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Current Osteoporosis Reports
Published in: Current Osteoporosis Reports 6/2019

01-12-2019 | Glucocorticoid | Kidney and Bone (I Salusky and T Nickolas, Section Editors)

Bone Health in Glomerular Kidney Disease

Authors: Dorey A. Glenn, Michelle R. Denburg

Published in: Current Osteoporosis Reports | Issue 6/2019

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Abstract

Purpose of Review

To summarize the literature regarding alterations in bone health in patients with glomerular kidney disease and highlight areas in need of additional investigation.

Recent Findings

There is mounting evidence that children and adults with glomerular conditions, with or without compromised kidney function, comprise a distinct subgroup of patients with unique risk factors for altered bone health.

Summary

Patients with glomerular kidney disease are exposed to both disease-related and treatment-related factors that affect bone structure and function. In addition to chronic kidney disease–related risk factors for impaired bone health, high rates of exposure to osteotoxic medications, varying degrees of systemic inflammation, and altered vitamin D metabolism may contribute to compromised bone health in individuals with glomerular disease. Further study is needed to better understand these risk factors and the complex interaction between the immune system and bone cells in glomerular disease.
Literature
1.
2.
3.
Saran R, Robinson B, Abbott KC, Agodoa LYC, Albertus P, Ayanian J, et al. US Renal Data System 2016 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis Off J Natl Kidney Found. 2017;69:A7–8.CrossRef
4.
Minimal change nephrotic syndrome in children: deaths during the first 5 to 15 years’ observation. Pediatrics. 1984;73:497.
5.
Adedoyin O, Frank R, Vento S, Vergara M, Gauthier B, Trachtman H. Cardiac disease in children with primary glomerular disorders—role of focal segmental glomerulosclerosis. Pediatr Nephrol. 2004;19:408–12.PubMedCrossRef
6.
Ordoñez JD, Hiatt RA, Killebrew EJ, Fireman BH. The increased risk of coronary heart disease associated with nephrotic syndrome. Kidney Int. 1993;44:638–42.PubMedCrossRef
7.
8.
Tain YL, Lin G, Cher TW. Microbiological spectrum of septicemia and peritonitis in nephrotic children. Pediatr Nephrol Berl Ger. 1999;13:835–7.CrossRef
9.
Watts GF, Herrmann S, Dogra GK, Playford DA, Best JD, Thomas MAB, et al. Vascular function of the peripheral circulation in patients with nephrosis. Kidney Int. 2001;60:182–9.PubMedCrossRef
10.
Zhang Q, Zeng C, Cheng Z, Xie K, Zhang J, Liu Z. Primary focal segmental glomerulosclerosis in nephrotic patients: common complications and risk factors. J Nephrol. 2012;25:679–88.PubMedCrossRef
11.
Kerlin BA, Blatt NB, Fuh B, Zhao S, Lehman A, Blanchong C, et al. Epidemiology and risk factors for thromboembolic complications of childhood nephrotic syndrome: a Midwest Pediatric Nephrology Consortium (MWPNC) study. J Pediatr. 2009;155:105–110.e1.PubMedCentralCrossRef
12.
Rüth E-M, Landolt MA, Neuhaus TJ, Kemper MJ. Health-related quality of life and psychosocial adjustment in steroid-sensitive nephrotic syndrome. J Pediatr. 2004;145:778–83.PubMedCrossRef
13.
El Desoky S, Farag YM, Safdar E, Shalaby MA, Singh AK, Kari JA. Prevalence of hyperparathyroidism, mineral and bone disorders in children with advanced chronic kidney disease. Indian J Pediatr. 2016;83:420–5.PubMedCrossRef
14.
Isakova T, Nickolas TL, Denburg M, Yarlagadda S, Weiner DE, Gutiérrez OM, et al. 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. 2017;70:737–51.PubMedCrossRef
15.
Groothoff JW, Offringa M, van Eck-Smit BLF, Gruppen MP, van de Kar NJ, Wolff ED, et al. Severe bone disease and low bone mineral density after juvenile renal failure. Kidney Int. 2003;63:266–75.PubMedCrossRef
16.
Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Update Work Group. 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. 2017;7:1–59.
17.
•• Hanudel MR, Salusky IB. Treatment of pediatric chronic kidney disease-mineral and bone disorder. Curr Osteoporos Rep. 2017;15:198–206. The authors provide a succinct review of the pathophysiology and treatment of CKD-MBD in children. PubMedPubMedCentralCrossRef
18.
Beaubrun AC, Kilpatrick RD, Freburger JK, Bradbury BD, Wang L, Brookhart MA. Temporal trends in fracture rates and postdischarge outcomes among hemodialysis patients. J Am Soc Nephrol JASN. 2013;24:1461–9.PubMedCrossRef
19.
