Skip to main content
Log in

Vertebral fractures at hospitalization predict impaired respiratory function during follow-up of COVID-19 survivors

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

Abstract

Purpose

Morphometric vertebral fractures (VFs) have been recently reported as an important component of the endocrine phenotype of COVID-19 and emerging data show negative respiratory sequelae at long-term follow-up in COVID-19 survivors. The aim of this study was to evaluate the impact of VFs on respiratory function in COVID-19 survivors.

Methods

We included patients referred to our Hospital Emergency Department and re-evaluated during follow-up. VFs were detected on lateral chest X-rays on admission using a qualitative and semiquantitative assessment and pulmonary function tests were obtained by Jaeger-MasterScreen-Analyzer Unit 6 months after discharge.

Results

Fifty patients were included. Median age was 66 years and 66% were males. No respiratory function data were available at COVID-19 diagnosis. VFs were detected in 16 (32%) patients. No differences between fractured and non-fractured patients regarding age and sex were observed. Although no difference was observed between VF and non-VF patient groups in the severity of pneumonia as assessed by Radiological-Assessment-of-Lung-Edema score at admission, (5 vs. 6, p = 0.69), patients with VFs were characterized as compared to those without VFs by lower Forced Vital Capacity (FVC, 2.9 vs. 3.6 L, p = 0.006; 85% vs. 110% of predicted, respectively, p = 0.001), Forced Expiratory Volume 1st s (FEV1, 2.2 vs. 2.8 L, p = 0.005; 92% vs. 110% of predicted, respectively, p = 0.001) and Diffusing Capacity of the Lungs for Carbon Monoxide (DLCO 5.83 vs. 6.98 mmol/min/kPa, p = 0.036, 59% vs. 86.3% of predicted, respectively, p = 0.043) at 6-month follow up.

Conclusions

VFs, expression of the endocrine phenotype of the disease, appear to influence medium-term impaired respiratory function of COVID-19 survivors which may significantly influence their recovery. Therefore, our findings suggest that a VFs assessment at baseline may help in identifying patients needing a more intensive respiratory follow-up and patients showing persistent respiratory impairment without evidence of pulmonary disease may benefit from VFs assessment to preventing the vicious circle of further fractures and respiratory deterioration.

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

Similar content being viewed by others

Data availability

All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

References

  1. L. di Filippo, A.M. Formenti, M. Doga, E. Pedone, P. Rovere-Querini, A. Giustina, Radiological thoracic vertebral fractures are highly prevalent in COVID-19 and predict disease outcomes. J. Clin. Endocrinol. Metab. 106(2), e602–e614 (2021). https://doi.org/10.1210/clinem/dgaa738

    Article  PubMed  Google Scholar 

  2. M. Puig-Domingo, M. Marazuela, A. Giustina, COVID-19 and endocrine diseases. A statement from the European Society of Endocrinology. Endocrine 68(1), 2–5 (2020). https://doi.org/10.1007/s12020-020-02294-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. M. Marazuela, A. Giustina, M. Puig-Domingo, Endocrine and metabolic aspects of the COVID-19 pandemic [published correction appears in Rev Endocr Metab Disord. 2021 Mar;22(1):145]. Rev. Endocr. Metab. Disord. 21(4), 495–507 (2020). https://doi.org/10.1007/s11154-020-09569-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. A. Giustina, Hypovitaminosis D and the endocrine phenotype of COVID-19. Endocrine 72(1), 1–11 (2021). https://doi.org/10.1007/s12020-021-02671-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. A. Giustina, M. Marazuela, M. Reincke, B.O. Yildiz, M. Puig-Domingo, One year of the pandemic—how European endocrinologists responded to the crisis: a statement from the European Society of Endocrinology. Eur. J. Endocrinol. 185(2), C1–C7 (2021). https://doi.org/10.1530/EJE-21-0397

    Article  CAS  PubMed  Google Scholar 

  6. A. Giustina, J.P. Bilezikian, Revisiting the endocrine and metabolic manifestations of COVID-19 two years into the pandemic. Rev. Endocr. Metab. Disord. 23(2), 133–136 (2022). https://doi.org/10.1007/s11154-022-09716-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. C. Cooper, E.J. Atkinson, W.M. O’Fallon, L.J. Melton 3rd, Incidence of clinically diagnosed vertebral fractures: a population-based study in Rochester, Minnesota, 1985-1989. J. Bone Min. Res 7(2), 221–227 (1992). https://doi.org/10.1002/jbmr.5650070214

