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Experimental Brain Research

, Volume 237, Issue 1, pp 121–135 | Cite as

Biomechanical parameters of the elbow stretch reflex in chronic hemiparetic stroke

  • Jacob G. McPherson
  • Arno H. A. Stienen
  • Brian D. Schmit
  • Julius P. A. DewaldEmail author
Research Article
  • 131 Downloads

Abstract

We sought to determine the relative velocity sensitivity of stretch reflex threshold angle and reflex stiffness during stretches of the paretic elbow joint in individuals with chronic hemiparetic stroke, and to provide guidelines to streamline spasticity assessments. We applied ramp-and-hold elbow extension perturbations ranging from 15 to 150°/s over the full range of motion in 13 individuals with hemiparesis. After accounting for the effects of passive mechanical resistance, we modeled velocity-dependent reflex threshold angle and torque–angle slope to determine their correlation with overall resistance to movement. Reflex stiffness exhibited substantially greater velocity sensitivity than threshold angle, accounting for ~ 74% (vs. ~ 15%) of the overall velocity-dependent increases in movement resistance. Reflex stiffness is a sensitive descriptor of the overall velocity-dependence of movement resistance in spasticity. Clinical spasticity assessments can be streamlined using torque–angle slope, a measure of reflex stiffness, as their primary outcome measure, particularly at stretch velocities greater than 100°/s.

Keywords

Spasticity Stretch reflex Movement resistance Joint torque Threshold angle Stroke 

Notes

Acknowledgements

National Institutes of Health (NIH) Grant: 5R01HD039343.

