Determining Consistency of Elbow Joint Threshold Angle in Elbow Flexor Muscles With Spastic Hypertonia Background and Purpose. Threshold angle, the point in passive range of motion where a muscle response or torque change is elicited, may be a potentially valid measure of hypertonus. Because the relationship of initial muscle length to threshold angle has not been addressed previously, this preliminary study examined whether starting elbow joint position and speed of stretch to elbow flexor muscles affect threshold angle. Subjects. Five subjects with stroke-induced hypertonia of the elbow flexor muscles participated. Methods. Two starting angles and two designated stretch speeds were applied randomly by a torque motor at each of three testing sessions. Results. Starting angle, subject, and session affected threshold angle. A 90-degree starting angle at a stretch speed of approximately 1.0 radian/s produced the most consistent threshold angles between sessions within subjects, and threshold angle was relatively consistent for some subjects, irrespective of speed. Conclusion and Discussion. If future research indicates that these data can be generalized, the use of threshold angle as a consistent measure of hypertonia will require comparison within individuals, use of a consistent starting angle, and a movement condition of a 90-degree starting angle and an approximate movement speed of 1.0 radian/s across sessions. [Wolf SI,, Segal RL, Catlin PA, et al. Determining consistency of elbow joint threshold angle in elbow flexor muscles with spastic hypertonia. Phys Ther. 1996;76:586-600.1 Key Words: Elbow; Joints; Musde spasticity; Muscle tonus; Upper extremity. Steven L Wolf Richard L Segal Pamela A Catlin Julie Tschorn Tina Raleigh Heather Kon tos Patricia Pate Physical Therapy . Volume 76 . Number 6 . June 1996 ypertonia is a symptom associated with many central nervous system disorders that frequently contributes to impaired motion or compromised functional independence.l.2 Physical therapists use a variety of treatment techniques to contrlol hypertonia so that greater range of motion (ROM), strength, and functional ability can be achieved. Assessing the severity of muscle hypertonia, however, presents a challenge. The most common assessment used in the clinic is a manual determination of the amount of resistance perceived during a passive "quick stretch." This technique, however, requires clinicians to make judgments about the response, and the method may be prone to errors because of variability in the applied stretch. Measurements indicative of volitional movement, such as the Ashworth scale, provide valuable information but do not specifically assess hypertonia.' Improved measurement techniques are needed to accurately quantify the degree of hypertonia. Better quantification will allow therapists to draw correlations or inferential relationships with measures relating to physical therapy interventions and, ultimately, to changes in disability. Spastic hypertonia is observed in motor disorders that are characterized by velocity-dependent increases in SL Wolf, PhD, PT, FAPTA, is Professor and Director of Research, Department of Rehabilitation Medicine, and Associate Professor, Department of Anatomy and Cell Biology, Emory University School of Medicine, 1441 Clifto'n Rd NE, Atlanta, GA 30322 (USA) ([email protected]). Address all correspondence to Dr Wolf: RL Segal, PhD, PT, is Associate Professor, Department of Rehabilitation Medicine, Division of Physical Therapy, and Assistant Professor Department of Anatomy and Cell Biology, Emory University School of Medicine. PA (htlin, EdD, PT, is Professor and Director, Division of Physical Therapy, Department of Rehabilitation Medicine, Emory University School of Medicine. J Tschorn, PT, is Staff Physical Therapist, Grady Memorial Hospital, 80 Butler St SE, Atlanta. GA 30335. T Raleigh, PT, is Staff Physical Therapist, Promina Gwinnette Health Systems, Lawrenceville, GA 30245. H Kontos, PT, is Staff Physical Therapist, Tampa General Rehabilitation Hospital, Tampa. FL 33601. P Pate, PT, is Staff' Physical Therapist, Rancho Los Arnigos Hospital, Downey, CA 90242 Ms Tschorn, Ms Raleigh, Ms Konto5, and Ms Pate were graduate students, Division of Physical Therapy, Department of Rehabilitation Medicine, Emory University, during this study, which was undertaken in partial fulfillment of thr requirements for their Master of Physical Therapy degree. This stndy was supported in part by NIH Research Grant No. NS28784, US Public Health Service, Department of Health and Human Services, and was approved by the Emory University School of Medicine Human Investigation Committee. Thzs nrlzclv iunr ruhmztt~dMarch 4, 1995, and iuns arc~/)tpdF~brunry20, 1996. Physical Therapy . Volume 76 . Number 6 . June 1996 Wolf et al . 587 not be construed as suggesting that slower passive tonic stretch reflexes with exaggerated tendon jerks, resulting from hyperexcitability of the stretch r e f l e ~ . ~ stretches cannot also yield exaggerated muscle reflex responses. When a muscle is stretched, spindle afferent neurons initiate a short-latency motor response (the stretch The starting angle may be an indirect index of the point reflex) to correct the perturbation and return the musto which a muscle may be passively lengthened before cle toward its resting length. Motoneurons with memeliciting an EMG response (threshold). Speed of passive brane potentials that are nearer to threshold of activastretch may affect the magnitude of the hyperactive tion may be more readily excited by spindle afferent stretch reflex and the threshold angle. At present, the nerve input during sudden muscle lengthening. This effects of starting position (muscle length) and speed of situation, along with reduced inhibitory influences from passive stretch on the threshold angle of a joint acted interneurons, constitute one possible mechanism for upon by a hypertonic muscle are not well-documented. spastic h y p e r t ~ n i aThis . ~ enhanced motoneuron sensitivDevelopment of an effective measurement technique to ity may result in shorter latency of muscle response to a detect onset of muscle response to passive stretch may phasic length change and may be manifest as a heighthelp quantify hypertonia. ened muscle responsiveness to these imposed length changes. The threshold angle is the joint angle during a This study, therefore, examined the effect of starting passive stretch at which electromyographic (EMG) activangle and speed on the threshold angle in subjects ity increases above a resting l e ~ e l . l ,Threshold ~-~ angle is diagnosed with stroke-induced hypertonia. We see this presumably a measure of the relative state of motoneuimpairment-based evaluative approach as a necessary ron membrane depolarization and has been proposed as precursor to gathering information about the impact of a quantitative measure of h y p e r t ~ n i a . ~ , ~ interventions on sensitivity to muscle-length changes. Indeed, reliable intrasubject findings about the relationMechanical influences from muscle and connective tisship ofjoint starting angle, speed of passive motion, and The initial sue alter the manifestations of hypert~nia.'