    Article  CAS  Google Scholar 

  8. T. Jalava, S. Sarna, L. Pylkkänen et al. Association between vertebral fracture and increased mortality in osteoporotic patients. J. Bone Min. Res. 18(7), 1254–1260 (2003). https://doi.org/10.1359/jbmr.2003.18.7.1254

    Article  Google Scholar 

  9. N. Napoli, A.L. Elderkin, D.P. Kiel, S. Khosla, Managing fragility fractures during the COVID-19 pandemic. Nat. Rev. Endocrinol. 16(9), 467–468 (2020). https://doi.org/10.1038/s41574-020-0379-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. G.R. Emkey, S. Epstein, Secondary osteoporosis: pathophysiology & diagnosis. Best. Pr. Res Clin. Endocrinol. Metab. 28(6), 911–935 (2014). https://doi.org/10.1016/j.beem.2014.07.002

    Article  Google Scholar 

  11. E. Canalis, G. Mazziotti, A. Giustina, J.P. Bilezikian, Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos. Int. 18(10), 1319–1328 (2007). https://doi.org/10.1007/s00198-007-0394-0

    Article  CAS  PubMed  Google Scholar 

  12. M. Janghorbani, R.M. Van Dam, W.C. Willett, F.B. Hu, Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am. J. Epidemiol. 166(5), 495–505 (2007). https://doi.org/10.1093/aje/kwm106

    Article  PubMed  Google Scholar 

  13. S. Yang, N.D. Nguyen, J.R. Center, J.A. Eisman, T.V. Nguyen, Association between hypertension and fragility fracture: a longitudinal study. Osteoporos. Int. 25(1), 97–103 (2014). https://doi.org/10.1007/s00198-013-2457-8

    Article  CAS  PubMed  Google Scholar 

  14. G. Mazziotti, M. Baracca, M. Doga, T. Porcelli, P.P. Vescovi, A. Giustina, Prevalence of thoracic vertebral fractures in hospitalized elderly patients with heart failure. Eur. J. Endocrinol. 167(6), 865–872 (2012). https://doi.org/10.1530/EJE-12-0566

    Article  CAS  PubMed  Google Scholar 

  15. S.W. Lai, K.F. Liao, H.C. Lai et al. Risk of major osteoporotic fracture after cardiovascular disease: a population-based cohort study in Taiwan. J. Epidemiol. 23(2), 109–114 (2013). https://doi.org/10.2188/jea.je20120071

    Article  PubMed  PubMed Central  Google Scholar 

  16. S. Boussaid, Y. Makhlouf, S. Jammali, H. Sahli, M. Elleuch, S. Rekik, Association of SARS-COV2 and Lumbar spine fractures: causal or coincidental? [published online ahead of print, 2021 Nov 26]. J. Clin. Densitom. (2021). https://doi.org/10.1016/j.jocd.2021.11.006

  17. S. Battisti, N. Napoli, C. Pedone et al. Vertebral fractures and mortality risk in hospitalised patients during the COVID-19 pandemic emergency. Endocrine 74(3), 461–469 (2021). https://doi.org/10.1007/s12020-021-02872-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. J. Kottlors, N. Große Hokamp, P. Fervers et al. Early extrapulmonary prognostic features in chest computed tomography in COVID-19 pneumonia: bone mineral density is a relevant predictor for the clinical outcome—a multicenter feasibility study. Bone 144, 115790 (2021). https://doi.org/10.1016/j.bone.2020.115790

    Article  CAS  PubMed  Google Scholar 

  19. M. Tahtabasi, N. Kilicaslan, Y. Akin et al. The prognostic value of vertebral bone density on chest CT in hospitalized COVID-19 patients. J. Clin. Densitom. 24(4), 506–515 (2021). https://doi.org/10.1016/j.jocd.2021.07.007

    Article  PubMed  PubMed Central  Google Scholar 

  20. L. Di Filippo, A.M. Formenti, P. Rovere-Querini et al. Hypocalcemia is highly prevalent and predicts hospitalization in patients with COVID-19. Endocrine 68(3), 475–478 (2020). https://doi.org/10.1007/s12020-020-02383-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. L. di Filippo, A.M. Formenti, M. Doga et al. Hypocalcemia is a distinctive biochemical feature of hospitalized COVID-19 patients. Endocrine 71(1), 9–13 (2021). https://doi.org/10.1007/s12020-020-02541-9

