Pendulum test in chronic hemiplegic stroke population: additional ambulatory information beyond spasticity

Yin-Kai Dean Huang, Wei Li, Yi-Lin Chou, Erica Shih-Wei Hung, Jiunn-Horng Kang, Yin-Kai Dean Huang, Wei Li, Yi-Lin Chou, Erica Shih-Wei Hung, Jiunn-Horng Kang

Abstract

Spasticity measured by manual tests, such as modified Ashworth scale (MAS), may not sufficiently reflect mobility function in stroke survivors. This study aims to identify additional ambulatory information provided by the pendulum test. Clinical assessments including Brünnstrom recovery stage, manual muscle test, MAS, Tinetti test (TT), Timed up and go test, 10-m walk test (10-MWT), and Barthel index were applied to 40 ambulant chronic stroke patients. The pendular parameters, first swing excursion (FSE) and relaxation index (RI), were extracted by an electrogoniometer. The correlations among these variables were analyzed by the Spearman and Pearson partial correlation tests. After controlling the factor of motor recovery (Brünnstrom recovery stage), the MAS of paretic knee extensor was negatively correlated with the gait score of TT (r = - 0.355, p = 0.027), while the FSE revealed positive correlations to the balance score of TT (r = 0.378, p = 0.018). RI were associated with the comfortable speed of 10-MWT (r = 0.367, p = 0.022). These results suggest a decrease of knee extensor spasticity links to a better gait and balance in chronic stroke patients. The pendular parameters can provide additional ambulatory information, as complementary to the MAS. The pendulum test can be a potential tool for patient selection and outcome assessment after spasticity treatments in chronic stroke population.

Conflict of interest statement

The authors declare no competing interests.

© 2021. The Author(s).

Figures

Figure 1
Figure 1
Setting of pendulum test. (A) Starting position: the leg was raised at the horizon of maximal knee extension with the subject in supine position. (B) Swing phase: after the leg totally relaxed, the heel is released and allowed to oscillate by the influence of gravity. (C) Resting position: when the oscillation stopped without visible movement, the difference of knee angle between the starting and resting position was measured as the resting angle (RA).
Figure 2
Figure 2
Oscillation of knee angle. A knee reaches the angle of first swing excursion (FSE) at time S1 and ended at the resting angle (RA) after several periods of oscillation. R2 is the angle of first extensive excursion. S1 is the duration of knee from the starting position to FSE.