Danese MD, Kim J, Doan QV, Dylan M, Griffiths R, Chertow GM. PTH and the risks for hip, vertebral, and pelvic fractures among patients on dialysis. Am J Kidney Dis. 2006;47:149–56.PubMedCrossRef
20.
Mittalhenkle A, Gillen DL, Stehman-Breen CO. Increased risk of mortality associated with hip fracture in the dialysis population. Am J Kidney Dis. 2004;44:672–9.PubMedCrossRef
21.
Tentori F, McCullough K, Kilpatrick RD, Bradbury BD, Robinson BM, Kerr PG, et al. High rates of death and hospitalization follow bone fracture among hemodialysis patients. Kidney Int. 2014;85:166–73.PubMedCrossRef
22.
Denburg MR, Kumar J, Jemielita T, Brooks ER, Skversky A, Portale AA, et al. Fracture burden and risk factors in childhood CKD: results from the CKiD cohort study. J Am Soc Nephrol JASN. 2016;27:543–50.PubMedCrossRef
23.
Schmidt-Gayk H, Grawunder C, Tschöpe W, Schmitt W, Ritz E, Pietsch V, et al. 25-Hydroxy-vitamin-D in nephrotic syndrome. Lancet. 1977;310:105–8.CrossRef
24.
Barragry JM, Carter ND, Beer M, Cohen RD, France MW, Auton JA, et al. Vitamin-D metabolism in nephrotic syndrome. Lancet. 1977;310:629–32.CrossRef
25.
Koenig KG, Lindberg JS, Zerwekh JE, Padalino PK, Cushner HM, Copley JB. Free and total 1,25-dihydroxyvitamin D levels in subjects with renal disease. Kidney Int. 1992;41:161–5.PubMedCrossRef
26.
Auwerx J, De Keyser L, Bouillon R, De Moor P. Decreased free 1,25-dihydroxycholecalciferol index in patients with the nephrotic syndrome. Nephron. 1986;42:231–5.PubMedCrossRef
27.
Goldstein DA, Haldimann B, Sherman D, Norman AW, Massry SG. Vitamin D metabolites and calcium metabolism in patients with nephrotic syndrome and normal renal function. J Clin Endocrinol Metab. 1981;52:116–21.CrossRef
28.
Huang JP, Bai KM, Wang BL. Vitamin D and calcium metabolism in children with nephrotic syndrome of normal renal function. Chin Med J (Engl). 1992;105:828–32.
29.
Freundlich M, Bourgoignie JJ, Zilleruelo G, Abitbol C, Canterbury JM, Strauss J. Calcium and vitamin D metabolism in children with nephrotic syndrome. J Pediatr. 1986;108:383–7.PubMedCrossRef
30.
Grymonprez A, Proesmans W, Van Dyck M, Jans I, Goos G, Bouillon R. Vitamin D metabolites in childhood nephrotic syndrome. Pediatr Nephrol Berl Ger. 1995;9:278–81.CrossRef
31.
Sato KA, Gray RW, Lemann JJ. Urinary excretion of 25-hydroxyvitamin D in health and the nephrotic syndrome. J Lab Clin Med. 1982;99:325–30.PubMed
32.
Malluche HH, Goldstein DA, Massry SG. Osteomalacia and hyperparathyroid bone disease in patients with nephrotic syndrome. J Clin Invest. 1979;63:494–500.PubMedPubMedCentralCrossRef
33.
Tessitore N, Bonucci E, D’Angelo A, Lund B, Corgnati A, Lund B, et al. Bone histology and calcium metabolism in patients with nephrotic syndrome and normal or reduced renal function. Nephron. 1984;37:153–9.PubMedCrossRef
34.
Mittal SK, Dash SC, Tiwari SC, Agarwal SK, Saxena S, Fishbane S. Bone histology in patients with nephrotic syndrome and normal renal function. Kidney Int. 1999;55:1912–9.PubMedCrossRef
35.
Korkor A, Schwartz J, Bergfeld M, Teitelbaum S, Teitelbaum L, Klahr S, et al. Absence of metabolic bone disease in adult patients with the nephrotic syndrome and normal renal function. J Clin Endocrinol Metab. 1983;56:496–500.PubMedCrossRef
36.
Selewski DT, Chen A, Shatat IF, Pais P, Greenbaum LA, Geier P, et al. Vitamin D in incident nephrotic syndrome: a Midwest Pediatric Nephrology Consortium study. Pediatr Nephrol Berl Ger. 2016;31:465–72.CrossRef
37.
Weng FL, Shults J, Herskovitz RM, Zemel BS, Leonard MB. Vitamin D insufficiency in steroid-sensitive nephrotic syndrome in remission. Pediatr Nephrol. 2005;20:56–63.PubMedCrossRef
38.
Banerjee S, Basu S, Sengupta J. Vitamin D in nephrotic syndrome remission: a case–control study. Pediatr Nephrol. 2013;28:1983–9.PubMedCrossRef
39.
