Abstract
Objectives
There are no established criteria for stiffness after fusionless surgery for neuromuscular scoliosis (NMS). As a result, there is no consensus regarding the surgical strategy to propose at long-term follow-up. This study reports the first use of shear wave elastography for assessing the mechanical response of lumbar intervertebral discs (IVDs) after fusionless bipolar fixation (FBF) for NMS and compares them with healthy controls. The aim was to acquire evidence from the stiffness of the spine following FBF.
Patients and methods
Nineteen NMS operated on with FBF (18 ± 2y at last follow-up, 6 ± 1 y after surgery) were included prospectively. Preoperative Cobb was 89 ± 20° and 35 ± 1° at latest follow-up. All patients had reached skeletal maturity. Eighteen healthy patients (20 ± 4 y) were also included. Shear wave speed (SWS) was measured in the annulus fibrosus of L3L4, L4L5 and L5S1 IVDs and compared between the two groups. A measurement reliability was performed.
Results
In healthy subjects, average SWS (all disc levels pooled) was 7.5 ± 2.6 m/s. In NMS patients, SWS was significantly higher at 9.9 ± 1.4 m/s (p < 0.05). Differences were significant between L3L4 (9.3 ± 1.8 m/s vs. 7.0 ± 2.5 m/s, p = 0.004) and L4L5 (10.3 ± 2.3 m/s vs. 7.1 ± 1.1 m/s, p = 0.0006). No difference was observed for L5S1 (p = 0.2). No correlation was found with age at surgery, Cobb angle correction and age at the SWE measurement.
Conclusions
This study shows a significant increase in disc stiffness at the end of growth for NMS patients treated by FBF. These findings are a useful adjunct to CT-scan in assessing stiffness of the spine allowing the avoidance of surgical final fusion at skeletal maturity.
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Data availability
The data are available for 2 years, on request to the corresponding author.
References
Skaggs DL, Akbarnia BA, Flynn JM, Myung KS, Sponseller PD, Vitale MG (2014) A classification of growth friendly spine implant. J Pediatr Orthop 34(3):260–274
Xu D, Ren Z, Chen X, Zhuang Q, Hui S, Sheng L, Li S (2017) The further exploration of hidden bloodloss in posterior lumbar fusion surgery. Orthop Traumatol Surg Res 103(4):527–530
Ramo BA, Roberts DW, Tuason D, McClung A, Paraison LE, MooreHG SDJ (2014) Surgical site infections after posterior spinal fusion for neuromuscular scoliosis: a thirty-year experience at a single institution. J Bone Joint Surg Am 96(24):2038–2048
Bouthors C, Gaume M, Glorion C, Miladi L (2019) Outcomes at skeletal maturity of a growing rod technique. About a homogeneous series of 34 early-onset of scoliosis. Spine 44(23):1630–1637
Miladi L, Gaume M, Khouri N, Johnson M, Topouchian V, Glorion C (2018) Minimally invasive surgery for neuromuscular scoliosis. Results and complications in a series of one hundred patients. Spine 43(16):E968–E975
Gaume M, Langlais T, Loiselet K, Pannier S, Skalli W, Vergari C, Miladi L (2023) Spontaneous induced bone fusion in minimally invasive fusionless bipolar fixation in neuromuscular scoliosis: a computed tomography analysis. Eur Spine J 32(7):2550–2557. https://doi.org/10.1007/s00586-023-07745
Creze M, Nordez A, Soubeyrand M, Rocher L, Maître X, Bellin MF (2018) Shear wave sonoelastography of skeletal muscle: basic principles, biomechanical concepts, clinical applications, and future perspectives. Skelet Radiol 47(4):457–471. https://doi.org/10.1007/s00256-017-2843-y
Gennisson JL, Deffieux T, Fink M, Tanter M (2013) Ultrasound elastography: principles and techniques. Diagn Interv Imaging 94:487–495. https://doi.org/10.1016/j.diii.2013.01.022
Eby SF, Song P, Chen S, Chen Q, Greenleaf JF, An KN (2013) Validation of shear wave elastography in skeletal muscle. J Biomech 46(14):2381–2387. https://doi.org/10.1016/j.jbiomech.2013.07.033
Langlais T, Vergari C, Pietton R, Dubousset J, Skalli W, Vialle R (2018) Shear wave elastography can evaluate annulus fibrosus alteration in adolescent scoliosis. Eur Radiol 28:2830–3283
