Skip to main content
SpringerLink
Log in

Bone microstructure and volumetric bone mineral density in patients with global sagittal malalignment

  • Original Article
  • Published:
European Spine Journal Aims and scope Submit manuscript

Abstract

Purpose

Sagittal spinal malalignment often leads to surgical realignment, which is associated with major complications. Low bone mineral density (BMD) and impaired bone microstructure are risk factors for instrumentation failure. This study aims to demonstrate differences in volumetric BMD and bone microstructure between normal and pathological sagittal alignment and to determine the relationships among vBMD, microstructure, sagittal spinal and spinopelvic alignment.

Methods

A retrospective, cross-sectional study of patients who underwent lumbar fusion for degeneration was conducted. The vBMD of the lumbar spine was assessed by quantitative computed tomography. Bone biopsies were evaluated using microcomputed tomography (μCT). C7-S1 sagittal vertical axis (SVA; ≥ 50 mm malalignment) and spinopelvic alignment were measured. Univariate and multivariable linear regression analysis evaluated associations among the alignment, vBMD and μCT parameters.

Results

A total of 172 patients (55.8% female, 63.3 years, BMI 29.7 kg/m2, 43.0% with malalignment) including N = 106 bone biopsies were analyzed. The vBMD at levels L1, L2, L3 and L4 and the trabecular bone (BV) and total volume (TV) were significantly lower in the malalignment group. SVA was significantly correlated with vBMD at L1–L4 (ρ = -0.300, p < 0.001), BV (ρ = − 0.319, p = 0.006) and TV (ρ = − 0.276, p = 0.018). Significant associations were found between PT and L1–L4 vBMD (ρ = − 0.171, p = 0.029), PT and trabecular number (ρ = − 0.249, p = 0.032), PT and trabecular separation (ρ = 0.291, p = 0.012), and LL and trabecular thickness (ρ = 0.240, p = 0.017). In the multivariable analysis, a higher SVA was associated with lower vBMD (β = − 0.269; p = 0.002).

Conclusion

Sagittal malalignment is associated with lower lumbar vBMD and trabecular microstructure. Lumbar vBMD was significantly lower in patients with malalignment. These findings warrant attention, as malalignment patients may be at a higher risk of surgery-related complications due to impaired bone. Standardized preoperative assessment of vBMD may be advisable.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Glassman SD, Bridwell K, Dimar JR, Horton W, Berven S, Schwab F (2005) The impact of positive sagittal balance in adult spinal deformity. Spine 30(18):2024–2029. https://doi.org/10.1097/01.brs.0000179086.30449.96

    Article  PubMed  Google Scholar 

  2. Schwab FJ, Blondel B, Bess S, Hostin R, Shaffrey CI, Smith JS et al (2013) Radiographical spinopelvic parameters and disability in the setting of adult spinal deformity: a prospective multicenter analysis. Spine 38(13):E803–E812. https://doi.org/10.1097/BRS.0b013e318292b7b9

    Article  PubMed  Google Scholar 

  3. Pellisé F, Vila-Casademunt A, Ferrer M, Domingo-Sàbat M, Bagó J, Pérez-Grueso FJ et al (2015) Impact on health related quality of life of adult spinal deformity (ASD) compared with other chronic conditions. Eur Spine J 24(1):3–11

    Article  PubMed  Google Scholar 

  4. Good CR, Auerbach JD, O’Leary PT, Schuler TC (2011) Adult spine deformity. Curr Rev Musculoskelet Med 4(4):159–167

    Article  PubMed  PubMed Central  Google Scholar 

  5. Youssef JA, Orndorff DO, Patty CA, Scott MA, Price HL, Hamlin LF et al (2013) Current status of adult spinal deformity. Glob Spine J 3(1):51–62

    Article  CAS  Google Scholar 

  6. Yadla S, Maltenfort MG, Ratliff JK, Harrop JS (2010) Adult scoliosis surgery outcomes: a systematic review. Neurosurg Focus 28(3):E3

    Article  PubMed  Google Scholar 

  7. Daubs MD, Lenke LG, Cheh G, Stobbs G, Bridwell KH (2007) Adult spinal deformity surgery: complications and outcomes in patients over age 60. Spine 32(20):2238–2244. https://doi.org/10.1097/BRS.0b013e31814cf24a

    Article  PubMed  Google Scholar 

  8. Drazin D, Shirzadi A, Rosner J, Eboli P, Safee M, Baron EM et al (2011) Complications and outcomes after spinal deformity surgery in the elderly: review of the existing literature and future directions. Neurosurg Focus 31(4):E3

