Skip to main content

Advertisement

Log in

Denosumab for osteoporosis in patients with primary hyperparathyroidism and mild-to-moderate renal insufficiency

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

We aimed to assess the efficacy and safety of denosumab in postmenopausal women with primary hyperparathyroidism (PHPT)-related osteoporosis and chronic kidney disease (CKD).

Methods

Women over 50 years of age with PHPT or postmenopausal osteoporosis (PMO) were retrospectively recruited into this longitudinal study. These PHPT and PMO groups were further categorized into subgroups based on the presence of CKD (Glomerular filtration rate (GFR) < 60 mL/min/1.73 m2). All patients were given denosumab over 24 months due to verified osteoporosis. The primary outcomes were changes in bone mineral density (BMD) and serum calcium levels.

Results

145 postmenopausal women median age 69 [63;77] were recruited and assigned to one of the subgroups: PHPT patients with CKD (n = 22), PHPT patients without CKD (n = 38), PMO patients with CKD (n = 17) and PMO patients without CKD (n = 68). Denosumab treatment significantly increased BMD in patients with PHPT-related osteoporosis and CKD: median T-score L1–L4 from −2.0 to −1.35 (p < 0.001), femur neck from −2.4 to −2.1 (p = 0.012), radius 33% from −3.2 to −3 (p < 0.05)) at 24 months. Changes in BMD were similar in all four studied groups compared to baseline. A marked decline in calcium was noted in the primary study group of PHPT with CKD (median ΔCa = −0.24 mmol/L p < 0.001), compared to PHPT without CKD (median ΔCa = −0.08 mmol/L p < 0.001) and PMO with or without CKD. Denosumab treatment was well-tolerated with no serious adverse events.

Conclusion

Denosumab treatment was similarly effective at increasing BMD in patients with PHPT and PMO with and without renal insufficiency. The calcium lowering effects of denosumab were most significant in patients with PHPT and CKD. The safety of denosumab did not differ among participants with and without CKD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. J.P. Bilezikian, A.A. Khan, S.J. Silverberg, G.E.-H. Fuleihan, C. Marcocci, S. Minisola, N. Perrier, A. Sitges-Serra, R.V. Thakker, G. Guyatt, M. Mannstadt, J.T. Potts, B.L. Clarke, M.L. Brandi. On behalf of the International Workshop on Primary Hyperparathyroidism Evaluation and Management of Primary Hyperparathyroidism: Summary Statement and Guidelines from the Fifth International Workshop 2022. https://doi.org/10.1002/jbmr.4677

  2. J. Bollerslev, C. Schalin-Jäntti, L. Rejnmark, H. Siggelkow, H. Morreau, R. Thakker, A. Sitges-Serra, F. Cetani, C. Marcocci, Management of endocrine disease: Unmet therapeutic, educational and scientific needs in parathyroid disorders. Eur. J. Endocrinol. 181(3), P1–P19 (2019). https://doi.org/10.1530/EJE-19-0316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. S. Minisola, A. Arnold, Z. Belaya, M.L. Brandi, B.L. Clarke, F.M. Hannan, L.C. Hofbauer, K.L. Insogna, A. Lacroix, U. Liberman, A. Palermo, J. Pepe, R. Rizzoli, R. Wermers, R.V. Thakker, Epidemiology, pathophysiology, and genetics of primary hyperparathyroidism. J. Bone Min. Res. 2022 Aug. https://doi.org/10.1002/jbmr.4665

  4. L.J. Melton 3rd, Epidemiology of primary hyperparathyroidism. J. Bone Min. Res. 6(Suppl 2), S25–S30 (1991). https://doi.org/10.1002/jbmr.5650061409

    Article  Google Scholar 

  5. M.D. Walker, S.J. Silverberg, Primary hyperparathyroidism. Nat. Rev. Endocrinol. 14(2), 115–125 (2018). https://doi.org/10.1038/nrendo.2017.104

    Article  CAS  PubMed  Google Scholar 

  6. E. Mamedova, N. Mokrysheva, E. Vasilyev, V. Petrov, E. Pigarova, S. Kuznetsov, N. Kuznetsov, L. Rozhinskaya, G. Melnichenko, I. Dedov, A. Tiulpakov, Primary hyperparathyroidism in young patients in Russia: high frequency of hyperparathyroidism-jaw tumor syndrome. Endocr. Connect 6(Nov 8), 557–565 (2017). https://doi.org/10.1530/EC-17-0126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. A.E. Stephen, M. Mannstadt, R.A. Hodin, Indications for surgical management of hyperparathyroidism: a review. JAMA Surg. 152(9), 878–882 (2017). https://doi.org/10.1001/jamasurg.2017.1721

