Skip to main content
Top
Published in: Journal of Bone and Mineral Metabolism 5/2017

01-09-2017 | Original Article

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

Authors: Zhimin Chen, Jia Sun, Mathias Haarhaus, Peter Barany, Lars Wennberg, Jonaz Ripsweden, Torkel B. Brismar, Bengt Lindholm, Annika Wernerson, Magnus Söderberg, Peter Stenvinkel, Abdul Rashid Qureshi

Published in: Journal of Bone and Mineral Metabolism | Issue 5/2017

Login to get access

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.
Literature
1.
go back to reference Ghanekar H, Welch BJ, Moe OW, Sakhaee K (2006) Post-renal transplantation hypophosphatemia: a review and novel insights. Curr Opin Nephrol Hypertens 15:97–104CrossRefPubMed Ghanekar H, Welch BJ, Moe OW, Sakhaee K (2006) Post-renal transplantation hypophosphatemia: a review and novel insights. Curr Opin Nephrol Hypertens 15:97–104CrossRefPubMed
2.
go back to reference 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 26:720–726CrossRefPubMed 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 26:720–726CrossRefPubMed
3.
go back to reference 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 8:54–58CrossRefPubMed 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 8:54–58CrossRefPubMed
4.
go back to reference 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 71:438–441CrossRefPubMed 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 71:438–441CrossRefPubMed
5.
go back to reference Kooman JP, Kotanko P, Schols AM, Shiels PG, Stenvinkel P (2014) Chronic kidney disease and premature ageing. Nat Rev Nephrol 10:732–742CrossRefPubMed Kooman JP, Kotanko P, Schols AM, Shiels PG, Stenvinkel P (2014) Chronic kidney disease and premature ageing. Nat Rev Nephrol 10:732–742CrossRefPubMed
6.
go back to reference Ketteler M, Biggar PH (2009) Dietary and pharmacological control of calcium and phosphate metabolism in predialysis stages of chronic kidney disease. Blood Purif 27:345–349CrossRefPubMed Ketteler M, Biggar PH (2009) Dietary and pharmacological control of calcium and phosphate metabolism in predialysis stages of chronic kidney disease. Blood Purif 27:345–349CrossRefPubMed
7.
go back to reference 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 23:586–593CrossRefPubMed 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 23:586–593CrossRefPubMed
8.
go back to reference Trivedi DP, Khaw KT (2001) Bone mineral density at the hip predicts mortality in elderly men. Osteoporos Int 12(4):259–265CrossRefPubMed Trivedi DP, Khaw KT (2001) Bone mineral density at the hip predicts mortality in elderly men. Osteoporos Int 12(4):259–265CrossRefPubMed
9.
go back to reference 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 20:1912–1920CrossRefPubMed 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 20:1912–1920CrossRefPubMed
10.
go back to reference 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 37:33–38CrossRefPubMed 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 37:33–38CrossRefPubMed
11.
go back to reference 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 64:33–38CrossRefPubMed 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 64:33–38CrossRefPubMed
12.
go back to reference 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 26:2534–2544CrossRefPubMedPubMedCentral 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 26:2534–2544CrossRefPubMedPubMedCentral
13.
go back to reference Frye MA, Melton LJ 3rd, Bryant SC, Fitzpatrick LA, Wahner HW, Schwartz RS, Riggs BL (1992) Osteoporosis and calcification of the aorta. Bone Miner 19:185–194CrossRefPubMed Frye MA, Melton LJ 3rd, Bryant SC, Fitzpatrick LA, Wahner HW, Schwartz RS, Riggs BL (1992) Osteoporosis and calcification of the aorta. Bone Miner 19:185–194CrossRefPubMed
14.
go back to reference Barengolts EI, Berman M, Kukreja SC, Kouznetsova T, Lin C, Chomka EV (1998) Osteoporosis and coronary atherosclerosis in asymptomatic postmenopausal women. Calcif Tissue Int 62:209–213CrossRefPubMed Barengolts EI, Berman M, Kukreja SC, Kouznetsova T, Lin C, Chomka EV (1998) Osteoporosis and coronary atherosclerosis in asymptomatic postmenopausal women. Calcif Tissue Int 62:209–213CrossRefPubMed
15.
go back to reference 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 27:394–401CrossRefPubMed 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 27:394–401CrossRefPubMed
16.
go back to reference 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 33:844–854CrossRefPubMed 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 33:844–854CrossRefPubMed
17.
go back to reference 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 241:278–283CrossRefPubMed 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 241:278–283CrossRefPubMed
18.
go back to reference 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 29:369–376CrossRefPubMed 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 29:369–376CrossRefPubMed
