Skip to main content

Advertisement

SpringerLink
Log in

The association between lumbar paraspinal muscle functional cross-sectional area on MRI and regional volumetric bone mineral density measured by quantitative computed tomography

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

Osteosarcopenia is a common condition among elderly and postmenopausal female patients. Site-specific bone mineral density is more predictive of bone-related complications. Few studies have investigated muscle-bone associations. Our results demonstrated that in women, significant positive associations between paraspinal muscles FCSA and vBMD exist at different lumbosacral levels. These regional differences should be considered when interpreting bone-muscle associations in the lumbar spine.

Introduction

There is increasing evidence between bone and muscle volume associations. Previous studies have demonstrated comorbidity between osteoporosis and sarcopenia. Recent studies showed that sarcopenic subjects had a fourfold higher risk of concomitant osteoporosis compared to non-sarcopenic individuals. Although site-specific bone mineral density (BMD) assessments were reported to be more predictive of bone-related complications after spinal fusions than BMD assessments in general, there are few studies that have investigated level-specific bone-muscle interactions. The aim of this study is to investigate the associations between muscle functional cross-sectional area (FCSA) on magnetic resonance imaging (MRI) and site-specific quantitative computed tomography (QCT) volumetric bone mineral density (vBMD) in the lumbosacral region among spine surgery patients.

Methods

We retrospectively reviewed a prospective institutional database of posterior lumbar fusion patients. Patients with available MRI undergoing posterior lumbar fusion were included. Muscle measurements and FCSA were conducted and calculated utilizing a manual segmentation and custom-written program at the superior endplate of the L3–L5 vertebrae level. vBMD measurements were performed and calculated utilizing a QCT pro software at L1–L2 levels and bilateral sacral ala. We stratified by sex for all analyses.

Results

A total of 105 patients (mean age 61.5 years and 52.4% females) were included. We found that female patients had statistically significant lower muscle FCSA than male patients. After adjusting for age and body mass index (BMI), there were statistically significant positive associations between L1–L2 and S1 vBMD with L3 psoas FCSA as well as sacral ala vBMD with L3 posterior paraspinal and L5 psoas FCSA. These associations were not found in males.

Conclusions

Our results demonstrated that in women, significant positive associations between the psoas and posterior paraspinal muscle FCSA and vBMD exist in different lumbosacral levels, which are independent of age and BMI. These regional differences should be considered when interpreting bone and muscle associations in the lumbar spine.

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

References

  1. Clynes MA, Gregson CL, Bruyère O et al (2021) Osteosarcopenia: where osteoporosis and sarcopenia collide. Rheumatology (Oxford) 60:529–537. https://doi.org/10.1093/rheumatology/keaa755

    Article  CAS  Google Scholar 

  2. Teng Z, Zhu Y, Teng Y, Long Q, Hao Q, Yu X, Yang L, Lv Y, Liu J, Zheng Y, Lu S (2021) The analysis of osteosarcopenia as a risk factor for fractures, mortality, and falls. Osteoporos Int. https://doi.org/10.1007/s00198-021-05963-x

    Article  PubMed  Google Scholar 

  3. Huo YR, Suriyaarachchi P, Gomez F et al (2015) Phenotype of Osteosarcopenia in older individuals with a history of falling. J Am Med Dir Assoc 16:290–295. https://doi.org/10.1016/j.jamda.2014.10.018

    Article  PubMed  Google Scholar 

  4. Kirk B, Zanker J, Duque G (2020) Osteosarcopenia: epidemiology, diagnosis, and treatment—facts and numbers. J Cachexia Sarcopenia Muscle 11:609–618. https://doi.org/10.1002/jcsm.12567

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ward RJ, Roberts CC, Bencardino JT et al (2017) ACR Appropriateness Criteria® Osteoporosis and bone mineral density. J Am Coll Radiol 14:S189–S202. https://doi.org/10.1016/j.jacr.2017.02.018

    Article  PubMed  Google Scholar 

  6. Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis. Age Ageing 39:412–423. https://doi.org/10.1093/ageing/afq034

    Article  PubMed  PubMed Central  Google Scholar 

  7. Derstine BA, Holcombe SA, Ross BE et al (2018) Skeletal muscle cutoff values for sarcopenia diagnosis using T10 to L5 measurements in a healthy US population. Sci Rep 8:1–8. https://doi.org/10.1038/s41598-018-29825-5

