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Bone microarchitecture and metabolism in elderly male patients with signs of intravertebral cleft on MRI

  • Musculoskeletal
  • Published:
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Abstract

Objectives

Intravertebral cleft (IVC) is a common but not unique imaging manifestation in Kümmell’s disease. To date, great controversy exists regarding the specific mechanisms of IVC. In this study, we aimed to investigate the characteristics of microarchitecture and metabolism in patients with IVC and to analyse the correlations between degree of vertebral collapse and risk factors.

Methods

A total of 79 elderly men were included in this study. We divided all patients into two groups: the IVC group (30 patients) and the non-IVC group (49 patients). We compared the differences in microarchitecture and bone turnover marker (BTM) serum concentrations between the groups and analysed risk factors affecting vertebral collapse by using the Mann–Whitney U test and Spearman’s correlation test.

Results

Quantitative analysis of the microarchitecture showed higher content of necrotic bone (p < 0.001) and lower content of lamellar bone (p < 0.001) in the IVC group. Analysis of BTMs identified lower concentration of N-terminal propeptide of type I collagen (PINP, p = 0.002) and higher concentration of β-isomerized C-terminal telopeptide (β-CTX, p < 0.001) in the IVC group. The correlation analysis showed that lamellar bone content (p < 0.001) and spine T-score (p = 0.011) were significantly correlated with the degree of vertebral collapse.

Conclusions

IVC is a radiological feature of excessive bone resorption by higher activities of osteoclasts and decreased bone remodelling ability by lower activities of osteoblasts. Histomorphological feature in patients with IVC is delayed callus mineralisation, which may increase the risk of vertebral collapse.

Key Points

• A key histomorphological feature in patients with IVC is delayed callus mineralisation, which may aggravate the degree of vertebral collapse.

• We investigated bone metabolism in patients with IVC to evaluate the activities of osteoclasts and osteoblasts directly.

• We propose a novel hypothesis for the pathogenesis of IVC: bone resorption by higher activity of osteoclasts and decreased callus mineralisation ability by lower activity of osteoblasts are the main mechanisms leading to IVC.

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Abbreviations

ALP:

Alkaline phosphatase

BTMs:

Bone turnover markers

BV/TV:

Cancellous bone volume/tissue volume

EBV/TV:

Endochondral bone volume/tissue volume

FV/TV:

Fibrous tissue volume/tissue volume

IVC:

Intravertebral cleft

LBV/TV:

Lamellar bone volume/tissue volume

NBV/TV:

Necrotic bone volume/tissue volume

OST:

Osteocalcin

PINP:

N-terminal propeptide of type I collagen

PKP:

Percutaneous kyphoplasty

PMHC:

Percentage of middle height compression

WBV/TV:

Woven bone volume/tissue volume

β-CTX:

β-Isomerized C-terminal telopeptide

References

  1. Kümmell H (1895) Ueber die traumatischen Erkrankungen der Wirbelsäule1). Dtsch Med Wochenschr 21:180–181

    Article  Google Scholar 

  2. Matzaroglou C, Georgiou CS, Panagopoulos A et al (2014) Kümmell’s disease: clarifying the mechanisms and patients’ inclusion criteria. Open Orthop J 8:288–297

    Article  PubMed  PubMed Central  Google Scholar 

  3. Young WF, Brown D, Kendler A, Clements D (2002) Delayed post-traumatic osteonecrosis of a vertebral body (Kummell’s disease). Acta Orthop Belg 68:13

    CAS  PubMed  Google Scholar 

  4. Stell HH (1951) Kümmell’s disease. Am J Surg 81:161–7

    Article  Google Scholar 

  5. Malghem J, Maldague B, Labaisse MA et al (1993) Intravertebral vacuum cleft: changes in content after supine positioning. Radiology 187:483–487

    Article  CAS  PubMed  Google Scholar 

  6. Sarli M, Pérez Manghi FC, Gallo R, Zanchetta JR (2005) The vacuum cleft sign: an uncommon radiological sign. Osteoporos Int 16:1210–1214

    Article  CAS  PubMed  Google Scholar 

  7. Kumpan W, Salomonowitz E, Seidl G, Wittich GR (1986) The intravertebral vacuum phenomenon. Skeletal Radiol 15:444–447

    Article  CAS  PubMed  Google Scholar 

  8. Mirovsky Y, Anekstein Y, Shalmon E, Peer A (2005) Vacuum clefts of the vertebral bodies. AJNR Am J Neuroradiol 26:1634–1640