    Article  CAS  PubMed  Google Scholar 

  22. L. di Filippo, M. Doga, S. Frara, A. Giustina, Hypocalcemia in COVID-19: prevalence, clinical significance and therapeutic implications. Rev. Endocr. Metab. Disord. 1–10 (2021). https://doi.org/10.1007/s11154-021-09655-z

  23. L. di Filippo, A.M. Formenti, A. Giustina, Hypocalcemia: the quest for the cause of a major biochemical feature of COVID-19. Endocrine 70(3), 463–464 (2020). https://doi.org/10.1007/s12020-020-02525-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. L. di Filippo, A. Allora, M. Doga et al. Vitamin D levels are associated with blood glucose and BMI in COVID-19 patients, predicting disease severity. J. Clin. Endocrinol. Metab. 107(1), e348–e360 (2022). https://doi.org/10.1210/clinem/dgab599

    Article  PubMed  Google Scholar 

  25. L. di Filippo, A. Allora, M. Locatelli et al. Hypocalcemia in COVID-19 is associated with low vitamin D levels and impaired compensatory PTH response. Endocrine 74(2), 219–225 (2021). https://doi.org/10.1007/s12020-021-02882-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. L. di Filippo, S. Frara, A. Giustina, The emerging osteo-metabolic phenotype of COVID-19: clinical and pathophysiological aspects. Nat. Rev. Endocrinol. 17(8), 445–446 (2021). https://doi.org/10.1038/s41574-021-00516-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. M. Puig-Domingo, M. Marazuela, B.O. Yildiz, A. Giustina, COVID-19 and endocrine and metabolic diseases. An updated statement from the European Society of Endocrinology. Endocrine 72, 301–316 (2021). https://doi.org/10.1007/s12020-021-02734-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Y. Huang, C. Tan, J. Wu et al. Impact of coronavirus disease 2019 on pulmonary function in early convalescence phase. Respir. Res. 21(1), 163 (2020). https://doi.org/10.1186/s12931-020-01429-6. Published 2020 Jun 29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. X. Mo, W. Jian, Z. Su et al. Abnormal pulmonary function in COVID-19 patients at time of hospital discharge. Eur. Respir. J. 55(6), 2001217 (2020). https://doi.org/10.1183/13993003.01217-2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Y.M. Zhao, Y.M. Shang, W.B. Song et al. Follow-up study of the pulmonary function and related physiological characteristics of COVID-19 survivors three months after recovery. EClinicalMedicine 25, 100463 (2020). https://doi.org/10.1016/j.eclinm.2020.100463

    Article  PubMed  PubMed Central  Google Scholar 

  31. R. Méndez, A. Latorre, P. González-Jiménez et al. Reduced diffusion capacity in COVID-19 survivors. Ann. Am. Thorac. Soc. 18(7), 1253–1255 (2021). https://doi.org/10.1513/AnnalsATS.202011-1452RL

    Article  PubMed  PubMed Central  Google Scholar 

  32. N. Compagnone, D. Palumbo, G. Cremona et al. Residual lung damage following ARDS in COVID-19 ICU survivors. Acta. Anaesthesiol. Scand. (2021). https://doi.org/10.1111/aas.13996

  33. L.T. McDonald, Healing after COVID-19: are survivors at risk for pulmonary fibrosis? Am. J. Physiol. Lung Cell Mol. Physiol. 320(2), L257–L265 (2021). https://doi.org/10.1152/ajplung.00238.2020

    Article  CAS  PubMed  Google Scholar 

  34. M.J. Tobin, F. Laghi, A. Jubran, Caution about early intubation and mechanical ventilation in COVID-19. Ann. Intensive Care. 10(1), 78 (2020). https://doi.org/10.1186/s13613-020-00692-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. F. Wang, R.M. Kream, G.B. Stefano, Long-term respiratory and neurological sequelae of COVID-19. Med Sci. Monit. 26, e928996 (2020). https://doi.org/10.12659/MSM.928996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. A. Nalbandian, K. Sehgal, A. Gupta et al. Post-acute COVID-19 syndrome. Nat. Med 27(4), 601–615 (2021). https://doi.org/10.1038/s41591-021-01283-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. R. Watanabe, M. Shiraki, M. Saito, R. Okazaki, D. Inoue, Restrictive pulmonary dysfunction is associated with vertebral fractures and bone loss in elderly postmenopausal women. Osteoporos. Int. 29(3), 625–633 (2018). https://doi.org/10.1007/s00198-017-4337-0

