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Bone mineral density of extremities is associated with coronary calcification and biopsy-verified vascular calcification in living-donor renal transplant recipients

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Abstract

Chronic kidney disease (CKD) mineral and bone disorders (CKD-MBD) may lead to low bone mineral density (BMD) and vascular calcification (VC), but links to the latter are unclear. Here we investigated associations between BMD, coronary artery calcium (CAC) scores, and histological signs of VC in end-stage renal disease (ESRD) patients undergoing living-donor kidney transplantation (LD-Rtx). In 66 ESRD patients (median age 45 years, 68% males), BMD (by dual-energy X-ray absorptiometry, DXA), CAC score (by computed tomography, CT; n = 54), and degree of VC score (graded by histological examination of epigastric artery specimens collected at LD-Rtx; n = 55) were assessed at the time of LD-Rtx. Of the patients, 26% had osteopenia and 7% had osteoporosis. Of those undergoing artery biopsy, 16% had extensive VC, and of those undergoing CT 28% had high CAC score (>100 Agatston units). CAC scores correlated with BMD of legs and pelvis. BMDs of leg and pelvic sub-regions were significantly lower in patients with extensive VC. In multivariate regression analysis adjusted for age and gender, lower BMD of leg sub-region was associated with CAC score >100 AUs and extensive VC, and patients with extensive VC had significantly higher CAC score. Both high CAC and extensive VC were independently predicted by low BMD of legs. Low BMD has the potential to identify ESRD patients at risk of vascular calcification.

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References

  1. Ghanekar H, Welch BJ, Moe OW, Sakhaee K (2006) Post-renal transplantation hypophosphatemia: a review and novel insights. Curr Opin Nephrol Hypertens 15:97–104

    Article  CAS  PubMed  Google Scholar 

  2. Seyahi N, Kahveci A, Cebi D, Altiparmak MR, Akman C, Uslu I, Ataman R, Tasci H, Serdengecti K (2011) Coronary artery calcification and coronary ischaemia in renal transplant recipients. Nephrol Dial Transplant 26:720–726

    Article  PubMed  Google Scholar 

  3. Matsuoka M, Iseki K, Tamashiro M, Fujimoto N, Higa N, Touma T, Takishita S (2004) Impact of high coronary artery calcification score (CACS) on survival in patients on chronic hemodialysis. Clin Exp Nephrol 8:54–58

    Article  PubMed  Google Scholar 

  4. Block GA, Raggi P, Bellasi A, Kooienga L, Spiegel DM (2007) Mortality effect of coronary calcification and phosphate binder choice in incident hemodialysis patients. Kidney Int 71:438–441

    Article  CAS  PubMed  Google Scholar 

  5. Kooman JP, Kotanko P, Schols AM, Shiels PG, Stenvinkel P (2014) Chronic kidney disease and premature ageing. Nat Rev Nephrol 10:732–742

    Article  CAS  PubMed  Google Scholar 

  6. Ketteler M, Biggar PH (2009) Dietary and pharmacological control of calcium and phosphate metabolism in predialysis stages of chronic kidney disease. Blood Purif 27:345–349

    Article  CAS  PubMed  Google Scholar 

  7. Toussaint ND, Lau KK, Strauss BJ, Polkinghorne KR, Kerr PG (2008) Associations between vascular calcification, arterial stiffness and bone mineral density in chronic kidney disease. Nephrol Dial Transplant 23:586–593

    Article  PubMed  Google Scholar 

  8. Trivedi DP, Khaw KT (2001) Bone mineral density at the hip predicts mortality in elderly men. Osteoporos Int 12(4):259–265

    Article  CAS  PubMed  Google Scholar 

  9. Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR (2005) Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone Miner Res 20:1912–1920

    Article  PubMed  Google Scholar 

  10. Disthabanchong S, Jongjirasiri S, Adirekkiat S, Sumethkul V, Ingsathit A, Domrongkitchaiporn S, Phakdeekitcharoen B, Kantachuvesiri S, Kitiyakara C (2014) Low hip bone mineral density predicts mortality in maintenance hemodialysis patients: a five-year follow-up study. Blood Purif 37:33–38

    Article  CAS  PubMed  Google Scholar 

  11. Cejka D, Weber M, Diarra D, Reiter T, Kainberger F, Haas M (2014) Inverse association between bone microarchitecture assessed by HR-pQCT and coronary artery calcification in patients with end-stage renal disease. Bone 64:33–38

