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Published in: BMC Endocrine Disorders 1/2020

01-12-2020 | Bisphosphonate | Research article

Endocrine disorders after heart transplantation: national cohort study

Authors: Matej Rakusa, Bojan Vrtovec, Gregor Poglajen, Andrej Janez, Mojca Jensterle

Published in: BMC Endocrine Disorders | Issue 1/2020

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Abstract

Background

Endocrine disorders in patients after heart transplantation (HT) remain understudied. We aimed to assess endocrine profiles and management of HT recipients in the early post- transplant period.

Methods

We conducted a retrospective cohort study on 123 consecutive HT recipients in the Advanced Heart Failure and Transplantation Programme between 2009 and 2018. All recipients had per-protocol endocrine follow-up within the first postoperative year. The median time to first post-transplant endocrine follow-up was 3 months (IQR 2–4). We assessed the incidence of vitamin D deficiency, bone mineral density, history of low energy fractures, hypogonadism in male recipients, posttransplant diabetes mellitus, and thyroid and parathyroid function.

Results

We enrolled 22 women and 101 men of median age 57 years (IQR 50–63). Post-transplant diabetes mellitus developed in 14 patients (11.4%). 18 of 25 patients (14.6%) with preexisting type 2 diabetes mellitus required intensification of antidiabetic therapy. 38 male patients (40.4%) had hypogonadism. 5 patients (4.6%) were hypothyroid and 10 (9.3%) latent hyperthyroid. Secondary hyperparathyroidism was present in 19 (17.3%), 25-hydroxyvitamin D deficiency in 64 (54.7%) of patients. Osteoporosis was present in 26 (21.1%), osteopenia in 59 (48.0%) patients. 47 vertebral fractures, 3 hip and 1 humerus fractures occurred in 21 patients. Most of the patients had coincidence of two or three disorders, while less than 5% did not have any endocrine irregularities. All patients received calcium and vitamin D supplements. Forty-six patients (37.4%) were treated with zoledronic acid, 12 (9.8%) with oral bisphosphonates. Two patients were treated with teriparatide.