-~ position of a joint (starting angle) affects the length of reflex responses pave the way to ultimately correlating, the associated muscles; consequently, the degree of in a quantitative fashion, the relationships between a specified impairment (hypertonicity), interventions, and depolarization among motoneurons is influenced by the functional outcomes. spatial and temporal summation of cutaneous and proprioceptive inputs onto them at any given starting angle. Muscle response to a passive stretch and the threshold angle, therefore, would be affected. If threshold angle remains the same for each respective starting angle, then Design the threshold angle may be a valid measure of hyperFive subjects were randomly assigned to 1 of 24 possible tonia regardless of mechanical influences, such as sequences of movement at each of three sessions. No changes in connective tissue viscoelastic properties, or sequence was repeated. Each sequence included four the initial joint position. If threshold angle changes for conditions of either 70 or 90 degrees of starting elbow flexion and a target speed of either 0.5 or 1.0 radian/s of each respective starting angle, then threshold angle may be a valid measure of hypertonia only within the respecmovement. Data were collected for each of three stretches during each condition. tive starting angle. The measurement of threshold angle may require specification of joint position for which a reproducible threshold angle can be seen prior to Sample initiating any intervention. The measurement of threshSubjects were adults 31 years of age or older with old angle attempts to objectively reflect the variability of hypertonicity in the upper extremity secondary to stroke hypertonia seen clinically. occurring more than 4 months prior to data collection. Presence of hypertonicity was determined by detection The speed of stretch may affect muscle tension or torque of resistance to a manual passive stretch of the elbow development, altering the presentation of hyperflexors of the involved limb. Each subject's involved limb t ~ n i a . ~ , " ~ - I Vmagnitude he of stretch reflexes is observcould be passively moved through the entire elbow ROM ably altered by speeds greater than 1.0 radian/s (1 radineeded for the data-collection procedure, and no elbow joint contractures were present. Subjects were selected an=57.3"),yet the mechanism by which speed alters the from a registry of patients with stroke, and participation stretch reflex is controversial. Faster speeds could alter the stretch reflex by decreasing the threshold of was voluntary. Prior to participation, each subject signed a consent form approved by the Emory University School motoneuronal excitability, by increasing muscle stiffness secondary to speed-dependent viscoelastic properties, by of Medicine Human Investigations Committee. Physician consent for subject participation was obtained. The altering muscle spindle sensitivity, or by any combinarights and privacy of the subjects were protected. tion of these variables4 This situation, however, should 588 . Wolf et al Physical Therapy . Volume 76 . Number 6 . June 1996 Table 1. Characteristics of Subiects Characteristic Age (Y) Subject No. 1 2 3 4 5 58 42 42 41 31 Gender Female Female Male Female Male Site of lesion Bilateral lacunar lesions in basal ganglia, thalamus, and periventricular white matter Right frontal lobe and internal capsule Right middle cerebral artery infarct at right basal ganglion Basilar artery thrombosis at brain stem Left circle of Willis, intracranial Hand dominance Right Right Right Right Right Time since lesion (mo) Recovery stage' 4 4 18 72 7 3 2-3 3 4 3 Left Right Right Side of hypertonia Right Left The selection criteria included (1) presence of resistance to muscle stretch," (2) elbowjoint passive ROM of 10 to 90 degrees of flexion, (3) ability to achieve an appropriate sitting position for testing, (4) ability to follow verbal commands, (5) appropriate cognition,14 (6) stage 2 moving into 3 to 5 of recovery according to the Brunnstrom stages of re~overy,~"nd (7) EMG activity above a resting baseline level upon passive stretch. Measurements The starting angle was defined as the position of the elbow joint of the affected extremity measured just before an induced passive stretch using standard goniometric technique.l"tarting angles corresponding to functional length-tension relationships of the elbow flexor nluscles were chosen. These angles corresponded to slightly more than 50% of normal passive ROM. A series of three extension stretches were performed at a starting angle of 70 or 90 degrees of elbow flexion. Movemlent speed was defined as the speed of the extension stretch applied by the torque motor in servo mode. The mean of the baseline levels of elbow flexor muscle activity during passive stretch in four persons without hypertonia was obtained. These baseline values were typically around 4 pV (SD=3) for the biceps brachii muscle and 6 pV (SD=4.5) for the brachioradialis muscle. The threshold angle was then defined as the elbow joint position during stretch at which a subject's muscle activity exceeded two and a half standard deviations above this mean. The resultant criterion values required that biceps brachii muscle activity be greater than 10 pV and that brachioradialis muscle activity be greater than 15 pV. The EMG signal was amplified Physical Therapy. Volume 76 . Number 6 . June 1996 (X1,OOO) and filtered between 20 and 500 Hz. The actual threshold value was determined from filtered EMG activity. The EMG activity was measured with surface electrodes placed o n the skin over the bellies of the biceps brachii and brachioradialis muscles. The EMG activity and joint position were recorded during a stretch of a 1-radian (57.3") arc. The computer sampled the following measures at 1 kHz: joint angle, stretch speed, EMG activity of the biceps brachii and brachioradialis muscles, and torque. Electromyographic activity above the set criterion also was determined by the computer. Joint position versus EMG activity was graphed from computer data. Graphic representation of the threshold angle was used to visually confirm the computer criterion for designating the threshold angle. Subject Selection Subject characteristics and selection criteria were measured during a n initial screening session (Tab. l ) . Fortunately, enlistment of individuals with discretely different lesion sites was possible, allowing examination of consistency of responses. Information regarding age, gender, site of lesion, time since lesion, medical history, diagnosis, medical treatment received, past physical therapy treatment, aerobic exercise, and current medications was obtained by review of the medical record or subject interview prior to the initial screening session. During the initial screening session, side of hand dominance, upper-extremity recovery stage,]'. elbow passive ROM, ability to follow simple verbal commands, ability to achieve a comfortable sitting position, appropriate cognition, and EMG responses were determined by standard clinical tests. Cognition was considered normal Wolf et al . 589 if the subject responded correctly to all items on the modified Folstein Mini-Mental State Exam.14 Each subject answered questions concerning feelings of general health, level of relaxation, and amount of caffeine intake prior to both the initial screening session and each of two data-collection sessions. A variety of lesion sites are represented. Subject and Electrode Positioning Subject sitting position was controlled during each datacollection session. Position was determined at each session by measuring the following variables using standard goniometric technique: (1) knee flexion between 80 and 100 degrees, (2) hip flexion between 80 and 100 degrees, (3) shoulder abduction between 40 and 60 degrees, (4) shoulder flexion at 20 degrees, (5) elbow flexion at 70 or 90 degrees, (6) forearm in 10 to 20 degrees of pronation, and (7) wrist neutral.16 Subjects faced forward with feet shoulder width apart and the uninvolved upper extremity placed comfortably on their lap. Two silver-silver chloride electrodes with a Qmm recording surface were placed over each muscle at the beginning of the screening session. Electrode placement was determined by isolating the bellies of the biceps brachii and brachioradialis muscles during isometric contractions." Measurement of the anatomical point of widest girth of the biceps brachii or brachioradialis muscle during an isometric contraction of that muscle was used to isolate each muscle belly. The vertical and horizontal midpoint of the each muscle belly at the point of widest girth was marked with a felt-tip pen. The electrode pair was placed on either side of the marking, oriented parallel to the muscle-fiber direction." Electrode pairs were spaced at 1.7 cm center-to-center to improve specificity of the EMG signal. Isometric contractions also were used to verify correct electrode placements. All EMG activity was monitored on an oscilloscope to detect artifact during actual movements or prior to stretch. Impedance between the skin and the overlying electrode was reduced by abrading the skin with sandpaper and cleansing the skin with alcohol. Skin impedance, measured with an ohmmeter, between the ground electrode and each electrode was less than 5 kfl. The resistance between an electrode pair on each muscle belly was less than 2 kfl. After initial electrode placement was determined during the screening session, an anatomical skin map was made. The skin map measured electrode placement from nearby landmarks such as anatomical structures, scars, or prominent freckles. The distance from the acromion to the biceps brachii muscle electrode and the distance from the styloid process of the radius to the biceps 590 . Wolf et al brachii and brachioradialis muscle electrodes were measured. The skin map was used a t each session to ensure consistent electrode placement. Reliability Intrarater and interrater reliability of all measurements was maintained at 100% agreement of values, obtained by repeated measurements by the same researcher or by a second researcher. Total agreement was observed for defining age, gender, hand dominance, site of lesion, time since onset, side of hypertonicity, upper-extremity stage of synergy involvement,'%nd ability of the subject to achieve testing position. Total agreement also was achieved for identifying medical history, physical therapy treatments, exercise, medications, general health, level of relaxation, and caffeine intake. There was total intrarater and interrater reliability in defining subject cognition and onset of EMG responses. Starting angle was equal within 2 1 degree, subject position was equal or within ?3 degrees, skin map placement was equal within k0.5 mm, and skin impedance equaled exact agreement. Agreement on threshold angle was determined by comparing computer calculation with graphic displays, as described previously, and was always maintained at 100% when performed in this manner. Calibration of all equipment was maintained throughout data collection. Limb Movements Slow acceleration and deceleration of the forearm by the torque motor produced a smooth, passive stretch. The set speed produced by the torque motor was not instantaneous. The acceleration period needed by the torque motor to reach the set speed was affected by the inertia of the limb and the inherent delay in the acceleration phase of the motor. To ensure consistency of speed, responses were examined within and across sessions. Figure 1 shows such consistency for the 70-degree starting angle at 0.5 radian/s within a subject (A) and across sessions (B). T h e across-sessions graph exemplifies the