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Research Articles

Temporal Indices of Ankle Clonus and Relationship to Electrophysiologic and Clinical Measures in Persons With Spinal Cord Injury

Manella, Kathleen J. PT, PhD; Roach, Kathryn E. PT, PhD; Field-Fote, Edelle C. PT, PhD, FAPTA

Author Information
Journal of Neurologic Physical Therapy: October 2017 - Volume 41 - Issue 4 - p 229-238
doi: 10.1097/NPT.0000000000000197

Abstract

INTRODUCTION

Spinal cord injury (SCI) damages descending motor pathways resulting in muscle weakness, and also in loss of supraspinal modulation of spinal reflexes, which manifests as hyperreflexia.1 Plantar flexor hyperreflexia and the associated ankle clonus (ie, repetitive contraction of the plantar flexors following stretch) develop from loss of modulation of the stretch reflex2 and are manifestations of spasticity after SCI.3 Clonus commonly occurs at the ankle joint as involuntary rhythmic oscillations, with a frequency of 4 to 9 Hz.4–6 Ankle clonus may limit performance of self-care and mobility tasks, such as transfers, restricting independence and quality of life.7 In some individuals with SCI, severe ankle clonus has been cited as a primary contributor to the inability to stand or walk independently.8

Clonus is attributed to enhanced reflex effects of stretch receptor afferents on the motor neuron pools of paretic muscles because of loss of descending inhibition and maladaptive reorganization of spinal reflex circuitry.4,6,9,10 Although ankle clonus is typically elicited by plantar flexor stretch, other peripheral inputs may provoke clonus and activate central circuits that generate repetitive clonic contractions.5,11,12 Accordingly, clonus is thought to involve a complex interaction between peripheral and central mechanisms.13–15 Peripheral mechanisms may include reciprocal and presynaptic inhibition,16–19 muscle spindle and cutaneous receptor sensitivity,13,20 Ia, II, Ib, and cutaneous afferent activation,14,16,21 and α and γ-motor neuron activity.13,22 Central mechanisms may include loss of descending inhibition1,3,23 and central generator activation5,11,12,24–26 of spinal reflex circuitry. The soleus (SOL) H-reflex/M-wave (H/M) ratio is a commonly used electrophysiologic approach to assess excitability of the SOL stretch reflex arc.14 Although one study has reported that the H/M ratio is elevated in individuals who exhibit 4 or more reflex contractions (beats) of clonus following stretch of the plantar flexors,27 other studies have failed to find an association between neurophysiologic and clinical measures of plantar flexor hyperexcitability.28,29

Clinically, ankle clonus is easy to recognize but difficult to quantify. Physiologic clonus30 of less than 4 beats after plantar flexor stretch is considered a normal response31; conversely, 4 beats or more are indicative of pathologic clonus.27 Commonly used spasticity assessment tools, such as the Ashworth Scale,32 Modified Ashworth Scale,33 Modified Modified Ashworth Scale,34 Penn Spasm Frequency Scale,35 and dynamometer-based spasticity measure,36 do not quantify clonic activity. The Tardieu Scale37–39 and Spinal Cord Assessment Tool for Spastic reflexes (SCATS)40,41 are valid clinical tools to assess clonus severity. Good reliability of the SCATS clonus measure has been reported in persons with SCI41; however, this tool assesses only the duration of clonic activity.

Lack of precise, reproducible measures limits the quantification of ankle clonus that is necessary to evaluate the effectiveness of interventions directed at normalizing reflex excitability.38,42 Although electrophysiologic measures of plantar flexor hyperreflexia are common in the laboratory setting, these are typically not amenable for clinical use. The drop test is a biomechanical measure developed to quantify clonus elicited by a mechanical perturbation, which is the form in which plantar flexor hyperexcitibility is most commonly evoked during real-world activities. Various indices can be extracted from the drop test, including kinematic measures of sensitivity to stretch (reflex threshold angle), electromyographic measures of muscle cocontraction (soleus/tibialis anterior coactivation ratio), and temporal measures of sustained excitability (clonus duration and number of oscillations). The drop test plantar flexor reflex threshold angle has previously been shown to distinguish between clonus severity groups,43 and both reflex threshold angle and coactivation ratio are sensitive to training-related change in plantar flexor reflex excitability.43,44 In this study, we assessed the reliability and construct validity of the drop test temporal indices of sustained clonus, both duration and number of oscillations, using clinical and laboratory measures.

