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Robotics and Autonomous Systems 91 (2017) 169–178

Contents lists available at ScienceDirect

Robotics and Autonomous Systems


journal homepage: www.elsevier.com/locate/robot

Robotic wrist training after stroke: Adaptive modulation of assistance


in pediatric rehabilitation
Francesca Marini a , Charmayne M.L. Hughes b , Valentina Squeri a , Luca Doglio c ,
Paolo Moretti c , Pietro Morasso a , Lorenzo Masia d, *
a
Department of Robotics, Brain and Cognitive Sciences, Istituto Italiano di Tecnologia, Genova, Italy
b
Department of Kinesiology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, United States
c
Physical Medicine and Rehabilitation Institute G. Gaslini, Genova, Italy
d
Robotics Research Centre, School of Mechanical and Aerospace Engineering, Nanyang Technological University, 50 Nanyang Ave, Singapore 639798,
Singapore

highlights

• Pediatric stroke leads to limb hemiparesis, sensory impairments, and spasticity.


• A 14-year old stroke patient completed in a 3-month wrist robotic training program.
• The robot provided online adaptive modulation of assistance instantaneously during each trial.
• Robot therapy led to positive changes in upper limb motor coordination and function.
• In addition, the patient needed less robot assistance to complete each trial.

article info a b s t r a c t
Article history: In this paper we present a case study in which a 14-year-old, right-handed stroke patient with severe
Available online 25 January 2017 weakness, spasticity, and motor dysfunction of the left upper extremity participated in a three-month
distal robotic training program. The robotic device was compliant to the patient’s movements and
Keywords: was able to modulate the level of assistance continuously throughout the trial (i.e., online adaptive
Motor dysfunction
modulation). Standard clinical and robotic evaluations of upper extremity motor performance were
Robotic rehabilitation
conducted before and after robotic training. There were improvements in upper extremity spasticity and
Pediatric stroke
Wrist rehabilitation motor functions. In addition, robotic training lead to positive changes in wrist active range of motion
and kinematics: movements were smoother and there was a noticeable decrease in the level of robotic
intervention required to complete each trial. In sum, results of the present case study demonstrate
that distal upper extremity robotic rehabilitation that features the proposed adaptive control algorithm
promoted positive changes in upper limb motor coordination and function after pediatric stroke.
© 2017 Published by Elsevier B.V.

1. Introduction by muscle weakness, impaired motor coordination, and impair-


ments to sensory mechanisms of the affected paretic arm [3,4].
Stroke or cerebral vascular accident (CVA), caused by the oc- Functional loss of mobility due to hemiplegia has a significantly
clusion or rupture of cerebral blood vessels, is the leading cause negative impact on the ability to perform activities of daily living,
of neurological disability worldwide. It has been estimated that such as reaching and grasping and object manipulation. In addition
among the children who survive, between 50% and 80% will exhibit to hemiplegia, stroke patients often present with spasticity and
permanent upper extremity sensorimotor deficits [1]. The most contractures of the elbow, wrist, and finger muscles [5,6]. Upper
extremity spasticity can lead to pain, tendon retraction or muscle
common long-term impairments are hemiparesis (weakness of the
weakness, which has negative effects on a patient’s quality of life
entire left or right side of the body) or hemiplegia (total or partial
and rehabilitation outcomes [7,8].
paralysis on one side of the body) [2], which is often accompanied
Current conventional stroke rehabilitation therapies are a labor
intensive process that involve daily one-on-one interactions with
therapists that can last for several weeks. Fortunately, robotic
* Corresponding author.
E-mail address: lorenzo.masia@ntu.edu.sg (L. Masia). advancements in the last decade have provided researchers

http://dx.doi.org/10.1016/j.robot.2017.01.006
0921-8890/© 2017 Published by Elsevier B.V.
170 F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178