    PubMed  PubMed Central  Google Scholar 

  9. Sasaki Y, Aoki Y, Nakajima A et al (2013) Delayed neurologic deficit due to foraminal stenosis following osteoporotic late collapse of a lumbar spine vertebral body. Case Rep Orthop 2013:682075

    PubMed  PubMed Central  Google Scholar 

  10. He D, Yu W, Chen Z, Li L, Zhu K, Fan S (2016) Pathogenesis of the intravertebral vacuum of Kümmell’s disease (review). Exp Ther Med 12:879–882

    Article  PubMed  PubMed Central  Google Scholar 

  11. Heo DH, Chin DK, Yoon YS, Kuh SU (2009) Recollapse of previous vertebral compression fracture after percutaneous vertebroplasty. Osteoporos Int 20:473–480

    Article  CAS  PubMed  Google Scholar 

  12. Fang X, Yu F, Fu S, Song H (2015) Intravertebral clefts in osteoporotic compression fractures of the spine: incidence, characteristics, and therapeutic efficacy. Int J Clin Exp Med 8:16960–16968

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Niu J, Zhou H, Meng Q, Shi J, Meng B, Yang H (2015) Factors affecting recompression of augmented vertebrae after successful percutaneous balloon kyphoplasty: a retrospective analysis. Acta Radiol 56:1380–1387

    Article  PubMed  Google Scholar 

  14. Theodorou DJ (2001) The intravertebral vacuum cleft sign. Radiology 221:787–788

    Article  CAS  PubMed  Google Scholar 

  15. Ito Y, Hasegawa Y, Toda K, Nakahara S (2002) Pathogenesis and diagnosis of delayed vertebral collapse resulting from osteoporotic spinal fracture. Spine J 2(2):101–106

    Article  PubMed  Google Scholar 

  16. Maldague BE, Noel HM, Malghem JJ (1978) The intravertebral vacuum cleft: a sign of ischemic vertebral collapse 1. Radiology 129:23–29

    Article  CAS  PubMed  Google Scholar 

  17. Ratcliffe JF (1980) The arterial anatomy of the adult human lumbar vertebral body: a microarteriographic study. J Anat 131:57–79

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Van Eenenaam DP, el-Khoury GY (1993) Delayed post-traumatic vertebral collapse (Kummell’s disease): case report with serial radiographs, computed tomographic scans, and bone scans. Spine (Phila Pa 1976) 18: 1236–41.

  19. Naul LG, Peet GL, Maupin WB (1989) Avascular necrosis of the vertebral body: MR imaging. Radiology 172:219

    Article  CAS  PubMed  Google Scholar 

  20. Qi H, Xue J, Gao J, Zhang Y, Sun J, Wang G (2020) Changes of bone turnover markers and bone tissue content after severe osteoporotic vertebral compression fracture. Med Sci Monit 26:e923713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Qi H, Qi J, Gao J, Sun J, Wang G (2021) The impact of bone mineral density on bone metabolism and the fracture healing process in elderly Chinese patients with osteoporotic vertebral compression fractures. J Clin Densitom 24:135–145

    Article  PubMed  Google Scholar 

  22. Diamond TH, Clark WA, Kumar SV (2007) Histomorphometric analysis of fracture healing cascade in acute osteoporotic vertebral body fractures. Bone 40:775–780

    Article  PubMed  Google Scholar 

  23. Vernon-Roberts B, Pirie CJ (1973) Healing trabecular microfractures in the bodies of lumbar vertebrae. Ann Rheum Dis 32:406–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jelinek JS, Kransdorf MJ, Gray R, Aboulafia AJ, Malawer MM (1996) Percutaneous transpedicular biopsy of vertebral body lesions. Spine (Phila Pa 1976) 21: 2035–2040.