    Article  PubMed  Google Scholar 

  9. Martin BI, Mirza SK, Spina N, Spiker WR, Lawrence B, Brodke DS (2019) Trends in lumbar fusion procedure rates and associated hospital costs for degenerative spinal diseases in the united states, 2004 to 2015. Spine 44(5):369–376. https://doi.org/10.1097/BRS.0000000000002822

    Article  PubMed  Google Scholar 

  10. DeWald CJ, Stanley T (2006) Instrumentation-related complications of multilevel fusions for adult spinal deformity patients over age 65: surgical considerations and treatment options in patients with poor bone quality. Spine 31(Suppl):S144–S151. https://doi.org/10.1097/01.brs.0000236893.65878.39

    Article  PubMed  Google Scholar 

  11. Patrick T, BridwellLenkeGoodPichelmannBuchowski KHLGCRMAJM et al (2009) Risk factors and outcomes for catastrophic failures at the top of long pedicle screw constructs: a matched cohort analysis performed at a single center. Spine 34(20):2134–2139. https://doi.org/10.1097/BRS.0b013e3181b2e17e

    Article  Google Scholar 

  12. Schreiber JJ, Hughes AP, Taher F, Girardi FP (2014) An association can be found between hounsfield units and success of lumbar spine fusion. Hss j 10(1):25–29

    Article  PubMed  Google Scholar 

  13. Oh KW, Lee JH, Lee JH, Lee DY, Shim HJ (2017) The correlation between cage subsidence, bone mineral density, and clinical results in posterior lumbar interbody fusion. Clin Spine Surg 30(6):E683–E689

    Article  PubMed  Google Scholar 

  14. Matsumoto T, Okuda S, Maeno T, Yamashita T, Yamasaki R, Sugiura T et al (2017) Spinopelvic sagittal imbalance as a risk factor for adjacent-segment disease after single-segment posterior lumbar interbody fusion. J Neurosurg Spine 26(4):435–440

    Article  PubMed  Google Scholar 

  15. Seeman E, Delmas PD (2006) Bone quality–the material and structural basis of bone strength and fragility. N Engl J Med 354(21):2250–2261

    Article  CAS  PubMed  Google Scholar 

  16. Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S et al (2014) Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int 25(10):2359–2381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Dipaola CP, Bible JE, Biswas D, Dipaola M, Grauer JN, Rechtine GR (2009) Survey of spine surgeons on attitudes regarding osteoporosis and osteomalacia screening and treatment for fractures, fusion surgery, and pseudoarthrosis. Spine J 9(7):537–544

    Article  PubMed  Google Scholar 

  18. Rand T, Seidl G, Kainberger F, Resch A, Hittmair K, Schneider B et al (1997) Impact of spinal degenerative changes on the evaluation of bone mineral density with dual energy X-ray absorptiometry (DXA]. Calcif Tissue Int 60(5):430–433

    Article  CAS  PubMed  Google Scholar 

  19. Simonelli C, Adler RA, Blake GM, Caudill JP, Khan A, Leib E et al (2008) Dual-energy X-ray absorptiometry technical issues: the 2007 ISCD official positions. J Clin Densitom 11(1):109–122

    Article  PubMed  Google Scholar 

  20. Guglielmi G, Floriani I, Torri V, Li J, van Kuijk C, Genant HK et al (2005) Effect of spinal degenerative changes on volumetric bone mineral density of the central skeleton as measured by quantitative computed tomography. Acta Radiol 46(3):269–275

    Article  CAS  PubMed  Google Scholar 

  21. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25(7):1468–1486

    Article  PubMed  Google Scholar 

  22. Bao J, Zou D, Li W (2021) Characteristics of the DXA measurements in patients undergoing lumbar fusion for lumbar degenerative diseases: a retrospective analysis of over 1000 patients. Clin Interv Aging 16:1131–1137

    Article  PubMed  PubMed Central  Google Scholar 

  23. Steiger P, Block JE, Steiger S, Heuck AF, Friedlander A, Ettinger B et al (1990) Spinal bone mineral density measured with quantitative CT: effect of region of interest, vertebral level, and technique. Radiology 175(2):537–543

    Article  CAS  PubMed  Google Scholar 

  24. Cann CE, Genant HK (1980) Precise measurement of vertebral mineral content using computed tomography. J Comput Assist Tomogr 4(4):493–500