Kalkwarf HJ, Denburg MR, Strife CF, Zemel BS, Foerster D, Wetzsteon RJ, et al. Vitamin D deficiency is common in children and adolescents with chronic kidney disease. Kidney Int. 2012;81:690–7.PubMedCrossRef
40.
Kumar J, McDermott K, Abraham AG, Friedman LA, Johnson VL, Kaskel FJ, et al. Prevalence and correlates of 25-hydroxyvitamin D deficiency in the Chronic Kidney Disease in Children (CKiD) cohort. Pediatr Nephrol. 2016;31:121–9.PubMed
41.
Doyon A, Schmiedchen B, Sander A, Bayazit A, Duzova A, Canpolat N, et al. Genetic, environmental, and disease-associated correlates of vitamin D status in children with CKD. Clin J Am Soc Nephrol CJASN. 2016;11:1145–53.PubMedCrossRef
42.
Gulati S, Sharma RK, Gulati K, Singh U, Srivastava A. Longitudinal follow-up of bone mineral density in children with nephrotic syndrome and the role of calcium and vitamin D supplements. Nephrol Dial Transplant. 2005;20:1598–603.PubMedCrossRef
43.
Bak M, Serdaroglu E, Guclu R. Prophylactic calcium and vitamin D treatments in steroid-treated children with nephrotic syndrome. Pediatr Nephrol. 2006;21:350–4.PubMedCrossRef
44.
Choudhary S, Agarwal I, Seshadri MS. Calcium and vitamin D for osteoprotection in children with new-onset nephrotic syndrome treated with steroids: a prospective, randomized, controlled, interventional study. Pediatr Nephrol. 2014;29:1025–32.PubMedCrossRef
45.
46.
Verboven C, Rabijns A, De Maeyer M, Van Baelen H, Bouillon R, De Ranter C. A structural basis for the unique binding features of the human vitamin D-binding protein. Nat Struct Biol. 2002;9:131–6.PubMedCrossRef
47.
Feldman D, Pike W, Bouilon R, Giovannucci E, Goltzman D, Hawison M. The Vitamin D-Binding Protein. Vitam D. 4th ed. Elsevier Inc; 2018. p. 97–115.
48.
•• Denburg MR, Bhan I. Vitamin D-binding protein in health and chronic kidney disease. Semin Dial. 2015;28:636–44. The authors provide an in-depth review of vitamin D–binding protein physiology and function. PubMedCrossRef
49.
Safadi FF, Thornton P, Magiera H, Hollis BW, Gentile M, Haddad JG, et al. Osteopathy and resistance to vitamin D toxicity in mice null for vitamin D binding protein. J Clin Invest. 1999;103:239–51.PubMedPubMedCentralCrossRef
50.
Bikle D, Gee E. Free, and not total, 1,25-dihydroxyvitamin D regulates 25-hydroxyvitamin D metabolism by keratinocytes. Endocrinology. 1989;124:649–54.PubMedCrossRef
51.
Nielsen R, Christensen EI, Birn H. Megalin and cubilin in proximal tubule protein reabsorption: from experimental models to human disease. Kidney Int. 2016;89:58–67.PubMedCrossRef
52.
Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, et al. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell. 1999;96:507–15.PubMedCrossRef
53.
Arnaud J, Constans J. Affinity differences for vitamin D metabolites associated with the genetic isoforms of the human serum carrier protein (DBP). Hum Genet. 1993;92:183–8.PubMedCrossRef
54.
Cleve H, Constans J. The mutants of the vitamin-D-binding protein: more than 120 variants of the GC/DBP system. Vox Sang. 1988;54:215–25.PubMedCrossRef
55.
Powe CE, Evans MK, Wenger J, Zonderman AB, Berg AH, Nalls M, et al. Vitamin D–binding protein and vitamin D status of black Americans and white Americans. N Engl J Med. 2013;369:1991–2000.PubMedPubMedCentralCrossRef
56.
Denburg MR, Hoofnagle AN, Sayed S, Gupta J, de Boer IH, Appel LJ, et al. Comparison of two ELISA methods and mass spectrometry for measurement of vitamin D-binding protein: implications for the assessment of bioavailable vitamin D concentrations across genotypes. J Bone Miner Res Off J Am Soc Bone Miner Res. 2016;31:1128–36.CrossRef
57.
58.
Henderson CM, Lutsey PL, Misialek JR, Laha TJ, Selvin E, Eckfeldt JH, et al. Measurement by a novel LC-MS/MS methodology reveals similar serum concentrations of vitamin D-binding protein in blacks and whites. Clin Chem. 2016;62:179–87.PubMedCrossRef
59.
Bikle D, Bouillon R, Thadhani R, Schoenmakers I. Vitamin D metabolites in captivity? Should we measure free or total 25(OH) D to assess vitamin D status? 19th Vitam Workshop. 2017;173:105–16.
