HEXORR II therapy produced reductions in upper extremity impairments, as measured by significant gains in the Fugl-Meyer score. The largest changes were at the 6 month time point and included a significant reduction of flexor tone, increased finger ROM, and decreased finger extension deficit with the arm supported against gravity (Task 1). The improvement in finger extension is noteworthy, as we are aware of only one prior study of hand robotics that has reported an increase is extension range that was retained 6 months after the intervention.32 However, there were no changes on a measure of upper extremity function (ARAT). This was consistent with the kinematic analysis of a reach and grasp task (Task 3), which reported no changes in finger ROM and only a non-significant trend of decreased finger extension deficit. No dosage effects were found, with the exception of increased hand displacement during the task requiring forward reach (Task 4) in the high-dose group, and no change in the low-dose group.
We observed significant long-term reductions in hypertonia at the followup, as measured by the Modified Ashworth Scale. To our knowledge, this is a novel result not previously reported for hand robotic devices. While the passive stretching performed at the beginning of each session was limited to only a few repetitions, we applied a stretch and hold movement immediately after each active extension attempt during the Gate game. The possibility of co-contraction of flexors during this stretch would have led to eccentric contraction of flexors, which may decrease in hypertonia following neurologic injury.50 Studies with the X-Glove have shown that a 30 min period of cyclic passive stretching can transiently improve active motor performance in stroke patients, with effects carrying over across sessions in subacute stroke.51 Improvements in subacute stroke subjects were reported in measures of impairment and function following training that included 30 min of passive cyclic stretching followed by active-assisted, task practice.31 Authors attributed the passive stretching to facilitating the effectiveness of the active training and preventing any increases in spasticity. There is also some evidence that orthotic-based static stretching can decrease upper extremity spasticity, although there is no evidence this alone will improve motor performance.52,53 Thus, our results contribute to the evidence supporting further study into the use of robotics to integrate stretching protocols into active motor retraining.
One the unique aspects of this study was the detailed biomechanical analysis that reported the kinematics of finger and arm movements under several conditions. Results support the use of HEXORR II in combination with practice of functional upper extremity tasks. The HEXORR II focuses on hand movement with the forearm and wrist immobilized and the arm supported against gravity. Hand movements in conjunction with proximal arm movements were not practiced, as is required for functional use of the upper extremity. This might explain the gains in an impairment scale (Fugl-Meyer), but no gains in a test of function that tests the ability to pick up and place objects (ARAT). There is strong evidence that control of the fingers degrades when proximal muscles must support the arm against gravity.54–56 These studies are consistent with our kinematic results, as finger extension did improve significantly when tested with the arm supported against gravity, but finger extension during reach and grasp tasks did not improve significantly. In the water bottle task, there were mean improvements in finger extension, but the time factor in the RM-ANOVA only approached significance (p = .057). Thus, it appears the training of distal hand control did produce gains in the training task, but did not generalize strongly to improved function in reach and grasp tasks. Two large multisite clinical trials of whole arm and hand robotic training also found similar results. The Armin was found to produce greater gains in the Fugl-Meyer scale than conventional therapy, but had no advantages in a motor function scale.57 In the RATULS study, robotic therapy produced greater gains in the Fugl-Meyer compared to usual and customary care, but had no advantage on the ARAT.58 In contrast, studies which combined robotic hand training with functional task practice have reported gains in functional scales. A recent study with Amadeo reported gains in the 9-hole Peg test, when subjects received the robotic training after a 3 hour session of physiotherapy that included 45 min of occupational therapy and 45 min of biomechanical training of upper and lower limbs.34 Several other studies have used wearable hand robots (X-Glove31, VAEDA32, Hand-of-Hope35,36, HandSOME59) that enabled practice of reach, grasp and release tasks with robotic assistance to hand movement. All of these studies reporting significant gains on a variety of functional scales. Thus, functional gains with devices similar to HEXORR II that focus on distal control only, might be achieved by integrating practice of coordinated proximal and distal limb control, as is often done during conventional therapy. Robotic and conventional therapies promote distinct patterns of motor recovery60, and there is evidence from clinical trials that the addition of conventional task practice to robotic therapy is superior to robotic therapy alone.61–63