METHODS

Study Sample

Forty participants with chronic SCI (≥1 year) were recruited from The Miami Project to Cure Paralysis database. Subjects had SCI severity classified as American Spinal Injury Association Impairment Scale A to D45,46 (see Table 1 for participant characteristics). Inclusion criteria were adults (≥18 years) with chronic SCI who displayed clinical evidence of clonus in response to rapid stretch of the plantar flexors. Exclusion criteria were current orthopedic or active medical problems, or neurological conditions other than SCI. The study was approved by the University of Miami Human Subjects Research Office; all participants gave written informed consent.

Table 1 - Characteristics of Participantsa
Participant Gender Age, y Postinjury Interval, y Motor Level AIS SCATS Clonus Score Drop Test Group
1 Male 52 25 T5 B 2 1
2 Male 64 3 T6 C 2 1
3 Male 42 17 T10 A 1 1
4 Male 48 25 C5 A 1 1
5 Male 19 1 T5 A 3 1
6 Male 50 3 T5 C 2 1
7 Female 32 10 C4 D 3 1, 2, a, b
8 Male 31 10 C5 A 3 1
9 Male 23 2 T2 C 3 1
10 Male 51 12 T5 C 0 1, 2, b
11 Female 31 12 C7 A 1 1
12 Male 47 28 T5 A 3 1
13 Male 29 2 C5 D 3 1, 2, a
14 Male 22 2 C7 B 3 1, 2, a, b
15 Male 23 5 C6 D 3 1
16 Male 62 1 C6 C 2 1
17 Male 51 34 C7 B 3 1
18 Male 24 5 C6 C 3 1
19 Male 30 2 C5 B 3 1
20 Male 63 15 C7 B 3 1, 2, a
21 Female 46 24 C4 D 3 1
22 Male 33 4 C5 A 3 1, 2, a, b
23 Female 41 2 C2 C 2 1
24 Male 37 18 T2 C 2 1
25 Male 42 4 C5 C 3 2, a, b
26 Male 55 1 C5 D 3 2, a
27 Female 24 3 C6 D 3 2, a, b
28 Male 29 12 C5 C 2 2, a, b
29 Female 40 25 T11 C 1 2, a, b
30 Male 32 17 L1 C 2 2
31 Female 37 2 C3 D 1 2, b
32 Male 40 6 C4 D 1 2, b
33 Male 20 2 C6 D 3 2, a
34 Male 22 3 C7 A 1 2, b
35 Male 50 6 C7 D 3 2, a
36 Male 56 4 L1 C 1 2
37 Male 31 2 T9 C 1 2, b
38 Female 56 5 T9 D 1 2, b
39 Male 47 1 C6 D 1 2, b
40 Female 51 2 C7 B 1 2
Abbreviations: AIS, American Spinal Injury Association Impairment Scale45,46; C, cervical; L, lumbar; SCATS, Spinal Cord Assessment Test of Spinal reflexes40; T, thoracic.
a31 males, 9 females; mean age 39.6 ± 13 years; median level of injury, C7; median AIS, C; median SCATS score, 2 (1 = mild, 2 = moderate, 3 = severe); test group 1 = clonus duration, 2 = 10-second oscillations; a = subgroup of individuals with +drop test (at least 4 beats of clonus); b = subgroup of individuals who completed H-reflex test.

Depending on availability, participants engaged in one or both of 2 different assessments of the temporal parameters of clonus: duration and number of oscillations. For assessment of clonus duration (n = 24), we calculated intrarater, interrater, and test-retest reliability of the duration of clonic activity as measured with a stopwatch, and construct validity wherein we compared the timed clonus duration to the SCATS clonus severity score. For assessment of clonus oscillations (n = 22), we quantified the number of oscillations in the first 10-second interval following the drop test (hereafter referred to as 10-second oscillations) on the basis of optical motion capture. We calculated test-retest reliability of 10-second oscillations, as well as construct validity through comparison to SCATS clonus severity score. Six participants were available for both the clonus duration and 10-second oscillations tests. In 14 participants, we also acquired data related to the SOL H/M ratio. Participant flow and sample size for each test are illustrated in Figure 1.

Figure 1.
Figure 1.:
Flow chart of participant testing assignment.

Participants were instructed to maintain their usual medication schedule, including antispasmodics. To control for influence of extrinsic factors on ankle clonus severity, before testing, participants were queried about pain, illness, bowel or bladder problems, medication change, stress, and fatigue. Participant testing was rescheduled for any affirmative response to these questions. The weaker leg was tested, determined by lower extremity motor scores.45,46 In cases where lower extremity scores were the same in both legs, we tested the leg with more pronounced ankle clonus as determined by rapid stretch of the plantar flexors.