References

    1. Lance JW. What is spasticity? Lancet. 1990;335:606. doi: 10.1016/0140-6736(90)90389-m.
    1. Wissel J, Manack A, Brainin M. Toward an epidemiology of poststroke spasticity. Neurology. 2013;80:S13–19. doi: 10.1212/WNL.0b013e3182762448.
    1. Singer JC, Mansfield A, Danells CJ, McIlroy WE, Mochizuki G. The effect of post-stroke lower-limb spasticity on the control of standing balance: Inter-limb spatial and temporal synchronisation of centres of pressure. Clin. Biomech. (Bristol, Avon) 2013;28:921–926. doi: 10.1016/j.clinbiomech.2013.07.010.
    1. Soyuer F, Ozturk A. The effect of spasticity, sense and walking aids in falls of people after chronic stroke. Disabil. Rehabil. 2007;29:679–687. doi: 10.1080/09638280600925860.
    1. Schinwelski MJ, Sitek EJ, Waz P, Slawek JW. Prevalence and predictors of post-stroke spasticity and its impact on daily living and quality of life. Neurol. Neurochir. Pol. 2019;53:449–457. doi: 10.5603/PJNNS.a2019.0067.
    1. Decq P, Cuny E, Filipetti P, Feve A, Keravel Y. Peripheral neurotomy for the treatment of spasticity: indications, technique and outcome in the lower limbs. Neurochirurgie. 1998;44:175–182.
    1. Bleyenheuft C, et al. The effect of botulinum toxin injections on gait control in spastic stroke patients presenting with a stiff-knee gait. Gait Posture. 2009;30:168–172. doi: 10.1016/j.gaitpost.2009.04.003.
    1. Bohannon RW, Andrews AW. Correlation of knee extensor muscle torque and spasticity with gait speed in patients with stroke. Arch. Phys. Med. Rehabil. 1990;71:330–333.
    1. Nakamura R, Hosokawa T, Tsuji I. Relationship of muscle strength for knee extension to walking capacity in patients with spastic hemiparesis. Tohoku J. Exp. Med. 1985;145:335–340. doi: 10.1620/tjem.145.335.
    1. Ada L, Vattanasilp W, O'Dwyer NJ, Crosbie J. Does spasticity contribute to walking dysfunction after stroke? J. Neurol. Neurosurg. Psychiatry. 1998;64:628–635. doi: 10.1136/jnnp.64.5.628.
    1. Rosa MC, Marques A, Demain S, Metcalf CD. Knee posture during gait and global functioning post-stroke: a theoretical ICF framework using current measures in stroke rehabilitation. Disabil. Rehabil. 2015;37:904–913. doi: 10.3109/09638288.2014.948132.
    1. Yelnik A, Albert T, Bonan I, Laffont I. A clinical guide to assess the role of lower limb extensor overactivity in hemiplegic gait disorders. Stroke. 1999;30:580–585. doi: 10.1161/01.str.30.3.580.
    1. Caty GD, Detrembleur C, Bleyenheuft C, Deltombe T, Lejeune TM. Effect of simultaneous botulinum toxin injections into several muscles on impairment, activity, participation, and quality of life among stroke patients presenting with a stiff knee gait. Stroke. 2008;39:2803–2808. doi: 10.1161/STROKEAHA.108.516153.
    1. Tok F, Balaban B, Yasar E, Alaca R, Tan AK. The effects of onabotulinum toxin A injection into rectus femoris muscle in hemiplegic stroke patients with stiff-knee gait: a placebo-controlled, nonrandomized trial. Am. J. Phys. Med. Rehabil. 2012;91:321–326. doi: 10.1097/PHM.0b013e3182465feb.
    1. Lampire N, Roche N, Carne P, Cheze L, Pradon D. Effect of botulinum toxin injection on length and lengthening velocity of rectus femoris during gait in hemiparetic patients. Clin. Biomech. (Bristol, Avon) 2013;28:164–170. doi: 10.1016/j.clinbiomech.2012.12.006.
    1. Roche N, Boudarham J, Hardy A, Bonnyaud C, Bensmail B. Use of gait parameters to predict the effectiveness of botulinum toxin injection in the spastic rectus femoris muscle of stroke patients with stiff knee gait. Eur. J. Phys. Rehabil. Med. 2015;51:361–370.
    1. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67:206–207. doi: 10.1093/ptj/67.2.206.
    1. Gregson JM, et al. Reliability of the tone assessment scale and the modified Ashworth scale as clinical tools for assessing poststroke spasticity. Arch. Phys. Med. Rehabil. 1999;80:1013–1016. doi: 10.1016/s0003-9993(99)90053-9.