Our results are generally consistent with prior studies of tabletop robots that train the fingers in isolation from the proximal arm. We found a 2.9 point change in the Fugl-Meyer at followup, while therapy using the FINGER robot reported gains of 1.8–3.7 at followup37, and a study using the Amadeo robot reported a 5.1 Fugl-Meyer point change.33 Our previous clinical study using HEXORR I also reported an increase in finger extension ability and significant gains in the Fugl-Meyer hand section subscore after 18 hours of training.40 However our prior study also reported grip strength increases and significant gains in the ARAT in a subgroup of low tone subjects. Our current study did not find any changes in the ARAT or grip strength. This might be explained by fact that the prior HEXORR I training included a squeezing task that required generation of targeted isometric matching flexion forces from the fingers and thumb, followed by releasing of the grip within a certain time interval. This squeeze and release practice might have helped subjects improve in grip force and the ARAT, which involves grasping and releasing objects. We elected to drop the squeezing task from the current study to increase the number of repetitions focused on extension movement. The prior studies with the FINGER and Amadeo also reported gains in functional scales (ARAT, Box-and-Blocks, Jebsen Taylor Hand Function Test), while we did not see any improvement on functional scales in this study. One possible explanation is the low functional level of our subjects. Our mean intake Fugl-Meyer score was lower than these other two studies, and our intake ARAT scores were low (mean of 19/57 points), with 6 of our subjects having an intake ARAT of 6 points or less. In more severely impaired subjects, practice of grip or squeezing tasks might be important to include with finger extension training.
Gains were largest at the followup, with some metrics even showing no change immediately after training, but significant improvements at the 6 month time point (Fugl-Meyer, Ashworth, hand displacement). These improvements at the followup might have been due to more repetitions of hand and arm practice during the 6 month period between the end of training and the followup test. This practice during the followup period might have been more effective because of the improved finger control afforded by the training, or the subjects may have been encouraged to use the upper extremity more after noting the improvements in hand function during the training. The only significant between-group difference was as increase in hand displacement in the high dose group during a forward reaching task that appeared between post training and followup, which suggests practice of reaching tasks during this period. However, MAL scores did not indicate increased use of the more-affected arm within ADL tasks. Future studies may consider using objective methods to assess upper extremity activity as an outcome measure.64 It is unlikely the gains during the followup period were due to encouragement or guidance from therapists, since the interaction with therapists was limited to the clinical evaluations and subjects were not given a home therapy plan during the followup period.
This study randomly assigned participants to either 12 sessions or 24 sessions. Based on RM-ANONA analysis, the group*time factors were not significant for our clinical outcomes measures (Fugl-Meyer and ARAT). A strong dosage effect has been difficult to show in interventions that rely on repetitive task practice. Lang et al. found no differences in functional gains in chronic stroke patients randomized to different levels of movement repetitions of task practice, even as the dosage ranged from 3200 to 10,808 repetitions.65 The ICARE study in subacute stroke found no differences in functional gain between intensive task practice (28.3 hrs), conventional occupational therapy (26.7 hrs) and usual and customary care (11.2 hrs of therapy).66 Robotics has been touted as a means of increasing the number of movement repetitions per treatment session, however a large study of 770 stroke subjects did not find a significant difference between robotic therapy, repetitive task practice and usual care in terms of functional gains.58 More study is needed to understand why a dosage effect is often not present in neuro-rehabilitation clinical trials of the upper extremity.
This study has several limitations that should be noted. HEXORR II allows practice of isolated thumb movement, but the other 4 fingers are coupled together. Inability to isolate these 4 fingers may have limited the therapy’s effectiveness to target weak fingers, since a weak finger can be carried along by the actions of the other 3. Another limitation was that the automatic adaptation algorithm only operated during the Gate Game, and not the secondary games, which were commercially available PC games chosen for their professional graphics and potential to entertain the subject. However, the downside of this approach is that the robot controller has no knowledge of current performance during the game, so automatic adaptation of assistance was not possible. At times, the subject would be unable to play the video game, and the experimenter would have to try and manually adjust the assistance level via a GUI menu. This trial and error process was not always successful, and detracted from the therapy. Future efforts using this approach should incorporate feedback of performance during all of the games, so the adaptation algorithm can operate during all of the training. The device currently is not portable, but getting into the device was straightforward and the potential for a home based portable device that can be used independently by patients seems possible if the overall size and footprint of the device can be reduced.