- Email: [email protected]
Spasticity 30 years later: The truth is still in the eye of the beholder
Clinical Neurophysiology 121 (2010) 1789–1791
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
Spasticity 30 years later: The truth is still in the eye of the beholder See Article, pages 1939–1951
To be somebody you must last. – Ruth Gordon Jones, Actress (1896–1985). This year marks 3 decades since Lance (1980) offered the most commonly cited operational definition of spasticity (. . .motor disorder characterized by a velocity dependent increase in the tonic stretch reflex (‘muscle tone’) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome). During this time, spasticity has continuously attracted the interest of clinicians and researchers on topics ranging from pathophysiology to clinical relevance and treatment options. An example of this lasting interest is the number of recently published commentaries (Cramer, 2004; Levin, 2005; Sunnerhagen, 2010) and reviews (Gracies, 2005; Pandyan et al., 2005; Sheean and McGuire, 2009). Inconsistent and sometimes vastly opposite conclusions about the nature and relevance of spasticity perpetuate ongoing interest, further invigorated by discrepant views and sentiments about this phenomenon among clinicians and researchers. And the spark is unlikely to diminish any time soon. The study by Lorentzen et al. (2010) published in this issue of Clinical Neurophysiology exemplifies the intricacies we are confronted with when attempting to identify components of altered muscle tone in relation to spasticity, defined in the strict sense. In the background for the study, the authors rightly point out that the term spasticity is inconsistently used (Malhotra et al., 2009). This may lead to the misconstruing of the patient condition and the prescription of less than optimal treatments on the clinical side, and the addressing of questions inconsistent with the adopted definition and improper methodology on the research side. The research question posed by Lorentzen et al. is the ability to discern reflex and passive tissue changes by neurophysiological and biomechanical methods among people with or without clinical signs of stretch reflex hyperexcitability in the ankle plantar flexor muscles in comparison to healthy controls. The main findings are that the stretch reflex torque and EMG responses were significantly larger in patients than in controls at faster stretch velocities, with no difference between the subjects with or without clinical signs of stretch reflex hyperexcitability. In contrast, the passive ankle stiffness was greater in spastic then non-spastic patients but neither group was significantly different from controls. The implications are that reflex rather than passive changes discriminate between the patients and controls, whereas these two components of ankle joint stiffness cannot be reliably distinguished based on the clinical examination.
What kind of novelty does the study by Lorentzen et al. provide considering the already rich literature on this topic? The most obvious is the conclusion that reflex rather than passive component discriminates patients from controls, which contrasts some previous results. Also of interest in this regard is the overall approach, from the definition of construct under investigation to the procedures for patient selection and methods for data collection and analysis. Perhaps not surprisingly, different parts of the study and conclusions may not equally appeal to clinicians, neurophysiologists, and biomechanists. Lorentzen et al. focused on the hallmark of spasticity according to Lance’s definition – the hyperactive stretch reflex. Rather than selecting participants with clinical evidence of muscle hypertonia only or upper motor neuron syndrome in general, they reviewed medical records in search of subjects with previously documented features of spasticity that could be ascribed to hyperactive stretch reflex, namely hypertonia, hyperreflexia, and/or clonus. This approach ensured that the construct under investigation is consistent with the operational definition of spasticity and allowed the inclusion of a larger pool of subjects than by focusing on those with muscle hypertonia only. This sampling method likely appeals to neurophysiologists as it is consistent with the definition of spasticity and gives the study adequate construct validity. Conversely, clinicians and biomechanists may argue that it undermines ecological validity of the results assuming that the resistance to passive movement is the main culprit. All would probably agree that a relevant and unresolved issue is the relation between clinical, neurophysiological, and biomechanical measures of spasticity. That is what Lorentzen et al. addressed in subjects with multiple sclerosis, spinal cord injury, and stroke using a variation of a rather common experimental paradigm. After a ‘‘more thorough neurological examination”, the authors reported that 31 of 64 subjects with spasticity documented in medical records showed clinical signs of stretch reflex hyperexcitability, heretofore designated as ‘‘spastic” as opposed to ‘‘non-spastic”. This finding by itself supports the underlying premise that clinician-practitioners and clinician-researchers view spasticity from different angles. Since the data from medical records were not reported in the same detail, it is unknown to what extent these findings also reflect the research focus on ankle plantar flexors versus other segments designated as spastic in the medical records, examiner skills, inter-rater reliability, and changes in anti-spasticity treatment or disease course. Of note is that the use of anti-