    Article  CAS  PubMed  Google Scholar 

  25. Haffer H, Muellner M, Chiapparelli E, Moser M, Dodo Y, Zhu J et al (2022) Bone quality in patients with osteoporosis undergoing lumbar fusion surgery: analysis of the MRI-based vertebral bone quality score and the bone microstructure derived from microcomputed tomography. Spine J 22(10):1642–1650. https://doi.org/10.1016/j.spinee.2022.05.008

    Article  PubMed  Google Scholar 

  26. Brown JK, Timm W, Bodeen G, Chason A, Perry M, Vernacchia F et al (2017) Asynchronously calibrated quantitative bone densitometry. J Clin Densitom 20(2):216–225

    Article  CAS  PubMed  Google Scholar 

  27. Wang L, Su Y, Wang Q, Duanmu Y, Yang M, Yi C et al (2017) Validation of asynchronous quantitative bone densitometry of the spine: accuracy, short-term reproducibility, and a comparison with conventional quantitative computed tomography. Sci Rep 7(1):6284

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pickhardt PJ, Bodeen G, Brett A, Brown JK, Binkley N (2015) Comparison of femoral neck BMD evaluation obtained using Lunar DXA and QCT with asynchronous calibration from CT colonography. J Clin Densitom 18(1):5–12

    Article  PubMed  Google Scholar 

  29. Shepherd JA, Schousboe JT, Broy SB, Engelke K, Leslie WD (2015) Executive summary of the 2015 ISCD position development conference on advanced measures from DXA and QCT: fracture prediction beyond BMD. J Clin Densitom 18(3):274–286. https://doi.org/10.1016/j.jocd.2015.06.013

    Article  PubMed  Google Scholar 

  30. Radiology ACo (2018) ACR–SPR–SSR practice parameter for the performance of musculoskeletal quantitative computed tomography (QCT] 2018 revised [Available from: https://www.acr.org/-/media/ACR/Files/Practice-Parameters/qct.pdf

  31. Schwab F, Patel A, Ungar B, Farcy J-P, Lafage V (2010) adult spinal deformity—postoperative standing imbalance: how much can you tolerate? An overview of key parameters in assessing alignment and planning corrective surgery. Spine 35(25):2224–2231. https://doi.org/10.1097/BRS.0b013e3181ee6bd4

    Article  PubMed  Google Scholar 

  32. Dai J, Yu X, Huang S, Fan L, Zhu G, Sun H et al (2015) Relationship between sagittal spinal alignment and the incidence of vertebral fracture in menopausal women with osteoporosis: a multicenter longitudinal follow-up study. Eur Spine J 24(4):737–743

    Article  PubMed  Google Scholar 

  33. Lee JS, Lee HS, Shin JK, Goh TS, Son SM (2013) Prediction of sagittal balance in patients with osteoporosis using spinopelvic parameters. Eur Spine J 22(5):1053–1058

    Article  PubMed  PubMed Central  Google Scholar 

  34. Cho Y, Lee G, Aguinaldo J, Lee KJ, Kim K (2015) Correlates of bone mineral density and sagittal spinal balance in the aged. Ann Rehabil Med 39(1):100–107

    Article  PubMed  PubMed Central  Google Scholar 

  35. Wolff J (1892) Das gesetz der transformation der knochen. Verlag von August Hirschwald, Berlin

    Google Scholar 

  36. Le Huec JC, Charosky S, Barrey C, Rigal J, Aunoble S (2011) Sagittal imbalance cascade for simple degenerative spine and consequences: algorithm of decision for appropriate treatment. Eur Spine J 20(Suppl 5):699–703

    Article  PubMed  PubMed Central  Google Scholar 

  37. Pavlovic A, Nichols DL, Sanborn CF, Dimarco NM (2013) Relationship of thoracic kyphosis and lumbar lordosis to bone mineral density in women. Osteoporos Int 24(8):2269–2273

    Article  CAS  PubMed  Google Scholar 

  38. Okano I, Carlson BB, Chiapparelli E, Salzmann SN, Winter F, Shirahata T et al (2020) Local mechanical environment and spinal trabecular volumetric bone mineral density measured by quantitative computed tomography: a study on lumbar lordosis. World Neurosurg 135:e286–e292

    Article  PubMed  Google Scholar 

  39. Papadakis M, Papagelopoulos P, Papadokostakis G, Sapkas G, Damilakis J, Katonis P (2011) The impact of bone mineral density on the degree of curvature of the lumbar spine. J Musculoskelet Neuronal Interact 11(1):46–51

