Abstract
Organ transplantation has become increasingly common as a therapy for end-stage renal, liver, cardiac and pulmonary disease. The population of patients who have survived organ transplantation has grown dramatically over the last 2 decades. Although organ transplant recipients now benefit from greatly improved survival, long-term complications of organ transplantation, such as osteoporosis, adversely affect quality of life and must be addressed. In the early post-transplantation period, the effects of high dose glucocorticoids, combined with other immunosuppressive drugs such as cycosporine A and tacrolimus, cause rapid bone loss particularly at the spine and proximal femur. In this setting, fracture incidence rates as high as 25–65% have been reported. Treatment and prevention strategies must target this early post-transplant period, as well as the patient awaiting transplantation and the long-term transplant recipient. This review will discuss the clinical features of transplantation osteoporosis, the pathophysiology of post-transplantation bone loss and prevention and therapy of this unique bone disease.
Similar content being viewed by others
References
Goodman WG, Coburn JW, Slatopolsky E et al. (1999) Renal osteodystrophy in adults and children. In: Favus MJ, Christakos S (eds) Primer on the metabolic bone diseases and disorders of mineral metabolism, 4th edn. Lippincott-Raven, Philadelphia, pp 347–63
Elder G (2002) Pathophysiology and recent advances in the management of renal osteodystrophy. Osteoporos Int 17:2094–2105
Hruska KA, Teitelbaum SL (1995) Renal osteodystrophy. N Engl J Med 333:166–174
Stein M, Packham D, Ebeling P et al. (1996) Prevalence and risks factors for osteopoenia in dialysis patients. Am J Kidney Dis 28:515–522
Taal MW, Masud T, Green D et al. (1999) Risk factors for reduced bone density in haemodialysis patients. Nephrol Dial Transplant 14:1922–1928
Lechleitner P, Krimbacher E, Genser N et al. (1994) Bone mineral densitometry in dialyzed patients: quantitative computed tomography versus dual photon absorptiometry. Bone 15:387–391
Atsumi K, Kushida K, Yamazaki K et al. (1999) Risk factors for vertebral fractures in renal osteodystrophy. Am J Kidney Dis 33:287–293
Gupta A, Kallenbach LR, Divine GW (1997) Increased risk of hip fracture in US Medicare end-stage renal disease patients. J Bone Miner Res 12:S274
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
Ball AM, Gillen DL, Sherrard D et al. (2002) Risk of hip fracture among dialysis and renal transplant recipients. JAMA 288:3014–3018
Lee AH, Mull RL, Keenan GF et al. (1994) Osteoporosis and bone morbidity in cardiac transplant recipients. Am J Med 96:35–41
Muchmore JS, Cooper DKC, Ye Y et al. (1991) Loss of vertebral bone density in heart transplant patients. Transplant Proc 23:1184–1185
Shane E, Mancini D, Aaronson K et al. (1997) Bone mass, vitamin D deficiency and hyperparathyroidism in congestive heart failure. Am J Med 103:197–207
Maddrey WC (1990) Bone disease in patients with primary biliary cirrhosis. Prog. Liver Dis 9:537–554
Hodgson SF, Dickson ER, Wahner HW et al. (1980) Bone loss and reduced osteoblast function in primary biliary cirrhosis. Ann Int Med 103:855–860
Janes CH, Dickson ER, Okazaki R et al. (1995) Role of hyperbilirubinemia in the impairment of osteoblast proliferation associated with cholestatic jaundice. J Clin Invest 95:2581–2586
Friday KE, Howard GA (1991) Ethanol inhibits human bone cell proliferation and function in vitro. Metabolism 40:562–565
Bikle DD (1993) Alcohol-induced bone disease. World Rev Nutr Diet 73:53–79
Peris P, Guanabens N, Pares A et al. (1995) Vertebral fractures and osteopenia in chronic alcoholic patients. Calcif Tissue Int 57:111–114