De Reuver S, Moens AJ, Kruyt MC, Nievelstein RA, Ito K, Castelein RM (2022) Ultrasound shear wave elastography of the intervertebral disc and idiopathic scoliosis: a systematic review. Ultrasound Med Biol 48(5):721–729
Vergari C, Chanteux L, Pietton R, Langlais T, Vialle SW (2020) Shear wave elastography of lumbar annulus fibrosus in adolescent idiopathic scoliosis before and after surgical intervention. Eur Radiol 30(4):1980–1985
Vergari C, Dubois G, Vialle R et al (2015) Lumbar annulus fibrosus biomechanical characterization in healthy children by ultrasound shear wave elastography. Eur Radiol. https://doi.org/10.1007/s00330-015-3911-0
Romano A, Staber D, Grimm A, Kronlage C, Marquetand J (2021) Limitations of muscle ultrasound shear wave elastography for clinical routine-positioning and muscle selection. Sensors (Basel) 21(24):8490. https://doi.org/10.3390/s21248490
Vergari C, Rouch P, Dubois G, Bonneau D, Dubousset J, Tanter M, Gennisson JL, Skalli W (2014) Non-invasive biomechanical characterization of intervertebral discs by shear wave ultrasound elastography: a feasibility study. Eur Radiol 24(12):3210–3216. https://doi.org/10.1007/s00330-014-3382-8
Moreau B, Vergari C, Gad H, Sandoz B, Skalli W, Laporte S (2016) Non-invasive assessment of human multifidus muscle stiffness using ultrasound shear wave elastography: a feasibility study. Proc Inst Mech Eng H 230(8):809–814. https://doi.org/10.1177/0954411916656022
Poe-Kochert C, Shannon C, Pawelek JB, Thompson GH, Hardesty CK, Marks DS, Akbarnia BA, McCarthy RE, Emans JB (2016) Final fusion after growing-rod treatment for early onset scoliosis: is it final? J Bone Joint Surg Am 98(22):1913–1917
Gaume M, Vergari C, Khouri N, Skalli W, Glorion C, Miladi L (2021) Minimally invasive surgery for neuromuscular scoliosis: results and complications at a minimal follow-up of 5 years. Spine (Phila Pa 1976) 46(24):1696–1704
Gaume M, Persohn S, Vergari C, Glorion C, Skalli W, Miladi L (2020) Biomechanical cadaver study of proximal fixation in a minimally invasive bipolar construct. Spine Deform 8(1):33–38
Dubousset J, Gaume M, Miladi L (2021) Ilio-sacral screw pelvic fixation when correcting spinal deformities with or without pelvic obliquity: our experience over 40 years. Spine Deform 9(3):665–670
Harmon B, Wells M, Park D, Gao J (2019) Ultrasound elastography in neuromuscular and movement disorders. Clin Imaging 53:35–42
Lee SS, Gaebler-Spira D, Zhang LQ, Rymer WZ, Steele KM (2016) Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy. Clin Biomech (Bristol, Avon) 31:20–28. https://doi.org/10.1016/j.clinbiomech.2015.10.006
Langlais T, Desprairies P, Pietton R, Rohan PY, Dubousset J, Meakin JR, Winlove PC, Vialle R, Skalli W, Vergari C (2019) Microstructural characterization of annulus fibrosus by ultrasonography: a feasibility study with an in vivo and in vitro approach. Biomech Model Mechanobiol 18(6):1979–1986. https://doi.org/10.1007/s10237-019-01189-3
Deviren V, Berven S, Kleinstueck F, Antinnes J, Smith JA, Hu SS (2002) Predictors of flexibility and pain patterns in thoracolumbar and lumbar idiopathic scoliosis. Spine (Phila Pa 1976) 27(21):2346–2349. https://doi.org/10.1097/00007632-200211010-00007
Chen B, Liu C, Lin M, Deng W, Zhang Z (2021) Effects of body postures on the shear modulus of thoracolumbar fascia: a shear wave elastography study. Med Biol Eng Comput 59(2):383–390. https://doi.org/10.1007/s11517-021-02320-2
Sadeghi S, Quinlan K, Eilertson KE, Billy GG, Bible J, Sions M, Cortes D (2019) Changes in shear modulus of the lumbar multifidus muscle during different body positions. J Biomech Eng doi 10(1115/1):4043443
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Gaume, M., Loiselet, K., Chekir, H. et al. Evidence of spinal stiffening following fusionless bipolar fixation for neuromuscular scoliosis: a shear wave elastography assessment of lumbar annulus fibrosus. Eur Spine J 33, 1617–1623 (2024). https://doi.org/10.1007/s00586-023-08013-8
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DOI: https://doi.org/10.1007/s00586-023-08013-8