    1. Platz T, Eickhof C, Nuyens G, Vuadens P. Clinical scales for the assessment of spasticity, associated phenomena, and function: a systematic review of the literature. Disabil. Rehabil. 2005;27:7–18. doi: 10.1080/09638280400014634.
    1. Mehrholz J, et al. Reliability of the modified Tardieu Scale and the Modified Ashworth Scale in adult patients with severe brain injury: a comparison study. Clin. Rehabil. 2005;19:751–759. doi: 10.1191/0269215505cr889oa.
    1. Fleuren JF, Nederhand MJ, Hermens HJ. Influence of posture and muscle length on stretch reflex activity in poststroke patients with spasticity. Arch. Phys. Med. Rehabil. 2006;87:981–988. doi: 10.1016/j.apmr.2006.03.018.
    1. Li F, Wu Y, Li X. 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. 2014;50:9–15.
    1. Banky M, et al. Inter- and intra-rater variability of testing velocity when assessing lower limb spasticity. J. Rehabil. Med. 2019;51:54–60. doi: 10.2340/16501977-2496.
    1. Cakir T, Evcik FD, Subasi V, Demirdal US, Kavuncu V. Investigation of the H reflexes, F waves and sympathetic skin response with electromyography (EMG) in patients with stroke and the determination of the relationship with functional capacity. Acta Neurol. Belg. 2015;115:295–301. doi: 10.1007/s13760-014-0397-5.
    1. Biering-Sorensen F, Nielsen JB, Klinge K. Spasticity-assessment: a review. Spinal Cord. 2006;44:708–722. doi: 10.1038/sj.sc.3101928.
    1. Seoyoung C, Jonghyun K. Improving modified tardieu scale assessment using inertial measurement unit with visual biofeedback. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2016;4703–4706:2016. doi: 10.1109/EMBC.2016.7591777.
    1. Luo Z, Lo WLA, Bian R, Wong S, Li L. Advanced quantitative estimation methods for spasticity: a literature review. J. Int. Med. Res. 2019 doi: 10.1177/0300060519888425.
    1. Wartenberg R. Pendulousness of the legs as a diagnostic test. Neurology. 1951;1:18–24. doi: 10.1212/Wnl.1.1.18.
    1. Nance PW. A comparison of clonidine, cyproheptadine and baclofen in spastic spinal cord injured patients. J. Am. Paraplegia Soc. 1994;17:150–156. doi: 10.1080/01952307.1994.11735927.
    1. Bohannon RW, Harrison S, Kinsella-Shaw J. Reliability and validity of pendulum test measures of spasticity obtained with the Polhemus tracking system from patients with chronic stroke. J. Neuroeng. Rehabil. 2009;6:30. doi: 10.1186/1743-0003-6-30.
    1. Yeh CH, et al. Novel application of a Wii remote to measure spasticity with the pendulum test: proof of concept. Gait Posture. 2016;43:70–75. doi: 10.1016/j.gaitpost.2015.10.025.
    1. Katz RT, Rovai GP, Brait C, Rymer WZ. Objective quantification of spastic hypertonia: correlation with clinical findings. Arch. Phys. Med. Rehabil. 1992;73:339–347. doi: 10.1016/0003-9993(92)90007-j.
    1. Kim YW. Clinical usefulness of the pendulum test using a NK table to measure the spasticity of patients with brain lesions. J. Phys. Ther. Sci. 2013;25:1279–1283. doi: 10.1589/jpts.25.1279.
    1. Brown RA, et al. Does the Wartenberg pendulum test differentiate quantitatively between spasticity and rigidity? A study in elderly stroke and Parkinsonian patients. J. Neurol. Neurosurg. Psychiatry. 1988;51:1178–1186. doi: 10.1136/jnnp.51.9.1178.
    1. Brunnstrom S. Motor testing procedures in hemiplegia: based on sequential recovery stages. Phys. Ther. 1966;46:357–375. doi: 10.1093/ptj/46.4.357.
    1. Naghdi S, Ansari NN, Mansouri K, Hasson S. A neurophysiological and clinical study of Brunnstrom recovery stages in the upper limb following stroke. Brain Inj. 2010;24:1372–1378. doi: 10.3109/02699052.2010.506860.
    1. Canbek J, Fulk G, Nof L, Echternach J. Test-retest reliability and construct validity of the tinetti performance-oriented mobility assessment in people with stroke. J. Neurol. Phys. Ther. 2013;37:14–19. doi: 10.1097/NPT.0b013e318283ffcc.
    1. Flansbjer UB, Holmback AM, Downham D, Patten C, Lexell J. Reliability of gait performance tests in men and women with hemiparesis after stroke. J. Rehabil. Med. 2005;37:75–82. doi: 10.1080/16501970410017215.