    Article  CAS  PubMed  Google Scholar 

  38. J.H. Krege, D. Kendler, K. Krohn et al. Relationship between vertebral fracture burden, height loss, and pulmonary function in postmenopausal women with osteoporosis. J. Clin. Densitom. 18(4), 506–511 (2015). https://doi.org/10.1016/j.jocd.2015.02.004

    Article  PubMed  Google Scholar 

  39. B.A. Cotton, J.P. Pryor, I. Chinwalla, D.J. Wiebe, P.M. Reilly, C.W. Schwab, Respiratory complications and mortality risk associated with thoracic spine injury. J. Trauma 59(6), 1400–1409 (2005). https://doi.org/10.1097/01.ta.0000196005.49422.e6

    Article  PubMed  Google Scholar 

  40. B. Kim, J. Kim, Y.H. Jo et al. Risk of pneumonia after vertebral compression fracture in women with low bone density: a population-based study. Spine 43(14), E830–E835 (2018). https://doi.org/10.1097/BRS.0000000000002536

    Article  PubMed  Google Scholar 

  41. P. Rovere-Querini, C. Tresoldi, C. Conte et al. Biobanking for COVID-19 research. Panminerva. Med. (2020). https://doi.org/10.23736/S0031-0808.20.04168-3

  42. P. Rovere Querini, R. De Lorenzo, C. Conte et al. Post-COVID-19 follow-up clinic: depicting chronicity of a new disease. Acta Biomed. 91(9-S), 22–28 (2020). https://doi.org/10.23750/abm.v91i9-S.10146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. M.A. Warren, Z. Zhao, T. Koyama et al. Severity scoring of lung oedema on the chest radiograph is associated with clinical outcomes in ARDS. Thorax 73(9), 840–846 (2018). https://doi.org/10.1136/thoraxjnl-2017-211280

    Article  PubMed  Google Scholar 

  44. H.K. Genant, C.Y. Wu, C. van Kuijk, M.C. Nevitt, Vertebral fracture assessment using a semiquantitative technique. J. Bone Min. Res. 8(9), 1137–1148 (1993). https://doi.org/10.1002/jbmr.5650080915

    Article  CAS  Google Scholar 

  45. G.G. Crans, H.K. Genant, J.H. Krege, Prognostic utility of a semiquantitative spinal deformity index. Bone 37(2), 175–179 (2005). https://doi.org/10.1016/j.bone.2005.04.003

    Article  PubMed  Google Scholar 

  46. B.L. Graham, I. Steenbruggen, M.R. Miller et al. Standardization of Spirometry 2019 Update. An Official American Thoracic Society and European Respiratory Society Technical Statement. Am. J. Respir. Crit. Care Med. 200(8), e70–e88 (2019). https://doi.org/10.1164/rccm.201908-1590ST

    Article  PubMed  PubMed Central  Google Scholar 

  47. S. Stanojevic, B.L. Graham, B.G. Cooper et al. Official ERS technical standards: global lung function initiative reference values for the carbon monoxide transfer factor for Caucasians [published correction appears in Eur Respir J. 2020 Oct 15;56(4):]. Eur. Respir. J. 50(3), 1700010 (2017). https://doi.org/10.1183/13993003.00010-2017

    Article  PubMed  Google Scholar 

  48. C. Crimi, P. Impellizzeri, R. Campisi, S. Nolasco, A. Spanevello, N. Crimi, Practical considerations for spirometry during the COVID-19 outbreak: literature review and insights. Pulmonology 27(5), 438–447 (2021). https://doi.org/10.1016/j.pulmoe.2020.07.011

    Article  PubMed  Google Scholar 

  49. B. van den Borst, J.B. Peters, M. Brink et al. Comprehensive health assessment 3 months after recovery from acute Coronavirus Disease 2019 (COVID-19). Clin. Infect. Dis. 73(5), e1089–e1098 (2021). https://doi.org/10.1093/cid/ciaa1750