Trautwein C, Possienke M, Schlitt H et al. (2000) Bone density and metabolism in patients with viral hepatitis and cholestatic liver diseases before and after liver transplantation. Am J Gastroenterol 95:2343–2451
Diamond T, Stiel D, Posen S (1989) Osteoporosis in hemochromatosis: iron excess, gonadal deficiency, or other factors? Ann Int Med 110:430–436
Stellon AJ, Davies A, Compston J et al. (1985) Bone loss in autoimmune chronic active hepatitis on maintenance corticosteroid therapy. Gastroenterology 89:1078–1083
Olsson R, Johansson C, Lindstedt G et al. (1994) Risk factors for bone loss in chronic active hepatitis and primary biliary cirrhosis. Scand J Gastroenterol 29:753–756
Crosbie OM, Freaney R, McKenna MJ et al. (1999) Bone density, vitamin D status, and disordered bone remodeling in end-stage chronic liver disease. Calcif Tissue Int 64:295–300
Monegal A, Navasa M, Guanabens N et al. (1997) Osteoporosis and bone mineral metabolism in cirrhotic patients referred for liver transplantation. Calcif Tissue Int 60:148–154
Floreani A, Mega A, Tizian L et al. (2001) Bone metabolism and gonad function in male patients undergoing liver transplantation: a two-year longitudinal study. Osteoporos Int 12:749–754
Ninkovic M, Love SA, Tom B et al. (2001) High prevalence of osteoporosis in patients with chronic liver disease prior to liver transplantation. Calcif Tissue Int 69:321–326
Monegal A, Navasa M, Guanabens N et al. 2001 Bone disease after liver transplantation: a long-term prospective study of bone mass changes, hormonal status and histomorphometric characteristics. Osteoporos Int 12:484–492
Ott SM, Aitken ML (1998) Osteoporosis in patients with cystic fibrosis. Clin Chest Med 19:555–567
Aris R, Neuringer I, Weiner M et al. (1996) Severe osteoporosis before and after lung transplantation. Chest 109:1176–1183
Donovan DS Jr, Papadopoulos A, Staron RB et al. (1998) Bone mass and vitamin D deficiency in adults with advanced cystic fibrosis lung disease. Am J Respir Crit Care Med 157:1892–1899
Shane E, Silverberg SJ, Donovan D et al. (1996) Osteoporosis in lung transplantation candidates with end stage pulmonary disease. Am J Med 101:262–269
Trombetti A, Gerbase MW, Spiliopoulos A et al. (2000) Bone mineral density in lung-transplant recipients before and after graft: prevention of lumbar spine post-transplantation-accelerated bone loss by pamidronate. J Heart Lung Transplant 19:736–743
Ferrari SL, Nicod LP, Hamacher J et al. (1996) Osteoporosis in patients undergoing lung transplantation. Eur Respir J 9:2378–2382
Lien D, Jackson K, Monkhouse P et al. (2001) Intervention prevents progression of osteoporosis in patients awaiting lung transplantation. J Heart Lung Transplant 20:225
Tschopp O, Boehler A, Speich R et al. (2002) Osteoporosis before lung transplantation: association with low body mass index, but not with underlying disease. Am J Transplant 2:167–172
Aris RM, Renner JB, Winders AD et al. (1998) Increased rate of fractures and severe kyphosis: sequelae of living into adulthood with cystic fibrosis. Ann Int Med 128:186–193
Elkin SL, Fairney A, Burnett S et al. (2001) Vertebral deformities and low bone mineral density in adults with cystic fibrosis: a cross-sectional study. Osteoporos Int 12:366–372
Haworth CS, Selby PL, Webb AK et al. (1999) Low bone mineral density in adults with cystic fibrosis. Thorax 54:961–967
Elkin SL, Vedi S, Bord S et al. (2002) Histomorphometric analysis of bone biopsies from the iliac crest of adults with cystic fibrosis. Am J Respir Crit Care Med 166:1470–1474
Schulte C, Beelen D, Schaefer U et al. (2000) Bone loss in long-term survivors after transplantation of hematopoietic stem cells: a prospectiv estudy. Osteoporos Int 11:344–353
Cooper MS (2001) Glucocorticoid-induced osteoporosis. Curr Opin Endocrinol Diabet 8:140–145
