European Spine Journal

, Volume 25, Issue 9, pp 2929–2937 | Cite as

Role of muscle damage on loading at the level adjacent to a lumbar spine fusion: a biomechanical analysis

  • Masoud Malakoutian
  • John Street
  • Hans-Joachim Wilke
  • Ian Stavness
  • Marcel Dvorak
  • Sidney Fels
  • Thomas OxlandEmail author
Original Article



It is well established that posterior spinal surgery results in damage to the paraspinal musculature. The effects of such iatrogenic changes on spinal loading have not been previously investigated, particularly at levels adjacent to a spinal fusion. Therefore, the objective of this study was to investigate the effect of simulated muscle damage on post-operative spinal loading at the adjacent levels to a spinal fusion during upright postures using a mathematical model.


A musculoskeletal model of the spine using ArtiSynth with 210 muscle fascicles was used to predict spinal loading in an upright posture. The loading at L1–L2 and L5–S1 were estimated before and after simulated paraspinal muscle damage (i.e., removal of muscle attachments at L2–L5) along the lumbar spine, both with a spinal fusion at L2–L5 and without a spinal fusion.


The axial compressive forces at the adjacent levels increased after simulated muscle damage, with the largest changes being at the rostral level (78 % increase in presence of spinal fusion; 73 % increase without spinal fusion) compared to the caudal level (41 % in presence of fusion and 32 % without fusion). Shear forces increased in a similar manner at both the rostral and caudal levels. These changes in loading were due to a redistribution of muscle activity from the local lumbar to the global spinal musculature.


The results suggest that the paraspinal muscles of the lumbar spine play an important role in adjacent segment loading of a spinal fusion, independent of the presence of rigid spinal instrumentation.


Muscle damage Adjacent segment degeneration Lumbar spine  Biomechanics Musculoskeletal model ArtiSynth 



The authors gratefully acknowledge financial support from the Natural Sciences and Engineering Research Council of Canada (NSERC).