1388-2457/$36.00 Ó 2010 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2010.04.015
1790
Editorial / Clinical Neurophysiology 121 (2010) 1789–1791
spasticity medication at the time of examination was not related to the presence of stretch reflex hyperexcitability in ankle plantar flexors. This could be interpreted as unnecessary prescription of medication to the ‘‘non-spastic” group but also that the involved upper limbs or proximal lower limbs were the reason for treatment. Unfortunately, not performing a neurological examination as a part of the screening process led to unbalanced sample sizes across the three study populations thereby limiting the strength of comparisons within and between these groups that are thought to differ in the nature and predominant features of spasticity. This seems particularly relevant for the stroke sample comprised of only 10 subjects and all designated as spastic. Perhaps the most controversial, but in some aspects also innovative part of the study is the approach for evaluating contributions of passive and reflex stiffness. The authors placed a more spastic ankle in 10 deg of plantar flexion from the neutral position and produced 16 stretches at each of 17 different velocities over the 6-deg range of motion while recording the evoked ankle torque and EMG from the soleus muscle. They also supramaximally stimulated the tibial nerve in the popliteal fossa to record the muscle twitch and M wave responses used for normalizing the torque and EMG perturbation data. The control experiment with ischemia in healthy subjects served to ascertain that passive stiffness is not dependent on stretch velocity. This approach deserves several comments. The main controversy arises from evoking the responses in only one ankle position with short stretches that ended even before the ankle reached a neutral angle. Indeed, this approach does not resemble clinical assessment of hypertonia, which can be viewed as yet another concern about the ecological validity of the study. An experimental paradigm that closely approximates the clinical examination is mandatory if the goal is to directly compare clinical to laboratory assessment of hypertonia (Alibiglou et al., 2008). But this is not the case here since the focus of Lorentzen et al. is more global, i.e., on neurophysiological and biomechanical responses to stretch perturbation in relation to the presence or absence of clinical signs of stretch reflex hyperexcitability, only one of which is hypertonia. Nevertheless, the impact of the chosen experimental paradigm on the results needs to be considered. Of major concern is the possibility that overall passive stiffness was underestimated as many previous reports support the contention that passive stiffness varies across the ankle range of motion. The results in subjects after stroke (Mirbagheri et al., 2007) and spinal cord injury (Mirbagheri et al., 2001) indicate that passive stiffness is in fact the lowest at about the neutral ankle position. Somewhat different but complimentary results were reported in people with acquired brain injury (Singer et al., 2004) where the passive stiffness differed from controls only after the ankle passed the neutral position and became more pronounced with increased dorsiflexion angle. The cited work in a stroke sample indicates that changes in passive stiffness are rather small up to about neutral ankle position with an increase thereafter (Lamontagne et al., 1998). Thus, a valid point of contention is that passive stiffness was likely underestimated with the chosen experimental paradigm. Conversely, the same paradigm may be the least prone to a potential confounding of passive stiffness, making it easier to isolate changes in reflex stiffness. The innovative part of the study is that Lorentzen et al. used finely graded perturbation velocities and expressed the torque and EMG responses not only in absolute terms but also relative to those evoked by the supramaximal tibial nerve stimulation. As the authors point out, normalization of torque and EMG data in studies of spasticity is not commonly done, yet it is a routine procedure in most neurophysiologic studies. Normalizing data brought out significantly larger passive stiffness in clinically ‘‘spastic” than ‘‘nonspastic” patients, significantly larger reflex EMG responses at faster
stretch velocities in patients than controls, and an increase in the proportion of subjects with the maximal reflex torque and EMG responses above the control values. In summary, normalization apparently improved the discriminative ability of the method. The use of normalization may also have its proponents and critics. From the neurophysiologic standpoint, it makes sense to account for changes in muscle membrane and contractile properties after the upper motor neuron lesion. The opposing argument could be that it is the absolute torque that is clinically perceived, actually measured, and perhaps interfering with motor functions, thus demonstrating difference in relative terms is of lesser relevance. Not surprisingly, normalization affected EMG more than torque data. Assuming that the torque evoked by short stretches resembles an impulse, normalizing perturbation torque data to the supramaximal twitch amplitude seems appropriate. However, it is possible that even greater separation