Drop Test

Participants were seated in a wheelchair or padded chair with hip and knee angles at 90° ± 10°, with test foot shoe removed and sock left on. The ball (metatarsal heads) of the test foot was placed on the edge of a 10-cm high platform, and the horizontal arm of an adjustable T-bar was positioned 10 cm above the knee. The leg was grasped below the knee joint and lifted until the knee contacted the T-bar arm, suspending the foot over the platform. The leg was then released allowing the foot to drop with forefoot striking the platform edge, which provided a rapid plantar flexor stretch to elicit clonus (Figure 2). In preliminary tests we found that the 10-cm height of the T-bar horizontal arm was sufficient to provide rapid plantar flexor stretch, allow consistent point of impact of the ball of the foot with the platform edge, minimize extraneous foot movements, and maintain heel clearance from the floor during clonus. For purposes of this study, the temporal parameters associated with sustained clonus were of interest: (1) clonus duration and (2) 10-second oscillations. These temporal parameters associated with plantar flexors spasticity are of particular interest, as they are equivalent to the parameters that have been shown to be of value in the pendulum test,47 a validated biomechanical test of quadriceps spasticity.

Figure 2.
Figure 2.:
Drop test setup. Illustration of drop test setup in a participant.

Drop Test Clonus Duration

Prior to the initiation of the testing sessions, the examiner (KJM) and 3 raters (A, B, and C) completed a 2-hour training session with an individual with SCI who had ankle clonus. For the testing sessions clonus duration data were acquired during 3 sessions consisting of 2 drop test trials per session (Figure 1). Stopwatches were used to determine clonus duration. Sessions 1 and 2 were intended to assess same-day test-retest reliability and were completed on the same day, with 60 minutes between sessions. Participants were instructed to refrain from lower extremity activity between sessions 1 and 2. The examiner performed the drop test while the 3 raters recorded clonus duration for each trial. Intrarater, interrater, and 1-hour test-retest reliability were assessed on the basis of test data collected by the 3 raters.

To assess 1-week test-retest reliability, session 3 was completed 5 to 7 days following the day of sessions 1 and 2, and at approximately the same time of day. Rater A from session 1 was designated the rater for session 3. In preliminary trials, clonus duration in excess of 25 minutes was recorded. To accommodate participant test tolerance, we limited recording of clonus duration to 10 minutes; 3 participants exceeded this limit.

Drop Test 10-Second Oscillations

Drop test 10-second oscillations data were acquired during 1 session (Figure 1). We captured the number of oscillations (beats) of clonus through the kinematic record of ankle angle (see Supplemental Digital Content 2, http://links.lww.com/JNPT/A180; Video, drop test assessment). Reflective markers were attached to the fifth metatarsal head, lateral heel, lateral malleolus, lateral knee above the joint space, and greater trochanter. Data were captured by an 8-camera motion analysis system (Peak Motus 8.5, Vicon, Centennial, Colorado) at a sampling rate of 60 Hz. Five drop test trials with a 60-second rest between trials were conducted. Thirty seconds of kinematic data was recorded for each trial.

To calculate the 10-second oscillations, we graphed and analyzed the initial 10 seconds after the forefoot struck the platform. This time frame was selected, as it corresponds to the 10-second criterion for the SCATS severe clonus score.40 An oscillation was defined as ankle angle excursion of at least 1° between maximum dorsiflexion and maximum plantar flexion. We counted the number of oscillations that occurred during the initial 10 seconds (Figure 3). Considering the criteria for physiologic clonus30,31 and the work of Koelman et al27 who delineated pathologic clonus as 4 beats or more of clonus after abrupt dorsiflexion, 2 subgroups were identified: participants with 4 beats or more of clonus classified as positive [+]drop test oscillation count (n = 7), and participants with less than 4 beats of clonus classified as negative [−]drop test oscillation count (n = 7).

Figure 3.
Figure 3.:
Calculation of 10-second oscillation measure. Example of graphic output of kinematic recording for 1 drop test trial. Bold black vertical lines delineate the initial 10 seconds after plantar flexor stretch. In this example, the 10-second oscillation measure result is 37.