60.
61.
Okamoto K, Nakashima T, Shinohara M, Negishi-Koga T, Komatsu N, Terashima A, et al. Osteoimmunology: the conceptual framework unifying the immune and skeletal systems. Physiol Rev. 2017;97:1295–349.PubMedCrossRef
62.
63.
Atkins RC. Inflammatory cytokines in glomerulonephritis. Nephrology. 2008;7:S2–6.CrossRef
64.
Gilbert L, He X, Farmer P, Rubin J, Drissi H, van Wijnen AJ, et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2αA) is inhibited by tumor necrosis factor-α. J Biol Chem. 2002;277:2695–701.PubMedCrossRef
65.
Ahuja SS, Zhao S, Bellido T, Plotkin LI, Jimenez F, Bonewald LF. CD40 ligand blocks apoptosis induced by tumor necrosis factor α, glucocorticoids, and etoposide in osteoblasts and the osteocyte-like cell line murine long bone osteocyte-Y4. Endocrinology. 2003;144:1761–9.PubMedCrossRef
66.
Osami K, Yosuke F, Ichiro I, Afsie S, Takehiko T, Athanasou Nicholas A. Proinflammatory cytokine (TNFα/IL-1α) induction of human osteoclast formation. J Pathol. 2002;198:220–7.CrossRef
67.
Steeve KT, Marc P, Sandrine T, Dominique H, Yannick F. IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev. 2004;15:49–60.CrossRef
68.
Hendy GN, Canaff L. Calcium-sensing receptor, proinflammatory cytokines and calcium homeostasis. Semin Cell Dev Biol 2016;49:37–43.CrossRef
69.
Liu N, Nguyen L, Chun RF, Lagishetty V, Ren S, Wu S, et al. Altered endocrine and autocrine metabolism of vitamin D in a mouse model of gastrointestinal inflammation. Endocrinology. 2008;149:4799–808.PubMedPubMedCentralCrossRef
70.
Uno JK, Kolek OI, Hines ER, Xu H, Timmermann BN, Kiela PR, et al. The role of tumor necrosis factor α in down-regulation of osteoblast Phex gene expression in experimental murine colitis. Gastroenterology. 2006;131:497–509.PubMedCrossRef
71.
Inoue Y, Segawa H, Kaneko I, Yamanaka S, Kusano K, Kawakami E, et al. Role of the vitamin D receptor in FGF23 action on phosphate metabolism. Biochem J. 2005;390:325–31.PubMedPubMedCentralCrossRef
72.
Ben-Dov IZ, Galitzer H, Lavi-Moshayoff V, Goetz R, Kuro-o M, Mohammadi M, et al. The parathyroid is a target organ for FGF23 in rats. J Clin Invest. 2007;117:4003–8.
73.
74.
Raphael I, Nalawade S, Eagar TN, Forsthuber TG. T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokines Immune Pathog Ther. 2015;74:5–17.
75.
Boyce BF, Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Highlight Issue Bone Remodel Facts Perspect. 2008;473:139–46.
76.
Krebs CF, Schmidt T, Riedel J-H, Panzer U. T helper type 17 cells in immune-mediated glomerular disease. Nat Rev Nephrol. 2017;13:647–59.PubMedCrossRef
77.
Yuan F-L, Li X, Lu W-G, Xu R-S, Zhao Y-Q, Li C-W, et al. Regulatory T cells as a potent target for controlling bone loss. Biochem Biophys Res Commun. 2010;402:173–6.PubMedCrossRef
78.
Glowacki AJ, Yoshizawa S, Jhunjhunwala S, Vieira AE, Garlet GP, Sfeir C, et al. Prevention of inflammation-mediated bone loss in murine and canine periodontal disease via recruitment of regulatory lymphocytes. Proc Natl Acad Sci U S A. 2013;110:18525–30.PubMedPubMedCentralCrossRef
79.
Burnham JM. Inflammatory diseases and bone health in children. Curr Opin Rheumatoldenburg. 2012;24:548–53.PubMedCrossRef
80.
Freundlich M, Alonzo E, Bellorin-Font E, Weisinger JR. Increased osteoblastic activity and expression of receptor activator of NF-κB ligand in nonuremic nephrotic syndrome. J Am Soc Nephrol. 2005;16:2198–204.PubMedCrossRef
81.
Ensrud KE, Barbour K, Canales MT, Danielson ME, Boudreau RM, Bauer DC, et al. Renal function and nonvertebral fracture risk in multiethnic women: the Women’s Health Initiative (WHI). Osteoporos Int. 2012;23:887–99.PubMedCrossRef
82.
Lombel RM, Gipson DS, Hodson EM. Treatment of steroid-sensitive nephrotic syndrome: new guidelines from KDIGO. Pediatr Nephrol. 2013;28:415–26.PubMedCrossRef
83.
