308

Late Motor Recovery Is Inuenced by Muscle Tone Changes After Stroke

Rita Formisano, MD, PhD, Patrizia Pantano, MD, PhD, M. Gabriella Buzzi, MD, PhD, Vincenzo Vinicola, MD, Francesca Penta, Piero Barbanti, MD, PhD, Gian Luigi Lenzi, MD
ABSTRACT. Formisano R, Pantano P, Buzzi G, Vinicola V, Penta F, Barbanti P, Lenzi GL. Late motor recover is inuenced by muscle tone changes after stroke.Arch Phys Med Rehabil 2005;86:308-11. Objectives: To evaluate the time course of motor recovery in a poststroke period ranging from 2 to 6 months and its correlation with both the severity of motor decit and the muscle tone disturbances (accidity or spasticity) of the affected limbs. Design: Prospective cohort study. Setting: A comprehensive rehabilitation hospital. Participants: Forty consecutive stroke patients (21 men, 19 women) with rst ischemic stroke who met the inclusion criteria. Interventions: Not applicable. Main Outcome Measure: Change in motor decit as evaluated by the Adams Hemispheric Stroke Scale. Results: Stepwise regression analysis indicated that the most signicant factors inuencing motor recovery were the time elapsed since stroke and muscle tone. Conclusions: Rehabilitation of stroke patients is more effective in the rst months after the event rather than later, considering the signicant correlation observed between motor recovery and time elapsed since stroke. Flaccid patients appear to need 3 months or more before reaching the nal plateau, because motor recovery occurs later and/or proceeds more slowly, whereas outcomes for spastic patients with spasticity appears to occur in the rst months after stroke. Key Words: Flaccid muscle tone; Motor skills; Rehabilitation; Stroke. 2005 by American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation MUSCULAR FLACCIDITY after appears to be a in the prognosis the P ROLONGEDnegative indicatorprevious studies,ofstrokenal outcome for stroke patients. In we ob1,2 3-5

The plateau phase is generally dened in rehabilitation as the level from which little or no further recovery is expected.1-6 Although the general pattern of recovery from stroke is one in which a plateau is reached from 6 months to 1 year after stroke,7-9 other studies suggest that in many patients, motor recovery is almost complete after 8 to 12 weeks.8,10,11 The possibility of late motor improvement, which may be induced or enhanced by rehabilitation, is unpredictable and varies. Therefore, identifying patients who may benet from rehabilitation in the later phase of stroke is desirable to avoid unnecessary expenses related to hospitalization and rehabilitation therapy.12-14 We previously reported15 that the degree of motor recovery in the late phase of stroke correlated negatively with the time elapsed since stroke and positively with preserved perfusion of basal ganglia, thalamus, and premotor cortex of the undamaged hemisphere. In the present study, we evaluated the time course of motor recovery in stroke patients during the poststroke period ranging from 2 to 6 months and its correlation with both the severity of motor decit and muscle tone disturbances (accidity or spasticity) of the affected limbs. METHODS Forty patients (21 men, 19 women) with a mean age of 62.2 12 years (range, 40 83y) who had had a single hemispheric ischemic stroke in the middle cerebral artery territory causing unilateral motor decit were consecutively enrolled. Only patients with hemiparesis and hemiplegia (and not monoparesis) were included. Patients with previous rehabilitation hospital treatment were excluded. Severity of motor impairment was measured with the Adams Hemispheric Stroke Scale16 (range, 0 [normal] to 28 [complete hemiplegia]) on admission to the rehabilitation hospital (from 2 to 6mo after stroke) (Adams 1) and 2 months after admission (Adams 2). Muscle tone changes, deep sensory disturbances, unilateral spatial neglect, and aphasia were also assessed at admission. Motor recovery was measured as the difference between the 2 scores of the Adams scale. Assessment of muscle tone and deep sensory disturbances was undertaken by 2 independent ratersa physician and a physiotherapist both blind to the research project. Categorization of patients as having either prolonged muscular accidity or muscular spasticity was based on the raters independent and concordant judgments with regard to decreased or increased muscular tone in all the articular segments (shoulder, elbow, wrist, ngers, hip, knee, ankle) of the affected side. No attempt was made to quantify the muscular tone disturbance. All subjects wore comfortable clothing and the ambient room temperature was constant. Patients were evaluated while seated in a stroke chair, as reported in previous studies.17 The assessment procedure was not standardized, because previous studies using standard measurements have found poor reliability.18 In fact, research is hampered by the lack of a valid and reliable clinical measure of the full spectrum of muscle tone, including accidity observed after stroke.18

served that motor decit, assessed 2 to 3 months after stroke, was signicantly more severe in patients with accidity than in those with spasticity, irrespective of the extent of brain lesions shown by computerized tomography (CT) or magnetic resonance imaging (MRI).