superimposition of the first stretch. Periodically, threshold angle was reached before the torque motor achieved the preset speed (ie, the limb was still accelerating). The actual speed at the occurrence of threshold was determined for every stretch using the slope of time versus joint angle. Intrarater and interrater determinations of actual speed agreed 100%. All calculations regarding threshold angles were made at the actual speed at which they occurred. Thus, in calculating data by conditions, although the true speeds were used, we refer to conditions in the sense that the torque motor was programmed to move at either 0.5 or 1.0 radian/s. Data in Figures 2 and 3, for example, depict the actual speed at which the threshold angle was achieved, and computations made in Table 2 were based on actual speeds. Physical Therapy . Volume 7 6 . Number 6 . June 1996 20 - L A 30 - - 40 - - 50 - / W y - $ m 5.0: 70 * ~ T l B - ~ l l ~ l 0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0 ~ n ~ l 0 l1 ~l 1 ~ 1 ~ 1 ~~ 1 ~ 1 ~ 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0 TIME (s) TIME (s) _I -- Plot of tirr~eversus ioint angle from typical biceps brachii muscle stretches showing approximately linear speed. Speed was calculated as the slope of the graph at the threshold angle. (A) Superimposition of three stretches from one session. (B)Superimposition of first stretch at each of three sessions. Actual excursion is approximately 0.93 radian; actual speed is 0.46 radian/s. Y axis is identical in A and B. Proced~rre If a subject met all screening criteria, the first datacollection session was begun immediately. Prior to the screening session and each data-collection session, the subject was asked a set of pretrial questions to assess his or her emotional and physical state at the time of data collection. Electrode placement sites over the biceps brachii and brachioradialis muscles were determined at the screening session. The subject's skin was prepared, and the electrodes were placed on the electrode sites. Skin impedance was measured. The subject was positioned in the chair, the involved forearm was placed in the prefabricated arm splint, and the elbow was aligned to the axis of the 7.2-hp torque motor (Fig. 4).* The electrodes were connected to the amplification system and to the oscilloscope. Electromyographic activity was preamplified at the source ( X 10) and subsequently amplified ( X 100) prior to analog-to-digital processing. The subject was asked to contract and relax the upperextremity muscles to check for EMG activity o n the oscilloscope and then was positioned correctly with the involved elbow placed at the selected starting angle. The speed was set using a computer servo-mode program. Subjects were instructed to maintain the testing positioin without movement prior to testing. The muscles under the electrodes were determined to be passive prior to testing by recording a baseline of EMG activity 100 milliseconds prior to stretch while the subject remained relaxed. Three stretches were performed during each of the four conditions. All stretches were separated by at least a 60-second interval. The procedure was repeated for two additional sessions, separated by 1 to 7 days. Each of the remaining data-collection sessions began by positioning the subject at the torque motor in the servo mode. The skin map was used to locate the electrode placement sites. The subject received a different random sequence of the four conditions at each of the three data-collection sessions. Data Analysis A computer graphics program plotted the raw data on a graph, with joint position on the X axis and EMG activity of the biceps brachii or brachioradialis muscle o n the Y axis. Typical changes in the biceps brachii muscle during stretch are depicted by the arrows in Figures 5A and 5B. The occurrence of threshold angle can vary. Figure 5A demonstrates a n abrupt EMG response to stretch, and Figure 5B demonstrates a more gradual response for the same muscle but from a different subject. Threshold angle was determined for the biceps brachii and brachioradialis muscles during each stretch. A mean threshold angle also was calculated for each muscle "'PMIMotion Technologies, 49 Mall Dr, Commack, NY 11725. Physical Therapy . Volume 76 . Number 6 . June 1996 Wolf et al . 591 1 ~ / 90. STARTING ANGLE & 0.5 radianls +70° STARTING ANGLE & 1.0 radianls A BICEPS BRACHll MUSCLE 0.90 0.80 1.00 5 + 00 =aB O -fft a 0 G9 -ltPr 0.70 - @@ -tttt#k n 0.60 E B 0.50 W a V) 0.40 - @ .- - 0 Q ~ @ 0 = ' . - 0.30 - 0.10 - 00 0.20 0.00 -1,,,,,,,,,1,,,,,,,,,Irrrmllljlllllllltl 0 10 20 30 40 50 60 70 80 90 THRESHOLD ANGLE ( O ) 90" STARTING ANGLE 8 0.5 radianls +70° STARTING ANGLE & 1.0 radianls B BRACHlORADlALlS MUSCLE 1.00 - - 0.90 - - -9e -r? .-m u W P v, 0.80 0.70 - 0 during each condition per session. The EMG activity was monitored during each stretch for torque motor noise, and data for a stretch were discarded if the baseline showed harmonics of 60-cycle activity. Trials that were discarded for this reason were repeated. Graphic representation of muscle activity during each stretch was examined to detect movement artifact. For 12 of 360 data points, information was irretrievable from disks, and a program for maximum likelihood estimation that assumes compound symmetry was used to estimate stretches. Using the Statistical Analysis System (SAS) program,t riormality of distribution of threshold angle per muscle was assured prior to statistical analysis, based on assessment of the skewness and kurtosis of the data. The difference in threshold angles within conditions, within subjects, behveen testing sessions, and per muscle was determined using a one-way repeated-measures analysis of variance (ANOVA). The Tukey pair-wise procedure was performed post hoc when a statistically significant effect was found. The difference in threshold angles behveen conditions, within subjects, and per muscle was determined using a two-way (starting angle X speed) ANOVA. A Bonferroni post hoc multiplecomparison procedure was performed when a statistically significant effect was found.lHFor all tests, P<.05 was considered significant. A power analysis to determine the applicability of the results to a larger population could not be undertaken due to the complexity of the design and of the data analysis. The SAS program was used to calculate the ANOVAs.lWata analysis across subjects was not performed, as it was determined that these analyses would be irrelevant due to expected differences in muscle response to passive stretch across individual^.