Lombel RM, Hodson EM, Gipson DS. Treatment of steroid-resistant nephrotic syndrome in children: new guidelines from KDIGO. Pediatr Nephrol. 2013;28:409–14.PubMedCrossRef
84.
•• Weinstein RS. Glucocorticoid-induced bone disease. N Engl J Med. 2011;365:62–70. The author provides a review of glucocorticoid-associated osteoporosis and offers strategies to reduce the risk of skeletal fracture. PubMedCrossRef
85.
Van Staa TP, Leufkens HGM, Abenhaim L, Zhang B, Cooper C. Use of oral corticosteroids and risk of fractures. J Bone Miner Res. 2000;15:993–1000.PubMedCrossRef
86.
van Staa TP, van Staa TP, van Staa TP, Leufkens HGM, Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int. 2002;13:777–87.PubMedCrossRef
87.
Gipson DS, Massengill SF, Yao L, Nagaraj S, Smoyer WE, Mahan JD, et al. Management of childhood onset nephrotic syndrome. Pediatrics. 2009;124:747–57.PubMedCrossRef
88.
van Staa TP, Cooper C, Leufkens H, Bishop N. Children and the risk of fractures caused by oral corticosteroids. J Bone Miner Res. 2003;18:913–8.PubMedCrossRef
89.
90.
Weinstein RS, Jilka RL, Parfitt AM, Manolagas SC. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J Clin Invest. 1998;102:274–82.PubMedPubMedCentralCrossRef
91.
Vestergaard P, Rejnmark L, Mosekilde L. Fracture risk associated with different types of oral corticosteroids and effect of termination of corticosteroids on the risk of fractures. Calcif Tissue Int. 2008;82:249–57.PubMedCrossRef
92.
Phan V, Blydt-Hansen T, Feber J, Alos N, Arora S, Atkinson S, et al. Skeletal findings in the first 12 months following initiation of glucocorticoid therapy for pediatric nephrotic syndrome. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2014;25:627–37.CrossRef
93.
Leonard MB, Feldman HI, Shults J, Zemel BS, Foster BJ, Stallings VA. Long-term, high-dose glucocorticoids and bone mineral content in childhood glucocorticoid-sensitive nephrotic syndrome. N Engl J Med. 2004;351:868–75.PubMedCrossRef
94.
Bhudhikanok GS, Lim J, Marcus R, Harkins A, Moss RB, Bachrach LK. Correlates of osteopenia in patients with cystic fibrosis. Pediatrics. 1996;97:103.PubMed
95.
Gunhild L, Berit F, Margaretha H, Odd V, Dag S, Knut D, et al. Frequency of osteopenia in adolescents with early-onset juvenile idiopathic arthritis: a long-term outcome study of one hundred five patients. Arthritis Rheum. 2003;48:2214–23.CrossRef
96.
Boot AM, Bouquet J, Krenning EP, de Muinck K-SSMPF. Bone mineral density and nutritional status in children with chronic inflammatory bowel disease. Gut. 1998;42:188–94.PubMedPubMedCentralCrossRef
97.
Briner VA, Landmann J, Brunner FP, Thiel G. Cyclosporin A-induced transient rise in plasma alkaline phosphatase in kidney transplant patients. Transpl Int. 1993;6:99–107.PubMedCrossRef
98.
Aubia J, Masramón J, Serrano S, Lloveras J, Marinoso L, Bourbigot B, et al. Bone histology in renal transplant patients receiving cyclosporin. Lancet. 1988;331:1048–9.CrossRef
99.
Grotz WH, Alexander Mundinger F, Gugel B, Exner VM, Kirste G, Schollmeyer PJ. Bone mineral density after kidney transplantation: a cross - sectional study in 190 graft recipients up to 20 years after transplantation. Transplantation. 1995;59:982–6.PubMedCrossRef
100.
McIntyre HD, Menzies B, Rigby R, Perry-Keene DA, Hawley CM, Hardie IR. Long-term bone loss after renal transplantation: comparison of immmunosuppressive regimens. Clin Transpl. 1995;9:20–4.
101.
Westeel FP, Mazouz H, Ezaitouni F, Hottelart C, Ivan C, Fardellone P, et al. Cyclosporine bone remodeling effect prevents steroid osteopenia after kidney transplantation. Kidney Int. 2000;58:1788–96.PubMedCrossRef
102.
Torregrosa J-V, Campistol J-M, Montesinos M, Fenollosa B, Pons F, De Osaba M-JM, et al. Factors involved in the loss of bone mineral density after renal transplantation. Transplant Proc. 1995;27:2224–5.PubMed
103.
Parry RG, Jackson J, Stevens JM, Higgins B, Altmann P. Long-term bone densitometry post-renal transplantation in patients treated with either cyclosporin or prednisolone [11]. Nephrol Dial Transplant. 1998;13:531–2.PubMedCrossRef
104.