Van Staa TP, Leufkens HG, Abenhaim L et al. (2000) Use of oral corticosteroids and risk of fractures. J Bone Miner Res 15:993–1000
Lane NE, Lukert B (1998) The science and therapy of glucocorticoid-induced bone loss. Endocrinol Metab Clin N Am 27:465–483
Weinstein R, Jilka R, Parfitt M et al. (1998) Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids: potential mechanisms of their deleterious effects on bone. J Clin Invest 102:274–282
Dempster DW (1989) Bone histomorphometry in glucocorticoid-induced osteoporosis. J Bone Miner Res 4:137–141
Kahan BD (1989) Cyclosporine. N Engl J Med 321:1725–1738
Suthanthiran M, Strom TB (1994) Renal transplantation. N Engl J Med 331:365–376
Epstein S (1996) Post-transplantation bone disease: the role of immunosuppressive agents on the skeleton. J Bone Miner Res 11:1–7
Cvetkovic M, Mann GN, Romero DF et al. (1994) The deleterious effects of long term cyclosporin A, cyclosporin G and FK506 on bone mineral metabolism in vivo. Transplantation 57:1231–1237
Orcel P, Denne MA, de Vernejoul MC (1991) Cyclosporin-A in vitro decreases bone resorption, osteoclast formation, and the fusion of cells of the monocyte-macrophage lineage. Endocrinology 128:1638–1646
Schlosberg M, Movsowitz C, Epstein S et al. (1989) The effects of cyclosporin A administration and its withdrawal on bone mineral metabolism in the rat. Endocrinology 124:2179–2184
Movsowitz C, Epstein S, Fallon M et al. (1988) Cyclosporin A in vivo produces severe osteopenia in the rat: effect of dose and duration of administration. Endocrinology 123:2571–2577
Movsowitz C, Epstein S, Ismail F et al. (1989) Cyclosporin A in the oophorectomized rat: unexpected severe bone resorption. J Bone Miner Res 4:393–398
Bowman AR, Sass DA, Dissanayake IR et al. (1997) The role of testosterone in cyclosporine-induced osteopenia. J Bone Miner Res 12:607–615
Epstein S, Dissanayake A, Goodman GR et al. (2001) Effect of the interaction of parathyroid hormone and cyclosporine A on bone mineral metabolism in the rat. Calcif Tissue Int 68:240–247
Joffe I, Katz I, Jacobs T et al. (1992) 17 Beta estradiol prevents osteopenia in the oophorectomized rat treated with cyclosporin A. Endocrinology 130:1578–1586
Bowman A, Sass D, Marshall I et al. (1995) Raloxifene analog (Ly 117018-HCL) ameliorates cyclosporin A induced osteopenia. J Bone Miner Res 10:350
Stein B, Takizawa M, Katz I et al. (1991) Salmon calcitonin prevents cyclosporin A induced high turnover bone loss. Endocrinology 129:92–98
Sass DA, Bowman AR, Marshall I et al. (1997) Alendronate prevents cyclosporin-induced osteopenia in the rat. Bone 21:65–70
Awumey E, Moonga B, Sodam B et al. (1999) Molecular and functional evidence for calcineurin alpha and beta isoforms in the osteoclasts. Novel insights into the mode of action of cyclosporine A. Biochem Biophys Res Commun 254:148–252
Buchinsky F, Ma Y, Mann G et al. (1996) T lymphocytes play a critical role in the development of cyclosporine induced osteopenia. Endocrinology 59:2278–2285
Ponticelli C, Aroldi A (2001) Osteoporosis after organ transplantation. Lancet 357:1623
Grotz W, Mundinger A, Gugel B et al. (1994) Missing impact of cyclosporine on osteoporosis in renal transplant recipients. Transplant Proc 26:2652–2653
McIntyre HD, Menzies B, Rigby R et al. (1995) Long-term bone loss after renal transplantation: comparison of immunosuppressive regimens. Clin Transplant 9:20–24
Inoue T, Kawamura I, Matsuo M et al. (2000) Lesser reduction in bone mineral density by the immunosuppresant, FK506, compared with cyclosporine in rats. Transplantation 70:774–779
Stempfle HU, Werner C, Echtler S et al. (1998) Rapid trabecular bone loss after cardiac transplantation using FK506 (tacrolimus)-based immunosuppression. Transplant Proc 30:1132–1133