SCATS Clonus Test

The SCATS clonus test40 was conducted in the same participants from whom the drop test clonus duration data (n = 24) and drop test 10-second oscillation data were acquired (n = 22). For comparisons between the SCATS clonus test and drop test clonus duration data, at the start of session 3, 3 trials of the SCATS clonus test were performed. Following the SCATS clonus test, a 15-minute quiet rest was provided before performing the drop test clonus duration assessment. For comparisons between the SCATS clonus test and drop test 10-second oscillation data, at the start of session 1, 3 trials of the SCATS clonus test were performed. Following the SCATS clonus test, a 15-minute quiet rest was provided before performing the drop test 10-second oscillation assessment.

The SCATS test was performed according to the published protocol.40 The participant was positioned in supine with the lower extremity supported by the examiner in 90° of hip and knee flexion. With the examiner's hand on the plantar surface of the forefoot, a quick stretch was applied to the plantar flexors. Duration of clonus was recorded by an assistant using a stopwatch, with the examiner providing a verbal cue to indicate the start and end of clonus (ie, “on” at the start and “off” at the end). Three SCATS clonus trials were conducted and the responses were scored.

H/M Ratio

Electrophysiologic assessment of SOL H-reflex excitability was conducted in the same participants from whom the 10-second oscillation data were acquired, within 3 days of the 10-second oscillation test. SOL H-reflex and M-wave recruitment curves were acquired according to the protocol described by Pierrot-Deseilligny and Mazevet14 using a constant current stimulator (Digitimer DS7A, Digitimer Ltd, Hertfordshire, England), AC amplifier (Grass P511, Grass Technologies, West Warwick, Rhode Island), analog-to-digital converter (CED 1401, Cambridge Electronic Design, Cambridge, England). Using peak detection software (Cambridge Electronic Design, Cambridge, England), maximal peak-to-peak amplitude (mV) of the SOL H-reflex (Hmax) and M-wave (Mmax) was identified. The SOL H/M ratio was calculated as the percentage of SOL Hmax to SOL Mmax. Of the 22 participants in the 10-second oscillation test, 18 returned for electrophysiologic testing. The SOL H/M ratio was calculated for 14 of the 18 participants; in 3 participants no SOL H-reflex could be elicited, and 1 participant was not able to tolerate the stimulus intensity required to elicit Mmax.

Statistical Analysis

All analyses were performed with SPSS 23 software (SPSS, Inc, Chicago, Illinois). For each participant, we calculated mean clonus duration, mean 10-second oscillations, median SCATS score (SCATS is an ordinal scale), and SOL H/M ratio.

Reliability and Construct Validity of Drop Test Clonus Duration

Intrarater and interrater reliability of drop test clonus duration was assessed with the intraclass correlation coefficient [ICC (2, 1)]48,49(p591) wherein a single measure by each rater was analyzed for each trial in sessions 1 and 2. To examine test-retest reliability, the ICCs (2, 2)48,49(p591) were calculated. For the 1-hour test-retest reliability (session 1 vs 2), comparisons were made of the average duration of the 2 trials as measured by each of the 3 raters. To examine 1-week test-retest reliability (session 1 vs 3), comparisons were made of the average duration of 2 trials measured by rater A. Identification of outliers50(p549) was determined with Box Plot analyses of 1-hour and 1-week test-retest data. Participants for whom the mean difference between sessions 1 and 2 (1-hour test-retest) or sessions 1 and 3 (1-week test-retest) exceeded 3 times the standard deviation (SD)50(p551),51,52 were determined to be outliers and were removed from ICC analysis. Spearman rank correlation coefficients were used to analyze construct validity53 of the clonus duration measure with SCATS clonus score as the referent measure.

Reliability and Construct Validity of 10-Second Oscillations

To examine test-retest reliability of the 10-second oscillation measure, the ICC (2, 1)48,49(p591) was calculated for pairwise comparison of trials 1 to 5 conducted during session 1. As described earlier, based on the work of Koelman et al,27 we classified participants into 2 subgroups on the basis of the number of oscillations (beats) of clonus evoked: (1) participants with a +drop test oscillation count (≥4 beats) and (2) participants with a −drop test oscillation count (<4 beats). For each of these 2 subgroups, scatterplots overlaid with a trend line were used to examine linearity of the relationship between drop test 10-second oscillations and SCATS clonus score, and between drop test 10-second oscillations and SOL H/M ratio. All ICCs were interpreted as good (>0.75) and moderate to poor (≤0.75).48,49(p595) For clinical tests used to assess individual progress, an ICC of more than 0.90 is recommended.48,49(p595)

To examine construct validity, for each of the 2 subgroups Spearman rank correlation coefficients54(p531) were used to analyze the relationships between drop test 10-second oscillations and SCATS clonus score, and between drop test 10-second oscillations and SOL H/M ratio. All Spearman rank coefficient correlations were interpreted as strong (>0.75), moderate (0.5-0.75), fair (0.25 to <0.5), and poor (<0.25).54(p525) Difference in SOL H/M ratio between the +drop test oscillation count and −drop test oscillation count subgroups was examined with Mann-Whitney U statistic.