From the IRCCS Rehabilitation Hospital Santa Lucia Foundation (Formisano, Buzzi, Vinicola, Penta) and Department of Neurological Sciences, University La Sapienza (Pantano, Barbanti, Lenzi), Rome, Italy. No commercial party having a direct interest in the results of the research supporting this article has or will confer a benet on the author(s) or on any organization with which the author(s) is/are associated. Reprint requests to Rita Formisano, MD, IRCCS Rehabilitation Hospital Santa Lucia Foundation, Via Ardeatina 306, 00179 Rome, Italy, e-mail: r.formisano@hsantalucia.it. 0003-9993/05/8602-9062$30.00/0 doi:10.1016/j.apmr.2004.08.001

Arch Phys Med Rehabil Vol 86, February 2005

MOTOR RECOVERY AFTER STROKE, Formisano Table 1: Demographics and Clinical Characteristics of 40 Stroke Patients
Characteristic Values

309

Table 2: Degree of Motor Recovery in 40 Stroke Patients According to Clinical Characteristics

No. of Patients Adams Score Changes (mean SD)

Age SD (y) Sex (M/F) Time since stroke SD (mo) Motor severity at entry SD (Adams score) Unilateral spatial neglect (Y/N) Aphasia (Y/N) Deep sensory loss (Y/N) Lesion volume SD (mL)

62.2 12.0 21/19 3.5 1.5 19.7 6.0 11/29 16/24 20/20 42.7 50.0

Clinical Characteristic

Abbreviations: F, female; M, male; N, no; SD, standard deviation; Y, yes.

All patients were evaluated by neuropsychologists who sought to detect aphasia in patients with left-brain damage,19 whereas a specic battery to detect unilateral spatial neglect was administered to all patients with right-brain damage.20 In particular, unilateral spatial neglect was evaluated by means of the Barrage test, the letter cancellation test, the sentence reading test, and the Wundt-Jastrow area illusion test, as elsewhere described.3 All patients underwent cerebral CT or MRI to evaluate the site and the extent of the lesion. The volume of the cerebral lesion was measured with a dedicated software that allows measurement of the affected areas from CT or MRI (T1) images using a video display and cursor system, according to a method previously described.4 Infarcts were classied as cortical or subcortical based on involvement or sparing of cortical matter. All patients were consecutively assigned to the same 2 physical therapists, who treated them using the proprioceptive neuromuscular facilitation technique, according to the Bobath method,21 as is usually done in stroke rehabilitation. In this method, facilitation and inhibition techniques are used with selected sensory inputs to obtain automatic high-quality motor output. Data were analyzed by comparing subgroups of patients, separated according to time since stroke, muscle tone disturbance, unilateral spatial neglect, aphasia, and deep sensory loss, using the 2-tailed t test. We used stepwise multiple linear regression analysis to evaluate which of 8 clinical variables age, time since stroke, Adams 1, unilateral spatial neglect, aphasia, deep sensory loss, muscle tone, and lesion volume would be signicantly associated with motor recovery. Finally, the main effects and interaction of the above clinical features with motor recovery were analyzed 2-factor nonrepeated-measures analysis of variance (ANOVA). The signicance level was set to P equal to .05 or less. RESULTS Demographic and clinical characteristics of the patients we evaluated are shown in table 1. The mean interval since stroke was 3.5 1.5 months (range, 2 6mo). The severity of motor impairment at admission was similar in spastic and accid patients. The extent of the ischemic lesions, evaluated either by CT or MRI scans, varied from 1.3 to 194.0mL (mean, 42.7 50.0mL). The degree of motor recovery as evaluated by differences in Adams scale scores obtained at hospital admission and 2 months later varied greatly, ranging from 0 to 8 (mean standard deviation, 1.82 2.21). Degree of motor recovery was 2.6 2.2 in patients evaluated within the rst 3 months after stroke and 0.8 1.7 (P .01) in

Time since stroke 3mo 3mo Muscle tone disturbance PMF MSP Unilateral spatial neglect Yes No Aphasia Yes No Deep sensory loss Yes No

.01 23 17 23 17 11 29 16 24 20 20 2.6 2.2 0.8 1.7 .02 2.5 2.5 0.9 1.3 .33 2.0 2.2 1.3 2.2 .64 1.6 2.0 2.0 2.4 .67 1.8 2.1 1.9 2.3

Abbreviations: MSP, muscular spasticity; PMF, prolonged muscular accidity.