Park KM, Hay JE, Lee SG et al. (1996) Bone loss after orthotopic liver transplantation: FK 506 versus cyclosporine. Transplant Proc 28:1738–1740
Goffin E, Devogelaer JP, Depresseux G et al. (2001) Osteoporosis after organ transplantation. Lancet 357:1623
Monegal A, Navasa M, Guanabens N et al. (2001) Bone mass and mineral metabolism in liver transplant patients treated with FK506 or cyclosporine A. Calcif Tissue Int 68:83–86
Bryer HP, Isserow JA, Armstrong EC et al. (1995) Azathioprine alone is bone sparing and does not alter cyclosporine A induced osteopenia in the rat. J Bone Miner Res 10:132–138
Dissanayake IR, Goodman GR, Bowman AR et al. (1998) Mycophenolate mofetil; a promising new immunosuppressant that does not cause bone loss in the rat. Transplantation 65:275–278
Romero D, Buchinsky F, Rucinski B et al. (1995) Rapamycin: a bone sparing immunosuppressant? J Bone Miner Res 10:1556–1565
Julian BA, Laskow DA, Dubovsky J et al. (1991) Rapid loss of vertebral bone density after renal transplantation. N Engl J Med 325:544–550
Grotz W, Nagel C, Poeschel D et al. (2001) Effect of ibandronate on bone loss and renal function after kidney transplantation. J Am Soc Nephrol 12:1530–1537
Cayco AV, Wysolmerski J, Simpson C et al. (2000) Posttransplant bone disease: evidence for a high bone resorption state. Transplantation 70:1722–1728
Carlini RG, Rojas E, Weisinger JR et al. (2000) Bone disease in patients with long-term renal transplantation and normal renal function. Am J Kidney Dis 36:160–166
Monier-Faugere M, Mawad H, Qi Q et al. (2000) High prevalence of low bone turnover and occurrence of osteomalacia after kidney transplantation. J Am Soc Nephrol 11:1093–1099
Cueto-Manzano A, Konel S, Hutchinson AJ et al. (1999) Bone loss in long term renal transplantation. Histopathology and densitometry analysis. Kidney Int 55:2021–2029
Bagni B, Gilli P, Cavallini A et al. (1994) Continuing loss of vertebral mineral density in renal transplant recipients. Eur J Nucl Med 21:108–112
Pichette V, Bonnardeaux A, Prudhomme L et al. (1996) Long-term bone loss in kidney transplant recipients: a cross-sectional and longitudinal study. Am J Kidney Dis 28:105–114
Boot AM, Nauta J, Hokken-Koelega ACS et al. (1995) Renal transplantation and osteoporosis. Arch Dis Child 72:502–506
Heaf J, Tvedegaard E, Kanstrup IL et al. (2000) Bone loss after renal transplantation: role of hyperparathyroidism, acidosis, cyclosporine and systemic disease. Clin Transplant 14:457–463
Durieux S, Mercadal L, Orcel P et al. (2002) Bone mineral density and fracture prevalence in long-term kidney graft recipients. Transplantation 74:496–500
Ugur A, Guvener N, Isiklar I et al. (2001) Osteoporosis after renal transplantation: single center experience. Transplantation 71:645–649
Renau A, Yoldi B, Farrerons J et al. (2002) Bone mass and mineral metabolism in kidney transplant patients. Transplant Proc 34:407
Wolpaw T, Deal CL, Fleming-Brooks S et al. (1994) Factors influencing vertebral bone density after renal transplantation. Transplantation 58:1186–1189
Torregrosa JV, Campistol JM, Montesinos M et al. (1995) Factors involved in the loss of bone mineral density after renal transplantation. Transplant Proc 27:2224–2225
Yun YS, Kim BJ, Hong TW et al. (1996) Changes of bone metabolism indices in patients receiving immunosuppressive therapy including low doses of steroids after transplantation. Transplant Proc 28:1561–1564
Horber FF, Casez JP, Steiger U et al. (1994) Changes in bone mass early after kidney transplantation. J Bone Miner Res 9:1–9
Almond MK, Kwan JTC, Evans K et al. (1994) Loss of regional bone mineral density in the first 12 months following renal transplantation. Nephron 66:52–57
Moreno A, Torregrosa JV, Pons F et al. (1999) Bone mineral density after renal transplantation: long-term follow-up. Transplant Proc 31:2322–2323