    1. Podsiadlo D, Richardson S. The timed "Up & Go": a test of basic functional mobility for frail elderly persons. J. Am. Geriatr. Soc. 1991;39:142–148. doi: 10.1111/j.1532-5415.1991.tb01616.x.
    1. Steffen TM, Hacker TA, Mollinger L. Age- and gender-related test performance in community-dwelling elderly people: six-minute Walk Test, Berg Balance Scale, timed up & go test, and gait speeds. Phys. Ther. 2002;82:128–137. doi: 10.1093/ptj/82.2.128.
    1. Ng SS, Hui-Chan CW. The timed up & go test: its reliability and association with lower-limb impairments and locomotor capacities in people with chronic stroke. Arch. Phys. Med. Rehabil. 2005;86:1641–1647. doi: 10.1016/j.apmr.2005.01.011.
    1. Stillman B, McMeeken J. A video-based version of the pendulum test: technique and normal response. Arch. Phys. Med. Rehabil. 1995;76:166–176. doi: 10.1016/s0003-9993(95)80026-3.
    1. Yeh CH, et al. Quantifying spasticity with limited swinging cycles using pendulum test based on phase amplitude coupling. IEEE Trans. Neural Syst. Rehabil. 2016;24:1081–1088. doi: 10.1109/Tnsre.2016.2521612.
    1. Ansari NN, Naghdi S, Arab TK, Jalaie S. The interrater and intrarater reliability of the mzodified Ashworth Scale in the assessment of muscle spasticity: limb and muscle group effect. NeuroRehabilitation. 2008;23:231–237. doi: 10.3233/NRE-2008-23304.
    1. Sheffler LR, Knutson JS, Gunzler D, Chae J. Relationship between body mass index and rehabilitation outcomes in chronic stroke. Am. J. Phys. Med. Rehabil. 2012;91:951–956. doi: 10.1097/PHM.0b013e31826458c6.
    1. Roy-O’Reilly M, McCullough LD. Age and Sex Are Critical Factors in Ischemic Stroke Pathology. Endocrinology. 2018;159:3120–3131. doi: 10.1210/en.2018-00465.
    1. O'Brien RM. A caution regarding rules of thumb for variance inflation factors. Qual. Quant. 2007;41:673–690. doi: 10.1007/s11135-006-9018-6.
    1. Shah SK, Harasymiw SJ, Stahl PL. Stroke rehabilitation—outcome based on Brunnstrom recovery stages. Occup. Ther. J. Res. 1986;6:365–376. doi: 10.1177/153944928600600604.
    1. de Haart M, Geurts AC, Huidekoper SC, Fasotti L, van Limbeek J. Recovery of standing balance in postacute stroke patients: a rehabilitation cohort study. Arch. Phys. Med. Rehabil. 2004;85:886–895. doi: 10.1016/j.apmr.2003.05.012.
    1. Sakai T, Tanaka K, Holland GJ. Functional and locomotive characteristics of stroke survivors in Japanese community-based rehabilitation. Am. J. Phys. Med. Rehabil. 2002;81:675–683. doi: 10.1097/00002060-200209000-00007.
    1. Pandian S, Arya KN, Davidson EWR. Comparison of Brunnstrom movement therapy and motor relearning program in rehabilitation of post-stroke hemiparetic hand: a randomized trial. J. Bodyw. Mov. Ther. 2012;16:330–337. doi: 10.1016/j.jbmt.2011.11.002.
    1. Sunnerhagen KS, Olver J, Francisco GE. Assessing and treating functional impairment in poststroke spasticity. Neurology. 2013;80:S35–44. doi: 10.1212/WNL.0b013e3182764aa2.
    1. Francisco GE, Boake C. Improvement in walking speed in poststroke spastic hemiplegia after intrathecal baclofen therapy: a preliminary study. Arch. Phys. Med. Rehabil. 2003;84:1194–1199. doi: 10.1016/s0003-9993(03)00134-5.
    1. Baetens T, De Kegel A, Calders P, Vanderstraeten G, Cambier D. Prediction of falling among stroke patients in rehabilitation. J. Rehabil. Med. 2011;43:876–883. doi: 10.2340/16501977-0873.
    1. Bland MD, et al. Prediction of discharge walking ability from initial assessment in a stroke inpatient rehabilitation facility population. Arch. Phys. Med. Rehabil. 2012;93:1441–1447. doi: 10.1016/j.apmr.2012.02.029.
    1. Bakheit AM, Maynard VA, Curnow J, Hudson N, Kodapala S. 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. 2003;74:646–648. doi: 10.1136/jnnp.74.5.646.
    1. Katz RT, Rymer WZ. Spastic hypertonia: mechanisms and measurement. Arch. Phys. Med. Rehabil. 1989;70:144–155.
    1. van der Krogt MM, Doorenbosch CA, Becher JG, Harlaar J. Dynamic spasticity of plantar flexor muscles in cerebral palsy gait. J. Rehabil. Med. 2010;42:656–663. doi: 10.2340/16501977-0579.