  25. Chaudhary RK, Acharya S, Chahal RS, Kalra KL (2019) Fluoroscopy guided percutaneous transpedicular biopsy of vertebral body lesion. J Nepal Health Res Counc 17:163–167

    Article  PubMed  Google Scholar 

  26. Baur A, Stäbler A, Arbogast S, Duerr HR, Bartl R, Reiser M (2002) Acute osteoporotic and neoplastic vertebral compression fractures: fluid sign at MR imaging. Radiology 225:730

    Article  PubMed  Google Scholar 

  27. Peh WC, Gelbart MS, Gilula LA, Peck DD (2003) Percutaneous vertebroplasty: treatment of painful vertebral compression fractures with intraosseous vacuum phenomena. AJR Am J Roentgenol 180:1411–1417

  28. Hiwatashi A, Ohgiya Y, Kakimoto N, Westesson PL (2007) Cement leakage during vertebroplasty can be predicted on preoperative MRI. AJR Am J Roentgenol 188:1089–1093

  29. Tanigawa N, Kariya S, Komemushi A et al (2009) Cement leakage in percutaneous vertebroplasty for osteoporotic compression fractures with or without intravertebral clefts. AJR Am J Roentgenol 193:W442–W445

  30. Klazen CA, Lohle PN, De Vries J et al (2010) Vertebroplasty versus conservative treatment in acute osteoporotic vertebral compression fractures (Vertos II): an open-label randomised trial. Lancet 376:1085–1092

    Article  PubMed  Google Scholar 

  31. Yu CW, Hsu CY, Shih TT, Chen BB, Fu CJ (2007) Vertebral osteonecrosis: MR imaging findings and related changes on adjacent levels. AJNR Am J Neuroradiol 28:42–47

    PubMed  PubMed Central  Google Scholar 

  32. Lane JI, Maus TP, Wald JT, Thielen KR, Bobra S, Luetmer PH (2002) Intravertebral clefts opacified during vertebroplasty: pathogenesis, technical implications, and prognostic significance. AJNR Am J Neuroradiol 23:1642–1646

    PubMed  PubMed Central  Google Scholar 

  33. Tsoumakido G, Too CW, Koch G et al (2017) CIRSE guidelines on percutaneous vertebral augmentation. Cardiovasc Intervent Radiol 40:331–342

    Article  Google Scholar 

  34. Einhorn TA (2005) The science of fracture healing. J Orthop Trauma 19:S4-6

    Article  PubMed  Google Scholar 

  35. Hsu WE, Su KC, Chen KH, Pan CC, Lu WH, Lee CH (2019) The evaluation of different radiological measurement parameters of the degree of collapse of the vertebral body in vertebral compression fractures. Appl Bionics Biomech 2019:1–5

    Article  Google Scholar 

  36. Sousa CP, Dias IR, Lopez-Peña M et al (2015) Bone turnover markers for early detection of fracture healing disturbances: a review of the scientific literature. An Acad Bras Cienc 87:1049–1061

    Article  CAS  PubMed  Google Scholar 

  37. Leeming DJ, Alexandersen P, Karsdal MA, Qvist P, Schaller S, Tankó LB (2006) An update on biomarkers of bone turnover and their utility in biomedical research and clinical practice. Eur J Clin Pharmacol 62:781–792

    Article  CAS  PubMed  Google Scholar 

  38. Veitch SW, Findlay SC, Hamer AJ, Blumsohn A, Eastell R, Ingle BM (2006) Changes in bone mass and bone turnover following tibial shaft fracture. Osteoporos Int 17:364–372

    Article  CAS  PubMed  Google Scholar 

  39. Whitmarsh T, Humbert L, Del Río Barquero LM, Di Gregorio S, Frangi AF (2013) 3D reconstruction of the lumbar vertebrae from anteroposterior and lateral dual-energy X-ray absorptiometry. Med Image Anal 17:475–487

    Article  PubMed  Google Scholar 

  40. Finkelstein JS, Cleary RL, Butler JP et al (1994) A comparison of lateral versus anterior-posterior spine dual energy x-ray absorptiometry for the diagnosis of osteopenia. J Clin Endocrinol Metab 78:724–730

    CAS  PubMed  Google Scholar 

  41. Larnach TA, Boyd SJ, Smart RC, Butler SP, Rohl PG, Diamond TH (1992) Reproducibility of lateral spine scans using dual energy X-ray absorptiometry. Calcif Tissue Int 51:255

    Article  CAS  PubMed  Google Scholar 

  42. Franck H, Munz M, Scherrer M, v Lilienfeld-Toal H, (1995) Lateral spine dual-energy X-ray absorptiometry bone mineral measurement with fan-beam design: effect of osteophytic calcifications on lateral and anteroposterior spine BMD. Rheumatol Int 15:151–154