could have been achieved had the torque been normalized to brief tetani, which typically differ more than twitches among and between patients and controls. In essence, Lorentzen et al. demonstrated an increase in stretch reflex gain for both torque and EMG data in patients compared to controls with no difference in stretch reflex velocity threshold. Of interest is that the chosen joint position may also have favored the detection of increased stretch reflex gain as the reflex contribution to the stiffness seems to be the largest around the neutral ankle position (Mirbagheri et al., 2007). It appears, therefore, that the selected paradigm had a high yield for identifying the velocitydependent reflex component with the least noise from the passive component. This also could have contributed to inability to discriminate between clinically ‘‘spastic” and ‘‘non-spastic” patients based on the reflex EMG and torque data, aside from limitations of the clinical examination. The study by Lorentzen et al. provokes some additional thoughts. First and foremost, it is evident that methods for identifying reflex and passive stiffness vary greatly between different studies (see Mirbagheri et al. (2007) for discussion), making comparisons of published results virtually impossible. Indeed, the approach should be driven by the question asked, but many previous studies asked similar if not identical questions yet employed different methodology without proper justification. Thus, it appears that the selection of methods is sometimes more a matter of convenience than scientific rationale. Limited access and lack of familiarity with different, particularly advanced methods make replicating the reported results unfeasible. Thus, method comparison studies in the context of clinically relevant questions are warranted in order to move us away from the trees to better see the forest. The second thought deals with the purpose of clinical assessment of spasticity. As we hopefully soon bring to a closure perpetual investigations on the limitations of Ashworth scale (Craven and Morris, 2010; Fleuren et al., 2010), efforts should be focused on developing and validating alternatives acceptable from neurophysiologic and biomechanical perspectives. Thus, encouraging are the emphases toward ensuring proper use of the Tardeau scale (Gracies et al., 2010), demonstrating that stretch reflex underlies the perception of catch detected by the Spasticity Test (van den Noort et al., 2010), and applications of hand-held devices (Calota et al., 2008). But just as relevant an issue is what kind of clinical instrument we need. If changes in spasticity/hypertonia are at best only weakly related to changes in motor performance after anti-spasticity treatment (Francis et al., 2004), it is questionable whether we should insist on the spasticity instrument with adequate properties to reliably evaluate outcomes of interventions. Perhaps it may suffice to assess spasticity/hypertonia for descriptive purposes at baseline and then focus on clinical and laboratory assessments of real-life motor tasks before and after treatment, leaving changes
Editorial / Clinical Neurophysiology 121 (2010) 1789–1791
in spasticity/hypertonia aside (Bensmail et al., 2010; Fridman et al., 2010) or use the baseline information to discriminate and hopefully predict responders and non-responders. The third thought is about Lance’s definition of spasticity. Lance’s definition may be taken as an example of scientific reductionism since it emphasizes the contribution of stretch reflex excitability to altered muscle tone and motor disorder after upper motor neuron lesion. At the time it was proposed, the passive tissue changes in the ankle muscles had already become apparent (Herman, 1970). However, Lance’s definition was based on studies performed mainly at the knee joint (Burke et al., 1970, 1971) where, as we recently learned (van den Noort et al., 2010), the clinical perception of catch during fast stretching of the hamstrings muscle is regularly accompanied by the reflex response, which is less frequently observed in the plantar flexors. Indeed, most studies since then have focused on the ankle joint, perhaps because of pronounced stiffness. Despite limitations that became apparent over the past 30 years, Lance’s definition has been for the most part credibly used to test specific hypotheses and conduct sound scientific inquiries. Considering that the field is evolving and new definitions of spasticity are being proposed (Malhotra et al., 2009; Pandyan et al., 2005), proper use of more inclusive but less specific definitions may be challenging if the underlying constructs remain subject to variable interpretations without explicitly postulated pathophysiologic mechanisms. Finally, it is important to ask whether we were good stewards of Lance’s definition. Did we happen to conduct and review studies that ventured out of the proposed frame of reference, perhaps leading clinicians, neurophysiologists, and biomechanists to see spasticity in their own ways? If sufficient evidence has accumulated to reconsider stretch reflex hyperexcitability as one of the constructs underlying spasticity, Lance’s definition has achieved its purpose and may need to be revised or abandoned. As we voice opinions, the contribution of Lorentzen et al. gives us an opportunity to broaden views and move out of trenches in order to reconcile our positions. Acknowledgement The author thanks A. Arturo Leis, M.D. for insightful comments.