    Article  CAS  PubMed  Google Scholar 

  50. C.C. Kennedy, G. Ioannidis, K. Rockwood et al. A Frailty Index predicts 10-year fracture risk in adults age 25 years and older: results from the Canadian Multicentre Osteoporosis Study (CaMos). Osteoporos. Int. 25(12), 2825–2832 (2014). https://doi.org/10.1007/s00198-014-2828-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. H.J. Kim, S. Park, S.H. Park et al. Prevalence of frailty in patients with osteoporotic vertebral compression fracture and its association with numbers of fractures. Yonsei Med. J. 59(2), 317–324 (2018). https://doi.org/10.3349/ymj.2018.59.2.317

    Article  PubMed  Google Scholar 

  52. I. Lombardi Jr, L.M. Oliveira, A.F. Mayer, J.R. Jardim, J. Natour, Evaluation of pulmonary function and quality of life in women with osteoporosis. Osteoporos. Int. 16(10), 1247–1253 (2005). https://doi.org/10.1007/s00198-005-1834-3

    Article  PubMed  Google Scholar 

  53. J.A. Leech, C. Dulberg, S. Kellie, L. Pattee, J. Gay, Relationship of lung function to severity of osteoporosis in women. Am. Rev. Respir. Dis. 141(1), 68–71 (1990). https://doi.org/10.1164/ajrccm/141.1.68

    Article  CAS  PubMed  Google Scholar 

  54. R.A. Harrison, K. Siminoski, D. Vethanayagam, S.R. Majumdar, Osteoporosis-related kyphosis and impairments in pulmonary function: a systematic review. J. Bone Min. Res. 22(3), 447–457 (2007). https://doi.org/10.1359/jbmr.061202

    Article  Google Scholar 

  55. N. Tanigawa, S. Kariya, A. Komemushi, M. Nakatani, R. Yagi, S. Sawada, Added value of percutaneous vertebroplasty: effects on respiratory function. Am. J. Roentgenol. 198(1), W51–W54 (2012). https://doi.org/10.2214/AJR.11.6730

    Article  Google Scholar 

  56. J.S. Lee, K.W. Kim, K.Y. Ha, The effect of vertebroplasty on pulmonary function in patients with osteoporotic compression fractures of the thoracic spine. J. Spinal Disord. Tech. 24(2), E11–E15 (2011). https://doi.org/10.1097/BSD.0b013e3181dd812f

    Article  PubMed  Google Scholar 

  57. R. Dong, L. Chen, Y. Gu et al. Improvement in respiratory function after vertebroplasty and kyphoplasty. Int. Orthop. 33(6), 1689–1694 (2009). https://doi.org/10.1007/s00264-008-0680-2

    Article  PubMed  Google Scholar 

  58. D.J. Hole, G.C. Watt, G. Davey-Smith, C.L. Hart, C.R. Gillis, V.M. Hawthorne, Impaired lung function and mortality risk in men and women: findings from the Renfrew and Paisley prospective population study. BMJ 313(7059), 711–716 (1996). https://doi.org/10.1136/bmj.313.7059.711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. G.D. Friedman, A.L. Klatsky, A.B. Siegelaub, Lung function and risk of myocardial infarction and sudden cardiac death. N. Engl. J. Med. 294(20), 1071–1075 (1976). https://doi.org/10.1056/NEJM197605132942001

    Article  CAS  PubMed  Google Scholar 

  60. P. Lange, J. Nyboe, M. Appleyard, G. Jensen, P. Schnohr, Spirometric findings and mortality in never-smokers. J. Clin. Epidemiol. 43(9), 867–873 (1990). https://doi.org/10.1016/0895-4356(90)90070-6

    Article  CAS  PubMed  Google Scholar 

  61. H.J. Schünemann, J. Dorn, B.J. Grant, W. Winkelstein Jr, M. Trevisan, Pulmonary function is a long-term predictor of mortality in the general population: 29-year follow-up of the Buffalo Health Study. Chest 118(3), 656–664 (2000). https://doi.org/10.1378/chest.118.3.656