with instruments that can reduce the burden on therapists and The present work provides a further contribution in this di-
healthcare systems [9]. Robot-aided rehabilitation affords several rection by assessing the clinical effects of distal upper extremity
potential advantages to conventional therapy, including high re- robotic training program that incorporates an adaptive modulation
peatability, accurate control of robotic assistance or resistance of assistance each single instant of the movement during a trial.
levels, and objective measurement of patients’ kinematic and dy- In contrast to previous control algorithms, the proposed one was
namic performance [10,11]. In addition, rehabilitation robotics designed in such a way that the robotic intervention provided
leverage virtual reality multi-dimensional non-immersive games assistance along the target direction in a point to point task. The
to increase patient engagement and provide additional motiva- magnitude of the assistive elastic component is online modulated,
tional components across the rehabilitation lifespan [12]. on a moment-by-moment basis, so as to have a level of assistance
One of the most important aspect of integrating robotic de- always tailored to the participant’s capabilities. Specifically, the
vice in clinical rehabilitation has always been the choice of the robotic device provides more assistance during the trial when the
most effective control algorithm [13]. Early rehabilitation robotic patient requires it, and less intervention when the participant is
devices implemented control algorithms that attempted to mimic able to move toward the target.
the actions of the therapist by using a robot to help completing In this case study we describe the potential benefit of our
the movement task if the patient is unable to [14]. Initial clinical control algorithm in the rehabilitation of a pediatric stroke patient
results indicated that these active assistance algorithms lead to an with severe weakness, spasticity, and motor dysfunction of the left
increase in arm strength and a noticeable recovery of functional upper extremity who did not benefit from conventional therapy.
independence [10] with benefits lasting more than 3 years [15]. Improvements were assessed using clinical and robotic evaluations
Several groups proposed a different approach based on active mod- of upper extremity motor performance. It was hypothesized that
ulation of robotic assistance indicated as adaptive control strat- robotic training with our distal control algorithm would be particu-
egy [12,16]. This assistance-as-needed control strategy evaluates larly effective in improving upper extremity function in this patient
performance across trials using different variables collected during without increasing spasticity.
the therapeutic protocol (e.g., elapsed time, force generated by the
patient, limb velocity) and provides the patient with the minimal 2. Methods
amount of robotic assistance necessary for to complete a task,
modulating the flow of control authority and avoiding the device 2.1. Case description
assistance is perceived too invasive or provides a drastic reduction
of voluntary action modulation. The patient was a 14-year-old, right-handed female with no
Ideally, assistance should be adjusted with respect to the cur- family history of vascular or hematologic disorders who had a
rent amount of voluntary control. As the latter is not readily first-occurrence stroke , participated in robot-assisted distal upper
available, most schemes of regulation are driven by the observed extremity training twice per week for a total of three months.
performance. Among the several ways to provide assistance, and Neurological examination presented severe weakness and motor
to continuously regulate it, optimal solutions have been proposed impairment to the left upper extremity, more strongly affecting
for simple, specific tasks, like lifting a weight [17,18], or for lower distal than proximal limb function. Initial assessment revealed a
limb rehabilitation tasks, in which the robot adaptively takes into noticeable bias from the neutral configuration at the paretic wrist
account the patient’s intention rather than imposing an inflexible joint at rest, which resulted in accentuated pathological flexion.
control strategy. This adaptive law is an error-based strategy that The patient presented with high levels of hypertonia in the paretic
adjusts a control parameter from trial to trial based on measured wrist, and even when the patient was asked to relax her muscles
participant performance [19]. Another approach is to pose the (i.e., adopt a neutral limb position) the configuration of the wrist
assistance-as-needed problem as one in which the goal is to mini- was characterized by exaggerated flexion indicating the presence
mize a cost that is the sum of kinematic error (ensuring the task is of hypertonia. This bias caused the wrist to freeze in an unnatural
completed) and robotic assistance (ensuring that the robot assists posture, restricting the ability of the patient to use her hand and en-
as little as possible) [20]. Recently, Wolbrecht and coll. [21] pro- tire upper extremity during the performance of functional actions
posed an adaptive control scheme in which a controller negotiates and skilled activities of daily life. Acute neurological assessment
an error-reducing and an effort-reducing component. This keeps indicated the presence of an intracranial hemorrhage of idiopathic
assistance to a minimum and to automatically adapt it to task origin. Magnetic Resonance Imaging (MRI) revealed a low T2 sig-
performance, while providing enough assistance to support task nal intensity haemosiderin staining in the left cerebral peduncle,
completion. This technique does not explicitly aim to augment the left midbrain tegmentum, and left superior and middle cerebellar
degree of voluntary control. Such an increase is assumed to result peduncles, indicating that the patient suffered from a hemorrhagic
from the ability to successfully complete the task. stroke affecting the midbrain and cerebellum. After hospitalization
In general, clinical studies in adult stroke populations have the patient received intensive gait training and occupational ther-
demonstrated that assistance-as-needed algorithms lead to reduc- apy for a period of sixteen weeks. Four months from the stroke
tions in upper extremity spasticity and improvements in the ability onset, the patient was enrolled in a robotic rehabilitation program,
to perform functional movements [22,23]. as upper extremity spasticity and functional independence did
However, there are limitations in the aforementioned control not improve during the sixteen weeks of conventional therapy.
approach. First, there is an evidence of a slacking response, in Informed consent was obtained from the parents of the patient
which the patient triggers the robotic assistance by producing an prior to participation in the study. The experiment was approved
initial movement, but then decreases the level of muscular activa- by the ethical committee, and was conducted in accordance with
tion and voluntary movement so that the adaptive controller takes local ethical guidelines.
over the task [24,25]. Second, although the assistance-as-needed
algorithms adapt the level of robotic assistance on a trial-to-trial 2.2. Experimental setup
or session-by-session basis, assistance modulation is not updated
continuously within a single trial. This is unfortunate as one of the The experimental device (Fig. 1A) used in this study was a 3
important features of the robotic therapy is the possibility to tailor degree of freedom (DoF) exoskeleton developed specifically for
exercises to the specific initial impairments of the patient and their the study of human motor control and neurorehabilitation. The
progress over the course of rehabilitation lifespan [26]. device allows full range of motion for the human wrist across its
F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178 171