Conclusions

The prevalence of multiple endocrine disorders early after heart transplantation is high. Assessment and management of increased fracture risk and all other potentially affected endocrine axes should be considered as a standard of care in this early period.
Literature
1.
go back to reference DePasquale EC, Schweiger M, Ross HJ. A contemporary review of adult heart transplantation: 2012 to 2013. J Heart Lung Transplant. 2014;33:775–84.PubMedCrossRef DePasquale EC, Schweiger M, Ross HJ. A contemporary review of adult heart transplantation: 2012 to 2013. J Heart Lung Transplant. 2014;33:775–84.PubMedCrossRef
2.
go back to reference Stein EM, Cohen A, Freeby M, Rogers H, Kokolus S, Scott V, et al. Severe vitamin D deficiency among heart and liver transplant recipients. Clin Transpl. 2009;23:861–5.CrossRef Stein EM, Cohen A, Freeby M, Rogers H, Kokolus S, Scott V, et al. Severe vitamin D deficiency among heart and liver transplant recipients. Clin Transpl. 2009;23:861–5.CrossRef
3.
go back to reference Fleischer J, McMahon DJ, Hembree W, Addesso V, Longcope C, Shane E. Serum testosterone levels after cardiac transplantation. Transplantation. 2008;85:834–9.PubMedPubMedCentralCrossRef Fleischer J, McMahon DJ, Hembree W, Addesso V, Longcope C, Shane E. Serum testosterone levels after cardiac transplantation. Transplantation. 2008;85:834–9.PubMedPubMedCentralCrossRef
4.
go back to reference Shane E, Rivas M, McMahon DJ, Staron RB, Silverberg SJ, Seibel MJ, et al. Bone loss and turnover after cardiac transplantation. J Clin Endocrinol Metab. 1997;82:1497–506.PubMed Shane E, Rivas M, McMahon DJ, Staron RB, Silverberg SJ, Seibel MJ, et al. Bone loss and turnover after cardiac transplantation. J Clin Endocrinol Metab. 1997;82:1497–506.PubMed
5.
go back to reference Ye X, Kuo H-T, Sampaio M, Jiang Y, Reddy P, Bunnapradist S. Risk factors for development of new-onset diabetes mellitus in adult heart transplant recipients. Transplantation. 2010;89:1526–32.PubMedCrossRef Ye X, Kuo H-T, Sampaio M, Jiang Y, Reddy P, Bunnapradist S. Risk factors for development of new-onset diabetes mellitus in adult heart transplant recipients. Transplantation. 2010;89:1526–32.PubMedCrossRef
6.
go back to reference Glendenning P, Kent GN, Adler BD, Matz L, Watson I, O'Drisoll GJ, et al. High prevalence of osteoporosis in cardiac transplant recipients and discordance between biochemical turnover markers and bone histomorphometry. Clin Endocrinol. 1999;50:347–55.CrossRef Glendenning P, Kent GN, Adler BD, Matz L, Watson I, O'Drisoll GJ, et al. High prevalence of osteoporosis in cardiac transplant recipients and discordance between biochemical turnover markers and bone histomorphometry. Clin Endocrinol. 1999;50:347–55.CrossRef
7.
go back to reference Dhesi JK, Bearne LM, Moniz C, Hurley MV, Jackon SH, Swift CG, et al. Neuromuscular and psychomotor function in elderly subjects who fall and the relationship with vitamin D status. J Bone Miner Res. 2002;17:891–7.PubMedCrossRef Dhesi JK, Bearne LM, Moniz C, Hurley MV, Jackon SH, Swift CG, et al. Neuromuscular and psychomotor function in elderly subjects who fall and the relationship with vitamin D status. J Bone Miner Res. 2002;17:891–7.PubMedCrossRef
8.
go back to reference Sambrook PN, Kelly PJ, Fontana D, Nguyen T, Keogh A, Macdonald P, et al. Mechanisms of rapid bone loss following cardiac transplantation. Osteoporos Int. 1994;4:273–6.PubMedCrossRef Sambrook PN, Kelly PJ, Fontana D, Nguyen T, Keogh A, Macdonald P, et al. Mechanisms of rapid bone loss following cardiac transplantation. Osteoporos Int. 1994;4:273–6.PubMedCrossRef
9.
go back to reference Marelli D, Laks H, Patel B, Kermani R, Marmureanu A, Patel J, et al. Heart transplantation in patients with diabetes mellitus in the current era. J Heart Lung Transplant. 2003;22:1091–7.PubMedCrossRef Marelli D, Laks H, Patel B, Kermani R, Marmureanu A, Patel J, et al. Heart transplantation in patients with diabetes mellitus in the current era. J Heart Lung Transplant. 2003;22:1091–7.PubMedCrossRef
10.
go back to reference Whittier X, Saag KG. Glucocorticoid-induced osteoporosis. Rheum Dis Clin N Am. 2016;42:177–89.CrossRef Whittier X, Saag KG. Glucocorticoid-induced osteoporosis. Rheum Dis Clin N Am. 2016;42:177–89.CrossRef