    CAS  PubMed  Google Scholar 

  40. Barrey C, Roussouly P, Le Huec JC, D’Acunzi G, Perrin G (2013) Compensatory mechanisms contributing to keep the sagittal balance of the spine. Eur Spine J 22(Suppl 6):S834–S841

    Article  PubMed  Google Scholar 

  41. Lin T, Lu J, Zhang Y, Wang Z, Chen G, Gu Y et al (2021) Does spinal sagittal imbalance lead to future vertebral compression fractures in osteoporosis patients? Spine J 21(8):1362–1375

    Article  PubMed  Google Scholar 

  42. Matsunaga T, Miyagi M, Nakazawa T, Murata K, Kawakubo A, Fujimaki H et al (2021) Prevalence and characteristics of spinal sagittal malalignment in patients with osteoporosis. J Clin Med 10(13):2827. https://doi.org/10.3390/jcm10132827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Schwab F, Ungar B, Blondel B, Buchowski J, Coe J, Deinlein D, DeWald C, Mehdian H, Shaffrey C, Tribus C, Lafage V (2012) Scoliosis research society—schwab adult spinal deformity classification: a validation study. Spine 37(12):1077–1082. https://doi.org/10.1097/BRS.0b013e31823e15e2

    Article  PubMed  Google Scholar 

  44. Lafage V, Schwab F, Patel A, Hawkinson N, Farcy J-P (2009) Pelvic tilt and truncal inclination: two key radiographic parameters in the setting of adults with spinal deformity. Spine 34(17):E599–E606. https://doi.org/10.1097/BRS.0b013e3181aad219

    Article  PubMed  Google Scholar 

  45. Bjerke BT, Zarrabian M, Aleem IS, Fogelson JL, Currier BL, Freedman BA et al (2018) Incidence of osteoporosis-related complications following posterior lumbar fusion. Glob Spine J 8(6):563–569

    Article  Google Scholar 

  46. Yilgor C, Sogunmez N, Boissiere L, Yavuz Y, Obeid I, Kleinstück F et al (2017) Global alignment and proportion (GAP] score: development and validation of a new method of analyzing spinopelvic alignment to predict mechanical complications after adult spinal deformity surgery. J Bone Joint Surg Am 99(19):1661–1672

    Article  PubMed  Google Scholar 

  47. Noh SH, Ha Y, Obeid I, Park JY, Kuh SU, Chin DK et al (2020) Modified global alignment and proportion scoring with body mass index and bone mineral density (GAPB) for improving predictions of mechanical complications after adult spinal deformity surgery. Spine J 20(5):776–784

    Article  PubMed  Google Scholar 

  48. Kolz JM, Freedman BA, Nassr AN (2021) The value of cement augmentation in patients with diminished bone quality undergoing thoracolumbar fusion surgery: a review. Glob Spine J 11(1_suppl):37S-44S. https://doi.org/10.1177/2192568220965526

    Article  Google Scholar 

  49. Salzmann SN, Shirahata T, Yang J, Miller CO, Carlson BB, Rentenberger C et al (2019) Regional bone mineral density differences measured by quantitative computed tomography: does the standard clinically used L1–L2 average correlate with the entire lumbosacral spine? Spine J 19(4):695–702

    Article  PubMed  Google Scholar 

  50. Britton JM, Davie MW (1990) Mechanical properties of bone from iliac crest and relationship to L5 vertebral bone. Bone 11(1):21–28

    Article  CAS  PubMed  Google Scholar 

  51. Dempster DW, Ferguson-Pell MW, Mellish RW, Cochran GV, Xie F, Fey C et al (1993) Relationships between bone structure in the iliac crest and bone structure and strength in the lumbar spine. Osteoporos Int 3(2):90–96

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Hayat Benlarb from the Research Division at the Hospital for Special Surgery for assistance with the microcomputed tomography experiments.

Funding

Research reported in this publication was supported by the National Center for Advancing Translational Science of the National Institute of Health Under Award Number UL1TR002384.