three DoFs (Fig. 1B) and is fully backdrivable, thereby making it We decided to use the speed to adjust the controller on the basis
suitable for use in the current experiment [27]. The range of motion of subject’s kind of impairment. Indeed, the subject was hemiplegic
(RoM) for the three DoFs approximates that of a normal human with a high degree of anisotropy in the active range of motion of
wrist (flexion/extension: human = 65◦ /70◦ , robot = 72◦ /72◦ ; the two DoFs (Flexion/Extension and Abduction/adduction). We
adduction/abduction (AA): human = 19◦ /30◦ , robot = 45◦ /27◦ ; assumed that, when the speed was too low, or close to zero the
pronation/supination (PS): human = 90◦ /90◦ , robot = 80◦ /80◦ ). subject was unable to move and complete the task and the stiffness
The robot is powered by four brushless motors that enable accu- k had therefore to be linearly increased. As soon as the assistance
rate haptic rendering, the weight and inertia compensation of the was sufficient for the subject to start moving again (and conse-
device, and it can overcome muscular contraction and allow for the quently for the speed to increase), the assistive force had to remain
manipulation of joints in case of hypertonia. One of the four motors constant since the subject was able to move by herself. When the
actuates the FE and one actuates the PS, while the remaining two movement was performed with a high level of speed we assumed
motors actuate the AA mechanism. They are symmetrically located that the movement could be easily accomplished and there was no
need for that level of assistance, that accordingly, was decreased.
on each side of the robot and serve to balance and provide gravity
The performance evaluator updated the magnitude of the stiff-
compensation of the FE element. The axis of rotation of both motors
ness K after an instantaneous check of EE speed. A preset min-
is rotated by 90◦ thanks to conic couplings. They allow the axis
imal speed threshold provided the means by which to decide if
of rotation to coincide with each other with the human wrist’s
the stiffness K of the controller must be increased or decreased
axis of rotation. The continuous torque range at the different wrist when patient’s movement was lower or higher to the threshold
joints is 1.53 N m, 1.63 N m, and 2.77 N m for FE, AA, and PS, respectively. When the speed of the EE was lower than 0.05 rad/s
respectively [28]. the stiffness K of the assistive force field increased linearly with
The system was integrated into a virtual reality (VR) environ- a 0.1 [N m/rad/s] slope. Once the speed exceeded 0.3 rad/s the K
ment that provided visual feedback to the user during the task slope was reversed to a decreasing trend. K was kept constant if
(Fig. 1C). The patient controlled the position of an end-effector the speed was in a 0.05–0.3 rad/s range.
(EE), represented on the screen as a gray dot. The configuration of
v < vt1 K ↑
{
wrist joints for FE and AA motions were represented as a projection
on the screen on x and y axes of the virtual reality environment k = k(v ) = vt1 < v < vt2 K = cost (2)
respectively. The EE displacement along the two coordinate axes
v > vt2 K ↓
(x, y) was linearly proportional to the rotation of the wrist around As such, the adaptive controller changes the value of K throughout
the FE and AA axes. The scaling coefficient was chosen so that the the trial and serves to provide to the force field generator the
dimensions of the computer monitor matched the wrist RoM of amplitude of the proper amount of force that has to be delivered
the patient. The targets in the virtual environment were selected to the participant.
so that there were movements that required a single DoF as well
as movements that required the coordinated use of two DoFs. 2.4. Procedure
The maximum angular span in the workspace was determined by
assessing the patient’s active FE and AA RoM prior to enrollment in The patient sat comfortably in front of a screen with the torso