    Article  PubMed  Google Scholar 

  8. J. Bollerslev, L. Rejnmark, A. Zahn, A. Heck, N.M. Appelman-Dijkstra, L. Cardoso, F.M. Hannan, F. Cetani, T. Sikjær, A.M. Formenti, S. Björnsdottir, C. Schalin-Jantti, Z. Belaya, F.W. Gibb, B. Lapauw, K. Amrein, C. Wicke, C. Grasemann, M. Krebs, E.M. Ryhänen, O. Makay, S. Minisola, S. Gaujoux, J.P. Bertocchio, Z.K. Hassan-Smith, A. Linglart, E.M. Winter, M. Kollmann, H.G. Zmierczak, E. Tsourdi, S. Pilz, H. Siggelkow, N.J. Gittoes, C. Marcocci, P. Kamenicky, European Expert Consensus on Practical Management of Specific Aspects of Parathyroid Disorders in Adults and in Pregnancy: Recommendations of the ESE Educational Program of Parathyroid Disorders. Eur. J. Endocrinol. 2021 Dec:EJE-21-1044.R1. https://doi.org/10.1530/EJE-21-1044

  9. J.S. Leere, J. Karmisholt, M. Robaczyk, P. Vestergaard, Contemporary medical management of primary hyperparathyroidism: a systematic review. Front. Endocrinol. 8, (2017). https://doi.org/10.3389/fendo.2017.00079

  10. L. Wang, L. Quarles, R. Spurney, Unmasking the osteoinductive effects of a G-protein-coupled receptor (GPCR) kinase (GRK) inhibitor by treatment with PTH (1–34). J. Bone Min. Res. 19(10), 1661–1670 (2004). https://doi.org/10.1359/JBMR.040708

    Article  CAS  Google Scholar 

  11. Y. Ma, R. Cain, D. Halladay, X. Yang, Q. Zeng, R. Miles, S. Chandrasekhar, T. Martin, J. Onyia, Catabolic effects of continuous human PTH (1–38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and geneassociated bone formation. Endocrinology 142(9), 4047–4054 (2001). https://doi.org/10.1210/endo.142.9.8356

    Article  CAS  PubMed  Google Scholar 

  12. Y. Ueno, T. Shinki, Y. Nagai, H. Murayama, K. Fujii, T. Suda, In vivo administration of 1,25-dihydroxyvitamin D3 suppresses the expression of RANKL mRNA in bone of thyroparathyroidectomized rats constantly infused with PTH. J. Cell Biochem 90(Oct 2), 267–277 (2003). https://doi.org/10.1002/jcb.10623

    Article  CAS  PubMed  Google Scholar 

  13. A.D. Anastasilakis, D.G. Goulis, S.A. Polyzos, S. Gerou, V. Pavlidou, G. Koukoulis, A. Avramidis, Acute changes in serum osteoprotegerin and receptor activator for nuclear factor-kB ligand levels in women with established osteoporosis treated with teriparatide. Eur. J. Endocrinol. 158(3), 411–415 (2008). https://doi.org/10.1530/EJE-07-0528

    Article  CAS  PubMed  Google Scholar 

  14. L. Stilgren, E. Rettmer, E. Eriksen, L. Hegedus, H. Beck-Nielsen, B. Abrahamsen, Skeletal changes in osteoprotegerin and receptor activator of nuclear factor-kb ligand mRNA levels in primary hyperparathyroidism: effect of parathyroidectomy and association with. Bone Metab. Bone 35(Jul 1), 256–265 (2004). https://doi.org/10.1016/j.bone.2004.03.012

    Article  CAS  Google Scholar 

  15. S. Khosla, L.C. Hofbauer, Osteoporosis treatment: recent developments and ongoing challenges. Lancet Diabetes Endocrinol. 5(11), 898–907 (2017). https://doi.org/10.1016/S2213-8587(17)30188-2

    Article  PubMed  PubMed Central  Google Scholar 

  16. S.R. Cummings, J. San Martin, M.R. McClung, E.S. Siris, R. Eastell, I.R. Reid, P. Delmas, H.B. Zoog, M. Austin, A. Wang, S. Kutilek, S. Adami, J. Zanchetta, C. Libanati, S. Siddhanti, C. Christiansen, Freedom Trial. Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N. Engl. J. Med. 361(Aug 8), 756–765 (2009). https://doi.org/10.1056/NEJMoa0809493