^,"^^ 0.60 - 0.40 0.50 0 Results 0 - Om% 9 0.30 0.20 0.10 0.w - 0 10 20 30 40 50 60 70 80 90 THRESHOLD ANGLE (") Figure 2. Composite threshold angles at specified speeds for (A) biceps brachii muscle and (B) brachioradialis muscle. There is wide variation of threshold angles across all subiects, demonstrating inconsistency in threshold angles between subjects. The complete distribution of threshold angle determination for all subjects is shown in Table 3. Figures 2A and 2B present, for the biceps brachii and brachioradialis muscles, respectively, the actual threshold angles for all stretches among all subjects and demonstrate the wide variability across subjects per condition. If the threshold angle would have been consistent, a vertical orientation of threshold angles across subjects would be expected for each condition. The effect of session on threshold angle was variable and dependent on muscle and condition (Tabs. 4 and 5 ) . Table 4 shows Fstatistic values for significant session effects seen at all conditions except at a 90-degree starting angle and a stretch speed of 1.0 radian/s. For the condition of 90-degree starting angle and 1.0- 'SAS Institute Inc, PO Box 8000, Cary, NC 2751 1 592 . Wolf et al Physical Therapy . Volume 76 . Number 6 . June 1996 radian/s stretch, no effects were found in the brachioradialis muscle and only subject 4 showed a n effect for the biceps brachii muscle. For the condition of 70-degree starting angle and 0.5-radian/s stretch, three subjects (1, 2, and 4) showed a difference in threshold angle for the biceps brachii muscle and only subject 4 showed a difference for both muscles. Three subjects (2, 3, and 4) showed a difference in threshold angle in the biceps brachii muscle as well as the brachioradialis muscle for the condition of 90degree :starting angle and 0.5-radian/s stretch. Two subjects showed a difference in threshold angle in the biceps brachii muscle as well as the brachioradialis muscle fix the condition of 70-degree starting angle and 1.0-radian/s stretch. Only subject 1 showed a difference in threshold angle for both muscles. An examination of the data1 presented in Table 5 reveals no consistent pattern of session effect of the mean threshold angles. Figures 3A and 3B demonstrate the magnitude of consistency between mean threshold angles per session per subject iin the biceps brachii and brachioradialis muscles. In both muscles, this consistency is most observable in the condition of 90-degree starting angle and 1.0radian/s stretch. Each data point represents mean threshold angle per subject per session. The symbols were most clustered in a vertical pattern for each subject at the 90-degree and 1.0-radian/s condition. The more vertically superimposed the symbols representing a subject were, the more consistent was the response. Only the biceps brachii muscle response of subject 4 in the 90-degree and 1.0-radian/s condition showed substantial variance (Fig. 3A). For most subjects, the vertical distribution of mean session responses for the brachioradialis muscle showed tight vertical clustering in the 90-degree and 1.O-radian/s condition (Fig. 3B). Threshold angle was not affected by speed for the biceps brachii or brachioradialis milscle among individual subjects (Tab. 2). In an effort to determine the relationship between the true speed of movement and the threshold angle, a one-way repeated-measures analysis of covariance was performed, substituting the actual speeds of movement for all five subjects over three sessions for each muscle. These results also showed n o relationship between threshold angle and speed. Threshold angle responses, however, were affected by the starting angle. The starting angle had an effect on threshold angle for the biceps brachii muscle for subjects 1, 3, and 5 and for the brachioradialis muscle for subjects 1, 3, and 4. Table 6 shows the relationship between the starting angles ;at which an excursion was found. Clearly, a stretch from a 90-degree starting angle consistently showed a greater amount of limb excursion prior to occurrence of threshold angle than did a stretch from a 70-degree starting angle. Physical Therapy . Volume 76 . Number 6 . June 1996 The actual threshold angle also was recorded among all subjects at select speeds and starting angles. This record provides a surrogate measure for muscle length at the time an elevated response in muscle activity was observed. Despite the greater excursion seen at a starting angle of 90 degrees, the threshold angles for some subjects were remarkably similar to those seen at a starting angle of 70 degrees. We calculated actual threshold angles averaged across trials among subjects who had complete data sets (subjects 1, 3, and 5 for the biceps brachii muscle and subjects 1 and 3 for the brachioradialis muscle) and who also showed differences in excursion, as depicted in Table 6. Among these differences, subject 1, for example, exhibited only a 2-degree difference in the actual value of threshold angle for the biceps brachii muscle between 70 and 90 degrees (Fig. 3A) arid a 1-degree difference for the brachioradialis muscle (Fig. 3B) for threshold angles recorded at 0.5 radian/s. The most extreme averaged differences in actual threshold angle with different starting angles were measured in the biceps brachii muscle for subject 3 at 0.5 radian/s (15", compare top left and right panels, Fig. 3A). Discussion Muscle responsiveness to passive lengthening using threshold angle as a measurement has been presented by Rymer and c ~ l l e a g u e s l ,as ~ ,a~justifiable ~~ technique for assessing hypertonia. Extraction of information from their studies suggests that threshold angle can be influenced by factors such as time of testing, individual attributes, viscoelastic properties of the muscle, starting muscle length, and speed of stretch. Of these factors, the resting length of a muscle exhibiting hypertonia and the speeds at which the muscle is moved have not been presented in terms of their consistency to produce a threshold angle response within