    Article  CAS  Google Scholar 

  8. Van Der Werf A, Langius JAE, De Van Der Schueren MAE et al (2018) Percentiles for skeletal muscle index, area and radiation attenuation based on computed tomography imaging in a healthy Caucasian population. Eur J Clin Nutr 72:288–296. https://doi.org/10.1038/s41430-017-0034-5

    Article  PubMed  Google Scholar 

  9. Hirschfeld HP, Kinsella R, Duque G (2017) Osteosarcopenia: where bone, muscle, and fat collide. Osteoporos Int 10:2781–2790. https://doi.org/10.1007/s00198-017-4151-8

    Article  CAS  Google Scholar 

  10. Isaacson J, Brotto M (2014) Physiology of mechanotransduction: how do muscle and bone “talk” to one another? Clin Rev Bone Miner Metab 12:77–85. https://doi.org/10.1007/s12018-013-9152-3

    Article  PubMed  Google Scholar 

  11. Pollintine P, Dolan P, Tobias JH, Adams MA (2004) Intervertebral disc degeneration can lead to “stress-shielding” of the anterior vertebral body: a cause of osteoporotic vertebral fracture? Spine 29:774–782. https://doi.org/10.1097/01.BRS.0000119401.23006.D2

    Article  PubMed  Google Scholar 

  12. Okano I, Carlson BB, Chiapparelli E 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. https://doi.org/10.1016/j.wneu.2019.11.139

    Article  PubMed  Google Scholar 

  13. Okano I, Salzmann SN, Jones C et al (2021) The effect of obesity, diabetes, and epidural steroid injection on regional volumetric bone mineral density measured by quantitative computed tomography in the lumbosacral spine. Eur Spine J 30:13–21. https://doi.org/10.1007/s00586-020-06610-5

    Article  PubMed  Google Scholar 

  14. Jones C, Okano I, Salzmann SN et al (2021) Endplate volumetric bone mineral density is a predictor for cage subsidence following lateral lumbar interbody fusion: a risk factor analysis. Spine J 000:1–9. https://doi.org/10.1016/j.spinee.2021.02.021

    Article  Google Scholar 

  15. Sakai Y, Takenaka S, Matsuo Y et al (2018) Hounsfield unit of screw trajectory as a predictor of pedicle screw loosening after single level lumbar interbody fusion. J Orthop Sci 23:734–738. https://doi.org/10.1016/j.jos.2018.04.006

    Article  PubMed  Google Scholar 

  16. Salzmann SN, Okano I, Rentenberger C et al (2019) Skin ultrasound measurement as a potential marker of bone quality: a prospective pilot study of patients undergoing lumbar spinal fusion. J Orthop Res 37:2508–2515. https://doi.org/10.1002/jor.24438

    Article  CAS  PubMed  Google Scholar 

  17. Okano I, Salzmann SN, Ortiz Miller C et al (2020) Correlation between urine N-terminal telopeptide and Fourier transform infrared spectroscopy parameters: a preliminary study. J Osteoporos 2020.https://doi.org/10.1155/2020/5725086

  18. Weaver DJ, Malik AT, Jain N, Yu E, Kim J, Khan S (2018) The modified 5-item frailty index: a concise and useful tool for assesing the impact of frailty on postoperative morbidity following elective posteior lumbar fusion. World Neurosurg 124:626–632. https://doi.org/10.1016/j.wneu.2018.12.168

    Article  Google Scholar 

  19. Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128. https://doi.org/10.1016/j.neuroimage.2006.01.015

    Article  PubMed  Google Scholar 

  20. Otsu N (1979) A Threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern 9(1):62–66. https://doi.org/10.1109/TSMC.1979.4310076

    Article  Google Scholar 

  21. Salzmann SN, Ortiz Miller C, Carrino JA et al (2019) BMI and gender increase risk of sacral fractures after multilevel instrumented spinal fusion compared with bone mineral density and pelvic parameters. Spine J 19:238–245. https://doi.org/10.1016/j.spinee.2018.05.021

    Article  PubMed  Google Scholar 

  22. Brown JK, Timm W, Bodeen G et al (2017) Asynchronously calibrated quantitative bone densitometry. J Clin Densitom 20:216–225. https://doi.org/10.1016/j.jocd.2015.11.001