    Article  CAS  PubMed  Google Scholar 

  43. Hart DJ, Mootoosamy I, Doyle DV, Spector TD (1994) The relationship between osteoarthritis and osteoporosis in the general population: the Chingford Study. Ann Rheum Dis 53:158–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Orwoll ES, Oviatt SK, Mann T (1990) The impact of osteophytic and vascular calcifications on vertebral mineral density measurements in men. J Clin Endocrinol Metab 70:1202–1207

    Article  CAS  PubMed  Google Scholar 

  45. Pocock NA, Eberl S, Eisman JA et al (1987) Dual-photon bone densitometry in normal Australian women: a cross-sectional study. Med J Aust 146:293–297

    Article  CAS  PubMed  Google Scholar 

  46. Reid IR, Evans MC, Stapleton J (1992) Lateral spine densitometry is a more sensitive indicator of glucocorticoid-induced bone loss. J Bone Miner Res 7:1221–1225

    Article  CAS  PubMed  Google Scholar 

  47. Jergas M, Breitenseher M, Glüer CC et al (1995) Which vertebrae should be assessed using lateral dual-energy X-ray absorptiometry of the lumbar spine. Osteoporos Int 5:196–204

    Article  CAS  PubMed  Google Scholar 

  48. Nakamae T, Fujimoto Y, Yamada K et al (2017) Relationship between clinical symptoms of osteoporotic vertebral fracture with intravertebral cleft and radiographic findings. J Orthop Sci 22:201

    Article  PubMed  Google Scholar 

  49. Stäbler A, Schneider P, Link TM et al (1999) Intravertebral vacuum phenomenon following fractures: CT study on frequency and etiology. J Comput Assist Tomogr 23:976–980

    Article  PubMed  Google Scholar 

  50. Freedman BA, Heller JG (2009) Kummel disease: a not-so-rare complication of osteoporotic vertebral compression fractures. J Am Board Fam Med 22:75–78

    Article  PubMed  Google Scholar 

  51. Lafforgue P (2006) Pathophysiology and natural history of avascular necrosis of bone. Joint Bone Spine 73:500–507

    Article  CAS  PubMed  Google Scholar 

  52. Kim DY, Lee SH, Jang JS, Chung SK, Lee HY (2004) Intravertebral vacuum phenomenon in osteoporotic compression fracture: report of 67 cases with quantitative evaluation of intravertebral instability. J Neurosurg 100:24–31

    PubMed  Google Scholar 

  53. Liu SH, Yang RS, al-Shaikh R, Lane JM (1995) Collagen in tendon, ligament, and bone healing. A current review. Clin Orthop Relat Res 1995:265–78

    Google Scholar 

  54. Kurdy NM (2000) Serology of abnormal fracture healing: the role of PIIINP, PICP, and BsALP. J Orthop Trauma 14:48

    Article  CAS  PubMed  Google Scholar 

  55. Lu C, Miclau T, Hu D et al (2005) Cellular basis for age-related changes in fracture repair. J Orthop Res 23:1300–1307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Techniques of specimen preparation and measurement were supported by the Pathology Laboratory of Shandong Provincial Hospital and Jinan Infectious Diseases Hospital.

Funding

The authors state that this work has not received any funding.

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Authors and Affiliations

  1. Department of Spine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250000, China

    Haoran Qi, Jianmin Sun & Guodong Wang

  2. School of Medicine, Shandong University, Jinan, 250000, China

    Haoran Qi & Jianmin Sun

  3. Laboratory Department, Jinan Infectious Diseases Hospital, Jinan, 250000, China

    Jun Qi

  4. Pathological Department, Jinan Infectious Diseases Hospital, Jinan, 250000, China

    Ye Sun

  5. Ocean University of China, Qingdao, 266003, China

    Junying Gao

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  1. Haoran Qi
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  5. Jianmin Sun
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Correspondence to Jianmin Sun or Guodong Wang.

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The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article

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Qi, H., Qi, J., Sun, Y. et al. Bone microarchitecture and metabolism in elderly male patients with signs of intravertebral cleft on MRI. Eur Radiol 32, 3931–3943 (2022). https://doi.org/10.1007/s00330-021-08458-9

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  • DOI: https://doi.org/10.1007/s00330-021-08458-9

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