subjects with hypertonia. Our data shed light on these issues. Within any subject or condition, no pattern of session effect could be determined (Tab. 5). Results from previous studies4.6 suggest a change in threshold angle between sessions. The variability of the threshold angle may be explained by the pseudorandom reflex proposed by Dietz and Berger," who found that motoneuronal firing may be altered by a functional movement and may change the occurrence of threshold. Dietz and Berger suggest that the strength of the hypertonic reflex response is decreased because the motoneuronal firing is dampened by a functional position. A 90-degree starting angle and a specified 1.0-radian/s speed had the most reproducibility across sessions, with only one session effect for the biceps brachii muscle for subject 4 (Tab. 5). The condition of a 90-degree starting angle and an approximate speed of 1.0 radian/s may produce the most consistent threshold arigle response within each subject due to a combination of the shorter muscle Wolf et al . 593 A BICEPS BRACHll MUSCLE 0 CONDITION 70' & 0.5 radianls 1.0 1.0 - 0.9 - 0.8 - 0.7 - $ 0.6 - 6 0.5 --_ 0.4 - 0.9 0.8 0.7 c .- 0.8 - 0.4 V) A - 0.5 B E .u - B - V) -- fi Y . A - 0.3 - 0.2 - 0.2 - 0.1 - 0.1 - 0.0 0 - - 0.0 0 10 20 30 40 50 60 70 0 THRESHOLD ANGLE (O) - 1.0 - 0.9 - 0.9 - 0.8 - 0.8 - 0.7 - 0.7 - 0.6 - 0.6 - 0.5 - 0.4 - A f .-m u 0.5 - 0 w 0.4 V) 0 2 0 3 0 4 0 5 0 6 0 7 0 8 0 9 0 CONDITION go0 & 1.o radianls 1.0 .u 1 THRESHOLD ANGLE (O) 1.o radianls CONDITION 700 6 radianls 0.3 - - -$ SUBJECT 4 SUBJECT 5 CONDITION 90' & 0.5 - A + A SUBJECT 1 SUBJECT 2 B - + +4 V) 0.3 - 0.3 - 0.2 - 0.2 - 0.1 - 0.1 - 0.0 0 0.0 1 I I II I I 1 II ,I, 0 I0 20 p 30 40 THRESHOLD ANGLE ( O ) igure 3. 50 60 70 0 1 0 2 0 3 0 4 0 5 0 6 THRESHOLD ANGLE (O) 0 7 0 8 0 9 0 - ~resholdangle determinations shown for each condition for [A) biceps brachii muscle and [B) brachioradialis muscle. Each symbol represents the ean for threshold angles for one session for each subiect. Note that the 90degree and 1 .O-radian/s condition shows the most vertical clustering means within subiects, demonstrating more consistent threshold angles than the other conditions. Some data points are missing for subject 4 due artifact when eliciting threshold angle responses at 9 0 degrees and 0.5 radian/s and at 9 0 degrees and 1.0 radian/s. 594 . Wolf et al Physical Therapy . Volume 76 . Number 6 . June 1996 BRACHlORADlALlS MUSCLE B radianls COND~T~ON 70' & 0.5 -$ .-m CONDITION go0 & 0.5 radianls 1.0 - 1.0 - 0.9 - 0.9 - 0.8 - 0.8 - 0.7 - 0.7 - 0.6 - 0.5 - .r? c m .u u g 9 f A SUBJECT 2 I +SUBJECT SUBJECT 4 5 0.4 0.8- g 0.5- g 0.4- 9 - V) V) 0.3 - 03 - 0.2 - 0.2 - 0.1 - 0.1 - 0.0 - 0 1 0 M 3 0 4 0 5 0 6 0 7 0 0 1 0 2 THRESHOLD ANGLE (O) CONDITION 700 & 1.o radianls -$ .- 1.0 - 0.9 - 0.8 - 0.7 - 0.6 - n 0.5 +A 0 4 + -$ .-m Oco - 0 4 0 5 0 6 0 7 0 8 0 9 0 - 1.0 -7 0.9 - 0.8 - 0.7 - 0.6 - 0.5 - 0.4 - A A%o u * W 0.4 3 CONDITION go0 & 1 .o radianls u g 0 THRESHOLDANGLE (O) g n w V) V) 0.3 - 0.3 - 0.2 - 0.2 - 0.1 - 0.1 - 0.0 - 0.0 - 0 1 0 2 0 3 0 4 0 5 0 6 0 7 0 THRESHOLD ANGLE ( O ) length prior to stretch and the specified speed of stretch. The act.ual speed of movement when threshold was reached was close to 1.0 radian/s at the starting position of 90 degrees for most stretches. The greater reproducibility in. this condition may be due to the actual speed being more consistently generated than at the condition of 70 degrees and 1.0 radian/s. Physical Therapy. Volume 76 . Number 6 . June 1996 0 1 0 2 0 3 0 4 0 5 0 6 0 7 0 8 0 9 0 THRESHOLD ANGLE ( O ) Pretrial questions revealed consistency within all subjects for caffeine intake, medications, level of relaxation, and perception of general health. All subjects also were tested at the same time for each testing session. These factors, apparently, did not contribute an explanation for the variability in session effect. Wolf et al . 595 Table 2. Two-Way Analysis of Variance Testing for a Condition Effect for Threshold Angles Within Subjects Speed Subject No. F Starting Angle P F Interaction P F P Biceps brachii muscle 1 2 3 4 5 Brachioradialis muscle 1 2 3 4 5 The lack of an effect for speed within subjects on threshold angle does not support the clinical evidence The that hypertonia is speeddependent (Tab. 2) fastest speed used in this study, 1.0 radian/s, may not be as fast as the "quick stretch" performed in clinical settings to assess hypertonia. Given et al" recently found that speed of movement did not strongly affect stretch reflex behavior within four subjects who had sustained a stroke, using speeds ranging from 0.1 to 2.0 radian/s. Their subject with the greatest hypertonia assessed clinically, however, required a lower stretch speed to reach threshold than did a subject with mild hypertonia. Previous studies4."~'"have found an effect of speed on reflex threshold in some subjects, with a decrease in threshold angle occurring as a function of an increase in speed. These studies used stretch speeds ranging from 0.25 to 3.0 radian/s. The large range may explain the reported impact of speed on threshold. Our study used only speeds approximating 0.5 and 1.0 radian/s, which may not have been fast enough to create a speed effect on threshold angle. These speeds were chosen, however, to allow accurate comparison of results with those of previous studies that used similar speeds during data collection. .43"9-12 A correlation between decreased limb excursion prior to reaching the threshold angle and greater sensitivity to stretch was reported by Powers et al,H who did not consider the relationship of the starting position before the stretch occurred. In our study, an effect of starting angle on the magnitude of joint excursion to reach threshold angle was noted for both the biceps brachii and brachioradialis muscles in three subjects (Tab. 2). These effects accounted for 60% of total threshold angle values. The smaller excursion to reach the threshold 596 . Wolf et al angle occurring frorn a 70-degree starting angle or the larger excursion to reach threshold angle occurring from a 90-degree starting angle may be a result of increased stretch reflex sensitivity at the 70-degree position. Table 6 shows that the 90-degree starting angle permitted a greater limb excursion prior to reaching the threshold