Compliance with ethical standards

Conflict of interest



  1. 1.
    Park P, Garton HJ, Gala VC et al (2004) Adjacent segment disease after lumbar or lumbosacral fusion: review of the literature. Spine (Phila Pa 1976) 29:1938–1944CrossRefGoogle Scholar
  2. 2.
    Wai EK, Santos ERG, Morcom RA, Fraser RD (2006) Magnetic resonance imaging 20 years after anterior lumbar interbody fusion. Spine (Phila Pa 1976) 31:1952–1956CrossRefGoogle Scholar
  3. 3.
    Axelsson P, Johnsson R, Strömqvist B (2007) Adjacent segment hypermobility after lumbar spine fusion after surgery. Acta Orthop 78:834–839. doi: 10.1080/17453670710014635 CrossRefPubMedGoogle Scholar
  4. 4.
    Seitsalo S, Schlenzka D (1997) Disc degeneration in young patients with isthmic spondylolisthesis treated operatively or conservatively: a long-term follow-up. Eur Spine J 6:393–397CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Korovessis P, Repantis T, Zacharatos S, Zafiropoulos A (2009) Does Wallis implant reduce adjacent segment degeneration above lumbosacral instrumented fusion? Eur Spine J 18:830–840. doi: 10.1007/s00586-009-0976-y CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Kaito T, Hosono N, Mukai Y et al (2010) Induction of early degeneration of the adjacent segment after posterior lumbar interbody fusion by excessive distraction of lumbar disc space. J Neurosurg Spine 12:671–679. doi: 10.3171/2009.12.SPINE08823 CrossRefPubMedGoogle Scholar
  7. 7.
    Mannion AF, Leivseth G, Brox J-I, et al. (2014) Long-term follow up suggests spinal fusion is associated with increased adjacent segment disc degeneration but without influence on clinical outcome: results of a combined follow-up from 4 RCTs. Spine (Phila. Pa. 1976) 39:1373–83. doi: 10.1097/BRS.0000000000000437
  8. 8.
    Lotz JC, Chin JR (2000) Intervertebral disc cell death is dependent on the magnitude and duration of spinal loading. Spine (Phila Pa 1976) 25:1477–1483CrossRefGoogle Scholar
  9. 9.
    Stokes IAF, Iatridis JC (2004) Mechanical conditions that accelerate intervertebral disc degeneration: overload versus immobilization. Spine (Phila Pa 1976) 29:2724–2732CrossRefGoogle Scholar
  10. 10.
    Walter BA, Korecki CL, Purmessur D et al (2011) Complex loading affects intervertebral disc mechanics and biology. Osteoarthr Cartil 19:1011–1018CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Chan SCW, Ferguson SJ, Gantenbein-Ritter B (2011) The effects of dynamic loading on the intervertebral disc. Eur Spine J 20:1796–1812CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Kim J, Yang S-J, Kim H et al (2012) Effect of shear force on intervertebral disc (IVD) degeneration: an in vivo rat study. Ann Biomed Eng 40:1996–2004CrossRefPubMedGoogle Scholar
  13. 13.
    Hodges PW, Richardson CA (1996) Inefficient muscular stabilization of the lumbar spine associated with low back pain: a motor control evaluation of transversus abdominis. Spine (Phila Pa 1976) 21:2640–2650CrossRefGoogle Scholar
  14. 14.
    Cholewicki J, Silfies SP, Shah RA et al (2005) Delayed trunk muscle reflex responses increase the risk of low back injuries. Spine (Phila Pa 1976) 30:2614–2620CrossRefGoogle Scholar
  15. 15.
    Lee AS, Cholewicki J, Reeves NP et al (2010) Comparison of trunk proprioception between patients with low back pain and healthy controls. Arch Phys Med Rehabil 91:1327–1331CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Tsao H, Tucker KJ, Hodges PW (2011) Changes in excitability of corticomotor inputs to the trunk muscles during experimentally-induced acute low back pain. Neuroscience 181:127–133CrossRefPubMedGoogle Scholar
  17. 17.