Masse M, Girardin C, Ouimet D et al. (2001) Initial bone loss in kidney transplant recipients: a prospective study. Transplant Proc 33:1211
Cruz DN, Wysolmerski JJ, Brickel HM et al. (2001) Parameters of high bone-turnover predict bone loss in renal transplant patients: a longitudinal study. Transplantation 72:83–88
Farmer CKT, Hampson G, Vaja S et al. (2002) Late low dose steroid withdrawal in renal transplant recipients increases bone formation and bone mineral density without altering renal function: a randomized controlled trial. J Bone Miner Res 17:S158
Shane E, Epstein S (2001) Transplantation osteoporosis. Transplant Rev 15:11–32
Ramsey-Goldman R, Dunn JE, Dunlop DD et al. (1999) Increased risk of fracture in patients receiving solid organ transplants. J Bone Miner Res 14:456–463
Nisbeth U, Lindh E, Ljunghall S et al. (1999) Increased fracture rate in diabetes mellitus and females after renal transplantation. Transplantation 67:1218–1222
O'Shaughnessy EA, Dahl DC, Smith CL et al. (2002) Risk factors for fractures in kidney transplantation. Transplantation 74:362–366
Nisbeth U, Lindh E, Ljunghall S et al. (1994) Fracture frequency after kidney transplantation. Transplant Proc 26:1764
Vautour L, Melton LJ, Clarke BL et al. (2002) Long-term fracture risk following renal transplantation: a population-based study. J Bone Miner Res 17:S174
Smets YF, van der Pijl JW, de Fijter JW et al. (1998) Low bone mass and high incidence of fractures after successful simultaneous pancreas-kidney transplantation. Nephrol Dial Transplant 13:1250–1255
Chiu MY, Sprague SM, Bruce DS et al. (1998) Analysis of fracture prevalence in kidney-pancreas allograft recipients. J Am Soc Nephrol 9:677–683
Shane E, Rivas MDC, Silverberg SJ et al. (1993) Osteoporosis after cardiac transplantation. Am J Med 94:257–264
Shane E, Rivas M, McMahon DJ et al. (1997) Bone loss and turnover after cardiac transplantation. J Clin Endocrinol Metab 82:1497–1506
Sambrook PN, Kelly PJ, Keogh A et al. (1994) Bone loss after cardiac transplantation: a prospective study. J Heart Lung Transplant 13:116–121
Valimaki MJ, Kinnunen K, Tahtela R et al. (1999) A prospective study of bone loss and turnover after cardiac transplantation: effect of calcium supplementation with or without calcitonin. Osteoporos Int 10:128–136
Thiebaud D, Krieg M, Gillard-Berguer D et al. (1996) Cyclosporine induces high turnover and may contribute to bone loss after heart transplantation. Eur J Clin Invest 26:549–555
Berguer DG, Krieg MA, Thiebaud D et al. (1994) Osteoporosis in heart transplant recipients: a longitudinal study. Transplant Proc 26:2649–2651
Van Cleemput J, Daenen W, Nijs J et al. (1995) Timing and quantification of bone loss in cardiac transplant recipients. Transplant Int 8:196–200
Shane E, Addesso V, Namerow P et al. (2002) Prevention of bone loss after cardiac transplantation with alendronate or calcitriol: efficacy and safety. J Bone Miner Res 17:S135
Henderson NK, Sambrook PN, Kelly PJ et al. (1995) Bone mineral loss and recovery after cardiac transplantation [letter]. Lancet 346:905
Glendenning P, Kent GN, Adler BD et al. (1999) High prevalence of osteoporosis in cardiac transplant recipients and discordance between biochemical turnover markers and bone histomorphometry. Clin Endocrinol (Oxf) 50:347–355
Shane E, Rivas M, Staron RB et al. (1996) Fracture after cardiac transplantation: a prospective longitudinal study. J Clin Endocrinol Metab 81:1740–1746
Leidig-Bruckner G, Hosch S, Dodidou P et al. (2001) Frequency and predictors of osteoporotic fractures after cardiac or liver transplantation: a follow-up study. Lancet 357:342–347
Sambrook PN, Kelly PJ, Fontana D et al. (1994) Mechanisms of rapid bone loss following cardiac transplantation. Osteoporos Int 4:273–276