11.
go back to reference Movsowitz C, Epstein S, Fallon M, Ismail F, Thomas S. Cyclosporin-a in vivo produces severe osteopenia in the rat: effect of dose and duration of administration. Endocrinology. 1988;123:2571–7.PubMedCrossRef Movsowitz C, Epstein S, Fallon M, Ismail F, Thomas S. Cyclosporin-a in vivo produces severe osteopenia in the rat: effect of dose and duration of administration. Endocrinology. 1988;123:2571–7.PubMedCrossRef
12.
go back to reference Bone histology in renal transplant patients receiving cyclosporin. Lancet. 1988;1:1048–9. Bone histology in renal transplant patients receiving cyclosporin. Lancet. 1988;1:1048–9.
13.
go back to reference Montero N, Pascual J. Immunosuppression and post-transplant hyperglycemia. Curr Diabetes Rev. 2015;11:144–54.PubMedCrossRef Montero N, Pascual J. Immunosuppression and post-transplant hyperglycemia. Curr Diabetes Rev. 2015;11:144–54.PubMedCrossRef
14.
go back to reference Reichrath J. Dermatologic management, sun avoidance and vitamin D status in organ transplant recipients (OTR). J Photochem Photobiol B. 2010;101:150–9.PubMedCrossRef Reichrath J. Dermatologic management, sun avoidance and vitamin D status in organ transplant recipients (OTR). J Photochem Photobiol B. 2010;101:150–9.PubMedCrossRef
16.
go back to reference Guo C-Y, Johnson A, Locke TJ, Eastell R. Mechanisms of bone loss after cardiac transplantation. Bone. 1998;22:267–71.PubMedCrossRef Guo C-Y, Johnson A, Locke TJ, Eastell R. Mechanisms of bone loss after cardiac transplantation. Bone. 1998;22:267–71.PubMedCrossRef
17.
go back to reference Dopff C, de Talancé N, Hottier E, Mattei MF, Carteaux JP, Burlet C, et al. Consequences of heart transplantation on calcium metabolism. Transplant Proc. 1998;30:2833–4.PubMedCrossRef Dopff C, de Talancé N, Hottier E, Mattei MF, Carteaux JP, Burlet C, et al. Consequences of heart transplantation on calcium metabolism. Transplant Proc. 1998;30:2833–4.PubMedCrossRef
18.
go back to reference Cohen A, Addonizio LJ, Lamour JM, Addesso V, Staron RB, Gao P, et al. Osteoporosis in adult survivors of adolescent cardiac transplantation may be related to hyperparathyroidism, mild renal insufficiency, and increased bone turnover. J Heart Lung Transplant. 2005;24:696–702.PubMedCrossRef Cohen A, Addonizio LJ, Lamour JM, Addesso V, Staron RB, Gao P, et al. Osteoporosis in adult survivors of adolescent cardiac transplantation may be related to hyperparathyroidism, mild renal insufficiency, and increased bone turnover. J Heart Lung Transplant. 2005;24:696–702.PubMedCrossRef
19.
go back to reference Wozniak-Grygiel E, Zeglen S, Stanjek-Cichoracka A, Zakliczyński M, Kucewicz Czech E, et al. Urinary iodine concentrations should be monitored to diagnose some thyroid gland diseases in heart transplant recipients. Transplant Proc. 2009;41:3232–4.PubMedCrossRef Wozniak-Grygiel E, Zeglen S, Stanjek-Cichoracka A, Zakliczyński M, Kucewicz Czech E, et al. Urinary iodine concentrations should be monitored to diagnose some thyroid gland diseases in heart transplant recipients. Transplant Proc. 2009;41:3232–4.PubMedCrossRef
20.
go back to reference Kowalczuk-Wieteska AM, Barańska-Kosakowska A, Zakliczyński M, Lindon S, Zembala M. Do thyroid disorders affect the postoperative course of patients in the early post-heart transplant period? Ann Transplant. 2011;16:77–81.PubMedCrossRef Kowalczuk-Wieteska AM, Barańska-Kosakowska A, Zakliczyński M, Lindon S, Zembala M. Do thyroid disorders affect the postoperative course of patients in the early post-heart transplant period? Ann Transplant. 2011;16:77–81.PubMedCrossRef
21.
go back to reference Siccama R, Balk AH, de Herder WW, van Domburg R, Vantrimpont P, van Gelder T. Amiodarone therapy before heart transplantation as a predictor of thyroid dysfunction after transplantation. J Heart Lung Transplant. 2003;22:857–61.PubMedCrossRef Siccama R, Balk AH, de Herder WW, van Domburg R, Vantrimpont P, van Gelder T. Amiodarone therapy before heart transplantation as a predictor of thyroid dysfunction after transplantation. J Heart Lung Transplant. 2003;22:857–61.PubMedCrossRef