References

  1. Alibiglou L, Rymer WZ, Harvey RL, Mirbagheri MM (2008) The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke. J Neuroeng Rehabil 5:18.  https://doi.org/10.1186/1743-0003-5-18 CrossRefGoogle Scholar
  2. Ashworth B (1964) Preliminary trial of carisoprodol in multiple sclerosis. Practitioner 192:540–542Google Scholar
  3. Bakheit AM, Maynard VA, Curnow J, Hudson N, Kodapala S (2003) The relation between Ashworth scale scores and the excitability of the alpha motor neurones in patients with post-stroke muscle spasticity. J Neurol Neurosurg Psychiatry 74:646–648CrossRefGoogle Scholar
  4. Bennett DJ, Hollerbach JM, Xu Y, Hunter IW (1992) Time-varying stiffness of human elbow joint during cyclic voluntary movement. Exp Brain Res 88:433–442CrossRefGoogle Scholar
  5. Ben-Shabat E, Palit M, Fini NA, Brooks CT, Winter A, Holland AE (2013) Intra- and interrater reliability of the Modified Tardieu Scale for the assessment of lower limb spasticity in adults with neurologic injuries. Arch Phys Med Rehabil 94:2494–2501.  https://doi.org/10.1016/j.apmr.2013.06.026 CrossRefGoogle Scholar
  6. Bhadane MY, Gao F, Francisco GE, Zhou P, Li S (2015) Correlation of resting elbow angle with spasticity in chronic stroke. Survivors Front Neurol 6:183.  https://doi.org/10.3389/fneur.2015.00183 Google Scholar
  7. Blanchette AK, Mullick AA, Moin-Darbari K, Levin MF (2016) Tonic stretch reflex threshold as a measure of ankle plantar-flexor spasticity after. Stroke Phys Ther 96:687–695.  https://doi.org/10.2522/ptj.20140243 CrossRefGoogle Scholar
  8. Brunnstrom S (1966) Motor testing procedures in hemiplegia: based on sequential recovery stages. Phys Ther 46:357–375CrossRefGoogle Scholar
  9. Burne JA, Carleton VL, O’Dwyer NJ (2005) The spasticity paradox: movement disorder or disorder of resting limbs? J Neurol Neurosurg Psychiatry 76:47–54.  https://doi.org/10.1136/jnnp.2003.034785 CrossRefGoogle Scholar
  10. Calota A, Feldman AG, Levin MF (2008) Spasticity measurement based on tonic stretch reflex threshold in stroke using a portable device. Clin Neurophysiol 119:2329–2337.  https://doi.org/10.1016/j.clinph.2008.07.215 CrossRefGoogle Scholar
  11. Condliffe EG, Clark DJ, Patten C (2005) Reliability of elbow stretch reflex assessment in chronic post-stroke hemiparesis. Clin Neurophysiol 116:1870–1878.  https://doi.org/10.1016/j.clinph.2005.02.030 CrossRefGoogle Scholar
  12. de Vlugt E, van der Helm FC, Schouten AC, Brouwn GG (2001) Analysis of the reflexive feedback control loop during posture maintenance. Biol Cybern 84:133–141CrossRefGoogle Scholar
  13. de Vlugt E, de Groot JH, Schenkeveld KE, Arendzen JH, van der Helm FC, Meskers CG (2010) The relation between neuromechanical parameters and Ashworth score in stroke patients. J Neuroeng Rehabil 7:35.  https://doi.org/10.1186/1743-0003-7-35 CrossRefGoogle Scholar
  14. Dewald JP, Pope PS, Given JD, Buchanan TS, Rymer WZ (1995) Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. Brain J Neurol 118(Pt 2):495–510CrossRefGoogle Scholar
  15. Dewald JP, Given JD, Rymer WZ (1996) Long-lasting reductions of spasticity induced by skin electrical stimulation. IEEE Trans Rehabil Eng 4:231–242CrossRefGoogle Scholar
  16. Ellis MD, Sukal T, DeMott T, Dewald JP (2008) Augmenting clinical evaluation of hemiparetic arm movement with a laboratory-based quantitative measurement of kinematics as a function of limb loading. Neurorehabil Neural Repair 22:321–329.  https://doi.org/10.1177/1545968307313509 CrossRefGoogle Scholar
  17. Ellis MD, Schut I, Dewald JPA (2017) Flexion synergy overshadows flexor spasticity during reaching in chronic moderate to severe hemiparetic stroke. Clin Neurophysiol 128:1308–1314.  https://doi.org/10.1016/j.clinph.2017.04.028 CrossRefGoogle Scholar
  18. Feldman AG (1986) Once more on the equilibrium-point hypothesis (lambda model) for motor control. J Mot Behav 18:17–54CrossRefGoogle Scholar
  19. Fleuren JF, Voerman GE, Erren-Wolters CV, Snoek GJ, Rietman JS, Hermens HJ, Nene AV (2010) Stop using the Ashworth Scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry 81:46–52.  https://doi.org/10.1136/jnnp.2009.177071 CrossRefGoogle Scholar
  20. Forbes PA, Happee R, van der Helm FC, Schouten AC (2011) EMG feedback tasks reduce reflexive stiffness during force and position perturbations. Exp Brain Res 213:49–61.  https://doi.org/10.1007/s00221-011-2776-y CrossRefGoogle Scholar
  21. Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med 7:13–31Google Scholar