    Article  CAS  PubMed  Google Scholar 

  17. S. Papapoulos, K. Lippuner, C. Roux, C.J. Lin, D.L. Kendler, E.M. Lewiecki, M.L. Brandi, E. Czerwiński, E. Franek, P. Lakatos, C. Mautalen, S. Minisola, J.Y. Reginster, S. Jensen, N.S. Daizadeh, A. Wang, M. Gavin, C. Libanati, R.B. Wagman, H.G. Bone, The effect of 8 or 5 years of denosumab treatment in postmenopausal women with osteoporosis: results from the FREEDOM Extension study. Osteoporos. Int. 26(12), 2773–2783 (2015). https://doi.org/10.1007/s00198-015-3234-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. I.R. Reid, P.D. Miller, J.P. Brown, D.L. Kendler, A. Fahrleitner-Pammer, I. Valter, K. Maasalu, M.A. Bolognese, G. Woodson, H. Bone, B. Ding, R.B. Wagman, J. San Martin, M.S. Ominsky, D.W. Dempster, Denosumab phase 3 bone Histology Study Group. Effects of denosumab on bone histomorphometry: the FREEDOM and STAND studies. J. Bone Min. Res. 25(10), 2256–2265 (2010). https://doi.org/10.1002/jbmr.149

    Article  CAS  Google Scholar 

  19. Z.E. Belaya, J.P. Bilezikian, O.B. Ershova, O.M. Lesnyak, L.A. Marchenkova, S.S. Rodionova, L.Y. Rozhinskaya, N.V. Toroptsova, S.V. Yureneva, Long-term treatment options for postmenopausal osteoporosis: results of recent clinical studies of Denosumab. Osteoporos. Bone Dis. 21(1), 17–22 (2018). https://doi.org/10.14341/osteo9760

    Article  Google Scholar 

  20. E. Tsourdi, M.C. Zillikens, C. Meier, J.J. Body, E. Gonzalez Rodriguez, A.D. Anastasilakis, B. Abrahamsen, E. McCloskey, L.C. Hofbauer, N. Guañabens, B. Obermayer-Pietsch, S.H. Ralston, R. Eastell, J. Pepe, A. Palermo, B. Langdahl, Fracture risk and management of discontinuation of denosumab therapy: a systematic review and position statement by ECTS. J. Clin. Endocrinol. Metab. 2020 Oct:dgaa756. https://doi.org/10.1210/clinem/dgaa756

  21. C. Beaudoin, S. Jean, L. Bessette, L.G. Ste-Marie, L. Moore, J.P. Brown, Denosumab compared to other treatments to prevent or treat osteoporosis in individuals at risk of fracture: a systematic review and meta-analysis. Osteoporos. Int. 2016 27(9), 2835–2844 (2016). https://doi.org/10.1007/s00198-016-3607-6

    Article  CAS  Google Scholar 

  22. E. Seeman, P.D. Delmas, D.A. Hanley, D. Sellmeyer, A.M. Cheung, E. Shane, A. Kearns, T. Thomas, S.K. Boyd, S. Boutroy, C. Bogado, S. Majumdar, M. Fan, C. Libanati, J. Zanchetta, Microarchitectural deterioration of cortical and trabecular bone: differing effects of denosumab and alendronate. J. Bone Min. Res. 25(8), 1886–1894 (2010). https://doi.org/10.1002/jbmr.81

    Article  Google Scholar 

  23. J.P. Brown, C. Roux, P.R. Ho, M.A. Bolognese, J. Hall, H.G. Bone, S. Bonnick, J.P. van den Bergh, I. Ferreira, P. Dakin, R.B. Wagman, C. Recknor, Denosumab significantly increases bone mineral density and reduces bone turnover compared with monthly oral ibandronate and risedronate in postmenopausal women who remained at higher risk for fracture despite previous suboptimal treatment with an oral bisphosphonate. Osteoporos. Int. 25(7), 1953–1961 (2014). https://doi.org/10.1007/s00198-014-2692-7