patients evaluated at 3 months or later after stroke. Degree of motor recovery was 0.9 1.3 and 2.5 2.5 (P .02) in spastic and accid patients, respectively (table 2). No differences were found between lesion size, age, motor decit severity, presence of aphasia, unilateral spatial neglect, and deep sensory loss at admission and the degree of motor improvement. Multiple regression analysis of the degree of motor recovery and the clinical features of age, time since stroke, Adams 1, presence of unilateral spatial neglect or aphasia, deep sensory loss, muscle tone, and lesion volume indicated that only time since stroke and muscle tone were signicantly associated with motor recovery (table 3). The relationships between motor recovery, muscle tone, and time since stroke were further analyzed. Two-factor nonrepeated-measures ANOVA showed that both muscle tone and time since stroke had a signicant effect on motor recovery (F1 5.5, P .02; F1 5.6, P .02, respectively) without any signicant interaction between the 2 factors. The greatest degree of motor recovery (2.5 2.1) was in the 14 patients with a accid hemiparesis studied within 3 months of stroke. It is also noteworthy that 7 of 8 patients with spastic hemiparesis who were studied 3 or later months after stroke had no further motor recovery. Overall, 18 of the 40 patients (45%) had no improvement at all, as if the plateau phase of motor recovery had already been

Table 3: Multiple Regression Analysis Between Motor Recovery and Clinical Characteristics
Clinical Variables t P

Age Time since stroke Adams 1 scores Muscle tone Lesion volume Unilateral spatial neglect Aphasia Deep sensory loss

.075 .427 .006 .410 .042 .258 .048 .039

0.402 2.054 0.027 2.253 0.229 1.030 0.193 0.196

.691 .050 .979 .033 .821 .313 .848 .847

Arch Phys Med Rehabil Vol 86, February 2005

310

MOTOR RECOVERY AFTER STROKE, Formisano

Fig 1. Motor recovery in 40 patients with ischemic stroke. Recovery was signicantly higher in patients with prolonged muscular accidity than in patients with muscular spasticity admitted to rehabilitation within 3 months of stroke. Recovery was less frequent in the next 2-month period, but a statistically signicant higher number of prolonged muscular accidity patients still recovered later. Legend: <3 months, admitted less than 90 days after stroke; >3 months, admitted more than 90 days after stroke. Abbreviation: Pts, patients.

reached before our rst observation. Among these patients, 11 of 17 (65%) had spasticity and 7 of 23 (30%) had accidity. The distribution of patients who did not improve with respect to both time elapsed since stroke and muscle tone disturbances is shown in gure 1. DISCUSSION The sequence and time course of motor recovery after stroke is unpredictable and varies. The processes underlying recovery from stroke and the therapeutic interventions, in particular with regard to rehabilitation efforts, are still not clear.22 Good prognostic clinical indicators of the degree of motor recovery are the time elapsed since stroke and the initial severity of the motor decit.23-27 Recovery is generally faster and more evident in the rst weeks after stroke,8,10,11,28 but the plateau phase may be reached after a time interval exceeding 1 year.29-31 In our study, which included patients in the chronic phase, the correlation between motor recovery and time since stroke was conrmed. It is also generally accepted that patients with more severe motor decits tend to have poorer outcomes.32 However, in the chronic phase of stroke, the degree of further motor recovery no longer appears to be related to the severity of the motor decit at a given time, which in our study ranged from 2 to 6 months after stroke. Therefore, although the degree of impairment from stroke is a good prognostic indicator in the acute phase after the event, it may not be when patients are evaluated some months later. As for the signicant relation between motor recovery and time elapsed since stroke, rehabilitation is less effective when initiated more than 3 months after stroke, as previously reported.28,33 However, motor recovery may still occur after this period,22,28,31 as was seen in 4 of 17 patients admitted after 3 months who had a signicant improvement in motor function ranging from 2 to 6 score differences in the Adams scale in the following 2 months.
Arch Phys Med Rehabil Vol 86, February 2005