  22. Given JD, Dewald JP, Rymer WZ (1995) Joint dependent passive stiffness in paretic and contralateral limbs of spastic patients with hemiparetic stroke. J Neurol Neurosurg Psychiatr 59:271–279CrossRefGoogle Scholar
  23. Halaki M, O’Dwyer N, Cathers I (2006) Systematic nonlinear relations between displacement amplitude and joint mechanics at the human wrist. J Biomech 39:2171–2182.  https://doi.org/10.1016/j.jbiomech.2005.06.022 CrossRefGoogle Scholar
  24. Haugh AB, Pandyan AD, Johnson GR (2006) A systematic review of the Tardieu Scale for the measurement of spasticity. Disabil Rehabil 28:899–907.  https://doi.org/10.1080/09638280500404305 CrossRefGoogle Scholar
  25. Jin Y, Zhao Y (2018) Post-stroke upper limb spasticity incidence for different cerebral infarction. Site Open Med (Wars) 13:227–231.  https://doi.org/10.1515/med-2018-0035 CrossRefGoogle Scholar
  26. Kearney RE, Stein RB, Parameswaran L (1997) Identification of intrinsic and reflex contributions to human ankle stiffness dynamics. IEEE Trans Bio-med Eng 44:493–504.  https://doi.org/10.1109/10.581944 CrossRefGoogle Scholar
  27. Koo TK, Mak AF (2006) A neuromusculoskeletal model to simulate the constant angular velocity elbow extension test of spasticity. Med Eng Phys 28:60–69.  https://doi.org/10.1016/j.medengphy.2005.03.012 CrossRefGoogle Scholar
  28. Lambertz D, Goubel F, Kaspranski R, Perot C (2003) Influence of long-term spaceflight on neuromechanical properties of muscles in humans. J Appl Physiol 94:490–498.  https://doi.org/10.1152/japplphysiol.00666.2002 CrossRefGoogle Scholar
  29. Lance J (1980a) Pathophysiology of spasticity and clinical experience with baclofen. In: Feldman RGYR, Koella WP (eds) Spasticity: disordered motor control. Year Book Publishers, Chicago, pp 185–203Google Scholar
  30. Lance JW (1980b) The control of muscle tone, reflexes, and movement. Robert Wartenberg Lecture. Neurology 30:1303–1313CrossRefGoogle Scholar
  31. Li F, Wu Y, Li X (2014) Test–retest reliability and inter-rater reliability of the Modified Tardieu Scale and the Modified Ashworth Scale in hemiplegic patients with stroke. Eur J Phys Rehabil Med 50:9–15Google Scholar
  32. Lindberg PG, Gaverth J, Islam M, Fagergren A, Borg J, Forssberg H (2011) Validation of a new biomechanical model to measure muscle tone in spastic muscles. Neurorehabil Neural Repair 25:617–625.  https://doi.org/10.1177/1545968311403494 CrossRefGoogle Scholar
  33. Ludvig D, Visser TS, Giesbrecht H, Kearney RE (2011) Identification of time-varying intrinsic and reflex joint stiffness. IEEE Trans Bio-med Eng 58:1715–1723.  https://doi.org/10.1109/TBME.2011.2113184 CrossRefGoogle Scholar
  34. McPherson JG, Stienen AH, Drogos JM, Dewald JP (2011) The relationship between the flexion synergy and stretch reflexes in individuals with chronic hemiparetic stroke. IEEE Int Conf Rehabil Robot 2011:5975516.  https://doi.org/10.1109/ICORR.2011.5975516 Google Scholar
  35. McPherson LM, Negro F, Thompson CK, Sanchez L, Heckman CJ, Dewald J, Farina D (2016) Properties of the motor unit action potential shape in proximal and distal muscles of the upper limb in healthy and post-stroke individuals. Conf Proc IEEE Eng Med Biol Soc 2016:335–339.  https://doi.org/10.1109/EMBC.2016.7590708 Google Scholar
  36. McPherson JG, Stienen AH, Drogos JM, Dewald JP (2017) Modification of spastic stretch reflexes at the elbow by flexion synergy expression in individuals with chronic hemiparetic stroke. Arch Phys Med Rehabil.  https://doi.org/10.1016/j.apmr.2017.06.019 Google Scholar
  37. McPherson JG, Ellis MD, Harden RN, Carmona C, Drogos JM, Heckman CJ, Dewald J (2018a) Neuromodulatory inputs to motoneurons contribute to the loss of independent joint control in chronic moderate to severe hemiparetic stroke. Front Neurol.  https://doi.org/10.3389/fneur.2018.00470 Google Scholar
  38. McPherson JG, Stienen AH, Drogos JM, Dewald JP (2018b) Modification of spastic stretch reflexes at the elbow by flexion synergy expression in individuals with chronic hemiparetic stroke. Arch Phys Med Rehabil 99:491–500.  https://doi.org/10.1016/j.apmr.2017.06.019 CrossRefGoogle Scholar
  39. Miller LC, Thompson CK, Negro F, Heckman CJ, Farina D, Dewald JP (2014) High-density surface EMG decomposition allows for recording of motor unit discharge from proximal and distal flexion synergy muscles simultaneously in individuals with stroke. Conf Proc IEEE Eng Med Biol Soc 2014:5340–5344.  https://doi.org/10.1109/EMBC.2014.6944832 Google Scholar
  40. Mirbagheri MM, Niu X, Varoqui D (2012) Prediction of stroke motor recovery using reflex stiffness measures at one month. IEEE Trans Neural Syst Rehabil Eng 20:762–770.  https://doi.org/10.1109/TNSRE.2012.2205943 CrossRefGoogle Scholar