22.
go back to reference Levey AS, Coresh J, Greene T, Marsh J, Stevens LA, Kusek JW, et al. Expressing the modification of diet in renal disease study equation for estimating glomerular filtration rate with standardized serum Creatinine values. Clin Chem. 2007;53:766–72.PubMedCrossRef Levey AS, Coresh J, Greene T, Marsh J, Stevens LA, Kusek JW, et al. Expressing the modification of diet in renal disease study equation for estimating glomerular filtration rate with standardized serum Creatinine values. Clin Chem. 2007;53:766–72.PubMedCrossRef
23.
go back to reference Willis K, Cheung M, Slifer S. KDIGO 2012 clinical practice guideline for Evaluation & Management of CKD. Kidney Int Suppl. 2013;3:5–14.CrossRef Willis K, Cheung M, Slifer S. KDIGO 2012 clinical practice guideline for Evaluation & Management of CKD. Kidney Int Suppl. 2013;3:5–14.CrossRef
24.
go back to reference Bilezikian JP, Brandi ML, Eastell R, Silverberg SJ, Udelsman R, Marcocci C, et al. Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the fourth international workshop. Clin Endocrinol Metab. 2014;99:3561–9.CrossRef Bilezikian JP, Brandi ML, Eastell R, Silverberg SJ, Udelsman R, Marcocci C, et al. Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the fourth international workshop. Clin Endocrinol Metab. 2014;99:3561–9.CrossRef
25.
go back to reference Kanis JA, Cooper C, Rizzoli R, Reginster J. 2019 European Guideline. Osteoporos Int. 2019;30:3–44.PubMedCrossRef Kanis JA, Cooper C, Rizzoli R, Reginster J. 2019 European Guideline. Osteoporos Int. 2019;30:3–44.PubMedCrossRef
26.
go back to reference Bhasin S, Brito JP, Cunningham GR, Hayes FJ, Hodis HN, Matsumoto AM, et al. Testosterone therapy in men with Hypogonadism: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2018;103:1715–44.PubMedCrossRef Bhasin S, Brito JP, Cunningham GR, Hayes FJ, Hodis HN, Matsumoto AM, et al. Testosterone therapy in men with Hypogonadism: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2018;103:1715–44.PubMedCrossRef
27.
go back to reference Jonklaas J, Bianco AC, Bauer AJ, Burman KD, Cappola AR, Celi FS, et al. Guidelines for the treatment of hypothyroidism: prepared by the American Thyroid Association task force on thyroid hormone replacement. Thyroid. 2014;24:1670–751.PubMedPubMedCentralCrossRef Jonklaas J, Bianco AC, Bauer AJ, Burman KD, Cappola AR, Celi FS, et al. Guidelines for the treatment of hypothyroidism: prepared by the American Thyroid Association task force on thyroid hormone replacement. Thyroid. 2014;24:1670–751.PubMedPubMedCentralCrossRef
28.
go back to reference Ross DS, Burch HB, Cooper DS, Greenlee MC, Laurberg P, Maia AL, et al. 2016 American Thyroid Association guidelines for diagnosis and Management of Hyperthyroidism and Other Causes of thyrotoxicosis. Thyroid. 2016;26:1343–421.PubMedCrossRef Ross DS, Burch HB, Cooper DS, Greenlee MC, Laurberg P, Maia AL, et al. 2016 American Thyroid Association guidelines for diagnosis and Management of Hyperthyroidism and Other Causes of thyrotoxicosis. Thyroid. 2016;26:1343–421.PubMedCrossRef
29.
go back to reference Sharif A, Hecking M, de Vries AP, Porrini E, Hornum M, Rasoul-Rockenschaub S, et al. Proceedings from an international consensus meeting on posttransplantation diabetes mellitus: recommendations and future directions. Am J Transplant. 2014;14:1992–2000.PubMedPubMedCentralCrossRef Sharif A, Hecking M, de Vries AP, Porrini E, Hornum M, Rasoul-Rockenschaub S, et al. Proceedings from an international consensus meeting on posttransplantation diabetes mellitus: recommendations and future directions. Am J Transplant. 2014;14:1992–2000.PubMedPubMedCentralCrossRef
30.
go back to reference Jenssen T, Hartmann A. Post-transplant diabetes mellitus in patients with solid organ transplants. Nat Rev Endocrinol. 2019;15:172–88.PubMedCrossRef Jenssen T, Hartmann A. Post-transplant diabetes mellitus in patients with solid organ transplants. Nat Rev Endocrinol. 2019;15:172–88.PubMedCrossRef
31.