Multiple regression analysis showed that 2 clinical variables, time elapsed since stroke and muscle tone, were associated with the degree of motor recovery. In fact, 11 of the 18 patients who had already reached the plateau phase (ie, patients with no differences between Adams 1 and Adams 2 scores) had muscle spasticity. By contrast, only 7 of 23 accid patients, showed no motor recovery, whereas the remaining 16 patients continued to show recovery, suggesting the need for more time to reach the nal plateau. In this respect, our study seems to challenge the negative prognostic role of muscular accidity in the clinical outcome of patients, as previously reported.2,3 Twitchell1 reported that a prolonged period of accidity after stroke was associated with poor recovery but did not report the total follow-up time. It is possible that recovery mechanisms emerge later and/or proceed more slowly in accid patients. For our study, we used the Adams scale to observe possible changes in motor decits and their time course during rehabilitation. We did so because functional recovery of motor impairment, as measured by functional scales such as the Barthel Index,34 is inuenced by other factors such as psychologic reactions and social environment. The time course of motor recovery in our patients supports our previous cerebral blood ow (CBF) data obtained in patients with prolonged accidity and spasticity after stroke.4,5,15 Those studies suggest that persistent accidity might represent the clinical correlate of the persistent diaschisis phenomenon. This phenomenon is associated with muscular hypotonia or accidity and reduction of CBF in cerebral areas distant from the lesion site. Crossed cerebellar diaschisis35 may in fact be related to accidity and be compatible with further motor recovery. Therefore, because muscular accidity is correlated with a higher frequency of crossed cerebellar diaschisis which is a reversible phenomenonpatients with prolonged muscular accidity could recover from motor decit later and more slowly.35 The size of the cerebral lesion does not appear to play a role in motor recovery, at least insofar as the morphologic lesion is concerned, which is in agreement with results of previous studies.5 The lack of signicant correlation between unilateral spatial neglect and the degree of motor recovery may be secondary to the use of the Adams scale rather than to other functional scales used elsewhere.36-38 Additionally, other variables, such as age, motor decit severity at entry, deep sensory loss, and volume of ischemic lesion, would not affect the degree of motor recovery. Predicting the time of the nal plateau after stroke will likely require extensive studies, particularly regarding changes in muscle tone. Improving neurologic impairment after stroke is an important issue. Further research is needed to aid in planning stroke rehabilitation facilities, programs,39 and admission criteria to rehabilitation services for patients in the late phase after stroke. CONCLUSIONS Both the time interval from stroke to the beginning of rehabilitation and the changes in muscle tone after stroke (accidity vs spasticity) appear to condition the extent and time course of motor recovery in the late phase after stroke. Results of this pilot study need to be conrmed by further studies. If conrmed, the clinical factors affecting the outcome should be considered when selecting patients in the late phase of stroke for admission to rehabilitation hospitals, given the costs of hospitalization and rehabilitation therapy.

MOTOR RECOVERY AFTER STROKE, Formisano

311

References 1. Twitchell TE. The restoration of motor function following hemiplegia in man. Brain 1951;74:443-80. 2. Landau WM. Spasticity: the fable of a neurological demon and the emperors new therapy. Arch Neurol 1974;31:217-9. 3. Formisano R, Barbanti P, Catarci T, De Vuono G, Calisse P, Razzano C. Prolonged muscular accidity: frequency and association with unilateral spatial after stroke. Acta Neurol Scand 1993; 88:313-5. 4. Pantano P, Formisano R, Ricci M, et al. Prolonged muscular accidity in stroke patients is associated with crossed cerebellar diaschisis. Cerebrovasc Dis 1993;3:80-5. 5. Pantano P, Formisano R, Ricci M, et al. Prolonged muscular accidity after stroke. Morphological and functional brain alterations. Brain 1995;118(Pt 5):1329-38. 6. Duncan PW, Badke MB, editors. Motor decit following stroke. Chicago: Year Book; 1981. 7. Anderson E, Anderson TP, Kottke FJ. Stroke rehabilitation: maintenance of achieved gains. Arch Phys Med Rehabil 1977;58:345-52. 8. Andrews K, Brocklehurst JC, Richards B, Laycock PJ. The recovery of the severely disabled stroke patients. Rheum Rehabil 1982;21:225-30. 9. Katz S, Ford AB, Chinn AB, et al. Prognosis after strokes. II. Long-term course of 159 patients. Medicine (Baltimore) 1966;45: 236-46. 10. Skilbeck CE, Wade DT, Hewer RL, Wood VA. Recovery after stroke. J Neurol Neurosurg Psychiatry 1983;46:5-8. 11. Smith DL, Akhtar AJ, Garraway WM. Motor function after stroke. Age Ageing 1985;14:46-8. 12. Feigenson JS, Feigenson WD, Gitlow HS, McCarthy ML, Greenberg SD. Outcome and cost for stroke patients in academic and community hospitals: comparison of two groups referred to a regional rehabilitation center. JAMA 1978;240:1878-80. 13. Oster G, Huse DM, Lacey MJ, Epstein AM. Cost-effectiveness of ticlopidine in preventing stroke in high-risk patients [comment in: Stroke 1994;25:1097-8]. Stroke 1994;25:1149-56. 14. Smurawska LT, Alexandrov AV, Bladin CF, Norris JW. Cost of acute stroke care in Toronto, Canada. Stroke 1994;25:1268-31. 15. Pantano P, Formisano R, Ricci M, et al. Motor recovery after stroke: morphological and functional brain alterations. Brain 1996;119(Pt 6):1849-57. 16. Adams RJ, Meador KJ, Sethi KD, Grotta JC, Thomson DS. Graded neurologic scale for use in acute hemispheric stroke treatment protocols. Stroke 1987;18:665-9. 17. Gregson JM, Leathley MU, Moore AP, Smith TL, Sharma AK, Watkins CL. Reliability of measurements of muscle tone and muscle power in stroke patients. Age Ageing 2000;29:223-8. 18. Pomeroy VM, Dean D, Sykes L, et al. The unreliability of clinical measures of muscle tone: implication for stroke therapy. Age Ageing 2000;29:229-33. 19. Basso A. Approaches to neuropsychological rehabilitation: language disorders. In: Meter MJ, Benson AL, Dialer L, editors. Neuropsychological rehabilitation. Edinburgh: Churchill Livingstone; 1989. p 294-314.

