Cerebral palsy in adults: Independent effects of muscle strength and muscle tone

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Cerebral Palsy in Adults: Independent Effects of Muscle Strength and Muscle Tone Masaharu Maruishi, MD, Yukio Mano, MD, PhD, Tetsuto Sasaki, MD, PhD, Naoki Shinmyo, MD, Humie Sato, MD, Taro Ogawa, MD ABSTRACT. Maruishi M, Mano Y, Sasaki T, Shinmyo N, Sato H, Ogawa T. Cerebral palsy in adults: independent effects of muscle strength and muscle tone. Arch Phys Med Rehabil 2001;82:637-41. Objective: To investigate clinical characteristics and their contribution to activities of daily living (ADLs) in adults with cerebral palsy (CP). Design: Descriptions of the clinical features of medical disorders; survey. Setting: Rehabilitation counseling center in Japan. Patients: A case series of 256 patients (140 men, 116 women; mean age, 31.6yr; range, 17– 83yr) admitted to a rehabilitation center from January 1995 to December 1997. Main Outcome Measures: Characteristics investigated included severity of mental retardation, topography of motor deficits, motor power by manual muscle testing, muscle tone rated by using the muscle tone scale, deformity, sensory disturbance, and pain. ADLs were evaluated with the Barthel Index. Results: Patients showed severe impairment in terms of the Ashworth scale for grading spasticity and deformity, and moderate impairment on manual muscle testing. ADLs were influenced significantly by topography of motor deficits, manual muscle test scores, and muscle tone scale assessment (p ⬍ .0001). The muscle tone scale findings showed a significant correlation with deformity (p ⬍ .0001), but did not correlate with manual muscle testing. ADLs were affected by muscle power and muscle tone independently. Conclusion: Adults with CP showed markedly increased muscle tone and moderate muscle weakness. These 2 factors did not correlate with each other, and were independently responsible for worse ADLs. Key Words: Activities of daily living; Cerebral palsy; Rehabilitation. © 2001 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation EREBRAL PALSY (CP) is a motor disorder that results from a nonprogressive brain lesion that occurs during C prenatal or perinatal development. Motor function in patients 1

with CP changes with brain development. Therefore, clinical characteristics are assessed according to patterns of movement and developmental milestones.2,3 Assessment of activities of daily living (ADLs) has been widely substituted for quantita-

From the Department of Rehabilitation Medicine, Hokkaido University, School of Medicine (Maruishi, Mano, Shinmyo, Sato, Ogawa); and Hokkaido Rehabilitation Counseling Center for the Handicapped (Sasaki), Sapporo, Japan. Accepted in revised form July 25, 2000. The authors have chosen not to select a disclosure statement. Reprint requests to Masaharu Maruishi, MD, Dept of Rehabilitation Medicine N-15, W-7, Sapporo 060-0815, Japan, e-mail: [email protected]. 0003-9993/01/8205-5962$35.00/0 doi:10.1053/apmr.2001.22336

tive scales such as manual muscle testing to evaluate the severity of CP. Although CP is caused by a nonprogressive lesion, its symptoms persist into adulthood. There is little information about the clinical characteristics of CP in adults, though the increasing numbers of such patients present both social and medical problems. Because CP in adults is no longer affected by ongoing physiologic development, it may be more suitable for quantitative evaluation during adulthood than childhood. Assessment of clinical characteristics should be relevant to patient impairment and should be correlated with ADLs to assess disability properly. Such data have not been reported in the literature. This study examined 256 adult patients with CP to determine, with widely used grading scales, the severity of mental retardation, motor deficits, and sensory disturbances. Correlations between the scales and ADLs were analyzed statistically and certain features were found to be significant. There has been little information available about CP in adults. This study should help identify which impairments aggravate disability in adulthood, and help guide treatment plans. METHODS All patients aged 15 years and older with CP admitted to the Hokkaido Rehabilitation Counseling Center for the Handicapped from January 1995 to December 1997 were consecutively enrolled in the study. CP is defined as a motor disorder Table 1: Rating Scales for Neurologic Findings Muscle tone scale 1 No increase in tone 2 Slight increase in tone, giving a slight resistance when affected part(s) move in flexion or extension 3 More marked increase in tone but affected part(s) easily moved 4 Considerable increase in tone; passive movement difficult 5 Affected part(s) rigid Deformity 1 Normal; no deformity 2 Mild; deformity but affected part(s) easily moved 3 Moderate; deformity with passive movement possible 4 Severe; deformity and affected part rigid Sensory disturbance 1 Normal; no sensory disturbance 2 Mild; mild decrease in touch, pain, heat, or deep sensation 3 Moderate; moderate or severe decrease in touch, pain, heat, or deep sensation 4 Severe; anesthesia Pain 1 Normal; no pain 2 Mild; mild pain easily tolerated 3 Moderate or severe pain but tolerated 4 Severe; intractable pain