and forearm restrained to a rigid support by Velcro straps. This
the robotic training program (5◦ for both DoFs).
ensured the biomechanical and robot rotation axes were approxi-
mately aligned. After the patient grasped the handle of the EE with
2.3. Adaptive modulation of assistance control algorithm
the impaired hand, clinic staff member used a neoprene glove and
Velcro strap to assure a correct and continuous contact between
The control algorithm was designed to accurately provide the
hand and EE. The therapeutic team visually inspected forearm and
appropriate level of assistance and force during the task; the gains
wrist placement every 5 min in order to ensure that the patients
were opportunely chosen and tuned by the controller depending grasp on the robotic handle was maintained throughout the ses-
on the patient’s wrist movement ability and residual capacity of sion.
motion. In particular, the robot offered assistance when the par- The virtual environment was rendered in the form of a puzzle
ticipant was unable to reach targets without aid, (and thus would game (e.g., an animal, television or movie actor, landscape) in
not able to complete the trial) by providing active assistance as order to ensure patient motivation over the three-month training
needed [29]. In this way, the muscle activity of the patient was program. The patient performed a series of nine point-to-point
increased and neural plasticity was encouraged [30,15]. reaching actions in which she used the robotic handle to move
The control architecture included three main components the virtual EE (i.e., the gray circle) from the start position toward
(Fig. 2), a force field generator, a performance evaluator, and an a specified target (i.e., the red circle). Upon successfully reaching
adaptive controller. The force field generator was online modu- the target a portion of the puzzle was unveiled, and after a 2 s
lated by means of elastic and viscous components using the fol- pause the next target was displayed on the computer monitor. The
lowing impedance control scheme (Eq. (1)): complete puzzle was visible on the computer monitor after patient
successfully performed reaching movements to all nine targets.
F = K (θT − θW ) − Bθ̇W . (1) Visual feedback regarding the position of the virtual EE through-
out the duration of the trial (Fig. 1C). At the start of each session
The viscous force Bθ̇W was proportional to the joint angular the patient was informed that movement accuracy and comple-
speed and introduced a stabilizing effect during movement (i.e., fil- tion time was of utmost importance, and these instructions were
tering possible muscular tremor that may arise during motion). repeated throughout each training session, as needed. To moti-
Damping values were set to which based on prior experimen- vate the patient throughout the three months training program
tation [31,32], enabled simultaneous smooth and stable interac- the Virtual Environment was rendered in the form of a puzzle
tions between the device and the patient. This value was constant game (e.g., an animal, television or movie actor, landscape). After
throughout sessions. The elastic force (K (θT − θW )) was the main completion of each reaching movement (i.e., trial) a portion of the
component of the force field generator (F ) and was directed from puzzle was unveiled. The robotic training sessions were carried
the actual position of the EE to the target. As such, assistance out at the pediatric hospital Gaslini of Genoa, Italy, under the
intensity is proportional to the distance between the EE and the supervision of experienced clinical personnel and engineers. The
target and is online modulated (according to the motor abilities of patient did not receive any other rehabilitative treatment or advice
the patient) via EE speed monitoring. regarding the use of the paretic hand during the experiment period.
172 F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178