    Article  CAS  PubMed  Google Scholar 

  12. Malluche HH, Blomquist G, Monier-Faugere MC, Cantor TL, Davenport DL (2015) High parathyroid hormone level and osteoporosis predict progression of coronary artery calcification in patients on dialysis. J Am Soc Nephrol 26:2534–2544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Frye MA, Melton LJ 3rd, Bryant SC, Fitzpatrick LA, Wahner HW, Schwartz RS, Riggs BL (1992) Osteoporosis and calcification of the aorta. Bone Miner 19:185–194

    Article  CAS  PubMed  Google Scholar 

  14. Barengolts EI, Berman M, Kukreja SC, Kouznetsova T, Lin C, Chomka EV (1998) Osteoporosis and coronary atherosclerosis in asymptomatic postmenopausal women. Calcif Tissue Int 62:209–213

    Article  CAS  PubMed  Google Scholar 

  15. Braun J, Oldendorf M, Moshage W, Heidler R, Zeitler E, Luft FC (1996) Electron beam computed tomography in the evaluation of cardiac calcification in chronic dialysis patients. Am J Kidney Dis 27:394–401

    Article  CAS  PubMed  Google Scholar 

  16. Kirkpantur A, Altun B, Hazirolan T, Akata D, Arici M, Kirazli S, Turgan C (2009) Association among serum fetuin-A level, coronary artery calcification, and bone mineral densitometry in maintenance hemodialysis patients. Artif Organs 33:844–854

    Article  CAS  PubMed  Google Scholar 

  17. Campos-Obando N, Kavousi M, Roeters van Lennep JE, Rivadeneira F, Hofman A, Uitterlinden AG, Franco OH, Zillikens MC (2015) Bone health and coronary artery calcification: the Rotterdam Study. Atherosclerosis 241:278–283

    Article  CAS  PubMed  Google Scholar 

  18. Kim KI, Suh JW, Choi SY, Chang HJ, Choi DJ, Kim CH, Oh BH (2011) Is reduced bone mineral density independently associated with coronary artery calcification in subjects older than 50 years? J Bone Miner Metab 29:369–376

    Article  CAS  PubMed  Google Scholar 

  19. Shen H, Bielak LF, Streeten EA, Ryan KA, Rumberger JA, Sheedy PF, Shuldiner AR, Peyser PA, Mitchell BD (2007) Relationship between vascular calcification and bone mineral density in the Old-order Amish. Calcif Tissue Int 80:244–250

    Article  CAS  PubMed  Google Scholar 

  20. Sinnott B, Syed I, Sevrukov A, Barengolts E (2006) Coronary calcification and osteoporosis in men and postmenopausal women are independent processes associated with aging. Calcif Tissue Int 78:195–202

    Article  CAS  PubMed  Google Scholar 

  21. Barreto DV, Barreto FC, Carvalho AB, Cuppari L, Cendoroglo M, Draibe SA, Moyses RM, Neves KR, Jorgetti V, Blair A, Guiberteau R, Fernandes Canziani ME (2005) Coronary calcification in hemodialysis patients: the contribution of traditional and uremia-related risk factors. Kidney Int 67:1576–1582

    Article  PubMed  Google Scholar 

  22. Qureshi AR, Olauson H, Witasp A, Haarhaus M, Brandenburg V, Wernerson A, Lindholm B, Soderberg M, Wennberg L, Nordfors L, Ripsweden J, Barany P, Stenvinkel P (2015) Increased circulating sclerostin levels in end-stage renal disease predict biopsy-verified vascular medial calcification and coronary artery calcification. Kidney Int 88:1356–1364

    Article  CAS  PubMed  Google Scholar 

  23. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, Detrano R (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15:827–832

  24. He ZX, Hedrick TD, Pratt CM, Verani MS, Aquino V, Roberts R, Mahmarian JJ (2000) Severity of coronary artery calcification by electron beam computed tomography predicts silent myocardial ischemia. Circulation 101:244–251

    Article  CAS  PubMed  Google Scholar 

  25. Qureshi A, Alvestrand A, Danielsson A, Divino-Filho J, Gutierrez A, Lindholm B, Bergström J (1998) Factors predicting malnutrition in hemodialysis patients: a cross-sectional study. Kidney Int 53:773–782

    Article  CAS  PubMed  Google Scholar 

  26. Shanahan CM, Cary NR, Salisbury JR, Proudfoot D, Weissberg PL, Edmonds ME (1999) Medial localization of mineralization-regulating proteins in association with Mönckeberg’s sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation 100:2168–2176

    Article  CAS  PubMed  Google Scholar 

  27. Blacher J, Guerin AP, Pannier B, Marchais SJ, London GM (2001) Arterial calcifications, arterial stiffness, and cardiovascular risk in end-stage renal disease. Hypertension 38:938–942