20. Pizzamiglio L, Judica A, Razzano C, Zoccolotti P. Toward a comprehensive diagnosis of visual-spatial disorders in unilateral brain-damaged patients. Psychol Assess 1989;5:199-218. 21. Bobath B. Adult hemiplegia: evaluation and treatment. 2nd ed. London: Heinemann Medical; 1978. 22. Dombovy ML, Bach-y-Rita P. Clinical observations on recovery from stroke. Adv Neurol 1988;47:265-76. 23. Johnston MV, Keister M. Early rehabilitation for stroke patients: a new look. Arch Phys Med Rehabil 1984;65:437-41. 24. Novack TA, Sattereld WT, Connor M. Stroke onset and rehabilitation: time lag as a factor in treatment outcome. Arch Phys Med Rehabil 1984;65:316-9. 25. Andrews K, Brocklehurst JC, Richards B, Laycock PJ. The rate of recovery from stroke and its measurement. Int Rehabil Med 1981; 3:155-61. 26. Heinemann AW, Roth EJ. Cichowski K, Betts V. Multivariate analysis of improvement and outcome following stroke rehabilitation. Arch Neurol 1989;44:1167-72. 27. Lincoln NB, Blackburn M, Ellis S, et al. An investigation of factors affecting progress of patients on a stroke unit. J Neurol Neurosurg Psychiatry 1989;52:493-6. 28. Kotila M, Waltimo O, Niemi ML, Laaksonen R, Lempinen M. The prole of recovery from stroke and factors inuencing outcome. Stroke 1984;15:1039-44. 29. Byorneby ER, Reinvang IR. Acquiring and maintaining self care skills after stroke. Scand J Rehabil Med 1985;17:75-80. 30. Lehmann JF, DeLateur BJ, Fowler RS Jr, et al. Stroke: does rehabilitation affect outcome? Arch Phys Med Rehabil 1975;56: 375-82. 31. Ashlio B, Britton M, Murray V, Theorell T. Disablement and quality of life after stroke. Stroke 1984;15:886-90. 32. Wade DT. Stroke rehabilitation and long term care. Lancet 1992; 339:791-3. 33. Shah S, Vanclay F, Cooper B. Efciency, effectiveness and duration of stroke rehabilitation. Stroke 1990;21:241-6. 34. Barthel L, Mahoney F, Barthel DW. Functional evaluation: the Barthel index. Md State Med J 1965;14:61-5. 35. Pantano P, Baron JC, Samson Y, Bousser MG, Derouesne C, Comar D. Crossed cerebellar diaschisis. Further studies. Brain 1986;109:677-94. 36. Denes G, Semenza C, Stoppa E, Lis A. Unilateral spatial neglect and recovery from hemiplegia: a follow-up study. Brain 1982;105: 543-52. 37. Paolucci S, Antonucci G, Gialloreti LE, et al. Predicting stroke inpatient rehabilitation outcome: the prominent role of neuropsychological disorders. Eur Neurol 1996;36:385-90. 38. Paolucci S, Antonucci G, Pratesi L, Traballesi M, Lubich S, Grasso MG. Functional outcome in stroke inpatient rehabilitation: predicting no, low and high response patients. Cerebrovasc Dis 1998;8:228-34. 39. Dombovy ML, Basford JR, Whisnant JP, Bergstrahl E. Disability and use of rehabilitation services following stroke. Stroke 1987; 18:830-6.

Arch Phys Med Rehabil Vol 86, February 2005