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Fig 1. Distribution of adult patients with (A) CP for mental retardation, (B) distribution of motor deficits, (C) manual muscle testing, (D) muscle tone scale, (E) deformity, (F) sensory disturbance, and (G) pain. Abbreviations: Quadri-, quadriplegia; Di-, diplegia; Hemi-, hemiplegia; Mono-, monoplegia.

resulting from a nonprogressive brain lesion that occurred during prenatal or perinatal development.1 Of the 256 individuals in our study, 140 were men and 116 were women (mean age, 31.6yr; range, 17– 83yr). Patients were evaluated according to intelligence quotient (IQ), type of motor deficit, muscle power, muscle tone, deformity, sensory disturbance, and pain. Only 174 patients underwent an IQ test because the time available for evaluation was limited. IQ was estimated by using the Wechsler Adult Intelligence Score–Revised or the Stanford-Binet Intelligence Scale, and was classified into 1 of 4 grades (normal, ⱖ80; mild retardation, ⱖ60; moderate retardation, ⱖ40; severe retardation, ⬍40). We classified the topography of motor deficits into 4 categories (quadriplegia, diplegia, hemiplegia, monoplegia). Other characteristics (muscle power, muscle tone, deformity, sensory disturbance, pain) were evaluated in the most severely involved part of the body. Muscle strength was classified by manual testing into 6 grades. We classified muscle tone into 5 grades by using a muscle tone scale we made by modifying the Ashworth scale4 (table 1). Deformity, sensory disturbance, and pain were rated by severity as normal, mild, moderate, or severe. Arch Phys Med Rehabil Vol 82, May 2001

ADLs were evaluated by the Barthel Index. Correlations between the Barthel Index and other measures were analyzed statistically. RESULTS Clinical Characteristics Distributions of patients for the various disease features are shown in figure 1. Most of the patients were quadriplegic, including those with deformities, those with moderate impairment as determined by manual muscle testing, and patients with severe impairment as determined by the muscle tone scale. Characteristics of CP in adults were extracted from this analysis (fig 2). Activities of Daily Living The distribution of patients with respect to ADLs was bimodal. Some patients had a low Barthel Index score, whereas this score was high in others (fig 3). The Barthel Index did not

CEREBRAL PALSY IN ADULTS, Maruishi

Fig 2. Plot of clinical characteristics in adults with CP. Abnormalities decrease as the dots move outward. Muscle tone scale rating and deformity show worsening in this series.