    Haig AJ, London Z, Sandella DE (2013) Symmetry of paraspinal muscle denervation in clinical lumbar spinal stenosis: support for a hypothesis of posterior primary ramus stretching? Muscle Nerve 48:198–203CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Leinonen V, Määttä S, Taimela S et al (2003) Paraspinal muscle denervation, paradoxically good lumbar endurance, and an abnormal flexion–extension cycle in lumbar spinal stenosis. Spine (Phila Pa 1976) 28:324–331Google Scholar
  19. 19.
    Wang G, Karki SB, Xu S et al (2014) Quantitative MRI and X-ray analysis of disc degeneration and paraspinal muscle changes in degenerative spondylolisthesis. J Back Musculoskelet Rehabil. doi: 10.3233/BMR-140515 Google Scholar
  20. 20.
    Gejo R, Matsui H, Kawaguchi Y et al (1999) Serial changes in trunk muscle performance after posterior lumbar surgery. Spine (Phila Pa 1976) 24:1023–1028CrossRefGoogle Scholar
  21. 21.
    Kawaguchi Y, Matsui H, Gejo R, Tsuji H (1998) Preventive measures of back muscle injury after posterior lumbar spine surgery in rats. Spine (Phila Pa 1976) 23:2282–2287CrossRefGoogle Scholar
  22. 22.
    Kawaguchi Y, Matsui H, Tsuji H (1996) Back muscle injury after posterior lumbar spine surgery: a histologic and enzymatic analysis. Spine (Phila Pa 1976) 21:941–944CrossRefGoogle Scholar
  23. 23.
    Cawley DT, Alexander M, Morris S (2014) Multifidus innervation and muscle assessment post-spinal surgery. Eur Spine J 23:320–327CrossRefPubMedGoogle Scholar
  24. 24.
    Keller A, Gunderson R, Reikerås O, Brox JI (2003) Reliability of computed tomography measurements of paraspinal muscle cross-sectional area and density in patients with chronic low back pain. Spine (Phila Pa 1976) 28:1455–1460. doi: 10.1097/01.BRS.0000067094.55003.AD Google Scholar
  25. 25.
    Keller A, Brox JI, Gunderson R et al (2003) Trunk muscle strength, cross-sectional area, and density in patients with chronic low back pain randomized to lumbar fusion or cognitive intervention and exercises. Spine (Phila Pa 1976) 29:3–8CrossRefGoogle Scholar
  26. 26.
    Wang H-L, Lu F-Z, Jiang J-Y et al (2011) Minimally invasive lumbar interbody fusion via MAST Quadrant retractor versus open surgery: a prospective randomized clinical trial. Chin Med J-Beijing 124:3868Google Scholar
  27. 27.
    Kramer M, Katzmaier P, Eisele R et al (2001) Surface electromyography-verified muscular damage associated with the open dorsal approach to the lumbar spine. Eur Spine J 10:414–420CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Kim D-Y, Lee S-H, Chung SK, Lee H-Y (2004) Comparison of multifidus muscle atrophy and trunk extension muscle strength: percutaneous versus open pedicle screw fixation. Spine (Phila Pa 1976) 30:123–129CrossRefGoogle Scholar
  29. 29.
    Mayer TG, Vanharanta H, Gatchel RJ et al (1989) Comparison of CT scan muscle measurements and isokinetic trunk strength in postoperative patients. Spine (Phila Pa 1976) 14:33–36CrossRefGoogle Scholar
  30. 30.
    Panjabi MM (2007) Hybrid multidirectional test method to evaluate spinal adjacent-level effects. Clin Biomech (Bristol, Avon) 22:257–265. doi: 10.1016/j.clinbiomech.2006.08.006 CrossRefGoogle Scholar
  31. 31.
    Malakoutian M, Volkheimer D, Street J et al (2015) Do in vivo kinematic studies provide insight into adjacent segment degeneration?—a qualitative systematic literature review. Eur Spine J 24:1865–1881CrossRefPubMedGoogle Scholar
  32. 32.
    Anderst WJ, Donaldson WF, Lee JY, Kang JD (2013) Cervical spine intervertebral kinematics with respect to the head are different during flexion and extension motions. J Biomech 46:1471–1475CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Volkheimer D, Malakoutian M, Oxland TR, Wilke H-J (2015) Limitations of current in vitro test protocols for investigation of instrumented adjacent segment biomechanics: critical analysis of the literature. Eur J Spine 24:1882–1892CrossRefGoogle Scholar
  34. 34.