Rich GM, Mudge GH, Laffel GL et al. (1992) Cyclosporine A and prednisone-associated osteoporosis in heart transplant recipients. J Heart Lung Transplant 11:950–958
Guo C, Johnson A, Locke T et al. (1998) Mechanism of bone loss after cardiac transplantation. Bone 22:267–271
Arnold JC, Hauser R, Ziegler R et al. (1992) Bone disease after liver transplantation. Transplant Proc 24:2709–2710
McDonald JA, Dunstan CR, Dilworth P et al. (1991) Bone loss after liver transplantation. Hepatology 14:613–619
Navasa M, Monegal A, Guanabens N et al. (1994) Bone fractures in liver transplant patients. Br J Rheumatol 33:52–55
Eastell R, Dickson RE, Hodgson SF et al. (1991) Rates of vertebral bone loss before and after liver transplantation in women with primary biliary cirrhosis. Hepatology 14:296–300
Meys E, Fontanges E, Fourcade N et al. (1994) Bone loss after orthotopic liver transplantation. Am J Med 97:445–450
Keogh JB, Tsalamandris C, Sewell RB et al. (1999) Bone loss at the proximal femur and reduced lean mass following liver transplantation: a longitudinal study. Nutrition 15:661–664
Hamburg SM, Piers DA, van den Berg AP et al. 2000 Bone mineral density in the long term after liver transplantation. Osteoporos Int 11:600–606
Ninkovic M, Love S, Tom BD et al. (2002) Lack of effect of intravenous pamidronate on fracture incidence and bone mineral density after orthotopic liver transplantation. J Hepatol 37:93–100
Feller RB, McDonald JA, Sherbon KJ et al. (1999) Evidence of continuing bone recovery at a mean of 7 years after liver transplantation. Liver Transplant Surg 5:407–413
Giannini S, Nobile M, Ciuffreda M et al. (2000) Long-term persistence of low bone density in orthotopic liver transplantation. Osteoporos Int 11:417–424
Haagsma EB, Thijn CJP, Post JG et al. (1988) Bone disease after liver transplantation. J Hepatol 6:94–100
Ninkovic M, Skingle SJ, Bearcroft PW et al. (2000) Incidence of vertebral fractures in the first three months after orthotopic liver transplantation. Eur J Gastroenterol Hepatol 12:931–935
Valero M, Loinaz C, Larrodera L et al. (1995) Calcitonin and bisphosphonate treatment in bone loss after liver transplantation. Calcif Tissue Int 57:15–19
Abdelhadi M, Eriksson SA, Ljusk Eriksson S et al. (1995) Bone mineral status in end-stage liver disease and the effect of liver transplantation. Scand J Gastroenterol 30:1210–1215
Watson RG, Coulton L, Kanis JA et al. (1990) Circulating osteocalcin in primary biliary cirrhosis following liver transplantation and during treatment with ciclosporin. J Hepatol 11:354–358
Vedi J, Greer S, Skingle S et al. (1999) Mechanism of bone loss after liver transplantation: a histomorphometric analysis. J Bone Miner Res 14:281–287
Hawkins FG, Leon M, Lopez MB et al. (1994) Bone loss and turnover in patients with liver transplantation. Hepato-Gastroenterol 41:158–161
Compston J, Greer S, Skingle S et al. (1996) Early increase in plasma parathyroid hormone level following liver transplantation. J Hepatol 25:715–718
Spira A, Gutierrez C, Chaparro C et al. (2000) Osteoporosis and lung transplantation: a prospective study. Chest 117:476–481
Shane E, Papadopoulos A, Staron RB et al. (1999) Bone loss and fracture after lung transplantation. Transplantation 68:220–227
Aringer M, Kiener H, Koeller M et al. (1998) High turnover bone disease following lung transplantation. Bone 23:485–488
Haworth CS, Webb AK, Egan JJ et al. (2000) Bone histomorphometry in adult patients with cystic fibrosis. Chest 118:434–439
Stern JM, III CHC, Bruemmer B et al. (1996) Bone density loss during treatment of chronic GVHD. Bone Marrow Transplant 17:395–400
Ebeling P, Thomas D, Erbas B et al. (1999) Mechanism of bone loss following allogeneic and autologous hematopoeitic stem cell transplantation. J Bone Miner Res 14:342–350