correlate with intelligence (fig 4A). Correlations between other factors and ADLs were analyzed (fig 4A–G). Daily activities were affected significantly by topography of motor deficits, manual muscle testing scores, muscle tone scale ratings, and deformity. Independence of Clinical Factors To facilitate analysis of the contributions of these clinical factors to problems with daily activities, correlations were assessed between the various factors (table 2). The muscle tone scale showed significant correlation with deformity, but not with manual muscle testing. Thus, the main clinical factors affecting ADLs were the topography of motor deficits, muscle power, and muscle tone. Table 3 summarizes the results and the 95% confidence intervals (CIs) for incidence by manual muscle testing and muscle tone scales. DISCUSSION Many patients with CP have little opportunity for developmental learning or full habilitation, and, therefore, remain disabled.1,2 CP shows several important characteristics1: (1) lesions arise from many variable causes; (2) postural tone is abnormal because of stresses involving reciprocal innervation and inhibition, as well as tonic reflexes; and (3) onset occurs in the developing brain. These characteristics have led many clinicians to use patterns of movement and developmental milestones to evaluate CP. We attempted to use accepted grading scales to evaluate CP in adults, given that developmental effects in this age group would be negligible. This approach would be necessary to compare CP with other clinical entities. Although use of uniform assessment scales might be logically flawed, given that CP is heterogeneous with respect to cause and pathology, other patients—such as those recovering from stroke—are evaluated by a uniform scale.5 Thus, we thought that adults with CP might be assessed uniformly with respect to morbidity. We used the manual muscle testing and the muscle tone scale to evaluate motor deficits in the adults we studied. Motor abnormalities in CP may include 5 major types: spasticity, flaccidity, athetosis, ataxia, and mixed patterns.1 Although most clinicians attempt to classify such patients, distinction

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among these patterns may be difficult. Patients frequently appear to evolve from 1 pattern to another, leading to frequent classification as a mixed pattern. Such patient movements are characterized by the hyperexcitability of motoneurons and abnormalities of reciprocal inhibition during voluntary agonist activation, with extensive and variable coactivation of muscles.6,7 Hypertonus reportedly affects not only patients with spasticity but also patients with other types of abnormalities. Narabayashi and Nakamura8 reported that patients with all of the earlier-mentioned neurologic patterns showed rigid spasticity, except for patients with choreoathetosis, and the ratio of rigidity or spasticity determined the motor pattern. Therefore, muscle tone in adult CP would be suitable for evaluation with a uniform scale. We used a muscle tone scale (which was modified from the Ashworth scale) to rate muscle tone in our patients. Statistical investigation of adults with CP has been reported only rarely.9-11 We found no studies evaluating adults with CP that used grading scales for motor deficits. In some reports, 50% of the involved patients showed mental retardation, whereas 25% had normal intelligence, and another 25% had borderline intelligence.12,13 Our data show a similar distribution: 54 patients (31%) had normal intelligence scores, 45 (26%) showed mild mental retardation, and 75 (43%) showed moderate-to-severe mental retardation. As for physical function, table 3 shows that 50% of the patients had severely increased muscle tone (muscle tone scale score, 4 or 5), whereas 25% showed severe muscle weakness (manual muscle test score, ⱕ 2). No comparable previous data were available for assessing our findings, but the ratings were consistent with clinical characteristics reported previously.14 In the present series, some factors were correlated with others. Muscle tone correlated with deformity, which may, in part, result from persistent continuing abnormal muscle tone. Therefore, many deformities would appear to be preventable through reduction of abnormally increased muscle tone. In our series, 59 patients (23%) had a sensory disturbance that correlated with pain and manual muscle testing scores. There may have been secondary changes, such as cervical spondylosis, in these patients. Topography of motor deficits, the manual muscle testing score, the muscle tone scale, and deformity affected the Barthel Index. Because deformity was influenced by muscle tone, major factors having an impact on ADLs in adults with CP were topography of motor deficits, muscle power, and muscle tone. Among our patients, the Barthel Index score, decreased by about 20 points when there was severe hypertonus or severe deformity, and by 30 points when there was severe muscle weakness.

Fig 3. Distribution of patients (n ⴝ 256) for various ADLs, showing a bimodal distribution.

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Fig 4. Correlation between (A) the Barthel Index and IQ, (B) topography of motor deficits, (C) manual muscle testing, (D) muscle tone scale, (E) contracture, (F) sensory disturbance, and (G) pain. The Barthel Index score was about 20 points lower in patients with severe hypertonus, and 30 points lower in those with severe muscle weakness. The Barthel Index was significantly affected by low manual muscle testing scores, increased tone, and the deformity. * p < .0001, Spearman’s rank correlation coefficient.