    Article  PubMed  Google Scholar 

  62. S. Guerra, A.E. Carsin, D. Keidel et al. Health-related quality of life and risk factors associated with spirometric restriction. Eur. Respir. J. 49(5), 1602096 (2017). https://doi.org/10.1183/13993003.02096-2016

    Article  PubMed  Google Scholar 

  63. A.J. Collaro, A.B. Chang, J.M. Marchant et al. Associations between lung function and future cardiovascular morbidity and overall mortality in a predominantly First Nations population: a cohort study. Lancet Reg. Health West Pac. 13, 100188 (2021). https://doi.org/10.1016/j.lanwpc.2021.100188

    Article  PubMed  PubMed Central  Google Scholar 

  64. D.D. Sin, L. Wu, S.F. Man, The relationship between reduced lung function and cardiovascular mortality: a population-based study and a systematic review of the literature. Chest 127(6), 1952–1959 (2005). https://doi.org/10.1378/chest.127.6.1952

    Article  PubMed  Google Scholar 

  65. M.J. Cuttica, L.A. Colangelo, M.T. Dransfield et al. Lung function in young adults and risk of cardiovascular events over 29 years: the CARDIA Study. J. Am. Heart Assoc. 7(24), e010672 (2018). https://doi.org/10.1161/JAHA.118.010672

    Article  PubMed  PubMed Central  Google Scholar 

  66. M. Duong, S. Islam, S. Rangarajan et al. Mortality and cardiovascular and respiratory morbidity in individuals with impaired FEV1 (PURE): an international, community-based cohort study. Lancet Glob. Health 7(5), e613–e623 (2019). https://doi.org/10.1016/S2214-109X(19)30070-1

    Article  PubMed  Google Scholar 

  67. M.M. Vasquez, M. Zhou, C. Hu, F.D. Martinez, S. Guerra, Low lung function in young adult life is associated with early mortality. Am. J. Respir. Crit. Care Med. 195(10), 1399–1401 (2017). https://doi.org/10.1164/rccm.201608-1561LE

    Article  PubMed  PubMed Central  Google Scholar 

  68. R.R. McLean, Proinflammatory cytokines and osteoporosis. Curr. Osteoporos. Rep. 7(4), 134–139 (2009). https://doi.org/10.1007/s11914-009-0023-2

    Article  PubMed  Google Scholar 

  69. B. Mi, Y. Xiong, C. Zhang et al. SARS-CoV-2-induced overexpression of miR-4485 suppresses osteogenic differentiation and impairs fracture healing. Int. J. Biol. Sci. 17(5), 1277–1288 (2021). https://doi.org/10.7150/ijbs.56657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. S. Frara, A. Allora, L. di Filippo et al. Osteopathy in mild adrenal Cushing’s syndrome and Cushing disease. Best. Pr. Res. Clin. Endocrinol. Metab. 35(2), 101515 (2021). https://doi.org/10.1016/j.beem.2021.101515

    Article  CAS  Google Scholar 

  71. E. Canalis, J.P. Bilezikian, A. Angeli, A. Giustina, Perspectives on glucocorticoid-induced osteoporosis. Bone 34(4), 593–598 (2004). https://doi.org/10.1016/j.bone.2003.11.026

    Article  CAS  PubMed  Google Scholar 

  72. K. Liu, W. Zhang, Y. Yang, J. Zhang, Y. Li, Y. Chen, Respiratory rehabilitation in elderly patients with COVID-19: a randomized controlled study. Complement Ther. Clin. Pr. 39, 101166 (2020). https://doi.org/10.1016/j.ctcp.2020.101166

    Article  Google Scholar 

  73. E. Canalis, A. Giustina, J.P. Bilezikian, Mechanisms of anabolic therapies for osteoporosis. N. Engl. J. Med. 357(9), 905–916 (2007). https://doi.org/10.1056/NEJMra067395

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed equally.

Corresponding author

Correspondence to Andrea Giustina.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

The study protocol complies with the Declaration of Helsinki, was approved by the Hospital Ethics Committee (protocol no. 34/int/2020) and was registered on ClinicalTrials.gov (NCT04318366).

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

di Filippo, L., Compagnone, N., Frara, S. et al. Vertebral fractures at hospitalization predict impaired respiratory function during follow-up of COVID-19 survivors. Endocrine 77, 392–400 (2022). https://doi.org/10.1007/s12020-022-03096-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-022-03096-7

Keywords

Navigation