    Article  CAS  PubMed  Google Scholar 

  24. H. Lyu, B. Jundi, C. Xu, S.K. Tedeschi, K. Yoshida, S. Zhao, S.U. Nigwekar, B.Z. Leder, D.H. Solomon, Comparison of denosumab vs. bisphosphonates in osteoporosis patients: a meta-analysis of randomized controlled trials. J. Clin. Endocrinol. Metab. 104(5), 1753–1765 (2019). https://doi.org/10.1210/jc.2018-02236

    Article  PubMed  Google Scholar 

  25. J.S. Leere, J. Karmisholt, M. Robaczyk, S. Lykkeboe, A. Handberg, E. Steinkohl, J. Brøndum Frøkjær, P. Vestergaard, Denosumab and cinacalcet for primary hyperparathyroidism (DENOCINA): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Diabetes Endocrinol. 8(5), 407–417 (2020). https://doi.org/10.1016/S2213-8587(20)30063-2

    Article  CAS  PubMed  Google Scholar 

  26. H.G. Bone, R.B. Wagman, M.L. Brandi, J.P. Brown, R. Chapurlat, S.R. Cummings, E. Czerwiński, A. Fahrleitner-Pammer, D.L. Kendler, K. Lippuner, J.Y. Reginster, C. Roux, J. Malouf, M.N. Bradley, N.S. Daizadeh, A. Wang, P. Dakin, N. Pannacciulli, D.W. Dempster, S. Papapoulos, 10 years of denosumab treatment in postmenopausal women with osteoporosis: results from the 2017 phase 3 randomised FREEDOM trial and open-label extension. Lancet Diabetes Endocrinol. 5(7):513–523. https://doi.org/10.1016/S2213-8587(17)30138-9

  27. A. Broadwell, A. Chines, P.R. Ebeling, E. Franek, S. Huang, S. Smith, D. Kendler, O. Messina, P.D. Miller, Denosumab safety and efficacy among participants in the freedom extension study with mild to moderate chronic kidney disease. J. Clin. Endocrinol. Metab. 106(Jan 2), 397–409 (2021). https://doi.org/10.1210/clinem/dgaa851

    Article  PubMed  Google Scholar 

  28. ЕА Pigarova, L.Y. Rozhinskaya, Z.E. Belaya, L.K. Dzeranova, T.L. Karonova, A.V. Ilyin, G.A. Melnichenko, I.I. Dedov, Russian association of endocrinologists recommendations for diagnosis, treatment and prevention of vitamin D deficiency in adults. Probl. Endocrinol. 62(4), 60–84 (2016). https://doi.org/10.14341/probl201662460-84

    Article  Google Scholar 

  29. M. Ketteler, G.A. Block, P. Evenepoel, M. Fukagawa, C.A. Herzog, L. McCann, S.M. Moe, R. Shroff, M.A. Tonelli, N.D. Toussaint, M.G. Vervloet, M.B. Leonard, Executive summary of the 2017 KDIGO chronic kidney disease-mineral and bone disorder (CKD-MBD) guideline update: what’s changed and why it matters. Kidney Int. 92(Jul 1), 26–36 (2017). https://doi.org/10.1016/j.kint.2017.04.006

    Article  PubMed  Google Scholar 

  30. C. Chiang, The use of bone turnover markers in chronic kidney disease-mineral and bone disorders. Nephrol. (Carlton) 22(Mar Suppl 2), 11–13 (2017). https://doi.org/10.1111/nep.13014. PMID: 28429547

    Article  CAS  Google Scholar 

  31. S.A. Jamal, O. Ljunggren, C. Stehman-Breen, S.R. Cummings, M.R. McClung, S. Goemaere, P.R. Ebeling, E. Franek, Y.C. Yang, O.I. Egbuna, S. Boonen, P.D. Miller, Effects of denosumab on fracture and bone mineral density by level of kidney function. J. Bone Min. Res. 26(8), 1829–1835 (2011). https://doi.org/10.1002/jbmr.403

    Article  CAS  Google Scholar 

  32. C. Eller-Vainicher, S. Palmieri, E. Cairoli, G. Goggi, A. Scillitani, M. Arosio, A. Falchetti, I. Chiodini, Protective effect of denosumab on bone in older women with primary hyperparathyroidism. J. Am. Geriatr. Soc. 66(3), 518–524 (2018). https://doi.org/10.1111/jgs.15250

    Article  PubMed  Google Scholar 

  33. L.Y. Rozhinskaya, S.A. Gronskaya, E.O. Mamedova, Z.E. Belaya, G.A. Melnichenko, The comparative efficiency of denosumab treatment in patients with postmenopausal osteoporosis, primary hyperparathyroidism and glucocorticoid-induced osteoporosis in real clinical practice. Osteoporos. bone Dis. 23(1), 4–13 (2020). https://doi.org/10.14341/osteo12415