References Alibiglou L, Rymer WZ, Harvey RL, Mirbagheri MM. The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke. J Neuroeng Rehabil 2008;5:18. Bensmail D, Robertson JV, Fermanian C, Roby-Brami A. Botulinum toxin to treat upper-limb spasticity in hemiparetic patients: analysis of function and kinematics of reaching movements. Neurorehabil Neural Repair 2010;24:273–81. Burke D, Gillies JD, Lance JW. The quadriceps stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 1970;33:216–23. Burke D, Gillies JD, Lance JW. Hamstrings stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 1971;34:231–5. Calota A, Feldman AG, Levin MF. Spasticity measurement based on tonic stretch reflex threshold in stroke using a portable device. Clin Neurophysiol 2008;119:2329–37.
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Cramer SC. Editorial comment – spasticity after stroke: what’s the catch? Stroke 2004;35:139–40. Craven BC, Morris AR. Modified Ashworth scale reliability for measurement of lower extremity spasticity among patients with SCI. Spinal Cord 2010;48:207–13. Fleuren JF, Voerman GE, Erren-Wolters CV, Snoek GJ, Rietman JS, Hermens HJ, et al. Stop using the Ashworth Scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry 2010;81:46–52. Francis HP, Wade DT, Turner-Stokes L, Kingswell RS, Dott CS, Coxon EA. Does reducing spasticity translate into functional benefit? An exploratory metaanalysis. J Neurol Neurosurg Psychiatry 2004;75:1547–51. Fridman EA, Crespo M, Gomez AS, Degue L, Villarreal M, Bohlhalter S, et al. Kinematic improvement following botulinum toxin-A injection in upperlimb spasticity due to stroke. J Neurol Neurosurg Psychiatry 2010;81: 423–7. Gracies JM. Pathophysiology of spastic paresis. I: paresis and soft tissue changes. Muscle Nerve 2005;31:535–51. Gracies JM, Burke K, Clegg NJ, Browne R, Rushing C, Fehlings D, et al. Reliability of the Tardieu Scale for assessing spasticity in children with cerebral palsy. Arch Phys Med Rehabil 2010;91:421–8. Herman R. The myotatic reflex. Clinico-physiological aspects of spasticity and contracture. Brain 1970;93:273–312. Lamontagne A, Malouin F, Richards CL, Dumas F. Evaluation of reflex- and nonreflex-induced muscle resistance to stretch in adults with spinal cord injury using hand-held and isokinetic dynamometry. Phys Ther 1998;78:964–75. Lance JW. Symposium synopsis. In: Feldman RG, Young RR, Koella WP, editors. Spasticity: disordered motor control. Chicago: Year Book Medical; 1980. p. 485–94. Levin MF. On the nature and measurement of spasticity. Clin Neurophysiol 2005;116:1754–5. Lorentzen J, Grey MJ, Crone C, Mazevet D, Biering-Sorensen F, Nielsen JB. Distinguishing active from passive components of ankle plantar flexor stiffness in stroke, spinal cord injury and multiple sclerosis. Clin Neurophysiol 2010;121(11):1939–51. Malhotra S, Pandyan AD, Day CR, Jones PW, Hermens H. Spasticity, an impairment that is poorly defined and poorly measured. Clin Rehabil 2009;23:651–8. Mirbagheri MM, Barbeau H, Ladouceur M, Kearney RE. Intrinsic and reflex stiffness in normal and spastic, spinal cord injured subjects. Exp Brain Res 2001;141:446–59. Mirbagheri MM, Settle K, Harvey R, Rymer WZ. Neuromuscular abnormalities associated with spasticity of upper extremity muscles in hemiparetic stroke. J Neurophysiol 2007;98:629–37. Pandyan AD, Gregoric M, Barnes MP, Wood D, van WF WF, Burridge J, et al. Spasticity: clinical perceptions, neurological realities and meaningful measurement. Disabil Rehabil 2005;27:2–6. Sheean G, McGuire JR. Spastic hypertonia and movement disorders: pathophysiology, clinical presentation, and quantification. PM R 2009;1:827–33. Singer BJ, Jegasothy GM, Singer KP, Allison GT, Dunne JW. Incidence of ankle contracture after moderate to severe acquired brain injury. Arch Phys Med Rehabil 2004;85:1465–9. Sunnerhagen KS. Stop using the Ashworth scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry 2010;81:2. van den Noort JC, Scholtes VA, Becher JG, Harlaar J. Evaluation of the catch in spasticity assessment in children with cerebral palsy. Arch Phys Med Rehabil 2010;91:615–23.