Muscle weakness did not correlate with muscle tone in our study. Therefore, muscle strength and muscle tone must be separated to assess adults with CP. CONCLUSION Adults with CP showed markedly increased muscle tone and moderate muscle weakness. These 2 factors did not correlate with each other, and both worsened ADLs independently. Therefore, we must manage these 2 problems independently. Because there are few reports in the literature about the characteristics of adult patients with CP, our report is important in Arch Phys Med Rehabil Vol 82, May 2001

Table 2: Correlation Between Each Neurologic Finding in Adults With CP Manual Muscle Muscle Tone Sensory Testing Scale Deformity Disturbance Pain

Manual muscle testing Muscle tone scale Deformity Sensory disturbance Pain

1 –.129 1 –.192 .444* –.403* .038 –.25 –.106

1 .087 .115

* p ⬍ .0001, Spearman’s rank correlation coefficient.

1 .556*

1

CEREBRAL PALSY IN ADULTS, Maruishi Table 3: Proportion and 95% CI for Incidence by Manual Muscle Testing and Muscle Tone Scale in Adults With CP Patients (n)

Manual muscle testing 5 4 3 2 1 0 Unknown Muscle tone scale 1 2 3 4 5 Unknown Total

Ratio

95% CI

37 82 58 33 29 14 3

.145 .32 .227 .129 .113 .055 .012

.102–.188 .263–.377 .186–.268 .09–.168 .074–.152 .027–.083 (—)

31 21 53 84 62 5 256

.122 .082 .204 .322 .243 .02 1.0

.082–.162 .048–.116 .155–.253 .265–.379 .19–.296

that it shows the statistical significance of the characteristics of such patients. References 1. Gans BM. Rehabilitation of the pediatric patient. In: Delisa JA, Gans BM, editors. Rehabilitation medicine. 2nd ed. Philadelphia: Lippincott; 1993. p. 666-80.

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2. Petersen MC, Kube DA, Palmer FB. Classification of developmental delays. Semin Pediatr Neurol 1998;5:2-14. 3. Badell-Ribera A. Cerebral palsy: postural-locomotor prognosis in spastic diplegia. Arch Phys Med Rehabil 1985;66:614-9. 4. Ashworth B. Preliminary trial of carisoprodol in multiple sclerosis. Practitioner 1964;192:540-2. 5. Goldstein LB, Bertels C, Davis JN. Interrater reliability of the NIH stroke scale. Arch Neurol 1989;46:660-2. 6. Leonard CT, Moritani T, Hirshfeld H, Forssberg H. Deficits in reciprocal inhibition of children with cerebral palsy as revealed by H-reflex testing. Dev Med Child Neurol 1990;32:974-84. 7. Thilmann AF, Fellows SJ, Garms E. The mechanism of spastic muscle hypertonus: variation in reflex gain over the time course of spasticity. Brain 1991;114:233-44. 8. Narabayashi H, Nakamura R. Clinical picture of cerebral palsy in neurological understanding. Confin Neurol 1972;34:7-13. 9. Ando N, Ueda S. [Functional deterioration in adult with cerebral palsy] [Japanese]. No To Hattatsu 1998;30:233-7. 10. Murphy KP, Molnar GE, Lankasky K. Medical and functional status of adults with cerebral palsy. Dev Med Child Neurol 1995; 37:1075-84. 11. Nagashima T, Kurimura M, Nishimura M, Tokinobu H, Kato S, Kanda T, et al. [Late deterioration of functional abilities in adult cerebral palsy] [Japanese]. Rinsho Shinkeigaku 1993;33:939-44. 12. Cohen ME, Duffner PK. Prognostic indicators in hemiparetic cerebral palsy. Ann Neurol 1981;9:353-7. 13. Kanda T, Fukase H, Yamori Y, Yuge M. [Locomotor prognosis at 4 years in cerebral palsy] [Japanese]. No To Hattatsu 1987;19:16-21. 14. Bobath K, Bobath B. The facilitation of normal postural reactions and movements in the treatment of cerebral palsy. Physiotherapy 1964;50:246-62.

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