RESULTS

Drop Test Clonus Duration

Interrater and Test-Retest Reliability

Mean clonus duration for each participant across raters and sessions is illustrated in Table 2. Drop test clonus duration demonstrated good intra- and interrater reliability for all test sessions, trials, and rater pairs [n = 24, ICC (2, 1) = 0.99-1.00, P < 0.0001] (see Supplemental Digital Content 3, http://links.lww.com/JNPT/A181; online Appendix A; duration reliability outcomes). The mean difference and SD in clonus duration between sessions 1 and 2 (1-hour test-retest data) for raters A, B, and C were: −48.53 (SD: 152.11) seconds, −48.52 (SD: 152.15) seconds, and −51.04 (SD: 156.39) seconds, respectively. For 1-hour test-retest reliability, 2 outliers were identified (P17, P18) in whom differences in test-retest duration exceeded 3 SDs from the group mean. These participants exhibited a mean test-retest clonus duration difference of −597 seconds (3.9 × SD) and −492 seconds (3.2 × SD), respectively. With the 2 outliers removed, clonus duration demonstrated good 1-hour test-retest reliability [n = 22, ICC (2, 2) = 0.99 all raters, P < 0.0001] (see Supplemental Digital Content 4, http://links.lww.com/JNPT/A181; online Appendix B; box plot 1-hour and 1-week differences).

Table 2 - Participants Mean Clonus Duration (in Seconds) for all Raters and Sessions
Rater A A A B B C C
Session 1 2 3 1 2 1 2
Participant
1 0.32 0.42 0.65 0.45 0.42 0.89 0.69
2 0.67 0.58 0.61 0.52 0.46 0.61 0.52
4 0.38 0.67 0.63 0.51 0.49 0.74 0.83
5 0.95 0.88 0.55 0.98 0.86 0.98 0.95
6 0.55 0.77 0.82 0.80 0.73 0.80 0.71
7 19.19 5.89 0.90 19.04 5.93 19.11 5.77
8 1.53 1.00 0.79 1.06 0.84 1.29 0.82
9 0.83 0.96 0.77 0.66 0.81 0.65 0.82
10 0.37 0.57 0.72 0.38 0.43 0.58 0.36
11 0.53 0.57 0.55 0.48 0.66 0.62 0.78
13 0.86 0.90 0.88 1.14 0.86 1.37 1.13
14 55.88 51.80 1.60 53.74 51.50 55.98 51.80
16a 334.89 320.36 1.34 334.75 320.47 334.93 320.49
17a,b 600.00 4.11 182.46 600.00 4.00 600.00 4.15
18b 600.00 120.67 600.00 600.00 120.56 600.00 110.93
19 0.82 0.67 0.65 0.78 0.68 No datac No datac
20 0.77 0.65 0.63 0.88 0.80 1.07 0.97
22 30.29 40.83 34.23 30.51 41.00 30.25 40.94
23 0.75 0.65 0.82 0.85 0.69 0.92 0.92
25 6.53 4.81 No datad 6.60 4.86 6.46 4.71
26 18.12 13.34 8.48 18.13 13.23 17.57 13.50
27 60.79 3.71 68.15 60.97 3.28 60.28 3.74
28 0.69 0.73 0.68 0.76 0.90 0.89 1.02
29 19.86 15.23 10.10 20.17 15.24 20.05 15.57
aOutlier 1-week test retest, more than 3 × standard deviation for mean duration difference, sessions 1 and 3.
bOutlier 1-hour test retest, more than 3 × standard deviation for mean duration difference, sessions 1 and 2.
cRater not available for session.
dParticipant did not show for session.

The mean clonus duration difference between sessions 1 and 3 (1-week test-retest data) measured by rater A was 33.28 seconds (SD: 104.37). For 1-week test-retest reliability, 2 outliers were identified (P16, P17) who exhibited a mean clonus duration difference of 333.55 seconds (3.2 × SD) and 417.54 seconds (4.0 × SD), respectively. With the 2 outliers removed, clonus duration demonstrated good 1-week test-retest reliability [n = 21, ICC (2, 2) = 0.99, P < 0.0001].