go back to reference Przybyłowski P, Wasilewski G, Koc-Żórawska E, Małyszko J. Vitamin D concentration in patients after heart and kidney transplantation. Transplant Proc. 2018;50:2100–4.PubMedCrossRef Przybyłowski P, Wasilewski G, Koc-Żórawska E, Małyszko J. Vitamin D concentration in patients after heart and kidney transplantation. Transplant Proc. 2018;50:2100–4.PubMedCrossRef
32.
go back to reference Briffa NK, Keogh AM, Sambrook PN, Eisman JA. Reduction of immunosuppressant therapy requirement in heart transplantation by calcitriol. Transplantation. 2003;75:2133–4.PubMedCrossRef Briffa NK, Keogh AM, Sambrook PN, Eisman JA. Reduction of immunosuppressant therapy requirement in heart transplantation by calcitriol. Transplantation. 2003;75:2133–4.PubMedCrossRef
33.
go back to reference Serra E, Porcu M, Minerba L, Serra S, Oppo A, Orrù P, et al. High prevalence of male hypogonadism and sexual dysfunction in long-term clinically stable heart transplantation recipients. Int J Cardiol. 2012;155:476–7.PubMedCrossRef Serra E, Porcu M, Minerba L, Serra S, Oppo A, Orrù P, et al. High prevalence of male hypogonadism and sexual dysfunction in long-term clinically stable heart transplantation recipients. Int J Cardiol. 2012;155:476–7.PubMedCrossRef
34.
go back to reference Kamischke A, Kemper DE, Castel MA, Lüthke M, Rolf C, Behre HM, et al. Testosterone levels in men with chronic obstructive pulmonary disease with or without glucocorticoid therapy. Eur Respir J. 1998;11:41–5.PubMedCrossRef Kamischke A, Kemper DE, Castel MA, Lüthke M, Rolf C, Behre HM, et al. Testosterone levels in men with chronic obstructive pulmonary disease with or without glucocorticoid therapy. Eur Respir J. 1998;11:41–5.PubMedCrossRef
35.
go back to reference Woolf PD, Hamill RW, McDonald JV, Lee LA, Kelly M. Transient hypogonadotropic hypogonadism caused by critical illness. J Clin Endocrinol Metab. 1985;60:444–50.PubMedCrossRef Woolf PD, Hamill RW, McDonald JV, Lee LA, Kelly M. Transient hypogonadotropic hypogonadism caused by critical illness. J Clin Endocrinol Metab. 1985;60:444–50.PubMedCrossRef
36.
go back to reference Sikka SC, Bhasin S, Coy DC, Koyle MA, Swerdloff RS, Rajfer J. Effects of cyclosporine on the hypothalamic-pituitary-gonadal axis in the male rat: mechanism of action. Endocrinology. 1988;123:1069–74.PubMedCrossRef Sikka SC, Bhasin S, Coy DC, Koyle MA, Swerdloff RS, Rajfer J. Effects of cyclosporine on the hypothalamic-pituitary-gonadal axis in the male rat: mechanism of action. Endocrinology. 1988;123:1069–74.PubMedCrossRef
37.
go back to reference Seethalakshmi L, Flores C, Carboni AA, Bala R, Diamond DA, Menon M. Cyclosporine: its effects on testicular function and fertility in the prepubertal rat. J Andrology. 1990;11:17–24. Seethalakshmi L, Flores C, Carboni AA, Bala R, Diamond DA, Menon M. Cyclosporine: its effects on testicular function and fertility in the prepubertal rat. J Andrology. 1990;11:17–24.
38.
go back to reference Poglajen G, Jensterle M, Kravos N, Janež A, Vrtovec B. Low serum testosterone is associated with impaired graft function early after heart transplantation. Clin Transpl. 2017;31:e12970.CrossRef Poglajen G, Jensterle M, Kravos N, Janež A, Vrtovec B. Low serum testosterone is associated with impaired graft function early after heart transplantation. Clin Transpl. 2017;31:e12970.CrossRef
39.
go back to reference Cohen A, Sambrook P, Shane E. Management of bone loss after organ transplantation. J Bone Miner Res. 2004;19:1919–32.PubMedCrossRef Cohen A, Sambrook P, Shane E. Management of bone loss after organ transplantation. J Bone Miner Res. 2004;19:1919–32.PubMedCrossRef
40.
go back to reference Dalle Carbonare L, Zanatta M, Braga V, Sella S, Vilei MT, Feltrin G, et al. Densitometric threshold and vertebral fractures in heart transplant patients. Transplantation. 2011;92:106–11.PubMedCrossRef Dalle Carbonare L, Zanatta M, Braga V, Sella S, Vilei MT, Feltrin G, et al. Densitometric threshold and vertebral fractures in heart transplant patients. Transplantation. 2011;92:106–11.PubMedCrossRef
41.
