Is the measurement of muscle strength appropriate in patients with brain lesions? A special communication.

Is the Measurement of Muscle Strength Appropriate in Patients with Brain Lesions? A Special Communication The most obvious, although by no means ubiquitous or sole, consequence of cerebrovascular accidents (stroke) is a predominantly unilateral muscle weakness. [1] Nevertheless, some educators and authors have been suggesting for years that the measurement of muscle strength is inappropriate (ie, invalid) in patients with stroke. During the same time, many researchers have used a variety of methods to measure the strength of patients with hemiparesis. In addition to providing a well-founded precedent for such measurements, the researchers have demonstrated a relationship between muscle strength and functional capacity and outcome. The purposes of this special communication are to 1) discuss the issue of weakness following brain lesions, 2) address a few of the specific concerns that have been voiced by opponents to the strength testing of patients with brain lesions, 3) provide an indication of the magnitude of the support and precedent that exists for muscle strength testing of these patients, and 4) present information that relates muscle strength to functional capacity and outcome.

Muscle Weakness Following

Brain Lesions and Concerns

About Its Measurement

Given the demonstrated relationship between cortical and pyramidal tract activity and muscle force production in primates, [2-6] muscle weakness should be an expected result of lesions affecting corticomotoneuron cells, their projections, and their targets. Paresis from brain lesions can be classified as resulting primarily from reduced agonist output or from antagonist subtraction. [7] Reduced-output paresis is a result of a decreased ability of the motoneuron pool to drive the motor units of a target agonist muscle. [7] This reduced output has been documented in stroke patients during specified muscular efforts [8-10] and during activities requiring patterns of muscular recruitment. [11,12] Reduced output apparently affects the number and type of motor units recruited and the frequency of motor unit recruitment. [8,9,13-15] Subtraction paresis results from resistive antagonist forces. [7] In acknowledging the reality of subtraction paresis, it is important to note that 1) antagonist restraint can occur when the antagonist is electrically inactive (because of the passive stiffness of the antagonist) [12,16-18]; 2) active antagonist resistance is unusual during static or slow-speed force measurements [8,19,20]; 3) active antagonist restraint is more likely during rapid and possibly reciprocal muscle contraction [20,21]; and 4) coactivation of antagonists can be, but is not always, a problem during functional activities. [11,20-22]

The presence of subtraction paresis is probably one of the greatest concerns of those who recommend against strength testing hemiparetic patients. Bobath states that muscle weakness is not real but relative to opposition by spastic antagonists. [23] The literature outlined in the paragraph above, however, does not indicate that antagonist restraint should be a major problem during static strength testing. Other concerns about strength testing patients with brain damage include issues relevant to the position of testing [23,24] and issues relevant to muscular function during strength testing as compared with during other activities. In regard to position, the relative capacity of brain-damaged patients to activate their muscles in different positions may not be affected in the manner that therapists have come to believe. [25,26] For example, Sjostrom et al concluded that "placement of the legs within patterns believed to facilitate (0 [degrees] knee position) or inhibit (90 [degrees] knee position) extensor motoneurons did not give rise to systematic strength variations different from those of the control subjects." [25] Bohannon similarly showed that patients with hemiparesis had comparable gravity-eliminated sitting-supine knee flexion torque ratios on the paretic and nonparetic sides. [26] Muscles no doubt function differently depending on the circumstances of their activation. For example, the quadriceps femoris muscles of a patient with hemiparesis may act quite differently when used to extend the knee of a seated subject than when used during a sit-to-stand maneuver. This fact notwithstanding, strength testing may still provide an indication of brain-damaged patients' capacity to activate a muscle group under a known set of circumstances.

Support and Precedent for

Muscle Strength Testing

Despite the opposition that some have voiced for muscle strength testing in patients with intracranial lesions, [23,24] some clinical scientists hold paresis as a major problem [27-29] and as a problem worthy of measurement. Many investigators, some of considerable eminence, have measured muscle group strength in patients with hemiparesis. Muscle group strength has been measured with ordinal scales (eg, manual muscle testing) of 3 to 10 categories, [30-50] weights, [35] handgrip dynamometers, [51-53] hand-held dynamometers, [49,54-67] fixed dynamometers, [8,9,19,68-73] and dynamic dynamometers (sometimes used in isometric mode). [20,26,41,74-81 These investigations demonstrate that the clinical measurement of muscle strength in patients with hemiparesis has spanned nearly 80 years, has involved a host of investigators and institutions, and has included a variety of muscle groups and test conditions. Although such precedence alone does not justify the measurement of strength, it does demonstrate alternatives to the opinions of such clinicians as Bobath [23] and Davies. [24]