Kang MI, Lee WY, Oh KW et al. (2000) The short-term changes of bone mineral metabolism following bone marrow transplantation. Bone 26:275–279
Valimaki M, Kinnunen K, Volin L et al. (1999) A prospective study of bone loss and turnover after allogeneic bone marrow transplantation: effect of calcium supplementation with or without calcitonin. Bone Marrow Transplant 23:355–361
Lee WY, Cho SW, Oh ES et al. (2002) The effect of bone marrow transplantation on the osteoblastic differentiation of human bone marrow stromal cells. J Clin Endocrinol Metab 87:329–335
Carlson K, Simonsson B, Ljunghall S (1994) Acute effects of high dose chemotherapy followed by bone marrow transplantation on serum markers of bone metabolism. Calcif Tissue Int 55:408–411
Tauchmanova L, Serio B, Del Puente A et al. (2002) Long-lasting bone damage detected by dual-energy X-ray absorptiometry, phalangeal osteosonogrammetry, and in vitro growth of marrow stromal cells after allogeneic stem cell transplantation. J Clin Endocrinol Metab 87:5058–5065
Liberman UA, Weiss SR, Broll J et al. (1995) Effect of oral alendronate on bone mineral density and the incidence of fractures in postmenopausal osteoporosis. The Alendronate Phase III Osteoporosis Treatment Study Group. N Engl J Med 333:1437–1443
Saag K, Emkey R, Schnitzer T et al. (1998) Alendronate for the prevention and treatment of glucocorticoid-induced osteoporosis. N Engl J Med 339:292–299
Sambrook P (1999) Alfacalcidol and calcitriol in the prevention of bone loss after organ transplantation. Calcif Tissue Int 65:341–343
Lemire JM (1992) Immunomodulatory role of 1,25 Dihydroxyvitamin D3. J Cell Biochem 49:26–31
Lemire JM, Archer DC, Reddy GS (1994) Dihydroxy-24-oxo-16-ene-vitamin D3, a renal metabolite of the vitamin D analog 1,25-dihydroxy-16ene-vitamin D3, exerts immunosuppressive activity equal to its parent without causing hypercalcemia in vivo. Endocrinology 135:2818–2821
Meys E, Terreaux-Duvert F, Beaume-Six T et al. (1993) Effects of calcium, calcidiol, and monofluorophosphate on lumbar bone mass and parathyroid function in patients after cardiac transplantation. Osteoporos Int 3:329–332
Garcia-Delgado I, Prieto S, Fragnas LG et al. (1997) Calcitonin, editronate and calcidiol treatment in bone loss after cardiac transplantation. Calcif Tissue Int 60:155–159
Sambrook P, Henderson NK, Keogh A et al. (2000) Effect of calcitriol on bone loss after cardiac or lung transplantation. J Bone Miner Res 15:1818–1824
Neuhaus R, Kubo A, Lohmann R et al. (1999) Calcitriol in prevention and therapy of osteoporosis after liver transplantation. Transplant Proc 31:472–473
Henderson K, Eisman J, Keogh A et al. (2001) Protective effect of short-tem calcitriol or cyclical etidronate on bone loss after cardiac or lung transplantation. J Bone Miner Res 16:565–571
Ugur A, Guvener N, Isiklar I et al. (2000) Efficiency of preventive treatment for osteoporosis after renal transplantation. Transplant Proc 32:556–557
Stempfle HU, Werner C, Siebert U et al. (2002) The role of tacrolimus (FK506)-based immunosuppression on bone mineral density and bone turnover after cardiac transplantation: a prospective, longitudinal, randomized, double-blind trial with calcitriol. Transplantation 73:547–552
Neuhaus R, Lohmann R, Platz KP et al. (1995) Treatment of osteoporosis after liver transplantation. Transplant Proc 27:1226–1227
Van Cleemput J, Daenen W, Geusens P et al. (1996) Prevention of bone loss in cardiac transplant recipients. A comparison of biphosphonates and vitamin D. Transplantation 61:1495–1499
Cueto-Manzano AM, Konel S, Freemont AJ et al. (2000) Effect of 1,25-dihydroxyvitamin D3 and calcium carbonate on bone loss associated with long-term renal transplantation. Am J Kidney Dis 35:227–236