angle than did the 70-degree starting angle. Stretch reflex sensitivity is increased at 70 degrees, when stretch begins with the muscle in a more lengthened position. Muscle spindle sensitivity may be greater at a 70-degree starting angle, or motoneurons may be closer to threshold level, as evidenced by less excursion of the limb prior to the occurrence of threshold (Tab. 2). With a 90-degree starting angle, the limb goes through greater excursion prior to threshold, indicating either decreased stretch reflex sensitivity or a greater magnitude of "slack" in the muscle prior to activating sufficient spindle input to further depolarize motoneurons to threshold. Elevated stretch reflex sensitivity is thought to be due, in large part, to supraspinally mediated increased background levels of depolarization of motoneurons prior to stretch, manifest in a greater threshold angle.3 At a 70-degree starting angle, the motoneuron is closer to depolarization and therefore threshold angle occurs earlier. Powers et alRplaced their subject's biceps brachii muscle in a shortened position, at 120 degrees of elbow flexion, creating an even greater amount of slack than at 90 degrees. Threshold occurred broadly, at between 117 and 63 degrees of flexion.# This observation suggests that joint angles may have an important influence on threshold angle. If analysis was possible between the starting angles used in both studies, a 120-degree starting angle would probably allow greater limb excursion prior to reaching threshold angle than both the 70- and Physical Therapy . Volume 76 . Number 6 .June 1996 Fi ure 4. % Su ject sealed at the torque motor with elbow positioned at 9 0 degrees of flexion in a prefabricated splint. Note electrode placements on biceps brachii, brachioradialis, and triceps brachii muscles. 90-degree starting angles. Unfortunately, whether Powers et alHconsidered the effect that startingjoint position may have on the threshold angle is not clear. Our observations support the possibility that, among the three subjects who showed greater joint excursion to threshold angle for either the biceps brachii or brachiora.dialis muscle when the starting angle began at 90 degrees, the threshold angle was determined by muscle spindle sensitivity and not by muscle slack. The fact that our calculations within individual subjects yielded actual threshold angles that were similar in most instances, irrespective of starting angle or speed (0.5 or 1.0 radian/s) , suggests that each subject's stretch sensitivity was consistent under these circumstances. Close examination of the relationship of actual threshold angle to condition within subjects (X axis, Figs. 3A and 3B) sustains the notion that the joint angles at threshold were remarkably similar at conditions specified by speed within subjects 1,3, and 5 for the biceps brachii muscle and subjects 1 and 5 for the brachioradialis muscle. The fact that this close relationship between the occurrence of threshold angle and condition does not exist within all subjects highlights the reality of intersubject variability in spindle sensitivity across the spectrum of patients with stroke. limitations The small sample limits the generalization of the findings. This study, however, was not intended to explore a sizable group effect but rather to determine whether starting angle can affect the threshold angle response in subjects with biceps brachii and brachioradialis muscle hypertonia. Our results are limited by using only two starting angles and two speeds to determine the effect of starting angle and speed on threshold angle and may be applicable only to the two speeds used. A limited number of repeated measurements of threshold angle were Figure 5. (A) Biceps brachii muscle electromyographic (EMG] response, with a sharp rise in activity at occurrence of threshold angle, which i s shown by the arrow (72"); (B] biceps brachii muscle EMG response from another subiect, with a gradual rise in activity prior to threshold angle (40.5"). Note slightly different scaling in Y axes. Physical Therapy . Volume 7 6 . Number 6 . June 1996 Wolf et al . 597 Table 3. Mean and Standard Deviation Values of Threshold Angles for All Subiects at Every Condition Condition (Starting AngleISpeed) 70'10.5 radianls - Subject No. 70'1 1.o radianls 90'10.5 radian/s - SD SD X Session X 1 1 2 3 67.3 67.3 57.0 1.5 1.5 1.5 67.0 63.8 64.0 2.2 1.2 1.3 69.6 58.7 67.7 2 1 2 3 57.8 53.1 65.4 3.5 2.4 6.4 60.1 70.8 68.1 2.3 2.6 4.8 3 1 2 3 64.8 67.8 68.8 4.5 1.3 0.8 80.4 80.4 86.9 4 1 2 3 38.4 60.6 61.3 3.7 4.6 4.8 5 1 2 3 61.4 62.0 54.3 1 1 2 3 2 90'1 1.o radian/s - X SD 0.3 1.8 1.7 71 .O 67.9 75.6 1.3 3.7 10.6 67.3 67.2 55.3 0.6 2.1 3.2 75.3 72.4 79.1 4.7 1 .O 3.7 0.5 0.5 1.2 67.2 64.7 66.1 1.6 5.2 4.7 82.1 83.4 81.9 6.2 4.7 5.8 0 73.3 73.7 0 4.1 5.5 66.1 61.5 51.2 3.5 8.2 15.6 22.8 57.6 75.9 19.8 2.5 13.2 5.1 4.8 12.9 0 75.9 58.0 0 8.7 8.7 65.7 62.7 63.4 1.2 2.6 3.4 73.8 70.0 68.5 3.8 5.9 8.0 65.8 62.8 60.0 2.0 0 5.1 66.3 63.6 62.0 2.5 0.9 4.2 67.8 58.7 68.8 0.5 1.8 0.6 70.0 69.2 68.9 0.9 2.0 3.2 1 2 3 57.6 54.5 58.8 4.6 1.9 7.8 56.7 71.7 68.5 2.8 3.3 1 .O 67.3 65.5 57.5 0.6 3.3 6.9 74.7 74.4 71.2 6.3 2.4 3.3 3 1 2 3 65.5 67.5 64.4 3.4 1.2 2.6 68.5 81.2 82.3 3.7 1.7 3.5 63.5 68.1 67.5 8.8 0.1 2.0 85.0 80.5 78.3 3.7 1.6 6.0 4 1 2 3 25.3 56.9 33.9 1.8 3.3 4.4 0 56.6 0 0 0.6 0 60.9 43.2 49.5 7.4 5.9 16.0 0 0 0 5 1 2 3 55.8 48.9 21.6 4.2 8.6 37.5 62.8 71.9 58.0 2.7 11.3 8.1 59.5 48.3 40.2 0.3 1.1 2.8 69.7 64.7 53.3 X SD Biceps brachii muscle Brachioradialis muscle recorded. A greater number of measurements may be necessary to yield a more accurate measurement of threshold angle. The speed generated by the torque motor at different starting angles is an inherent feature of the motor and the mass being moved. As long as displacement is linear and reproducible and the approximate speed of the stretch is known, as was the case in this study, the motor itself should not be a deterrent to the generalization of interpretation of data. Future Investigations Suggestions for future research include examining the consistent use of a 90-degree starting angle and a 1.0-radian/s stretch to yield a reproducible threshold angle in elbow joint muscles within a subject over multiple testing sessions. The effect of consistency in 598 . Wolf et al 0 0 0 0.8 7.8 16.9 