Cueto-Manzano AM, Konel S, Hutchison AJ, Crowley V, France MW, Freemont AJ, et al. Bone loss in long-term renal transplantation: histopathology and densitometry analysis. Kidney Int. 1999;55:2021–9.PubMedCrossRef
105.
Chowdhury MH, Shen V, Dempster DW. Effects of cyclosporine a on chick osteoclastsIn vitro. Calcif Tissue Int. 1991;49:275–9.PubMedCrossRef
106.
Klaushofer K, Hoffmann O, Stewart PJ, Czerwenka E, Koller K, Peterlik M, et al. Cyclosporine A inhibits bone resorption in cultured neonatal mouse calvaria. J Pharmacol Exp Ther. 1987;243:584–90.PubMed
107.
Stein B, Halloran BP, Reinhardt T, Engstrom GW, Bales CW, Drezner MK, et al. Cyclosporin-A increases synthesis of 1,25-dihydroxyvitamin D3 in the rat and mouse. Endocrinology. 1991;128:1369–73.PubMedCrossRef
108.
109.
Buchinsky FJ, Ma Y, Mann GN, Rucinski B, Bryer HP, Romero DF, et al. T lymphocytes play a critical role in the development of cyclosporin A-induced osteopenia. Endocrinology. 1996;137:2278–85.PubMedCrossRef
110.
Shimizu C, Fujita T, Fuke Y, Yabuki M, Kajiwara M, Hemmi S, et al. Effects of cyclosporine on bone mineral density in patients with glucocorticoid-dependent nephrotic syndrome in remission. Int Urol Nephrol. 2013;45:803–8.PubMedCrossRef
111.
Susannah O’S, Andrew G. Adverse skeletal effects of drugs – beyond glucocorticoids. Clin Endocrinol. 2014;82:12–22.
112.
Carbone LD, Johnson KC, Bush AJ, Robbins J, Larson JC, Thomas A, et al. Loop diuretic use and fracture in postmenopausal women: findings from the Women’s Health Initiative. Arch Intern Med. 2009;169:132–40.PubMedCrossRef
113.
Rejnmark L, Vestergaard P, Heickendorff L, Andreasen F, Mosekilde L. Effects of long-term treatment with loop diuretics on bone mineral density, calcitropic hormones and bone turnover. J Intern Med. 2005;257:176–84.PubMedCrossRef
114.
Solomon DH, Mogun H, Garneau K, Fischer MA. Risk of fractures in older adults using antihypertensive medications. J Bone Miner Res. 2011;26:1561–7.PubMedCrossRef
115.
Lim LS, Fink HA, Blackwell T, Taylor BC, Ensrud KE. Loop diuretic use and rates of hip bone loss and risk of falls and fractures in older women. J Am Geriatr Soc. 2009;57:855–62.PubMedPubMedCentralCrossRef
116.
Berry SD, Zhu Y, Choi H, Kiel DP, Zhang Y. Diuretic initiation and the acute risk of hip fracture. Osteoporos Int. 2013;24:689–95.PubMedCrossRef
117.
Kocsis I, Arató A, Bodánszky H, Szönyi L, Szabó A, Tulassay T, et al. Short-term omeprazole treatment does not influence biochemical parameters of bone turnover in children. Calcif Tissue Int. 2002;71:129–32.PubMedCrossRef
118.
Ozdil K, Kahraman R, Sahin A, Calhan T, Gozden EH, Akyuz U, et al. Bone density in proton pump inhibitors users: a prospective study. Rheumatol Int. 2013;33:2255–60.PubMedCrossRef
119.
Yu EW, Blackwell T, Ensrud KE, Hillier TA, Lane NE, Orwoll E, et al. Acid-suppressive medications and risk of bone loss and fracture in older adults. Calcif Tissue Int. 2008;83:251–9.PubMedPubMedCentralCrossRef
120.
Cea Soriano L, Ruigómez A, Johansson S, García Rodríguez LA. Study of the association between hip fracture and acid-suppressive drug use in a UK primary care setting. Pharmacother J Hum Pharmacol Drug Ther. 2014;34:570–81.CrossRef
121.
Freedberg DE, Haynes K, Denburg MR, Zemel BS, Leonard MB, Abrams JA, et al. Use of proton pump inhibitors is associated with fractures in young adults: a population-based study. Osteoporos Int. 2015;26:2501–7.PubMedPubMedCentralCrossRef
122.
Liu J, Li X, Fan L, Yang J, Wang J, Sun J, et al. Proton pump inhibitors therapy and risk of bone diseases: an update meta-analysis. Life Sci. 2019;218:213–23.PubMedCrossRef
123.
Gulati S, Godbole M, Singh U, Gulati K, Srivastava A. Are children with idiopathic nephrotic syndrome at risk for metabolic bone disease? Am J Kidney Dis. 2003;41:1163–9.PubMedCrossRef
124.