    1. Damiano DL, et al. What does the Ashworth scale really measure and are instrumented measures more valid and precise? Dev. Med. Child Neurol. 2002;44:112–118. doi: 10.1017/s0012162201001761.
    1. Whittlesey SN, van Emmerik REA, Hamill J. The swing phase of human walking is not a passive movement. Mot. Control. 2000;4:273–292. doi: 10.1123/mcj.4.3.273.
    1. Le Cavorzin P, et al. A comprehensive model of spastic hypertonia derived from the pendulum test of the leg. Muscle Nerve. 2001;24:1612–1621. doi: 10.1002/mus.1196.
    1. Zhang LQ, et al. Simultaneous characterizations of reflex and nonreflex dynamic and static changes in spastic hemiparesis. J. Neurophysiol. 2013;110:418–430. doi: 10.1152/jn.00573.2012.
    1. Bajd T, Bowman B. Testing and modeling of spasticity. J. Biomed. Eng. 1982;4:90–96. doi: 10.1016/0141-5425(82)90067-X.
    1. Whelan A, Sexton A, Jones M, O'Connell C, McGibbon CA. Predictive value of the pendulum test for assessing knee extensor spasticity. J. Neuroeng. Rehabil. 2018;15:68. doi: 10.1186/s12984-018-0411-x.
    1. Fowler V, Canning CG, Carr JH, Shepherd RB. Muscle length effect on the pendulum test. Arch. Phys. Med. Rehabil. 1998;79:169–171. doi: 10.1016/S0003-9993(98)90294-5.
    1. Khiabani V, et al. Impact of spasticity on balance control during quiet standing in persons after stroke. Stroke Res. Treat. 2017 doi: 10.1155/2017/6153714.
    1. Peters S, et al. Motor planning for loading during gait in subacute stroke. Arch. Phys. Med. Rehabil. 2016;97:528–535. doi: 10.1016/j.apmr.2015.11.003.
    1. Middleton A, Fritz SL, Lusardi M. Walking speed: the functional vital sign. J. Aging Phys. Activ. 2015;23:314–322. doi: 10.1123/japa.2013-0236.
    1. Nadeau S, Arsenault AB, Gravel D, Bourbonnais D. Analysis of the clinical factors determining natural and maximal gait speeds in adults with a stroke. Am. J. Phys. Med. Rehab. 1999;78:123–130. doi: 10.1097/00002060-199903000-00007.
    1. Hsu AL, Tang PF, Jan MH. Analysis of impairments influencing gait velocity and asymmetry of hemiplegic patients after mild to moderate stroke. Arch. Phys. Med. Rehabil. 2003;84:1185–1193. doi: 10.1016/S0003-9993(03)00030-3.
    1. Johnson GR. Outcome measures of spasticity. Eur. J. Neurol. 2002 doi: 10.1046/j.1468-1331.2002.0090s1010.x.
    1. Monaghan K, et al. Physical treatment interventions for managing spasticity after stroke. Cochrane Database Syst. Rev. 2017 doi: 10.1002/14651858.CD009188.pub2.
    1. Bovend'Eerdt TJ, et al. The effects of stretching in spasticity: a systematic review. Arch. Phys. Med. Rehabil. 2008;89:1395–1406. doi: 10.1016/j.apmr.2008.02.015.
    1. Wu CL, et al. Effect on spasticity after performance of dynamic-repeated-passive ankle joint motion exercise in chronic stroke patients. Kaohsiung J. Med. Sci. 2006;22:610–617. doi: 10.1016/S1607-551X(09)70361-4.
    1. Meseguer-Henarejos AB, Sanchez-Meca J, Lopez-Pina JA, Carles-Hernandez R. Inter- and intra-rater reliability of the Modified Ashworth Scale: a systematic review and meta-analysis. Eur J Phys Rehabil Med. 2018;54:576–590. doi: 10.23736/S1973-9087.17.04796-7.
    1. Fleuren JFM, et al. Stop using the Ashworth Scale for the assessment of spasticity. J. Neurol. Neurosurg. Psychiatry. 2010;81:46. doi: 10.1136/jnnp.2009.177071.
    1. Ansari NN, Naghdi S, Younesian P, Shayeghan M. Inter- and intrarater reliability of the modified modified Ashworth Scale in patients with knee extensor poststroke spasticity. Physiother. Theory Pract. 2008;24:205–213. doi: 10.1080/09593980701523802.
    1. Borton DC, Walker K, Pirpiris M, Nattrass GR, Graham HK. Isolated calf lengthening in cerebral palsy. Outcome analysis of risk factors. J. Bone Joint Surg. Br. 2001;83:364–370. doi: 10.1302/0301-620x.83b3.10827.
    1. Campanini I, Disselhorst-Klug C, Rymer WZ, Merletti R. Surface EMG in clinical assessment and neurorehabilitation: barriers limiting its use. Front. Neurol. 2020;11:934. doi: 10.3389/fneur.2020.00934.

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