Abstract
Study design
This is a cross-sectional descriptive study.
Objectives
To quantify differences in hand muscle morphology between persons with cervical spinal cord injury (SCI) and uninjured adults.
Setting
The study was performed at the Guangdong Work Injury Rehabilitation Hospital.
Methods
We quantified hand muscle cross-sectional area (CSA), thickness, and echo intensity (EI) in 18 persons with subacute to chronic SCI and 23 controls using ultrasound imaging.
Results
Mean SCI abductor pollicis brevis (APB), abductor digiti minimi (ADM), and first dorsal interosseous (FDI) CSA were ~26%, 43%, and 37% smaller than the control means, the deficit in the APB being less than the ADM (P < 0.05). Muscle thickness was also smaller after SCI, but deficits in ADM (31%) and FDI (20%) thickness were less than the CSA deficits (P < 0.05). In five SCI persons, APB CSA and/or opponens pollicis (OP) thickness were normal despite complete motor paralysis. Mean longitudinal image EI was 40% higher in the OP and 15% higher in the flexor pollicis brevis (FPB) after SCI (P < 0.05), suggesting denervation-induced infiltration of fat and fibrous tissues. OP EI was related to OP thickness (r = −0.6, P = 0.007, n = 18). Mean axial image EI was 10% higher in the APB and ADM after SCI (P < 0.05). There were no significant correlations between muscle morphological properties and clinical features in the SCI participants.
Conclusion
Our results indicate significant SCI atrophy and elevated EI that are muscle dependent.
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Data availability
The individual data that support the findings of this study are included in the published article and its Supplementary information file.
References
Gupta S, Michelsen-Jost H. Anatomy and function of the thenar muscles. Hand Clin. 2012;28:1–7.
Pasquella JA, Levine P. Anatomy and function of the hypothenar muscles. Hand Clin. 2012;28:19–25.
Lee SK, Wisser JR. Restoration of pinch in intrinsic muscles of the hand. Hand Clin. 2012;28:45–51.
Curt A, Dietz V. Neurographic assessment of intramedullary motoneurone lesions in cervical spinal cord injury: consequences for hand function. Spinal Cord. 1996;34:326–32.
Harvey LA, Batty J, Jones R, Crosbie J. Hand function of C6 and C7 tetraplegics 1–16 years following injury. Spinal Cord. 2001;39:37–43.
Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2004;21:1371–83.
Kern H, Boncompagni S, Rossini K, Mayr W, Fanò G, Zanin ME, et al. Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus, which is reversible by functional electrical stimulation (FES): a role for myofiber regeneration? J Neuropathol Exp Neurol. 2004;63:919–31.
Panisset MG, Galea MP, El-Ansary D. Does early exercise attenuate muscle atrophy or bone loss after spinal cord injury? Spinal Cord. 2016;54:84–92.
Peckham PH, Keith MW, Kilgore KL, Grill JH, Wuolle KS, Thrope GB, et al. Efficacy of an implanted neuroprosthesis for restoring hand grasp in tetraplegia: a multicenter study. Arch Phys Med Rehabil. 2001;82:1380–8.
Berman SA, Young RR, Sarkarati M, Shefner JM. Injury zone denervation in traumatic quadriplegia in humans. Muscle Nerve. 1996;19:701–6.
Brandstater ME, Dinsdale SM. Electrophysiological studies in the assessment of spinal cord lesions. Arch Phys Med Rehabil. 1976;57:70–4.
Gorman PH, Kikta DG, Peckham PH. Neurophysiologic evaluation of lower motor neuron damage in tetraplegia. Muscle Nerve. 1998;21:1321–3.
Li L, Li X, Liu J, Zhou P. Alterations in multidimensional motor unit number index of hand muscles after incomplete cervical spinal cord injury. Front Hum Neurosci. 2015;9:238.
Peckham PH, Mortimer JT, Marsolais EB. Upper and lower motor neuron lesions in the upper extremity muscles of tetraplegics. Paraplegia. 1976;14:115–21.
Yang JF, Stein RB, Jhamandas J, Gordon T. Motor unit numbers and contractile properties after spinal cord injury. Ann Neurol. 1990;28:496–502.
Grumbles RM, Thomas CK. Motoneuron death after human spinal cord injury. J Neurotrauma. 2017;34:581–90.
Stilwill EW, Sahgal V. Histochemical and morphologic changes in skeletal muscle following cervical cord injury: a study of upper and lower motor neuron lesions. Arch Phys Med Rehabil. 1977;58:201–6.
Miller J, Gollee H, Purcell M. Ultrasound imaging as a diagnostic tool to assess the functional status of muscles after a spinal cord injury. Ultrasound Med Biol. 2021;47:386–97.
Mohseny B, Nijhuis TH, Hundepool CA, Janssen WG, Selles RW, Coert JH. Ultrasonographic quantification of intrinsic hand muscle cross-sectional area; reliability and validity for predicting muscle strength. Arch Phys Med Rehabil. 2015;96:845–53.
Simon NG, Ralph JW, Lomen-Hoerth C, Poncelet AN, Vucic S, Kiernan MC, et al. Quantitative ultrasound of denervated hand muscles. Muscle Nerve. 2015;52:221–30.
Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR. Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol. 1996;80:158–65.
Palakshappa JA, Reilly JP, Schweickert WD, Anderson BJ, Khoury V, Shashaty MG, et al. Quantitative peripheral muscle ultrasound in sepsis: Muscle area superior to thickness. J Crit Care. 2018;47:324–30.
Pillen S, Tak RO, Zwarts MJ, Lammens MM, Verrijp KN, Arts IM, et al. Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol. 2009;35:443–6.
Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE. Skeletal muscle sonography: a correlative study of echogenicity and morphology. J Ultrasound Med. 1993;12:73–7.
Ríos-Díaz J, Del Baño-Aledo ME. Quantitative neuromuscular ultrasound analysis as biomarkers in amyotrophic lateral sclerosis. Eur Radio. 2019;29:4266–75.
Gunreben G, Bogdahn U. Real-time sonography of acute and chronic muscle denervation. Muscle Nerve. 1991;14:654–64.
Schwennicke A, Bargfrede M, Reimers CD. Clinical, electromyographic, and ultrasonographic assessment of focal neuropathies. J Neuroimaging. 1998;8:136–43.
Thomas CK. Contractile properties of human thenar muscles paralyzed by spinal cord injury. Muscle Nerve. 1997;20:788–99.
Castro MJ, Apple DF Jr., Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol. 1999;80:373–8.
Malisoux L, Jamart C, Delplace K, Nielens H, Francaux M, Theisen D. Effect of long-term muscle paralysis on human single fiber mechanics. J Appl Physiol. 2007;102:340–9.
Bae JS, Sawai S, Misawa S, Kanai K, Isose S, Kuwabara S. Differences in excitability properties of FDI and ADM motor axons. Muscle Nerve. 2009;39:350–4.
Johnson MA, Polgar J, Weightman D, Appleton D. Data on the distribution of fibre types in thirty-six human muscles. Autops study J Neurol Sci. 1973;18:111–29.
Castro MJ, Apple DF Jr., Staron RS, Campos GE, Dudley GA. Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol. 1999;86:350–8.
Zijdewind I, Thomas CK. Spontaneous motor unit behavior in human thenar muscles after spinal cord injury. Muscle Nerve. 2001;24:952–62.
Catz A, Itzkovich M, Tesio L, Biering-Sorensen F, Weeks C, Laramee MT, et al. A multicenter international study on the Spinal Cord Independence Measure, version III: Rasch psychometric validation. Spinal Cord. 2007;45:275–91.
Misirlioglu TO, Ozyemisci Taskiran O. Reliability of sonographic muscle thickness measurements of the thenar and hypothenar muscles. Muscle Nerve. 2018;57:E14–E17.
Jacobson MD, Raab R, Fazeli BM, Abrams RA, Botte MJ, Lieber RL. Architectural design of the human intrinsic hand muscles. J Hand Surg Am. 1992;17:804–9.
Abraham A, Drory VE, Fainmesser Y, Lovblom LE, Bril V. Quantitative sonographic evaluation of muscle thickness and fasciculation prevalence in healthy subjects. Muscle Nerve. 2020;61:234–8.
Close PJ, Stokes MJ, L’Estrange PR, Rowell J. Ultrasonography of masseter muscle size in normal young adults. J Oral Rehabil. 1995;22:129–34.
Abraham A, Fainmesser Y, Drory VE, Bril V. Split-hand phenomenon in motor neuron diseases: sonographic assesment of muscle thickness. Clin Neurophysiol. 2020;131:1721–5.
Edgerton VR, Roy RR, Allen DL, Monti RJ. Adaptations in skeletal muscle disuse or decreased-use atrophy. Am J Phys Med Rehabil. 2002;81:S127–47.
Gordon T, Tyreman N. Sprouting capacity of lumbar motoneurons in normal and hemisected spinal cords of the rat. J Physiol. 2010;588:2745–68.
Kern H, Hofer C, Mödlin M, Mayr W, Vindigni V, Zampieri S, et al. Stable muscle atrophy in long-term paraplegics with complete upper motor neuron lesion from 3- to 20-year SCI. Spinal Cord. 2008;46:293–304.
Krasilovsky G. Nerve conduction studies in patients with cervical spinal cord injuries. Arch Phys Med Rehabil. 1980;61:204–9.
Kern H, Carraro U, Adami N, Biral D, Hofer C, Forstner C, et al. Home-based functional electrical stimulation rescues permanently denervated muscles in paraplegic patients with complete lower motor neuron lesion. Neurorehabil Neural Repair. 2010;24:709–21.
Abraham A, Drory VE, Fainmesser Y, Algom AA, Lovblom LE, Bril V. Muscle thickness measured by ultrasound is reduced in neuromuscular disorders and correlates with clinical and electrophysiological findings. Muscle Nerve. 2019;60:687–92.
Aisen ML, Brown W, Rubin M. Electrophysiologic changes in lumbar spinal cord after cervical cord injury. Neurology. 1992;42:623–6.
Needham-Shropshire BM, Klose KJ, Tucker ME, Thomas CK. Manual muscle test score and force comparisons after cervical spinal cord injury. J Spinal Cord Med. 1997;20:324–30.
Popovic MR, Thrasher TA, Adams ME, Takes V, Zivanovic V, Tonack MI. Functional electrical therapy: retraining grasping in spinal cord injury. Spinal Cord. 2006;44:143–51.
Funding
This study was supported by the Guangzhou Science and Technology Program (Grant nos 201904010256 and 201704030039).
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CSK, HL, CNZ, and XY conceived the idea of the study and contributed to the writing of the protocol. HL, CSK, and CNZ acquired and analyzed the data; HL and XY recruited the participants. XY provided all medical support. CSK wrote the first version of the manuscript. All authors read and contributed to the final version of the paper.
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Klein, C.S., Liu, H., Zhao, C.N. et al. Quantitative ultrasound imaging of intrinsic hand muscles after traumatic cervical spinal cord injury. Spinal Cord 60, 199–209 (2022). https://doi.org/10.1038/s41393-021-00653-1
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DOI: https://doi.org/10.1038/s41393-021-00653-1