go back to reference Leidig-Bruckner G, Hosch S, Dodidou P, Ritschel D, Conradt C, Klose C, et al. Frequency and predictors of osteoporotic fractures after cardiac or liver transplantation: a follow-up study. Lancet. 2001;357:342–7.PubMedCrossRef Leidig-Bruckner G, Hosch S, Dodidou P, Ritschel D, Conradt C, Klose C, et al. Frequency and predictors of osteoporotic fractures after cardiac or liver transplantation: a follow-up study. Lancet. 2001;357:342–7.PubMedCrossRef
42.
go back to reference Höfle G, Saely CH, Tautermann G, Aczél S, Holzmüller H, Drexel H. Relationship between various measures of bone mineral density and the prevalence of vertebral fractures in cardiac transplant recipients. Swiss Med Wkly. 2004;134:215–20.PubMed Höfle G, Saely CH, Tautermann G, Aczél S, Holzmüller H, Drexel H. Relationship between various measures of bone mineral density and the prevalence of vertebral fractures in cardiac transplant recipients. Swiss Med Wkly. 2004;134:215–20.PubMed
43.
go back to reference Kerschan-Schindl K, Ruzicka M, Mahr S, Paireder M, Krestan C, Gleiss A, et al. Unexpected low incidence of vertebral fractures in heart transplant recipients: analysis of bone turnover. Transpl Int. 2008;21:255–62.PubMedCrossRef Kerschan-Schindl K, Ruzicka M, Mahr S, Paireder M, Krestan C, Gleiss A, et al. Unexpected low incidence of vertebral fractures in heart transplant recipients: analysis of bone turnover. Transpl Int. 2008;21:255–62.PubMedCrossRef
44.
go back to reference Löfdahl E, Söderlund C, Rådegran G. Bone mineral density and osteoporosis in heart transplanted patients: A single-center retrospective study at Skåne University Hospital in Lund 1988–2016. Clin Transplant. 2019;33:e13477.PubMedCrossRef Löfdahl E, Söderlund C, Rådegran G. Bone mineral density and osteoporosis in heart transplanted patients: A single-center retrospective study at Skåne University Hospital in Lund 1988–2016. Clin Transplant. 2019;33:e13477.PubMedCrossRef
45.
go back to reference Shane E, Cohen A, Stein EM, McMahon DJ, Zhang C, Young P, et al. Zoledronic acid versus alendronate for the prevention of bone loss after heart or liver transplantation. J Clin Endocrinol Metab. 2012;97:4481–90.PubMedPubMedCentralCrossRef Shane E, Cohen A, Stein EM, McMahon DJ, Zhang C, Young P, et al. Zoledronic acid versus alendronate for the prevention of bone loss after heart or liver transplantation. J Clin Endocrinol Metab. 2012;97:4481–90.PubMedPubMedCentralCrossRef
46.
go back to reference Hariman A, Alex C, Heroux A, Camacho P. Incidence of fractures after cardiac and lung transplantation: a single center experience. J Osteoporos. 2014;2014:573041.PubMedPubMedCentralCrossRef Hariman A, Alex C, Heroux A, Camacho P. Incidence of fractures after cardiac and lung transplantation: a single center experience. J Osteoporos. 2014;2014:573041.PubMedPubMedCentralCrossRef
47.
go back to reference Costanzo MR, Dipchand A, Starling R, Anderson A, Chan M, Desai S, et al. The International Society of Heart and Lung Transplantation Guidelines for the care of heart transplant recipients. J Heart Lung Transplant. 2010;29:914–56.PubMedCrossRef Costanzo MR, Dipchand A, Starling R, Anderson A, Chan M, Desai S, et al. The International Society of Heart and Lung Transplantation Guidelines for the care of heart transplant recipients. J Heart Lung Transplant. 2010;29:914–56.PubMedCrossRef
48.
go back to reference Cauley JA, Thompson DE, Ensrud KC, Scott JC, Black D. Risk of mortality following clinical fractures. Osteoporos Int. 2000;11:556–61.PubMedCrossRef Cauley JA, Thompson DE, Ensrud KC, Scott JC, Black D. Risk of mortality following clinical fractures. Osteoporos Int. 2000;11:556–61.PubMedCrossRef
49.
go back to reference Melton LJ 3rd, Achenbach SJ, Atkinson EJ, Therneau TM, Amin S. Long-term mortality following fractures at different skeletal sites: a population-based cohort study. Osteoporos Int. 2013;24:1689–96.PubMedCrossRef Melton LJ 3rd, Achenbach SJ, Atkinson EJ, Therneau TM, Amin S. Long-term mortality following fractures at different skeletal sites: a population-based cohort study. Osteoporos Int. 2013;24:1689–96.PubMedCrossRef
Metadata
Title
Endocrine disorders after heart transplantation: national cohort study
Authors
Matej Rakusa
Bojan Vrtovec
Gregor Poglajen
Andrej Janez
Mojca Jensterle
Publication date
01-12-2020

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