Construct Validity

Construct validity of drop test clonus duration with SCATS clonus score was examined on the basis of data from rater A. Drop test duration and SCATS clonus score were moderately correlated (r = 0.58, P = 0.003).

Drop Test 10-Second Oscillations

Test-Retest Reliability

Good within-session test-retest reliability was demonstrated for comparisons among all 5 trials (ICC ≥ 0.75, range 0.79-0.88). The ICC was ≥0.90 (range 0.90-0.99) for all comparisons between trials 1 and 4 (see Supplemental Digital Content 5, http://links.lww.com/JNPT/A181; online Appendix C, 10-second oscillation test-retest reliability).

Construct Validity

Drop test 10-second oscillations demonstrated a strong correlation with SCATS clonus score (r = 0.86, P < 0.001). Drop test 10-second oscillations, SCATS, and SOL H/M ratio measures for the +drop test oscillation count and −drop test oscillation count subgroups are summarized in Table 3. Mean SOL H/M ratio was significantly greater for the +drop test oscillation count subgroup than for the −drop test oscillation count subgroup (P = 0.03). For the +drop test oscillation count subgroup, a strong correlation was found between drop test 10-second oscillations and SOL H/M ratio (r = 0.77, P = 0.04).

Table 3 - Drop Test 10-Second Oscillations, SCATS, and SOL H/M Measures for +Drop Test Oscillations Count and −Drop Test Oscillations Count Subgroupsa
Group Parameters Drop Test 10-s Oscillations SCATS Clonus Scorea Soleus H/M Ratio
+Drop test, n 12 12 7
Mean ± SD 36.0 ± 20.1 3 (median) 0.73 ± 0.14b
Range 4.0-56.4 1-3 0.49-0.91
−Drop test, n 10 10 7
Mean ± SD 1.4 ± 0.8 1 (median) 0.42 ± 0.28b
Range 0.6-2.4 0-1 0.06-0.77
Abbreviations: H/M, H-reflex/M-wave; SCATS, Spinal Cord Assessment Tool for Spastic reflexes40; SD, standard deviation.
aSCATS score: 0 = none, 1 = mild, 2 = moderate, 3 = severe; +drop test = participants with at least 4 beats of clonus; −drop test = participants with less than 4 beats of clonus.
bSoleus H/M ratio (italicized values indicate significant between-groups difference, P −0.03; Mann-Whitney U test).

DISCUSSION

Our results indicate that the temporal indices of the drop test are reliable and valid measures of plantar flexor spasticity. For the clonus duration parameter, there was good reliability both within and between raters, as well as good reliability for the 1-hour and 1-week test-retest. There was moderate construct validity of clonus duration when compared with SCATS clonus score. For the 10-second oscillation parameter, there was good within-session test-retest reliability, and strong construct validity when compared with SCATS clonus score. In participants with a +drop test oscillation count (≥4 beats of clonus), there was strong construct validity of the 10-second oscillation parameter when compared with the SOL H/M ratio. Participants with a +drop test oscillation count had significantly higher SOL H/M ratios compared with participants with a −drop test oscillation count (<4 beats of clonus).

Reliability and Construct Validity of Drop Test Clonus Duration

Good intra- and interrater and 1-hour and 1-week test-retest reliability were demonstrated for drop test clonus duration, and surpassed the recommended ICC of ≥0.90 for use as a clinical test. In 21 of the 24 participants, clonus durations of less than 120 seconds per trial were recorded. Interestingly, for the 1-hour test-retest, the 2 participants identified as outliers (P17, P18) exhibited clonus duration in excess of the test maximum of 10 minutes in both trials of session 1. It is possible that allowing clonic activation of the soleus to continue for 20 minutes in session 1 may have had a suppressive effect on the clonic response 1 hour later. For example, prolonged clonus may have activated spinal mechanisms associated with low-frequency depression,15 wherein the reflex response is suppressed (inhibited) with repeated activation.

For the 1-week test-retest, the 2 participants identified as outliers (P16, P17) exhibited clonus durations in excess of 5 and 10 minutes, respectively. Our findings of atypical clonic durations in excess of 5 minutes in these individuals suggest that, in addition to peripheral mechanisms of stretch-activated clonus, other mechanisms may underlie this type of excessive clonic activity. Mechanisms that underlie prolonged, sustained clonus may include loss of reciprocal and presynaptic inhibition,16–19 maladaptive antagonist reciprocal facilitation,18 change in muscle spindle and cutaneous receptor sensitivity,13,20 loss of descending inhibition,1,3,23 and central generator activation5,11,12,24–26 of spinal reflex circuitry. Stability of the clonic response may also be influenced by intrinsic factors such as diurnal fluctuations in spasticity55 or change in antispasmodic medication concentration.