Dobrivoje S. Stokic Center for Neuroscience and Neurological Recovery, Methodist Rehabilitation Center, 1350 E. Woodrow Wilson Dr., Jackson, MS, USA. Tel.: +1 601 364 3314; fax: +1 601 364 3305 E-mail address: [email protected] Available online 14 May 2010
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
Spasticity 30 years later: The truth is still in the eye of the beholder See Article, pages 1939–1951
To be somebody you must last. – Ruth Gordon Jones, Actress (1896–1985). This year marks 3 decades since Lance (1980) offered the most commonly cited operational definition of spasticity (. . .motor disorder characterized by a velocity dependent increase in the tonic stretch reflex (‘muscle tone’) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome). During this time, spasticity has continuously attracted the interest of clinicians and researchers on topics ranging from pathophysiology to clinical relevance and treatment options. An example of this lasting interest is the number of recently published commentaries (Cramer, 2004; Levin, 2005; Sunnerhagen, 2010) and reviews (Gracies, 2005; Pandyan et al., 2005; Sheean and McGuire, 2009). Inconsistent and sometimes vastly opposite conclusions about the nature and relevance of spasticity perpetuate ongoing interest, further invigorated by discrepant views and sentiments about this phenomenon among clinicians and researchers. And the spark is unlikely to diminish any time soon. The study by Lorentzen et al. (2010) published in this issue of Clinical Neurophysiology exemplifies the intricacies we are confronted with when attempting to identify components of altered muscle tone in relation to spasticity, defined in the strict sense. In the background for the study, the authors rightly point out that the term spasticity is inconsistently used (Malhotra et al., 2009). This may lead to the misconstruing of the patient condition and the prescription of less than optimal treatments on the clinical side, and the addressing of questions inconsistent with the adopted definition and improper methodology on the research side. The research question posed by Lorentzen et al. is the ability to discern reflex and passive tissue changes by neurophysiological and biomechanical methods among people with or without clinical signs of stretch reflex hyperexcitability in the ankle plantar flexor muscles in comparison to healthy controls. The main findings are that the stretch reflex torque and EMG responses were significantly larger in patients than in controls at faster stretch velocities, with no difference between the subjects with or without clinical signs of stretch reflex hyperexcitability. In contrast, the passive ankle stiffness was greater in spastic then non-spastic patients but neither group was significantly different from controls. The implications are that reflex rather than passive changes discriminate between the patients and controls, whereas these two components of ankle joint stiffness cannot be reliably distinguished based on the clinical examination.
What kind of novelty does the study by Lorentzen et al. provide considering the already rich literature on this topic? The most obvious is the conclusion that reflex rather than passive component discriminates patients from controls, which contrasts some previous results. Also of interest in this regard is the overall approach, from the definition of construct under investigation to the procedures for patient selection and methods for data collection and analysis. Perhaps not surprisingly, different parts of the study and conclusions may not equally appeal to clinicians, neurophysiologists, and biomechanists. Lorentzen et al. focused on the hallmark of spasticity according to Lance’s definition – the hyperactive stretch reflex. Rather than selecting participants with clinical evidence of muscle hypertonia only or upper motor neuron syndrome in general, they reviewed medical records in search of subjects with previously documented features of spasticity that could be ascribed to hyperactive stretch reflex, namely hypertonia, hyperreflexia, and/or clonus. This approach ensured that the construct under investigation is consistent with the operational definition of spasticity and allowed the inclusion of a larger pool of subjects than by focusing on those with muscle hypertonia only. This sampling method likely appeals to neurophysiologists as it is consistent with the definition of spasticity and gives the study adequate construct validity. Conversely, clinicians and biomechanists may argue that it undermines ecological validity of the results assuming that the resistance to passive movement is the main culprit. All would probably agree that a relevant and unresolved issue is the relation between clinical, neurophysiological, and biomechanical measures of spasticity. That is what Lorentzen et al. addressed in subjects with multiple sclerosis, spinal cord injury, and stroke using a variation of a rather common experimental paradigm. After a ‘‘more thorough neurological examination”, the authors reported that 31 of 64 subjects with spasticity documented in medical records showed clinical signs of stretch reflex hyperexcitability, heretofore designated as ‘‘spastic” as opposed to ‘‘non-spastic”. This finding by itself supports the underlying premise that clinician-practitioners and clinician-researchers view spasticity from different angles. Since the data from medical records were not reported in the same detail, it is unknown to what extent these findings also reflect the research focus on ankle plantar flexors versus other segments designated as spastic in the medical records, examiner skills, inter-rater reliability, and changes in anti-spasticity treatment or disease course. Of note is that the use of anti-