    Article  Google Scholar 

  34. J. Wu, Q. Zhang, G. Yan, X. Jin, Denosumab compared to bisphosphonates to treat postmenopausal osteoporosis: a meta-analysis. J. Orthop. Surg. Res. 13(Aug), 194 (2018). https://doi.org/10.1186/s13018-018-0865-3

    Article  PubMed  PubMed Central  Google Scholar 

  35. R.M. Zebaze, A. Ghasem-Zadeh, A. Bohte, S. Iuliano-Burns, M. Mirams, R.I. Price, E.J. Mackie, E. Seeman, Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet 375(May 9727), 1729–1736 (2010). https://doi.org/10.1016/S0140-6736(10)60320-0

    Article  PubMed  Google Scholar 

  36. H. Matsuno, Assessment of distal radius bone mineral density in osteoporosis patients receiving denosumab, including those with rheumatoid arthritis and those receiving oral glucocorticoids. Drugs R. D. 16(Dec), 347–353 (2016). https://doi.org/10.1007/s40268-016-0146-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. D. Segula, T. Nikolova, E. Marks, L. Ranganath, V. Mishra, Long term outcome of bisphosphonate therapy in patients with primary hyperparathyroidism. Int. J. Clin. Med. 5(5), 829–835 (2017). https://doi.org/10.4236/ijcm.2014.514111

    Article  CAS  Google Scholar 

  38. A. Eremkina, J. Krupinova, E. Dobreva, A. Gorbacheva, E. Bibik, M. Samsonova, A. Ajnetdinova, N. Mokrysheva, Denosumab for management of severe hypercalcemia in primary hyperparathyroidism. Endocr. Connect 9(10), 1019–1027 (2020). https://doi.org/10.1530/EC-20-0380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. E. Mamedova, A. Kolodkina, E.V. Vasilyev, V. Petrov, Z. Belaya, A. Tiulpakov, Successful use of denosumab for life-threatening hypercalcemia in a pediatric patient with primary hyperparathyroidism. Horm. Res Paediatr. 93(4), 272–278 (2020). https://doi.org/10.1159/000510625

    Article  CAS  PubMed  Google Scholar 

  40. M. Çalapkulu, O.O. Gul, S. Cander, C. Ersoy, E. Erturk, M.F. Sagiroglu, O. Saraydaroglu, Control of refractory hypercalcemia with denosumab in a case of metastatic parathyroid carcinoma. J. Coll. Physicians Surg. Pak. 30(7), 757–759 (2020). https://doi.org/10.29271/jcpsp.2020.07.757

    Article  PubMed  Google Scholar 

  41. O. Dahmani, C. Sophoclis, M. Kebir, D. Bouguern, A. Sakho, P. Demarchi, Denosumab for the treatment of bisphosphonate resistant hypercalcemia in a hemodialysis patient. Saudi J. Kidney Dis. Transpl. 28(1), 154–157 (2017). https://doi.org/10.4103/1319-2442.198239

    Article  PubMed  Google Scholar 

  42. Y. Li, C.Y. Fan, A. Manni, W.F. Simonds, Pitfalls of using denosumab preoperatively to treat refractory severe hypercalcaemia. BMJ Case Rep. 13(4), e233665 (2020). https://doi.org/10.1136/bcr-2019-233665

    Article  PubMed  PubMed Central  Google Scholar 

  43. D. Miyaoka, Y. Imanishi, E. Kato, N. Toi, Y. Nagata, M. Kurajoh, S. Yamada, M. Inaba, M. Emoto, Effects of denosumab as compared with parathyroidectomy regarding calcium, renal, and bone involvement in osteoporotic patients with primary hyperparathyroidism. Endocrine 69(3), 642–649 (2020). https://doi.org/10.1007/s12020-020-02401-6

    Article  CAS  PubMed  Google Scholar 

  44. K. Nitta, A. Yajima, K. Tsuchiya, Management of osteoporosis in chronic kidney disease. Intern Med. 56(24), 3271–3276 (2017). https://doi.org/10.2169/internalmedicine.8618-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. G.A. Block, H.G. Bone, L. Fang, E. Lee, D. Padhi, A single-dose study of denosumab in patients with various degrees of renal impairment. J. Bone Min. Res. 27(7), 1471–1479 (2012). https://doi.org/10.1002/jbmr.1613