Stempfle HU, Werner C, Echtler S et al. (1999) Prevention of osteoporosis after cardiac transplantation: a prospective, longitudinal, randomized, double-blind trial with calcitriol. Transplantation 68:523–530
Aris RM, Lester GE, Renner JB et al. (2000) Efficacy of pamidronate for osteoporosis in cystic fibrosis patients following lung transplantation. Am J Respir Crit Care Med 162:941
Bianda T, Linka A, Junga G et al. (2000) Prevention of osteoporosis in heart transplant recipients: a comparison of calcitriol with calcitonin and pamidronate. Calcif Tissue Int 67:116–121
Fan S, Almond MK, Ball E et al. (2000) Pamidronate therapy as prevention of bone loss following renal transplantation. Kidney Int 57:684–690
Kovac D, Lindic J, Kandus A et al. (2001) Prevention of bone loss in kidney graft recipients. Transplant Proc 33:1144–1145
Shane E, Rodino MA, McMahon DJ et al. (1998) Prevention of bone loss after heart transplantation with antiresorptive therapy: a pilot study. J Heart Lung Transplant 17:1089–1096
Hommann M, Abendroth K, Lehmann G et al. (2002) Effect of transplantation on bone: osteoporosis after liver and multivisceral transplantation. Transplant Proc 34:2296–2298
Arlen DJ, Lambert K, Ioannidis G et al. (2001) Treatment of established bone loss after renal transplantation with etidronate. Transplantation 71:669–673
Krieg M, Seydoux C, Sandini L et al. (2001) Intravenous pamidronate as a treatment for osteoporosis after heart transplantation: a prospective study. Osteoporos Int 12:112–116
Reeves H, Francis R, Manas D et al. (1998) Intravenous bisphosphonate prevents symptomatic osteoporotic vertebral collapse in patients after liver transplantation. Liver Transplant Surg 4:404–409
Riemens SC, Oostdijk A, Doormaal Jv et al. (1996) Bone loss after liver transplantation is not prevented by cyclical etidronate, calcium and alpha calcidiol. Osteoporos Int 6:213–218
Giannini S, Dangel A, Carraro G et al. (2001) Alendronate prevents further bone loss in renal transplant recipients. J Bone Miner Res 16:2111–2117
Sambrook PN, Birmingham J, Kelly P et al. (1993) Prevention of corticosteroid osteoporosis; a comparison of calcium, calcitriol and calcitonin. N Engl J Med 328:1747–1752
Mazzuoli G, Passeri M, Gennari C et al. (1986) Effects of salmon calcitonin in postmenopausal osteoporosis: a controlled double-blind clinical study. Calcif Tissue Int 38:3–8
Cremer J, Struber M, Wagenbreth I et al. (1999) Progression of steroid-associated osteoporosis after heart transplantation. Ann Thorac Surg 67:130–133
Hay JE, Malinchoc M, Dickson ER (2001) A controlled trial of calcitonin therapy for the prevention of post-liver transplantation atraumatic fractures in patients with primary biliary cirrhosis and primary sclerosing cholangitis. J Hepatol 34:292–298
Isoniemi H, Appelberg J, Nilsson CG et al. (2001) Transdermal oestrogen therapy protects postmenopausal liver transplant women from osteoporosis. A 2-year follow-up study. J Hepatol 34:299–305
Castelo-Branco C, Rovira M, Pons F et al. (1996) The effect of hormone replacement therapy on bone mass in patients with ovarian failure due to bone marrow transplantation. Maturitas 23:307–312
Rossouw JE, Anderson GL, Prentice RL et al. (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288:321–333
Fahrleitner A, Prenner G, Tscheliessnigg KH et al. (2002) Testosterone supplementation has additional benefits on bone metabolism in cardiac transplant recipients receiving intravenous bisphosphonate treatment: a prospective study. J Bone Miner Res 17:S388
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cohen, A., Shane, E. Osteoporosis after solid organ and bone marrow transplantation. Osteoporos Int 14, 617–630 (2003). https://doi.org/10.1007/s00198-003-1426-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-003-1426-z