    Article  CAS  PubMed  Google Scholar 

  23. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723. https://doi.org/10.1109/TAC.1974.1100705

    Article  Google Scholar 

  24. Yoshimura N, Muraki S, Oka H, Lidaka T, Kodama R, Horii C, Kawaguchi H, Nakamura K, Akune T, Tanaka S (2018) Do sarcopenia and/or osteoporosis increase the risk of frailty? A 4-year observation of the second and third ROAD study surveys. Osteoporos Int 29.https://doi.org/10.1007/s00198-018-4596-4

  25. Kalichman L, Guermazi A, LiHunter LD (2009) Association between age, sex, BMI and CT-evaluated spinal degeneration features. J Back Musculoskelet Rehabil 22:189–195. https://doi.org/10.3233/BMR-2009-0232

    Article  PubMed  Google Scholar 

  26. Kalichman L, Hodges P, Li L et al (2010) Changes in paraspinal muscles and their association with low back pain and spinal degeneration: CT study. Eur Spine J 19:1136–1144. https://doi.org/10.1007/s00586-009-1257-5

    Article  PubMed  Google Scholar 

  27. Zhu K, Briffa K, Smith A, Mountain J, Briggs A, Lye S, Pennel C, Straker C, Walsh J (2014) Gender differences in the relationships between lean body mass, fat mass and peak bone mass in young adults. Osteoporos Int 25:1563–1570. https://doi.org/10.1007/s00198-014-2665-x

    Article  CAS  PubMed  Google Scholar 

  28. Verschueren S, Gielen E, O’Neill TW et al (2013) Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int 24:87–98. https://doi.org/10.1007/s00198-012-2057-z

    Article  CAS  PubMed  Google Scholar 

  29. Hida T, Eastlack RK, Kanemura T et al (2021) Effect of race, age, and gender on lumbar muscle volume and fat infiltration in the degenerative spine. J Orthop Sci 26:69–74. https://doi.org/10.1016/j.jos.2019.09.006

    Article  PubMed  Google Scholar 

  30. D’Hooge R, Cagnie B, Crombez G et al (2012) Increased intramuscular fatty infiltration without differences in lumbar muscle cross-sectional area during remission of unilateral recurrent low back pain. Man Ther 17:584–588. https://doi.org/10.1016/j.math.2012.06.007

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  32. Shao Z, Rompe G, Schiltenwolf M (2002) Radiographic changes in the lumbar intervertebral discs and lumbar vertebrae with age. World Neurosurg 27:263–268. https://doi.org/10.1097/00007632-200202010-00013

    Article  Google Scholar 

  33. Zakaria HM, Wilkinson BM, Pennington Z et al (2020) Sarcopenia as a prognostic factor for 90-day and overall mortality in patients undergoing spine surgery for metastatic tumors: a multicenter retrospective cohort study. Neurosurgery 87:1025–1036. https://doi.org/10.1093/neuros/nyaa245

    Article  PubMed  Google Scholar 

  34. Matsumoto H, Matsumura K, Yamamoto Y et al (2020) Prognostic value of psoas muscle mass index in patients with non-st-segment-elevation myocardial infarction: a prospective observational study. J Am Heart Assoc 9:1–6. https://doi.org/10.1161/JAHA.120.017315

    Article  CAS  Google Scholar 

  35. Bae SJ, Lee SH (2021) Computed tomographic measurements of the psoas muscle as a predictor of mortality in hip fracture patients: muscle attenuation helps predict mortality in hip fracture patients. Injury 52:1456–1461. https://doi.org/10.1016/j.injury.2020.11.062

    Article  PubMed  Google Scholar 

  36. Katsu M, Ohba T, Ebata S et al (2020) Potential role of paraspinal musculature in the maintenance of spinopelvic alignment in patients with adult spinal deformities. Clin Spine Surg 33:E76–E80. https://doi.org/10.1097/BSD.0000000000000862

    Article  PubMed  Google Scholar 

  37. Lee SH, Park SW, Kim YB et al (2017) The fatty degeneration of lumbar paraspinal muscles on computed tomography scan according to age and disc level. Spine J 17:81–87. https://doi.org/10.1016/j.spinee.2016.08.001

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was approved by the Institutional Review Board (#2016-0751) at the Hospital for Special Surgery.