1388-2457/$36.00 Ó 2010 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2010.04.015
1790
Editorial / Clinical Neurophysiology 121 (2010) 1789–1791
spasticity medication at the time of examination was not related to the presence of stretch reflex hyperexcitability in ankle plantar flexors. This could be interpreted as unnecessary prescription of medication to the ‘‘non-spastic” group but also that the involved upper limbs or proximal lower limbs were the reason for treatment. Unfortunately, not performing a neurological examination as a part of the screening process led to unbalanced sample sizes across the three study populations thereby limiting the strength of comparisons within and between these groups that are thought to differ in the nature and predominant features of spasticity. This seems particularly relevant for the stroke sample comprised of only 10 subjects and all designated as spastic. Perhaps the most controversial, but in some aspects also innovative part of the study is the approach for evaluating contributions of passive and reflex stiffness. The authors placed a more spastic ankle in 10 deg of plantar flexion from the neutral position and produced 16 stretches at each of 17 different velocities over the 6-deg range of motion while recording the evoked ankle torque and EMG from the soleus muscle. They also supramaximally stimulated the tibial nerve in the popliteal fossa to record the muscle twitch and M wave responses used for normalizing the torque and EMG perturbation data. The control experiment with ischemia in healthy subjects served to ascertain that passive stiffness is not dependent on stretch velocity. This approach deserves several comments. The main controversy arises from evoking the responses in only one ankle position with short stretches that ended even before the ankle reached a neutral angle. Indeed, this approach does not resemble clinical assessment of hypertonia, which can be viewed as yet another concern about the ecological validity of the study. An experimental paradigm that closely approximates the clinical examination is mandatory if the goal is to directly compare clinical to laboratory assessment of hypertonia (Alibiglou et al., 2008). But this is not the case here since the focus of Lorentzen et al. is more global, i.e., on neurophysiological and biomechanical responses to stretch perturbation in relation to the presence or absence of clinical signs of stretch reflex hyperexcitability, only one of which is hypertonia. Nevertheless, the impact of the chosen experimental paradigm on the results needs to be considered. Of major concern is the possibility that overall passive stiffness was underestimated as many previous reports support the contention that passive stiffness varies across the ankle range of motion. The results in subjects after stroke (Mirbagheri et al., 2007) and spinal cord injury (Mirbagheri et al., 2001) indicate that passive stiffness is in fact the lowest at about the neutral ankle position. Somewhat different but complimentary results were reported in people with acquired brain injury (Singer et al., 2004) where the passive stiffness differed from controls only after the ankle passed the neutral position and became more pronounced with increased dorsiflexion angle. The cited work in a stroke sample indicates that changes in passive stiffness are rather small up to about neutral ankle position with an increase thereafter (Lamontagne et al., 1998). Thus, a valid point of contention is that passive stiffness was likely underestimated with the chosen experimental paradigm. Conversely, the same paradigm may be the least prone to a potential confounding of passive stiffness, making it easier to isolate changes in reflex stiffness. The innovative part of the study is that Lorentzen et al. used finely graded perturbation velocities and expressed the torque and EMG responses not only in absolute terms but also relative to those evoked by the supramaximal tibial nerve stimulation. As the authors point out, normalization of torque and EMG data in studies of spasticity is not commonly done, yet it is a routine procedure in most neurophysiologic studies. Normalizing data brought out significantly larger passive stiffness in clinically ‘‘spastic” than ‘‘nonspastic” patients, significantly larger reflex EMG responses at faster
stretch velocities in patients than controls, and an increase in the proportion of subjects with the maximal reflex torque and EMG responses above the control values. In summary, normalization apparently improved the discriminative ability of the method. The use of normalization may also have its proponents and critics. From the neurophysiologic standpoint, it makes sense to account for changes in muscle membrane and contractile properties after the upper motor neuron lesion. The opposing argument could be that it is the absolute torque that is clinically perceived, actually measured, and perhaps interfering with motor functions, thus demonstrating difference in relative terms is of lesser relevance. Not surprisingly, normalization affected EMG more than torque data. Assuming that the torque evoked by short stretches resembles an impulse, normalizing perturbation torque data to the supramaximal twitch amplitude seems appropriate. However, it is possible that even greater separation could have been achieved had the torque been normalized to brief tetani, which typically differ more than twitches among and between patients and controls. In essence, Lorentzen et al. demonstrated an increase in stretch reflex gain for both torque and EMG data in patients compared to controls with no difference in stretch reflex velocity threshold. Of interest is that the chosen joint position may also have favored the detection of increased stretch reflex gain as the reflex