Author information

Authors and Affiliations

  1. Department of Orthopaedic Surgery, Hospital for Special Surgery, Weill Cornell Medicine, New York City, NY, USA

    Henryk Haffer, Maximilian Muellner, Erika Chiapparelli, Yusuke Dodo, Manuel Moser, Jennifer Shue, Andrew A. Sama, Frank P. Cammisa, Federico P. Girardi & Alexander P. Hughes

  2. Center for Musculoskeletal Surgery, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany

    Henryk Haffer & Maximilian Muellner

  3. Department of Spine Surgery, Lucerne Cantonal Hospital, Lucerne, Switzerland

    Manuel Moser

  4. Department of Epidemiology and Biostatistics, Hospital for Special Surgery, Weill Cornell Medicine, New York City, NY, USA

    Jiaqi Zhu

Authors
  1. Henryk Haffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maximilian Muellner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erika Chiapparelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yusuke Dodo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuel Moser
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiaqi Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jennifer Shue
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrew A. Sama
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Frank P. Cammisa
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Federico P. Girardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Alexander P. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H.H. contributed to conceptualization, methodology, investigation, writing—original draft, and visualization; M.M. performed investigation, conceptualization, and writing—review and editing; E.C. performed investigation, writing—review and editing, and data curation; Y.D. performed investigation and writing—review and editing; J.Z. contributed to formal analysis, resources, and writing—review and editing; M.M. contributed to investigation, conceptualization, and writing—review and editing; J.S. contributed to data curation, writing—review and editing, project administration, and supervision; A.A.S., F.P.C., and F.P.G. performed project administration, funding acquisition, and writing—review and editing; A.P.H. contributed to project administration, funding acquisition, writing—review and editing, supervision, conceptualization, and methodology.

Corresponding author

Correspondence to Alexander P. Hughes.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest concerning materials or methods used in this study or the findings specified in this paper.

Disclosures

Dr. Sama reports royalties from Ortho Development, Corp.; private investments for Vestia Ventures MiRUS Investment, LLC, ISPH II, LLC, ISPH 3, LLC, and VBros Venture Partners X Centinel Spine; consulting fee from Clariance, Inc., Kuros Biosciences AG, and Medical Device Business Service, Inc.; speaking and teaching arrangements of DePuy Synthes Products, Inc.; membership of scientific advisory board of Clariance, Inc., and Kuros Biosciences AG; and trips/travel of Medical Device Business research support from Spinal Kinetics, Inc., outside the submitted work. Dr. Cammisa reports royalties from NuVasive, Inc.; private investments for 4WEB Medical/4WEB, Inc., Bonovo Orthopedics, Inc., Healthpoint Capital Partners, LP, ISPH II, LLC, ISPH 3 Holdings, LLC, Ivy Healthcare Capital Partners, LLC, Medical Device Partners II, LLC, Medical Device Partners III, LLC, Orthobond Corporation, Spine Biopharma, LLC, Synexis, LLC, Tissue Differentiation Intelligence, LLC, VBVP VI, LLC, VBVP X, LLC (Centinel] and Woven Orthopedics Technologies; consulting fees from 4WEB Medical/4WEB, Inc., DePuy Synthes Spine, NuVasive, Inc., Spine Biopharma, LLC, and Synexis, LLC; membership of scientific advisory board/other office of Healthpoint Capital Partners, LP, Medical Device Partners III, LLC, Orthobond Corporation, Spine Biopharma, LLC, Synexis, LLC, and Woven Orthopedic Technologies; and research support from 4WEB Medical/4WEB, Inc., Mallinckrodt Pharmaceuticals, Camber Spine, and Centinel Spine, outside the submitted work. Dr. Girardi reports royalties from Lanx, Inc., and Ortho Development Corp.; private investments for Centinel Spine, and BCMID; stock ownership of Healthpoint Capital Partners, LP; and consulting fees from NuVasive, Inc., and DePuy Synthes Spine, outside the submitted work. Dr. Hughes reports research support from NuVasive, Inc. and Kuros Biosciences AG; and fellowship support from NuVasive, Inc. and Kuros Biosciences AG, outside the submitted work.

Ethical approval

The study was approved by our hospital’s institutional review board (IRB 2014-084) and complied with the Declaration of Helsinki.

Informed consent

Our manuscript does not include copyrighted materials. We obtained signed patient consent forms prior study inclusion from all patients a bone biopsy was taken.

Additional information

Publisher's Note

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

The work was performed at Hospital for Special Surgery, New York City, NY, USA. The institutional review board of Hospital for Special Surgery approved this study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 18 KB)

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

Haffer, H., Muellner, M., Chiapparelli, E. et al. Bone microstructure and volumetric bone mineral density in patients with global sagittal malalignment. Eur Spine J 32, 2228–2237 (2023). https://doi.org/10.1007/s00586-023-07654-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00586-023-07654-z

Keywords

Search

Navigation