threshold angle for this condition should be assessed in a larger sample of subjects who have sustained a stroke and preferably those with similar, verifiable lesion sites. Research 011 the effect of starting position on threshold angle also should include evaluating a greater range of starting angles. These types of studies may well produce a more demonstrable relationship between starting angle and threshold angle and also will increase the ability to generalize our results to a larger population. In addition, use of torque motors that provide nearly instantaneous and accurately specified speeds would reduce the need to approximate the true speed at the time threshold angle is achieved. Clinicians who treat patients with hypertonia usually measure the amount of resistance to phasic stretch to Physical Therapy . Volume 76 . Number 6 . June 1996 Table 4. Significant0 Results of One-Way Repeated-Measures Analysis of Variance (d\ = 1 ) of Session Effect on Threshold Angle Condition (Stafiing Angle/Speed) Subject No. Biceps brachii muscle 1 2 3 4 5 70'/0.5 radian/s F=46.45 F=5.89 90'10.5 mdian/s F=26.29 F=7.85 F=64.34 F=953.28 F=71.91 F=28.86 F=18.81 F=28.66 Brachioradialis muscle 1 3 -- 90'/ 1.0 radian/s F=48.83 F=28.64 F= 1 1.47 F=68.47 2 4 5 70"/1.0 radian/s Fz96.44 Table 5. Tukey Pair-\~iseAnalysis of Significanto Session Effects Condition (Stadng Angle/Speed) Subject No. Biceps brachii muscle 1 2 3 4 5 70"/0.5 mdian/s 1 or 2>3 3>2 90'/0.5 mdian/s 2or3>1 2> 1 3>1 and 2 2>1 and 3 2>1 or 3 2 or 3>1 2 or 3>1 2>1 or 3 70"/1.0 mdian/s 90"/1.0 radian/s 1 or 3>2 1 or 213 2 or 3>1 Brachiorcrdiolis muscle 1 2 3 4 5 1 or 3>2 1 >2>3 Table 6. Bonferroni Significanta Post Hoc Multiple Comparison of Starting Angle Effects Within Subiects Subject No. 0.5 radian/s 1.0 mdian/s Biceps brachii muscle 1 2 3 4 5 Brachioradialis muscle 1 2 3 4 5 - Physical Therapy . Volume 76 . Number 6 . June 1996 Wolf et al . 599 determine the severity of hypertonia. There is also a need to examine a change in the severity of hypertonia resulting from an intenfention. This study illustrates the importance of controlling the starting position of the joint and the speed of the stretch when evaluating hypertonia from session to session to determine whether the hypertonia has really changed o r whether the conditions have caused a change in the presentation of the hypertonia. The importance of starting position of the joint controlled by a hypertonic muscle prior to stretch has been demonstrated. A difference in starting position from one assessment to the next may cause inaccurate and unreliable results. The need for further research on the development of an objective and reliable measurement of hypertonia, for the use of both researchers and clinicians, also has been emphasized. Conclusions If the analyses of data from these five subjects who sustained strokes can be generalized, a consistent starting angle prior to stretch should be used to determine a consistent threshold angle. The condition of a 90-degree starting angle and speeds approaching 1.0 radian/s within subjects and across sessions appears to yield a more reproducible threshold angle than the other three conditions. There is also a need to examine a greater range of starting angles a n d speeds and the related changes in threshold angle over time to specified interventions. Acknowledgments We express our appreciation to the following individuals who gave so much of their time and effort in helping to see this project to completion: Mr James Hudson, without whose resources, equipment modifications, and biomedical engineering background this project could not have been done; Mrs Jane Hudson, for her guidance and suggestions during the data collection procedure; and Mr John Kontos, for his assistance with data collection and counsel during data analysis. References 1 Katz RT, Rymer W'E. Spastic hypertonia: mechanisms and measurement. Arch Phys /Wed Rrhnbil. 1989;70:144-155. 2 (:are). JR, Burghardt TP. Movement dysfunction following central newous system lesions: a problenl of neurologic or muscular impairment? Phjs ?Xu.1993:73:538-547. 3 Lance JM'.The control of muscle tone, reflexes, and movement: Robert Wartenberg Lect~tre.,Yuurology. 1980;30:1303-1313. 5 Kate RT, Rovai GP, Brait (1, Rvmer WE. Objective quantification of spastic hypertonia: correlation with clinical findings. Arch P h y ~Med Rehnbil. 1992;73(suppl):339-347. 6 Powers RK, Campbell DL., Rymer WE. Stretch reflex dynamics in spastic elbow flexor muscles. Ann N~urol.1989;2.5:32-42. 7Vander AJ, Sherman JH, Iaciano DS. Muscle. In: Vander AJ, Sherman JH, Luciano DS, eds. Human Physiology: Thr M~rhanismsoJ Body F~inction. 5th ed. New York, NY McGraw-Hill Publishing (:o; 1990:283-324. 8 Powers RK, Marder-hlever .J, Rynier WE. Quantitative relations between hvpertonia and stretch reflex threshold in spastic hemiparesis. Ann Neurol. 1988;23:115-124. 9 Meyer M, Adorjani C. Tonic stretch teflex for quantification of pathologic muscle tone. In: Feldman RG, Young RR, Koella WP, eds. Sj~nsticity: Disordered Motor Conlrol. (;hicago, 111: Year Book Medical Publishers; 1980:315-330. 10 Herrnan R. The myotatic reflex: clinicophysiological aspects of spasticity and contraction. Brain. 1970;93:273-312. 11 Petajan JH. 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Electromyographic biofeedback (EMGBF) for neuromuscular relaxation and re-education. In: Gersh MG, ed. b.'l~ctrotheropy t n &habilitntzon. Philadelphia, Pa: FA Davis Co; 199T291-327. 18 Polit DF, Hungler BP. "v'urszng&imrch hnczplcr and Muthods. 4th ed. Philadelphia, Pa: JB Lippincott Co; 1991. 19 Brase CH, Brase CP. Underslandablr Statistirs: C o ~ ~ r ~and p t s Muthods. 4th ed. Lexington, Mass: DC Heath & Co; 1991. 20 Burke D, Ashby P. Are spinal "presynaptic" inhibitor) mechanisms suppressed in spasticity? J Neurol Sci. 1972;15:321-326. 21 Dietz V, Berger W. Norma1 and impaired regulation of muscle stiffness in gait: a new hypothesis about muscle hypertonia. Exp Neurol. 1983;79:680-687. 22 Given ID, Dewald PA, Rvmer WE. Dependence of stretch reflex of the response o n stretch velocity in spastic hemiparesis. In: Proc~~dings 24th Annztnl Meeting of t h Soriuty ~ for Nruro.~cienc~ Abstracts. 1994;20:339. Abstract. 4 Rymrr WE, Poxc~ersRK. 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