contribution to the stiffness seems to be the largest around the neutral ankle position (Mirbagheri et al., 2007). It appears, therefore, that the selected paradigm had a high yield for identifying the velocitydependent reflex component with the least noise from the passive component. This also could have contributed to inability to discriminate between clinically ‘‘spastic” and ‘‘non-spastic” patients based on the reflex EMG and torque data, aside from limitations of the clinical examination. The study by Lorentzen et al. provokes some additional thoughts. First and foremost, it is evident that methods for identifying reflex and passive stiffness vary greatly between different studies (see Mirbagheri et al. (2007) for discussion), making comparisons of published results virtually impossible. Indeed, the approach should be driven by the question asked, but many previous studies asked similar if not identical questions yet employed different methodology without proper justification. Thus, it appears that the selection of methods is sometimes more a matter of convenience than scientific rationale. Limited access and lack of familiarity with different, particularly advanced methods make replicating the reported results unfeasible. Thus, method comparison studies in the context of clinically relevant questions are warranted in order to move us away from the trees to better see the forest. The second thought deals with the purpose of clinical assessment of spasticity. As we hopefully soon bring to a closure perpetual investigations on the limitations of Ashworth scale (Craven and Morris, 2010; Fleuren et al., 2010), efforts should be focused on developing and validating alternatives acceptable from neurophysiologic and biomechanical perspectives. Thus, encouraging are the emphases toward ensuring proper use of the Tardeau scale (Gracies et al., 2010), demonstrating that stretch reflex underlies the perception of catch detected by the Spasticity Test (van den Noort et al., 2010), and applications of hand-held devices (Calota et al., 2008). But just as relevant an issue is what kind of clinical instrument we need. If changes in spasticity/hypertonia are at best only weakly related to changes in motor performance after anti-spasticity treatment (Francis et al., 2004), it is questionable whether we should insist on the spasticity instrument with adequate properties to reliably evaluate outcomes of interventions. Perhaps it may suffice to assess spasticity/hypertonia for descriptive purposes at baseline and then focus on clinical and laboratory assessments of real-life motor tasks before and after treatment, leaving changes
Editorial / Clinical Neurophysiology 121 (2010) 1789–1791
in spasticity/hypertonia aside (Bensmail et al., 2010; Fridman et al., 2010) or use the baseline information to discriminate and hopefully predict responders and non-responders. The third thought is about Lance’s definition of spasticity. Lance’s definition may be taken as an example of scientific reductionism since it emphasizes the contribution of stretch reflex excitability to altered muscle tone and motor disorder after upper motor neuron lesion. At the time it was proposed, the passive tissue changes in the ankle muscles had already become apparent (Herman, 1970). However, Lance’s definition was based on studies performed mainly at the knee joint (Burke et al., 1970, 1971) where, as we recently learned (van den Noort et al., 2010), the clinical perception of catch during fast stretching of the hamstrings muscle is regularly accompanied by the reflex response, which is less frequently observed in the plantar flexors. Indeed, most studies since then have focused on the ankle joint, perhaps because of pronounced stiffness. Despite limitations that became apparent over the past 30 years, Lance’s definition has been for the most part credibly used to test specific hypotheses and conduct sound scientific inquiries. Considering that the field is evolving and new definitions of spasticity are being proposed (Malhotra et al., 2009; Pandyan et al., 2005), proper use of more inclusive but less specific definitions may be challenging if the underlying constructs remain subject to variable interpretations without explicitly postulated pathophysiologic mechanisms. Finally, it is important to ask whether we were good stewards of Lance’s definition. Did we happen to conduct and review studies that ventured out of the proposed frame of reference, perhaps leading clinicians, neurophysiologists, and biomechanists to see spasticity in their own ways? If sufficient evidence has accumulated to reconsider stretch reflex hyperexcitability as one of the constructs underlying spasticity, Lance’s definition has achieved its purpose and may need to be revised or abandoned. As we voice opinions, the contribution of Lorentzen et al. gives us an opportunity to broaden views and move out of trenches in order to reconcile our positions. Acknowledgement The author thanks A. Arturo Leis, M.D. for insightful comments.
References Alibiglou L, Rymer WZ, Harvey RL, Mirbagheri MM. The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke. J Neuroeng Rehabil 2008;5:18. Bensmail D, Robertson JV, Fermanian C, Roby-Brami A. Botulinum toxin to treat upper-limb spasticity in hemiparetic patients: analysis of function and kinematics of reaching movements. Neurorehabil Neural Repair 2010;24:273–81. Burke D, Gillies JD, Lance JW. The quadriceps stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 1970;33:216–23. Burke D, Gillies JD, Lance JW. Hamstrings stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 1971;34:231–5. Calota A, Feldman AG, Levin MF. Spasticity measurement based on tonic stretch reflex threshold in stroke using a portable device. Clin Neurophysiol 2008;119:2329–37.