    Weinhoffer SL, Guyer RD, Herbert M, Griffith SL (1995) Intradiscal pressure measurements above an instrumented fusion: a cadaveric study. Spine (Phila Pa 1976) 20:526–531CrossRefGoogle Scholar
  35. 35.
    Chow DHK, Luk KDK, Evans JH, Leong JCY (1996) Effects of short anterior lumbar interbody fusion on biomechanics of neighboring unfused segments. Spine (Phila Pa 1976) 21:549–555CrossRefGoogle Scholar
  36. 36.
    Cunningham BW, Kotani Y, McNulty PS et al (1997) The effect of spinal destabilization and instrumentation on lumbar intradiscal pressure: an in vitro biomechanical analysis. Spine (Phila Pa 1976) 22:2655–2663CrossRefGoogle Scholar
  37. 37.
    Pfeiffer M, Hoffman H, Goel VK et al (1997) In vitro testing of a new transpedicular stabilization technique. Eur Spine J 6:249–255CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Bastian L, Lange U, Knop C et al (2001) Evaluation of the mobility of adjacent segments after posterior thoracolumbar fixation: a biomechanical study. Eur Spine J 10:295–300CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Schmoelz W, Huber JF, Nydegger T et al (2003) Dynamic stabilization of the lumbar spine and its effects on adjacent segments: an in vitro experiment. J Spinal Disord Tech 16:418–423CrossRefPubMedGoogle Scholar
  40. 40.
    Moore J, Yoganandan N, Pintar FA et al (2006) Tapered cages in anterior lumbar interbody fusion: biomechanics of segmental reactions. J Neurosurg Spine 5:330–335CrossRefPubMedGoogle Scholar
  41. 41.
    Schmoelz W, Huber JF, Nydegger T et al (2006) Influence of a dynamic stabilisation system on load bearing of a bridged disc: an in vitro study of intradiscal pressure. Eur Spine J 15:1276–1285CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    McGill SM, Norman RW (1986) Partitioning of the L4–L5 dynamic moment into disc, ligamentous, and muscular components during lifting. Spine (Phila Pa 1976) 11:666–678CrossRefGoogle Scholar
  43. 43.
    Stokes IAF, Gardner-Morse M (1995) Lumbar spine maximum efforts and muscle recruitment patterns predicted by a model with multijoint muscles and joints with stiffness. J Biomech 28:173–186CrossRefPubMedGoogle Scholar
  44. 44.
    Arjmand N, Shirazi-Adl A (2006) Model and in vivo studies on human trunk load partitioning and stability in isometric forward flexions. J Biomech 39:510–521. doi: 10.1016/j.jbiomech.2004.11.030 CrossRefPubMedGoogle Scholar
  45. 45.
    de Zee M, Hansen L, Wong C et al (2007) A generic detailed rigid-body lumbar spine model. J Biomech 40:1219–1227. doi: 10.1016/j.jbiomech.2006.05.030 CrossRefPubMedGoogle Scholar
  46. 46.
    Christophy M, Faruk Senan NA, Lotz JC, O’Reilly OM (2012) A musculoskeletal model for the lumbar spine. Biomech Model Mechanobiol 11:19–34. doi: 10.1007/s10237-011-0290-6 CrossRefPubMedGoogle Scholar
  47. 47.
    Han K-S, Zander T, Taylor WR, Rohlmann A (2012) An enhanced and validated generic thoraco-lumbar spine model for prediction of muscle forces. Med Eng Phys 34:709–716. doi: 10.1016/j.medengphy.2011.09.014 CrossRefPubMedGoogle Scholar
  48. 48.
    Bresnahan L, Fessler RG, Natarajan RN (2010) Evaluation of change in muscle activity as a result of posterior lumbar spine surgery using a dynamic modeling system. Spine (Phila Pa 1976) 35:E761–E767. doi: 10.1097/BRS.0b013e3181e45a6e CrossRefGoogle Scholar
  49. 49.
    Malakoutian M, Street J, Wilke H-J et al (2015) A musculoskeletal model of the lumbar spine using ArtiSynth—development and validation. Comput Methods Biomech Biomed Eng Imag Vis 1–8. doi: 10.1080/21681163.2016.1187087
  50. 50.
    Lloyd JE, Stavness I, Fels S (2012) ArtiSynth: A fast interactive biomechanical modeling toolkit combining multibody and finite element simulation. In: Soft Tissue Biomechanical Modeling for Computer Assisted Surgery. Springer, pp 355–394. doi: 10.1007/8415_2012_126
  51. 51.