Aceto G, D’Addato O, Messina G, Carbone V, Cavallo L, Brunetti G, et al. Bone health in children and adolescents with steroid-sensitive nephrotic syndrome assessed by DXA and QUS. Pediatr Nephrol. 2014;29:2147–55.PubMedCrossRef
125.
Kosan C, Ayar G, Orbak Z. Effects of steroid treatment on bone mineral metabolism in children with glucocorticoid-sensitive nephrotic syndrome. West Indian Med J. 2012;61:627–30.PubMed
126.
Pańczyk-Tomaszewska M, Adamczuk D, Kisiel A, Skrzypczyk P, Przedlacki J, Górska E, et al. Markers of bone metabolism in children with nephrotic syndrome treated with corticosteroids. In: Pokorski M, editor. Body Metab Exerc [internet]. Cham: Springer International Publishing; 2015. p. 21–8. https://​doi.​org/​10.​1007/​5584_​2014_​87.CrossRef
127.
Ribeiro D, Zawadynski S, Pittet LF, Chevalley T, Girardin E, Parvex P. Effect of glucocorticoids on growth and bone mineral density in children with nephrotic syndrome. Eur J Pediatr. 2015;174:911–7.PubMedCrossRef
128.
Kano K, Yamada Y, Nishikura K, Kojima E, Arisaka O. Low bone mineral density in nephrotic children with steroid dependence and/or frequent relapsers. Clin Nephrol. 2005;64:323–4.PubMedCrossRef
129.
Broyer M, Terzi F, Lehnert A, Gagnadoux MF, Guest G, Niaudet P. A controlled study of deflazacort in the treatment of idiopathic nephrotic syndrome. Pediatr Nephrol Berl Ger. 1997;11:418–22.CrossRef
130.
Lettgen B, Jeken C, Reiners C. Influence of steroid medication on bone mineral density in children with nephrotic syndrome. Pediatr Nephrol Berl Ger. 1994;8:667–70.CrossRef
131.
Takeda Y. Evaluation of bone mineral turnover in children with nephrotic syndrome--the implications of original disease and the effects of corticosteroids on bone metabolism. Nihon Jinzo Gakkai Shi. 1993;35:705–13.PubMed
132.
Mishra OP, Meena SK, Singh SK, Prasad R, Mishra RN. Bone mineral density in children with steroid-sensitive nephrotic syndrome. Indian J Pediatr. 2009;76:1237–9.PubMedCrossRef
133.
Moon R, Gilbert R, Page A, Murphy L, Taylor P, Cooper C, et al. Children with nephrotic syndrome have greater bone area but similar volumetric bone mineral density to healthy controls. Bone. 2014;58:108–13.PubMedCrossRef
134.
Wetzsteon Rachel J, Justine S, Zemel Babette S, Gupta Pooja U, Burnham Jon M, Herskovitz Rita M, et al. Divergent effects of glucocorticoids on cortical and trabecular compartment BMD in childhood nephrotic syndrome. J Bone Miner Res. 2009;24:503–13.PubMedCrossRef
135.
Tsampalieros A, Gupta P, Denburg MR, Justine S, Zemel BS, Sogol M-M, et al. Glucocorticoid effects on changes in bone mineral density and cortical structure in childhood nephrotic syndrome. J Bone Miner Res. 2012;28:480–8.CrossRef
136.
Hegarty J, Mughal MZ, Adams J, Webb NJA. Reduced bone mineral density in adults treated with high-dose corticosteroids for childhood nephrotic syndrome. Kidney Int. 2005;68:2304–9.PubMedCrossRef
137.
Kyrieleis HA, Löwik MM, Pronk I, Cruysberg HR, Kremer JA, Oyen WJ, et al. Long-term outcome of biopsy-proven, frequently relapsing minimal-change nephrotic syndrome in children. Clin J Am Soc Nephrol CJASN. 2009;4:1593–600.PubMedCrossRef
138.
Lim P, Jacob E, Tock EP, Pwee HS. Calcium and phosphorus metabolism in nephrotic syndrome. Q J Med. 1977;46:327–38.PubMed
139.
Freundlich M, Jofe M, Goodman WG, Salusky IB. Bone histology in steroid-treated children with non-azotemic nephrotic syndrome. Pediatr Nephrol. 2004;19:400–7.PubMedCrossRef
140.
Alem A, Sherrard D, Gillen D, Weiss N, Beresford S, Heckbert S, et al. Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int. 2000;58:396–9.PubMedCrossRef
141.
Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, et al. Risk of hip fracture among dialysis and renal transplant recipients. JAMA. 2002;288:3014–8.PubMedCrossRef
142.
Doan QV, Gleeson M, Kim J, Borker R, Griffiths R, Dubois RW. Economic burden of cardiovascular events and fractures among patients with end-stage renal disease. Curr Med Res Opin. 2007;23:1561–9.PubMedCrossRef
143.