Author information

Author notes

  1. E. Chiapparelli and I. Okano contributed equally to this work.

Authors and Affiliations

  1. Spine Care Institute, Hospital for Special Surgery, 535 East 70th Street, New York, NY, 10021, USA

    E. Chiapparelli, I. Okano, D. Adl Amini, J. Zhu, S. N. Salzmann, E. T. Tan, M. Moser, O. C. Sax, C. Echeverri, L. Oezel, J. Shue, A. A. Sama, F. P. Cammisa, F. P. Girardi & A. P. Hughes

  2. Department of Orthopedic Surgery and Traumatology, Charité University Hospital Berlin, Charitéplatz 1, 10117, Berlin, Germany

    D. Adl Amini

  3. Department of Orthopedic Surgery and Traumatology, University Hospital Duesseldorf, Moorenstr. 5, 40225, Düsseldorf, Germany

    L. Oezel

Authors
  1. E. Chiapparelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Okano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Adl Amini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. N. Salzmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. T. Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Moser
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. O. C. Sax
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. C. Echeverri
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. L. Oezel
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. J. Shue
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A. A. Sama
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. F. P. Cammisa
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. F. P. Girardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. A. P. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. P. Hughes.

Ethics declarations

Ethics approval

In this manuscript, no drug or device requiring FDA approval was discussed.

Conflicts of interest

Erika Chiapparelli, Ichiro Okano, Dominik Adl Amini, Jiaqi Zhu, Stephan N. Salzmann, Ek T. Tan, Manuel Moser, Oliver C. Sax, Cristian Echeverri, Lisa Oezel, and Jennifer Shue, declare that they have no conflict of interest.

Andrew A. Sama has received ownership interest from Paradigm Spine, LLC and Spinal Kinetics, Inc.; research support from Spinal Kinetics, Inc. and MiMedx Group, Inc. served as a consultant/scientific advisory board member for Clariance Inc., Nuvasive, Inc., Capital Royality, LP., Kuros Biosciences AG, Ortho Development Corp, 4WEB, Inc., Leerink Partners, LLC, and Depuy Orthopaedics, Inc.

Frank P. Cammisa has received royalties from Nuvasive, Inc., served as a consultant/scientific advisory board member Vertical Spine, LLC, 4WEB Medical, Healthpoint Capital Partners, LP, Orthobond Corporation, Woven Orthopedic Technologies, received ownership interest from VBVP VI, LLC, received research support from Spinal Kinetics, Inc.; Ivy Healthcare Capital Partners, LLC; ISPH II, LLC; NuVasive, Inc.,Mallinckrodt Pharmaceuticals, Centinel Spine, Inc. (fka Raymedica, LLC), Beatrice & Samuel A. Seaver Foundation, 4WEB Medical, Woven Orthopedic Technologies, Depuy Synthes, Orthobond Corporation, Pfizer, Inc., Paradigm Spine, LLC,7D Surgical, Inc. received others from Spinal Kinetics, Inc., Vertical Spine, LLC, Bonovo Orthopedics, Inc., Viscogliosi Brothers, LLC, Liventa Bioscience (fka AF Cell Medical), Woven Orthopedic Technologies, Healthpoint Capital Partners, LP, Paradigm Spine, LLC, amd Tissue Differentiation Intelligence, LLC.

Federico P. Girardi has received royalties from Lanx/Zimmer Biomet Spine, Depuy Synthes Spine, Nuvasive, Inc., Ortho Development Corp., ownership interest from Healthpoint Capital Partners, Paradigm Spine, LLC, Centinel Spine, Inc., and Liventa BioSciences, Inc., grant from Nuvasive, Inc., and MiMedx Group, Inc, outside of this work and served as a consultant for Ortho Development Corp, Nuvasive, Inc., Depuy Synthes Spine, and Lanx/Zimmer Biomet Spine.

Alexander P. Hughes has received research support from Pfizer, Inc., grants from Nuvasive, Inc, and 4WEB Medical.

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

Chiapparelli, E., Okano, I., Adl Amini, D. et al. The association between lumbar paraspinal muscle functional cross-sectional area on MRI and regional volumetric bone mineral density measured by quantitative computed tomography. Osteoporos Int 33, 2537–2545 (2022). https://doi.org/10.1007/s00198-022-06430-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-022-06430-x

Keywords

Search

Navigation