19.
go back to reference 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 80:244–250CrossRefPubMed 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 80:244–250CrossRefPubMed
20.
go back to reference 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 78:195–202CrossRefPubMed 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 78:195–202CrossRefPubMed
21.
go back to reference 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 67:1576–1582CrossRefPubMed 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 67:1576–1582CrossRefPubMed
22.
go back to reference 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 88:1356–1364CrossRefPubMed 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 88:1356–1364CrossRefPubMed
23.
go back to reference 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 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.
go back to reference 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 101:244–251CrossRefPubMed 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 101:244–251CrossRefPubMed
25.
go back to reference 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 53:773–782CrossRefPubMed 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 53:773–782CrossRefPubMed
26.
go back to reference 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 100:2168–2176CrossRefPubMed 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 100:2168–2176CrossRefPubMed
27.
go back to reference Blacher J, Guerin AP, Pannier B, Marchais SJ, London GM (2001) Arterial calcifications, arterial stiffness, and cardiovascular risk in end-stage renal disease. Hypertension 38:938–942CrossRefPubMed Blacher J, Guerin AP, Pannier B, Marchais SJ, London GM (2001) Arterial calcifications, arterial stiffness, and cardiovascular risk in end-stage renal disease. Hypertension 38:938–942CrossRefPubMed
28.
go back to reference London GM (2003) Cardiovascular disease in chronic renal failure: pathophysiologic aspects. Semin Dial 16:85–94CrossRefPubMed London GM (2003) Cardiovascular disease in chronic renal failure: pathophysiologic aspects. Semin Dial 16:85–94CrossRefPubMed
29.
go back to reference 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 342:1478–1483CrossRefPubMed 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 342:1478–1483CrossRefPubMed
30.
go back to reference 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 18:1731–1740CrossRefPubMed 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 18:1731–1740CrossRefPubMed
31.
go back to reference 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 50:2218–2225CrossRefPubMed 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 50:2218–2225CrossRefPubMed
32.
go back to reference 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 45:140–145CrossRefPubMed 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 45:140–145CrossRefPubMed
33.
go back to reference 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 21:1839–1846CrossRefPubMed 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 21:1839–1846CrossRefPubMed
34.
go back to reference 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 52:1139–1150CrossRefPubMed 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 52:1139–1150CrossRefPubMed
35.
go back to reference 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 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.
go back to reference 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 24:813–817CrossRefPubMed 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 24:813–817CrossRefPubMed
37.
go back to reference Uyama O, Yoshimoto Y, Yamamoto Y, Kawai A (1997) Bone changes and carotid atherosclerosis in postmenopausal women. Stroke 28:1730–1732CrossRefPubMed Uyama O, Yoshimoto Y, Yamamoto Y, Kawai A (1997) Bone changes and carotid atherosclerosis in postmenopausal women. Stroke 28:1730–1732CrossRefPubMed
38.
go back to reference 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 84:180–185CrossRefPubMed 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 84:180–185CrossRefPubMed
Metadata
Title
Bone mineral density of extremities is associated with coronary calcification and biopsy-verified vascular calcification in living-donor renal transplant recipients
Authors
Zhimin Chen
Jia Sun
Mathias Haarhaus
Peter Barany
Lars Wennberg
Jonaz Ripsweden
Torkel B. Brismar
Bengt Lindholm
Annika Wernerson
Magnus Söderberg
Peter Stenvinkel
Abdul Rashid Qureshi
Publication date
01-09-2017
Publisher
Springer Japan
Published in
Journal of Bone and Mineral Metabolism / Issue 5/2017
Print ISSN: 0914-8779
Electronic ISSN: 1435-5604
DOI
https://doi.org/10.1007/s00774-016-0788-1

Other articles of this Issue 5/2017

Journal of Bone and Mineral Metabolism 5/2017 Go to the issue