Inaba M, Okuno S, Kumeda Y, Yamakawa T, Ishimura E, Nishizawa Y. Increased incidence of vertebral fracture in older female hemodialyzed patients with type 2 diabetes mellitus. Calcif Tissue Int. 2005;76:256–60.PubMedCrossRef
144.
Jadoul M, Albert JM, Akiba T, Akizawa T, Arab L, Bragg-Gresham JL, et al. Incidence and risk factors for hip or other bone fractures among hemodialysis patients in the Dialysis Outcomes and Practice Patterns Study. Kidney Int. 2006;70:1358–66.PubMedCrossRef
145.
Stehman-Breen CO, Sherrard DJ, Alem AM, Gillen DL, Heckbert SR, Wong CS, et al. Risk factors for hip fracture among patients with end-stage renal disease. Kidney Int. 2000;58:2200–5.PubMedCrossRef
146.
147.
Kaji H, Yamauchi M, Yamaguchi T, Shigematsu T, Sugimoto T. Mild renal dysfunction is a risk factor for a decrease in bone mineral density and vertebral fractures in Japanese postmenopausal women. J Clin Endocrinol Metab. 2010;95:4635–42.PubMedCrossRef
148.
Nitsch D, Mylne A, Roderick PJ, Smeeth L, Hubbard R, Fletcher A. Chronic kidney disease and hip fracture-related mortality in older people in the UK. Nephrol Dial Transplant. 2009;24:1539–44.PubMedCrossRef
149.
Dooley AC, Weiss NS, Kestenbaum B. Increased risk of hip fracture among men with CKD. Am J Kidney Dis. 2008;51:38–44.PubMedCrossRef
150.
Dukas L, Schacht E, Stähelin HB. In elderly men and women treated for osteoporosis a low creatinine clearance of <65 ml/min is a risk factor for falls and fractures. Osteoporos Int. 2005;16:1683–90.PubMedCrossRef
151.
Ensrud KE, Lui L, Taylor BC, Ishani A, Shlipak MG, Stone KL, et al. Renal function and risk of hip and vertebral fractures in older women. Arch Intern Med. 2007;167:133–9.PubMedCrossRef
152.
Fried LF, Biggs ML, Shlipak MG, Seliger S, Kestenbaum B, Stehman-Breen C, et al. Association of kidney function with incident hip fracture in older adults. J Am Soc Nephrol. 2007;18:282–6.PubMedCrossRef
153.
Jassal SK, von Muhlen D, Barrett-Connor E. Measures of renal function, bone mineral density, bone loss and osteoporotic fracture in older adults: the Rancho Bernardo Study. J Bone Miner Res Off J Am Soc Bone Miner Res. 2007;22:203–10.CrossRef
154.
LaCroix AZ, Lee JS, Wu L, Cauley JA, Shlipak MG, Ott SM, et al. Cystatin-C, renal function and incidence of hip fracture in postmenopausal women. J Am Geriatr Soc. 2008;56:1434–41.PubMedPubMedCentralCrossRef
155.
Naylor KL, McArthur E, Leslie WD, Fraser L-A, Jamal SA, Cadarette SM, et al. The three-year incidence of fracture in chronic kidney disease. Kidney Int. 2014;86:810–8.PubMedCrossRef
156.
Nickolas TL, McMahon DJ, Shane E. Relationship between moderate to severe kidney disease and hip fracture in the United States. J Am Soc Nephrol. 2006;17:3223–32.PubMedCrossRef
157.
Isakova T, Craven TE, Scialla JJ, Nickolas TL, Schnall A, Barzilay J, et al. Change in estimated glomerular filtration rate and fracture risk in the action to control cardiovascular risk in diabetes trial. Bone. 2015;78:23–7.PubMedPubMedCentralCrossRef
158.
Clark SL, Denburg MR, Furth SL. Physical activity and screen time in adolescents in the chronic kidney disease in children (CKiD) cohort. Pediatr Nephrol Berl Ger. 2016;31:801–8.CrossRef
159.
Lai C-C, Chen W-S, Chang D-M, Tsao Y-P, Wu T-H, Chou C-T, et al. Increased serum fibroblast growth factor-23 and decreased bone turnover in patients with systemic lupus erythematosus under treatment with cyclosporine and steroid but not steroid only. Osteoporos Int. 2015;26:601–10.PubMedCrossRef
Metadata
Title
Bone Health in Glomerular Kidney Disease
Authors
Dorey A. Glenn
Michelle R. Denburg
Publication date
01-12-2019
Publisher
Springer US
Published in
Current Osteoporosis Reports / Issue 6/2019
Print ISSN: 1544-1873
Electronic ISSN: 1544-2241
DOI
https://doi.org/10.1007/s11914-019-00531-z

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Correction

Correction to: Are CT-Based Finite Element Model Predictions of Femoral Bone Strength Clinically Useful?