in CKD. Calcif Tissue Int 108, 496–511 (2021). https://doi.org/10.1007/s00223-020-00786-0

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