Fig. 1. (A) Wrist robotic device with associated representation of its three Degrees of freedom (B). (C) Workstation comprising the robotic device and a screen for the virtual
reality environment providing the visual feedback and ideal trajectories for 9 different targets during the pointing exercise.

Fig. 2. Assistive control algorithm consisting in three components: a performance evaluator, a force field generator and an adaptive controller.

2.5. Clinical and robotic measurements defined as the instant in which the wrist rotation speed exceeded
a threshold of 0.02 rad/s. Movement offset was defined as the
Clinical and robotic evaluations of upper extremity motor per- time at which the distance between EE and the target was less
formance were carried out one week before (t1) and one week after than 0.02 rad with angular speed below 0.02 rad/s. The following
the robotic therapy (t2). Each evaluation session lasted between kinematic performance indicators were calculated:
60 and 90 min hours. Clinical measures included the Melbourne
• Execution time (s): The time period between movement on-
Assessment of Unilateral Upper Limb Function, MAUULF [33], the
set and offset.
Assisting Hand Assessment, AHA, [34], and the Modified Ashworth
• Lateral deviation: mean distance between actual trajectory
Scale, MAS [35].
by the patient and the ideal straight trajectory between
We also evaluated performance using robot-based measures,
the center of two consecutive targets, calculated across the
as these have been found to have high resolution and repeata- entire trials.
bility, and provide complementary information regarding motor • Linearity index: The ratio between the length of ideal tra-
function [15]. To this end wrist joint rotation was recorded from jectory (the straight line connecting the starting point to
the robot’s incremental encoders: the patient’s wrist joint angular the target), and the trajectory covered by the end-effector.
RoM was estimated before (t1) and after robot training (t2). For A linearity index value of 1 (or 100%) indicates that the
each DoF (flexion/extension and abduction/abduction) the patient movement path was identical to that of the ideal trajectory,
freely moved the handle of the robot handle back and forth twenty whereas values below 1 (or 100%) indicate that the patient
times, attempting to achieve the maximum excursion of articu- is unable to achieve the final end point. Values above 1 (or
lar joints. RoM was calculated as the maximum excursion value 100%) indicate that the movement path was longer than
reached by the patient. During this test the motors of the robot the ideal trajectory and featured one or more corrective
were turned off, thus the patient moved the robotic handle without movements.
any assistance. • Smoothness index: The smoothness of the trajectory was
Wrist motion was post-processed to evaluate potential dif- evaluated using Teuling’s jerk indicator [36]. This indicator
ferences in motor recovery across the training program, and the is calculated from each trajectory by obtaining the jerk J(t)
robotic data were calculated for each trial. Movement onset was (the third time derivative of the trajectory) and computing
F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178 173