Some of these investigators have made statements that provide support for the testing of muscle strength. Others have noted limitations of strength testing. Barer et al stated that overall neurological scores are of "dubious validity" if the progress of patients with different patterns of disability are to be compared. [47] Instead, they recommended the monitoring of individual neurological signs, among them motor function (using an ordinal strength scale). Sjostrom et al suggested that "structural and strengthwise changes may be parallel signs of brain injury per se." [25] Demeurisse et al claimed that their "motricity index," which is based on ordinal strength scores, gives a rapid indication of patient progress in motor recovery and allows interpatient comparisons and the "establishment of correlations with other clinical data." [36] In a personal communication in 1988, Demeurisse stated, "The measurement of muscle strength is essential for monitoring a rehabilitation program and for establishing an early prognosis." Wade voiced a similar stand in a personal communication (DT Wade, personal communication, 1988). He said, "I have always suspected that strength weakness is a dominant factor in determining function after stroke." After comparing handgrip strength with three other measures of upper extremity function, Heller et al concluded that "recovery of recordable (30 mm Hg) grip strength nearly always preceded other measurements of arm function during recovery and suggests that it is the most sensitive test of initial recovery." [52] Watkins et al stated that the "Cybex II system can provide useful and objective information about altered motor behavior of patients with hemiparesis." [41] Kozlowski concluded, following a study of the reliability of isokinetic testing of patients with hemiparesis, that "it may be erroneous to assume that measures of strength in hemiplegic subjects are not reliable secondary to the influence of spasticity or abnormal postural reflexes." [75] I have demonstrated in two additional unpublished studies that knee extensor muscle strength can be measured reliably (ICC [is greater than] .90) in patients with stroke. Knutsson provided similar, but qualified, support for testing muscle force in patients with spastic hemiparesis. He stated: "With correction for gravitation and control of acceleration, isokinetic movements can be used for precise measurements of muscle force produced within a large range of movement speeds." [81] He also indicated, however, that assessments of motor capacity should preferably include estimates of such components as exaggerated stretch reflexes, contractures, and excessive coactivation. He recommended the incorporation of electromyography for this purpose. Concerns similar to those of Knutsson probably underlie the comment of Hammond et al that muscle strength measurements "do not provide an understanding of the neurophysiologic basis of functional impairment." [82] Winter has expressed similar concerns regarding gait analysis. [83] Accepting these concerns as legitimate, I would note that measures such as pulse rate, blood pressure, body temperature, and body weight are of value despite their failure to explain underlying mechanisms. I find little cause either for rejecting a measure simply because it does not indicate underlying mechanisms or for complacently accepting a measurement as indicative of all that I want to know if it does not indicate such mechanisms.

Relationship Between Muscle

Strength and Patient Capacity

and Outcome

Beyond the precedent presented above, additional support exists for the measurement of muscle force-torque production (strength) in patients with intracranial lesions. This support is founded on the relationships demonstrated, in numerous studies, between strength and patient (present) capacity and (future) outcome. The purpose of this section is to present evidence that force measurements can be used to explain a portion of the variance in present and future status. I believe, as does Perry, [84] that connective tissue flexibility, muscle strength, and selective neural control are all important to function.

Perhaps the most fundamental of findings related to muscle strength in brain-damaged patients is that measurements obtained at one point in time correlate with measurements obtained at a later time and with other motor indexes. This finding can be important when patients have questions such as, "Will I get my strength back?" Logigian et al found that final MMT scores were significantly correlated (r = .78, p [is less than] .01) with initial MMT scores in 42 patients undergoing rehabilitation. [45] Bohannon showed significant correlations (r = .56-.83) between initial and final force measurements obtained by hand-held dynamometry from 16 muscle groups of 38 hemiparetic patients. [55] Bohannon and Smith found similar relationships when upper extremity muscle strength deficits were compared between initial and final assessment in 58 stroke patients undergoing rehabilitation (r = .73-.85). [58]

Smedley et al, who measured upper extremity muscle strength using an ordinal scale, found it to be correlated (p [is less than] .05) with both fine and gross motor coordination in 50 hemiparetic patients. [37] Dohrmann and Nowack also found a significant relationship (p [is less than] .005) between upper extremity weakness and decreased skill. [34] They concluded that the relationship was logical "because a weak upper extremity cannot accomplish skilled movements." [34] Sjostrom et al reported the maximal plantar-flexion torque of the affected lower extremity to be significantly correlated with the extremity's Fugl-Meyer motor score ([r.sub.s] = .66, p [is less than] .05) in 19 subjects with hemiparesis. [25] Bohannon found a correlation (r) of .631 between knee flexion force and movement speed in the lower extremity of stroke patients. [67] The variance in movement speed explained by the strength of four lower extremity muscle groups was 49.5%. Sheikh et al used a very gross four-level scale to document limb muscle function. [43] They reported significant correlations (p [is less than] .001) between activities-of-daily-living scores and upper limb function (-.487) and lower limb function (-.544). Logigian et al reported significant correlations (r = .34) between MMT grades and scores on the Barthel Index (an ordinal scale rating 10 self-care and mobility activities). [45] The MMT-Barthel Index correlations were significant on admission, on discharge, and across time. Wade and Hewer obtained similar findings. [44] Their ordinal strength measurement scores for hemiparetic patients were correlated with the Barthel Index scores initially (.749), at three weeks postinjury (.774), and at six months postinjury (.610). Feigenson et al described weakness in stroke patients as "mild," "moderate," or "severe." [31] They found such weakness to be one of the strongest predictors of patient placement upon discharge; dressing, feeding, and hygiene performance; and bowel and bladder control.