The ICC values for clonus duration indicate that the drop test has strong intra- and interrater reliability. However, it is important to emphasize that there were 3 participants in whom the test-retest difference in duration of clonus exceeded 3 SDs from the mean, and these outlier data were excluded from the ICC analysis. These outlier data are evidence of a subset of individuals who exhibit variability in clonus duration that is significantly greater than what is typical. The construct validity of drop test clonus duration is supported by the moderate correlation with SCATS clonus score. The positive relationship between drop test clonus duration and SCATS clonus score, a validated measure of clonus severity,40,41 indicates the measures are likely assessing the same construct.

Reliability and Construct Validity of Drop Test 10-Second Oscillations

The drop test 10-second oscillation parameter exhibited good test-retest reliability across 5 trials during the test session. However, the pairwise ICCs for trials 1 to 4 were all at least 0.90, whereas comparisons that included trial 5 demonstrated lower reliability (ICC range 0.79-0.88), as trial 5 was more variable. This finding may suggest that an effect of repeated testing was evident, which either increased or decreased the trial 5 response. It is possible that repeated testing elicited a wind-up effect56 resulting in a heightened response, or low-frequency depression15 that lowered the response. On the basis of these findings, it is recommended that only 4 drop test trials be conducted.

Construct validity of drop test 10-second oscillations is supported by strong correlations with clinical measures of clonus. Our findings concur with Benz et al,40 who reported, in individuals with complete and incomplete SCI, moderate correlations between SCATS clonus score and clinical measures (plantar flexor Ashworth scores32 and Penn Spasm Frequency35 scores), and neurophysiologic measures (plantar flexor clonic activity duration as measured by electromyography). Plantar flexor Ashworth scores in individuals with SCI have been correlated with ankle clonus scores derived from electromyography.57 The drop test 10-second oscillation measure appears to be a sensitive index of clonic activity that may more accurately reflect the extent of plantar flexor excitability than clinical measures in individuals with spasticity.

Studies of SOL H/M Ratio and Clinical Plantar Flexor Spasticity Measures

In our study, participants who had a +drop test oscillation count exhibited greater mean SOL H/M ratios compared with participants with a −drop test oscillation count. This is consistent with Koelman et al27 who observed greater SOL H/M ratio in individuals with at least 4 beats of clonus (pathologic clonus) compared with those with normal plantar flexor tendon reflexes (<4 beats; physiologic clonus). Koelman et al27 also found that in individuals with central nervous system injury and spasticity SOL H/M ratio was moderately associated with reflex scores. There are, however, conflicting reports concerning the relationship between SOL H/M ratio and clinical spasticity measures. In individuals with central nervous system disorders, Biering-Sorensen et al23 found no correlation between H-reflex size and Ashworth32 or Modified Ashworth33 scores. Priebe et al58 in 85 individuals with SCI reported that plantar flexor Modified Ashworth scores were poorly correlated with plantar flexor tendon reflex responses and clinical clonus scores. Moreover, plantar flexor Ashworth32 and Modified Ashworth33 scores exhibited poor intra- and interrater reliability in individuals with SCI.59

Several prior studies have indicated that SOL H/M ratio does not distinguish between individuals with and without spasticity.16,28,29 However, it is importation to bear in mind that with the small sample sizes there may be insufficient power to distinguish between groups. In 5 individuals with chronic incomplete SCI, Boorman et al16 reported an SOL H/M ratio of 0.74 that was not significantly different from the 0.54 ratio for 9 nondisabled individuals. Calancie et al29 reported an SOL H/M ratio of 0.60 for 22 individuals with chronic complete or incomplete SCI that did not differ significantly from the 0.54 ratio for 16 nondisabled individuals. Comparing 9 individuals with chronic complete SCI and 20 nondisabled individuals, Schindler-Ivens and Shields28 found no difference in SOL H-reflex threshold, gain, or amplitude, and concluded people with complete SCI and clinical manifestations of spasticity do not exhibit elevated SOL H-reflex excitability. In these studies, spasticity was identified subjectively by presence of increased resistance to passive stretch, abnormally brisk tendon reflexes, flexion and/or extension spasms, and clonus. However, no objective measures of plantar flexor hyperreflexia or ankle clonus were reported.