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Cramer SC. Editorial comment – spasticity after stroke: what’s the catch? Stroke 2004;35:139–40. Craven BC, Morris AR. Modified Ashworth scale reliability for measurement of lower extremity spasticity among patients with SCI. Spinal Cord 2010;48:207–13. Fleuren JF, Voerman GE, Erren-Wolters CV, Snoek GJ, Rietman JS, Hermens HJ, et al. Stop using the Ashworth Scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry 2010;81:46–52. Francis HP, Wade DT, Turner-Stokes L, Kingswell RS, Dott CS, Coxon EA. Does reducing spasticity translate into functional benefit? An exploratory metaanalysis. J Neurol Neurosurg Psychiatry 2004;75:1547–51. Fridman EA, Crespo M, Gomez AS, Degue L, Villarreal M, Bohlhalter S, et al. Kinematic improvement following botulinum toxin-A injection in upperlimb spasticity due to stroke. J Neurol Neurosurg Psychiatry 2010;81: 423–7. Gracies JM. Pathophysiology of spastic paresis. I: paresis and soft tissue changes. Muscle Nerve 2005;31:535–51. Gracies JM, Burke K, Clegg NJ, Browne R, Rushing C, Fehlings D, et al. Reliability of the Tardieu Scale for assessing spasticity in children with cerebral palsy. Arch Phys Med Rehabil 2010;91:421–8. Herman R. The myotatic reflex. Clinico-physiological aspects of spasticity and contracture. Brain 1970;93:273–312. Lamontagne A, Malouin F, Richards CL, Dumas F. Evaluation of reflex- and nonreflex-induced muscle resistance to stretch in adults with spinal cord injury using hand-held and isokinetic dynamometry. Phys Ther 1998;78:964–75. Lance JW. Symposium synopsis. In: Feldman RG, Young RR, Koella WP, editors. Spasticity: disordered motor control. Chicago: Year Book Medical; 1980. p. 485–94. Levin MF. On the nature and measurement of spasticity. Clin Neurophysiol 2005;116:1754–5. Lorentzen J, Grey MJ, Crone C, Mazevet D, Biering-Sorensen F, Nielsen JB. Distinguishing active from passive components of ankle plantar flexor stiffness in stroke, spinal cord injury and multiple sclerosis. Clin Neurophysiol 2010;121(11):1939–51. Malhotra S, Pandyan AD, Day CR, Jones PW, Hermens H. Spasticity, an impairment that is poorly defined and poorly measured. Clin Rehabil 2009;23:651–8. Mirbagheri MM, Barbeau H, Ladouceur M, Kearney RE. Intrinsic and reflex stiffness in normal and spastic, spinal cord injured subjects. Exp Brain Res 2001;141:446–59. Mirbagheri MM, Settle K, Harvey R, Rymer WZ. Neuromuscular abnormalities associated with spasticity of upper extremity muscles in hemiparetic stroke. J Neurophysiol 2007;98:629–37. Pandyan AD, Gregoric M, Barnes MP, Wood D, van WF WF, Burridge J, et al. Spasticity: clinical perceptions, neurological realities and meaningful measurement. Disabil Rehabil 2005;27:2–6. Sheean G, McGuire JR. Spastic hypertonia and movement disorders: pathophysiology, clinical presentation, and quantification. PM R 2009;1:827–33. Singer BJ, Jegasothy GM, Singer KP, Allison GT, Dunne JW. Incidence of ankle contracture after moderate to severe acquired brain injury. Arch Phys Med Rehabil 2004;85:1465–9. Sunnerhagen KS. Stop using the Ashworth scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry 2010;81:2. van den Noort JC, Scholtes VA, Becher JG, Harlaar J. Evaluation of the catch in spasticity assessment in children with cerebral palsy. Arch Phys Med Rehabil 2010;91:615–23.
Dobrivoje S. Stokic Center for Neuroscience and Neurological Recovery, Methodist Rehabilitation Center, 1350 E. Woodrow Wilson Dr., Jackson, MS, USA. Tel.: +1 601 364 3314; fax: +1 601 364 3305 E-mail address: [email protected] Available online 14 May 2010