  41. Musampa NK, Mathieu PA, Levin MF (2007) Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity. Exp Brain Res 181:579–593.  https://doi.org/10.1007/s00221-007-0956-6 CrossRefGoogle Scholar
  42. Naghdi S, Ansari NN, Mansouri K, Olyaei GR, Asgari A, Kazemnejad A (2008) The correlation between Modified Ashworth Scale scores and the new index of alpha motoneurones excitability in post-stroke patients. Electromyogr Clin Neurophysiol 48:109–115Google Scholar
  43. Naghdi S, Ansari NN, Abolhasani H, Mansouri K, Ghotbi N, Hasson S (2014) Electrophysiological evaluation of the Modified Tardieu Scale (MTS) in assessing poststroke wrist flexor spasticity. NeuroRehabilitation 34:177–184  https://doi.org/10.3233/NRE-131016 Google Scholar
  44. Nelson CM, Murray WM, Dewald JPA (2018) Motor impairment-related alterations in biceps and triceps brachii fascicle lengths in chronic hemiparetic stroke. Neurorehabil Neural Repair.  https://doi.org/10.1177/1545968318792618 Google Scholar
  45. Perreault EJ, Crago PE, Kirsch RF (2000) Estimation of intrinsic and reflex contributions to muscle dynamics: a modeling study. IEEE Trans Bio Med Eng 47:1413–1421.  https://doi.org/10.1109/TBME.2000.880092 CrossRefGoogle Scholar
  46. Powers RK, Marder-Meyer J, Rymer WZ (1988) Quantitative relations between hypertonia and stretch reflex threshold in spastic hemiparesis. Ann Neurol 23:115–124.  https://doi.org/10.1002/ana.410230203 CrossRefGoogle Scholar
  47. Powers RK, Campbell DL, Rymer WZ (1989) Stretch reflex dynamics in spastic elbow flexor muscles. Ann Neurol 25:32–42.  https://doi.org/10.1002/ana.410250106 CrossRefGoogle Scholar
  48. Schmit BD, Rymer WZ (2001) Identification of static and dynamic components of reflex sensitivity in spastic elbow flexors using a muscle activation model. Ann Biomed Eng 29:330–339CrossRefGoogle Scholar
  49. Schmit BD, Dhaher Y, Dewald JP, Rymer WZ (1999) Reflex torque response to movement of the spastic elbow: theoretical analyses and implications for quantification of spasticity. Ann Biomed Eng 27:815–829CrossRefGoogle Scholar
  50. Schmit BD, Dewald JP, Rymer WZ (2000) Stretch reflex adaptation in elbow flexors during repeated passive movements in unilateral brain-injured patients. Arch Phys Med Rehabil 81:269–278CrossRefGoogle Scholar
  51. Sinkjaer T, Magnussen I (1994) Passive, intrinsic and reflex-mediated stiffness in the ankle extensors of hemiparetic patients. Brain J Neurol 117(Pt 2):355–363CrossRefGoogle Scholar
  52. Sommerfeld DK, Eek EU, Svensson AK, Holmqvist LW, von Arbin MH (2004) Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke 35:134–139.  https://doi.org/10.1161/01.STR.0000105386.05173.5E CrossRefGoogle Scholar
  53. Sommerfeld DK, Gripenstedt U, Welmer AK (2012) Spasticity after stroke: an overview of prevalence, test instruments, and treatments. Am J Phys Med Rehabil 91:814–820.  https://doi.org/10.1097/PHM.0b013e31825f13a3 CrossRefGoogle Scholar
  54. Sukal TM, Ellis MD, Dewald JP (2007) Shoulder abduction-induced reductions in reaching work area following hemiparetic stroke: neuroscientific implications. Exp Brain Res 183:215–223.  https://doi.org/10.1007/s00221-007-1029-6 CrossRefGoogle Scholar
  55. Tardieu G, Shentoub S, Delarue R (1954) Research on a technic for measurement of spasticity. Revue Neurologique 91:143–144Google Scholar
  56. Thilmann AF, Fellows SJ, Garms E (1991) The mechanism of spastic muscle hypertonus. Variation in reflex gain over the time course of spasticity. Brain J Neurol 114(Pt 1A):233–244Google Scholar
  57. Velozo CA, Woodbury ML (2011) Translating measurement findings into rehabilitation practice: an example using Fugl-Meyer assessment-upper extremity with patients following stroke. J Rehabil Res Dev 48:1211–1222CrossRefGoogle Scholar
  58. Zhang LQ, Rymer WZ (1997) Simultaneous and nonlinear identification of mechanical and reflex properties of human elbow joint muscles. IEEE Trans Bio-med Eng 44:1192–1209.  https://doi.org/10.1109/10.649991 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jacob G. McPherson
    • 1
  • Arno H. A. Stienen
    • 2
  • Brian D. Schmit
    • 3
  • Julius P. A. Dewald
    • 2
    Email author
  1. 1.Department of Biomedical EngineeringFlorida International UniversityMiamiUSA
  2. 2.Department of Physical Therapy and Human Movement Sciences, Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  3. 3.Department of Biomedical EngineeringMarquette UniversityMilwaukeeUSA

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