Divergent findings among different studies with respect to the relationship between SOL H/M ratio and plantar flexor spasticity may be attributable to several factors. Relationships between impairment and associated variables can only be identified if all variables are expressed in quantifiable terms.60,61 Various neurologic mechanisms underlie impairments that manifest as spasticity after SCI. To examine the contribution of a specific neural mechanism (eg, SOL H-reflex excitability) to clinical manifestation of impairment, it is necessary to quantify the severity of that impairment. The studies that assessed H-reflex hyperexcitability did not quantify plantar flexor hyperreflexia or ankle clonus; therefore, it is not known whether these impairments were actually present, and when present how severe the impairment was. Accordingly, in our study the mean SOL H/M ratio for all individuals with SCI was 0.58, similar to the reported ratios of 0.65 by Schindler-Ivens and Shields28 and 0.60 by Calancie et al.29 However, when participants were stratified on the basis of the severity subgroups of +drop test oscillation count (≥4 beats of clonus) versus −drop test oscillation count (<4 beats of clonus), the SOL H/M ratio for the +drop test oscillation count subgroup (0.73) was significantly greater than that for the −drop test oscillation count subgroup (0.42). Our findings of strong correlation between 10-second oscillations and SOL H/M ratio in the +drop test oscillation count subgroup, and also a greater SOL H/M ratio for the +drop test oscillation count subgroup, support the concept that ankle clonus severity and SOL H-reflex excitability are linked.

Implications for Clinical Use and Future Research

This study describes reliability and construct validity of 2 temporal parameters of the drop test. As a clinical outcome measure, drop test clonus duration recorded using a stopwatch provides an easily administered clinical test with good intrarater, interrater, and test-retest reliability that is a valid quantification of plantar flexor hyperreflexia and ankle clonus.

Clinically, the drop test clonus duration parameter could be a useful tool for assessing severity of ankle clonus and effectiveness of interventions designed to reduce plantar flexor hyperreflexia and ankle clonus. While the drop test plantar flexor reflex threshold angle has previously been shown to distinguish between clonus severity groups,43 clonus duration is a parameter that is easier to acquire. To provide a stable, reliable clonus duration outcome measure for test-retest purposes, it is recommended that 2 trials of clonus duration be acquired, and the average duration calculated. Our maximum test duration of 10 minutes was excessive, clonic activity of this duration may be unstable, and measurements of this duration may be of little value for clinical interpretation. In our participants, clonus duration was less than 120 seconds in the vast majority of trials; for this reason, an upper measurement time of 120 seconds is recommended.

The drop test 10-second oscillation parameter on the basis of kinematic data provides a reliable, valid, and precise measurement of clonus severity that is of value for use in studies designed to investigate underlying neurophysiologic mechanisms of plantar flexor reflex excitability, as well as to assess effectiveness of interventions. Clinically, it may be feasible to use an electrogoniometer, accelerometer,61,62 or smartphone video app (eg, Dartfish; http://www.dartfish.com) to record the number of oscillations for at least 10 seconds. Further study of these accessible, low-cost technologies would be of value to determine their clinical applicability. The temporal indices of the drop test address the need for a reliable and valid outcome measure to examine ankle clonus severity. Further research would be of value to determine whether the drop test temporal measures are sensitive to training-related change as has previously been shown for both the drop test reflex threshold angle and coactivation ratio,43,44 as well as to establish the minimal clinically important differences for these measures.

Limitations

For 3 participants who exceeded the 10-minute maximum test duration in at least 1 trial, the clonic response was not stable upon 1-hour and 1-week retesting. It is unclear whether drop test clonus duration would be stable or sensitive to change in clonus severity in these individuals.

The test-retest reliability of drop test 10-second oscillations was examined only within-session. A longer time frame for test-retest reliability of the 10-second oscillations measure warrants further investigation. Approximately 50% of the participants had a −drop test oscillation count; the strong correlation between the 10-second oscillations and soleus H/M ratio in the +drop test oscillation count subgroup is based on data from 7 participants. Future studies with larger samples of participants with a +drop test oscillation count are warranted to further substantiate our findings.

CONCLUSIONS

The temporal indices of clonus as measured on the basis of drop test clonus duration and number of oscillations are reliable and valid measures of plantar flexor hyperreflexia that are accessible for clinical use. Tools for objective quantification of plantar flexor hyperreflexia and ankle clonus severity are valuable for assessing effectiveness of interventions directed at normalizing reflex activity associated with spasticity. Further studies are warranted to substantiate these findings in other individuals with SCI and in other central nervous system disorders.

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Keywords:

H-reflex; human movement system; measurement; soleus excitability; spasticity

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