Weakness was also related to length of hospital stay. Hamrin et al reported positive and sometimes significant (8 of 24) correlations between elbow flexion-extension torques and the performance of hygiene, dressing, and household activities. [77] Fullerton et al studied the relationship between a host of predictor variables and mortality and functional outcome. [50] "Arm power" and "leg power," which were measured on a five-level ordinal scale, were among the significant predictors of functional outcome (p [is less than] .0001).

The performance of activities addressed directly by physical therapists has been correlated with measures of muscle strength. Primary among those activities is gait. Wade and Hewer found walking independence (ie, alone, with another person, unable) to be significantly correlated with ordinal measures of leg muscle strength ([gamma] = -.860). [44] Feigenson et al reported weakness to be a strong predictor of ambulation. [31]

In addition to a study by Bohannon, [62] at least four other studies have documented a relationship between quantitative measurements of muscle strength and gait performance. Hamrin et al reported that isokinetic torques of the paretic and nonparetic knees were correlated with locomotion. [77] The correlations were higher on the paretic side ([r.sub.s] = .71-.90) than on the nonparetic side ([r.sub.s] = .38-.67) Hamrin et al claimed that the highly significant correlations support the validity of the isokinetic strength test in the patients. In a more recent study, Bohannon found significant (p [is less than] .01) correlations between individual lower extremity paretic muscle group strength measurements and gait independence, distance, speed, and cadence ([r.sub.s] = .556-.840). The correlations were significant on initial assessment, final assessment, and across time. [85] In an earlier study, Bohannon investigated nine variables as potential explanations for four gait performance variables. [56] Although motor control and balance offered the best explanation of ambulatory capacity, normalized muscle strength of the paretic lower extremity was significantly correlated with gait velocity, cadence, appearance, and independence (r = .369-.511). In 11 hemiparetic patients, Nakamura et al found knee extension torque (isokinetic torque at 30 [degrees], 90 [degrees], and 180 [degrees]/sec and isometric torque at 90 [degrees] and 60 [degrees] of flexion) to be significantly correlated with walking speed (r = .595-.847) and cadence (r = .609-.853). [79] They used stepwise regression to further analyze their data and found that isokinetic torque at 90 [degrees]/sec explained 75.6% of the variance in gait speed and that isokinetic torque at 180 [degrees]/sec explained 72.7% of the variance in gait cadence. In another study on patients with stroke, Nakamura found that "strength of the affected side was the primary determinant of walking speed and that the variance explained by it gradually increased with a period of training." [80] Variance explained by strength of the affected side ranged from 25% at the initiation of gait training to 50% eight weeks later.

Among the other factors of specific interest to physical therapists and to which muscle strength measures are related are transfer performance, standing performance, rolling independence, and shoulder pain and shoulder-hand syndrome. In a study by Bohannon, the relationships between various paretic muscle group strengths and transfer independence were all significant on initial assessment ([r.sub.s] = .468-.643). [64] The correlations on final assessment and across time, although positive, were rarely significant ([r.sub.s] = .304-.477). The standing performance of 81 stroke patients was found by Bohannon to correlate significantly with the strength of six of seven muscle groups on both the paretic and nonparetic sides ([r.sub.s] = .255-.464). In an unpublished follow-up study, Bohannon confirmed the existence of significant correlations on initial assessment, final assessment, and across time. Although Bohannon, in a different study, did not find that muscle strength of the paretic side consistently explained rolling independence, he did find that the muscle strength of the nonparetic side explained rolling independence (r = .51-.75). [66] Chalsen et al concluded, from a study in which various potential causes of shoulder-hand syndrome were examined, that "weakness is a necessary but not sufficient cause for the development of shoulder-hand syndrome poststroke." [42] Bohannon found shoulder abduction and lateral (external) rotation force production to be negatively and significantly correlated with shoulder pain in hemiparetic patients on initial assessment, on final assessment, and across assessment times ([r.sub.s] = -.375 to -.583). [65] He concluded that "patients with greater weakness may be prone to the development of pain because their muscles lack adequate strength to move the joint and prevent adhesive capsulitis." [65]

Conclusion

Muscle strength is by no means a variable of such great importance that it can be justified as a sole indicator of status, change, capacity, or outcome in patients with brain lesions. Substantial precedents and evidence exist, nevertheless, to support the appropriateness of muscle strength testing in these patients. Before accepting the direction of those opposed to such testing, the clinician should consider the information presented in this communication. Because considerable variance in patient performance remains unexplained by muscle strength, the search should continue for even better targets of measurement and treatment.

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[85] Bohannon RW: Selected determinants of ambulatory capacity in patients with hemiplegia. Clinical Rehabilitation, to be published.

R. Bohannon, EdD, PT, is Associate Proffesor, Program in Physical Therapy, School of Allied Health Professions, University of Connecticut, PO Box U-101, 358 Mansfield Rd, Storrs, CT 06268 (USA).

This article was submitted August 4, 1988, and was accepted October 19, 1988.