    Article  CAS  Google Scholar 

  46. A.L.H. Huynh, S.T. Baker, A.J. Stewardson, D.F. Johnson, Denosumab-associated hypocalcaemia: incidence, severity and patient characteristics in a tertiary hospital setting. Pharmacoepidemiol Drug Saf. 25(11), 1274–1278 (2016). https://doi.org/10.1002/pds.4045

    Article  CAS  PubMed  Google Scholar 

  47. V. Dave, C.Y. Chiang, J. Booth, P.F. Mount, Hypocalcemia post denosumab in patients with chronic kidney disease stage 4-5. Am. J. Nephrol. 41(2), 129–137 (2015). https://doi.org/10.1159/000380960

    Article  CAS  PubMed  Google Scholar 

  48. R. Jalleh, G. Basu, R. Le Leu, S. Jesudason, Denosumab-induced severe hypocalcaemia in chronic kidney disease. Case Rep. Nephrol. 2018, 7384763 (2018). https://doi.org/10.1155/2018/7384763

    Article  PubMed  PubMed Central  Google Scholar 

  49. F. Festuccia, M.T. Jafari, A. Moioli, C. Fofi, S. Barberi, S. Amendola, S. Sciacchitano, G. Punzo, P. Menè, Safety and efficacy of denosumab in osteoporotic hemodialysed patients. J. Nephrol. 30(2), 271–279 (2017). https://doi.org/10.1007/s40620-016-0334-1

    Article  CAS  PubMed  Google Scholar 

  50. P. Anagnostis, S.A. Paschou, G. Mintziori, I. Ceausu, H. Depypere, I. Lambrinoudaki, A. Mueck, F.R. Pérez-López, M. Rees, L.M. Senturk, T. Simoncini, J.C. Stevenson, P. Stute, F.A. Trémollieres, D.G. Goulis, Drug holidays from bisphosphonates and denosumab in postmenopausal osteoporosis: EMAS position statement. Maturitas 101(Jul), 23–30 (2017). https://doi.org/10.1016/j.maturitas.2017.04.008

    Article  CAS  PubMed  Google Scholar 

  51. Z. ‘Belaya, L. Rozhinskaya, I. Dedov, O. Drapkina, V. Fadeev, O. Golounina, O. Lesnyak, E. Mamedova, G. Melnichenko, A. Petraikin, S. Rodionova, I. Skripnikova, O. Tkacheva, N. Toroptsova, S. Yureneva, J.A. Kanis, A summary of the Russian clinical guidelines on the diagnosis and treatment of osteoporosis. Osteoporos. Int 34(Mar 3), 429–447 (2023). https://doi.org/10.1007/s00198-022-06667-6

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Geoffrey Clayson for English editing work.

Funding

This research was supported by Ministry of Science and Higher Education of the Russian Federation (agreement no. 075-15-2020-899).

Author information

Authors and Affiliations

Authors

Contributions

S.G.—the design of the study, data collection, data analysis, draft writing, substantial contributions to conception and design; drafting the article; approval of the version to be published. Z.B.—the design of the study, conducting research, data analysis, article editing, substantial contributions to conception and design; drafting the article; approval of the version to be published. L.R.—the original concept of the study, conducting research, substantial contributions to conception and design; drafting the article; approval of the version to be published. E.M.—draft writing, conducting research, article editing, substantial contributions to conception and design; drafting the article; approval of the version to be published. M.V.—research design, article editing, substantial contributions to conception and design; drafting the article; approval of the version to be published. A.S.—data analysis, substantial contributions to conception and design; drafting the article; approval of the version to be published. O.G.—data collection, article editing, substantial contributions to conception and design; drafting the article; approval of the version to be published. G.M.—organization of the research, article editing, substantial contributions to conception and design; drafting the article; approval of the version to be published.

Corresponding author

Correspondence to Zhanna Belaya.

Ethics declarations

Conflict of interest

The authors S.G., Z.B., E.M., M.V., A.S., O.G. and G.M. declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The authors declare that they have no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gronskaya, S., Belaya, Z., Rozhinskaya, L. et al. Denosumab for osteoporosis in patients with primary hyperparathyroidism and mild-to-moderate renal insufficiency. Endocrine 81, 368–378 (2023). https://doi.org/10.1007/s12020-023-03381-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-023-03381-z

Keywords

Navigation