    Article  CAS  PubMed  Google Scholar 

  28. London GM (2003) Cardiovascular disease in chronic renal failure: pathophysiologic aspects. Semin Dial 16:85–94

    Article  PubMed  Google Scholar 

  29. Goodman WG, Goldin J, Kuizon BD, Yoon C, Gales B, Sider D, Wang Y, Chung J, Emerick A, Greaser L, Elashoff RM, Salusky IB (2000) Coronary-artery calcification in young adults with end-stage renal disease who are undergoing dialysis. N Engl J Med 342:1478–1483

    Article  CAS  PubMed  Google Scholar 

  30. London GM, Guérin AP, Marchais SJ, Métivier F, Pannier B, Adda H (2003) Arterial media calcification in end-stage renal disease: impact on all-cause and cardiovascular mortality. Nephrol Dial Transplant 18:1731–1740

    Article  PubMed  Google Scholar 

  31. Anand DV, Lim E, Darko D, Bassett P, Hopkins D, Lipkin D, Corder R, Lahiri A (2007) Determinants of progression of coronary artery calcification in type 2 diabetes role of glycemic control and inflammatory/vascular calcification markers. J Am Coll Cardiol 50:2218–2225

    Article  CAS  PubMed  Google Scholar 

  32. Vogt MT, Valentin RS, Forrest KYZ, Nevitt MC, Cauley JA (1997) Bone mineral density and aortic calcification: the study of osteoporotic fractures. J Am Geriatr Soc 45:140–145

    Article  CAS  PubMed  Google Scholar 

  33. Farhat GN, Cauley JA, Matthews KA, Newman AB, Johnston J, Mackey R, Edmundowicz D, Sutton-Tyrrell K (2006) Volumetric BMD and vascular calcification in middle-aged women: the Study of Women’s Health Across the Nation. J Bone Miner Res 21:1839–1846

    Article  PubMed  Google Scholar 

  34. Barreto DV, FeC Barreto, Carvalho AB, Cuppari L, Draibe SA, Dalboni MA, Moyses RM, Neves KR, Jorgetti V, Miname M, Santos RD, Canziani ME (2008) Association of changes in bone remodeling and coronary calcification in hemodialysis patients: a prospective study. Am J Kidney Dis 52:1139–1150

    Article  CAS  PubMed  Google Scholar 

  35. Chen Z, Qureshi AR, Ripsweden J, Wennberg L, Heimburger O, Lindholm B, Barany P, Haarhaus M, Brismar TB, Stenvinkel P (2016) Vertebral bone density associates with coronary artery calcification and is an independent predictor of poor outcome in end-stage renal disease patients. Bone 92:50–57

  36. Banks LM, Lees B, MacSweeney JE, Stevenson JC (1994) Effect of degenerative spinal and aortic calcification on bone density measurements in post-menopausal women: links between osteoporosis and cardiovascular disease? Eur J Clin Invest 24:813–817

    Article  CAS  PubMed  Google Scholar 

  37. Uyama O, Yoshimoto Y, Yamamoto Y, Kawai A (1997) Bone changes and carotid atherosclerosis in postmenopausal women. Stroke 28:1730–1732

    Article  CAS  PubMed  Google Scholar 

  38. Kohno K, Inaba M, Okuno S, Maeno Y, Maekawa K, Yamakawa T, Ishimura E, Nishizawa Y (2009) Association of reduction in bone mineral density with mortality in male hemodialysis patients. Calcif Tissue Int 84:180–185

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the patients who participated in the study. We are grateful to all those who carried out the extensive clinical work (Annika Nilsson, Anki Emmoth, Ulrika Jensen and Åsa Lindé) and laboratory work (Björn Anderstam, Monica Eriksson, and Ann-Christin Bragfors-Helin) in the current study. Zhimin Chen has a scholarship from the China Scholarship Council. Peter Stenvinkel’s research benefited from a Research Grant from Swedish Medical Research Council (VR). The study also benefited from generous support from Martin Rind Foundation (Abdul Rashid Qureshi). Baxter Novum is a result of a Grant from Baxter Healthcare to Karolinska Institutet.

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Correspondence to Abdul Rashid Qureshi.

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Dr. Bengt Lindholm is an employee of Baxter Healthcare.

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Chen, Z., Sun, J., Haarhaus, M. et al. Bone mineral density of extremities is associated with coronary calcification and biopsy-verified vascular calcification in living-donor renal transplant recipients. J Bone Miner Metab 35, 536–543 (2017). https://doi.org/10.1007/s00774-016-0788-1

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  • DOI: https://doi.org/10.1007/s00774-016-0788-1

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