    Stavness I, Lloyd JE, Payan Y, Fels S (2011) Coupled hard–soft tissue simulation with contact and constraints applied to jaw–tongue–hyoid dynamics. Int J Numer Method Biomed Eng 27:367–390CrossRefGoogle Scholar
  52. 52.
    Stavness I, Lloyd JE, Fels S (2012) Automatic prediction of tongue muscle activations using a finite element model. J Biomech 45:2841–2848CrossRefPubMedGoogle Scholar
  53. 53.
    Dao TT, Pouletaut P, Charleux F Lazáry Á, Eltes P, Varga PP, Tho MC (2014) Estimation of patient specific lumbar spine muscle forces using multi-physical musculoskeletal model and dynamic MRI. In: Huynh VN, Denoeux T, Tran DH, Le AC, Pham SB (eds) Knowledge and Systems Engineering vol. 2, Advances in Intelligent Systems and Computing. Springer International Publishing, Cham, pp 411–422. doi: 10.1007/978-3-319-02821-7_36
  54. 54.
    Panjabi MM, Brand RA Jr, White AA III (1976) Three-dimensional flexibility and stiffness properties of the human thoracic spine. J Biomech 9:185–192CrossRefPubMedGoogle Scholar
  55. 55.
    Heuer F, Schmidt H, Klezl Z et al (2007) Stepwise reduction of functional spinal structures increase range of motion and change lordosis angle. J Biomech 40:271–280CrossRefPubMedGoogle Scholar
  56. 56.
    Gardner-Morse MG, Stokes IA (2004) Structural behavior of human lumbar spinal motion segments. J Biomech 37:205–212. doi: 10.1016/j.jbiomech.2003.10.003 CrossRefPubMedGoogle Scholar
  57. 57.
    Millard M, Uchida T, Seth A, Delp SL (2013) Flexing computational muscle: modeling and simulation of musculotendon dynamics. J Biomech Eng 135:21005CrossRefGoogle Scholar
  58. 58.
    Cobb WS, Burns JM, Kercher KW et al (2005) Normal intraabdominal pressure in healthy adults. J Surg Res 129:231–235CrossRefPubMedGoogle Scholar
  59. 59.
    Stavness IK (2010) Byte your tongue. PhD dissertation, University of British Columbia Google Scholar
  60. 60.
    Wilke H-J, Neef P, Hinz B et al (2001) Intradiscal pressure together with anthropometric data—a data set for the validation of models. Clin Biomech 16:S111–S126CrossRefGoogle Scholar
  61. 61.
    Poh S-Y, Yue W-M, Chen JL-T et al (2011) Two-year outcomes of transforaminal lumbar interbody fusion. J Orthop Surg 19:135–140Google Scholar
  62. 62.
    Min J-H, Jang J-S, Lee S-H (2007) Comparison of anterior-and posterior-approach instrumented lumbar interbody fusion for spondylolisthesis. J Neurosurg Spine 7(1):21–26CrossRefPubMedGoogle Scholar
  63. 63.
    Chou W-Y, Hsu C-J, Chang W-N, Wong C-Y (2002) Adjacent segment degeneration after lumbar spinal posterolateral fusion with instrumentation in elderly patients. Arch Orthop Trauma Surg 122:39–43CrossRefPubMedGoogle Scholar
  64. 64.
    Yee TJ, Terman SW, La Marca F, Park P (2014) Comparison of adjacent segment disease after minimally invasive or open transforaminal lumbar interbody fusion. J Clin Neurosci Off J Neurosurg Soc Australas 21(10):1796–1801Google Scholar
  65. 65.
    Kim H-J, Moon S-H, Chun H-J et al (2009) Comparison of mechanical motion profiles following instrumented fusion and non-instrumented fusion at the L4–5 segment. Clin Invest Med 32:E64–E69PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Masoud Malakoutian
    • 1
  • John Street
    • 2
  • Hans-Joachim Wilke
    • 3
  • Ian Stavness
    • 4
  • Marcel Dvorak
    • 2
  • Sidney Fels
    • 5
  • Thomas Oxland
    • 1
    • 2
    Email author
  1. 1.Department of Mechanical EngineeringUniversity of British ColumbiaVancouverCanada
  2. 2.Department of OrthopaedicsUniversity of British ColumbiaVancouverCanada
  3. 3.Institute of Orthopaedic Research and Biomechanics, Center of Musculoskeletal ResearchUniversity of UlmUlmGermany
  4. 4.Department of Computer ScienceUniversity of SaskatchewanSaskatoonCanada
  5. 5.Department of Electrical and Computer EngineeringUniversity of British ColumbiaVancouverCanada

Personalised recommendations