Table 1 Table 2
Pre- and post-robotic training scores from the Melbourne Assessment of Unilateral Modified Ashworth Scale (MAS) scores of different joints of the upper extremity
Upper Limb Function (MAUULF) and the Assisting Hand Assessment (AHA). prior to (t1) and after (t2) robotic training.
t1 t2 Difference t2–t1 Pre-training (t1) Post-training (t2)
MAUULF (% scores) 11.89% 26.63% 14.75% Shoulder adduction 1+ 1
AHA (raw score) 36/88 50/88 14 points Shoulder abduction 1+ 1
Elbow flexor 2 1
Elbow extensor 1+ 1
Wrist flexor 3 2
the square root of the averaged norm of Jerk, normalized Wrist extensor 2 2
with respect to duration T and path length L (Eq. (3)): Finger flexor 2 2

T5

1
jerk index = ∥J(t)∥2 dt . (3)
2 L2 3.2. Robot-based measures
Teuling’s jerk is dimensionless and does not depend on
To determine the effect size of the distal upper extremity
movement duration and trajectory length. Reduced coordi-
robotic rehabilitation program that featured an adaptive mod-
nation results in multiple acceleration peaks (i.e., increased
ulation of assistance, Tau-U was calculated separately for each
jerk levels) with lower values indicating smoother move-
robot-based measure [39]. TAU-U is a non-parametric derivation of
ments and higher motor coordination and control
Kendall’s rank correlation and the Mann–Whitney U test between
• The level of robotic assistance (i.e., amount of torque gener-
groups (trend index and nonoverlap index, respectively) com-
ated by the robot to help the patient complete the trial) was
monly used in single case research that examines the percentage
also evaluated. Overall FE and AA torques were measured
of non-overlap of the data between phases (i.e., pre-training vs.
to quantify the total amount of assistance provided to the post-training [40]. Tau-U scores range from 0 to 1, with 0.93 to 1
subject to perform the task, as well as separately in order to considered a large effect, 0.66 to 0.92 a medium effect, and 0 to 0.65
determine the recovery trend for each wrist DoF. a small effect [41]. Alpha was set at 1.0; a Bonferroni correction was
• The stiffness (K ), modulated online by the control algorithm not applied as the measures tested were dependent.
has been quantified (Eq. (2)). Fig. 3A depicts mean values of wrist joint angular RoM before
(t1) and after robot training (t2), for the four motions (FL, EX,
ABB, ADD). Active flexion RoM was substantially greater after robot
3. Results training (∼68.5◦ ) was substantially greater than prior to robot
training (∼45.5◦ ), resulting in a ∼23◦ increase, Tau − U = 0.778,
The patient participated in robot therapy twice a week for a 90% CI = −0.06 to 1.0, p = 0.089. The improvements in wrist
period of three months, with a total of forty sessions completed. On extension (∼0.94◦ at t1 and ∼2◦ at t2) and wrist abduction RoM
average, the patient completed between 3 and 6 puzzles (between (∼2◦ at t1 and ∼4.5◦ at t2) also reached statistical significance,
27 and 54 trials) per robotic therapy session. Each session lasted Tau − U = 0.889, 90% CI = 0.156 to 1.0, p = 0.809 and
between 30 and 60 min, with the length of individual sessions Tau − U = 1.0, 90% CI = 0.162 to 1.0, p = 0.0495, respectively. The
depending on the level of collaboration, fatigue and psychological improvement in wrist adduction RoM apparent after robot training
status of the patient on that day. (∼24.5◦ at t1 and ∼38◦ at t2) failed to reach statistical significance,
Tau − U = 0.667, 90% CI = −0.067 to 1.0, p = 0.190.
3.1. Clinical measures
3.2.1. Kinematic measures
Representative movement trajectories are depicted in Fig. 3B,
Outcome scores from clinical evaluation obtained before (t1)
and mean values for all kinematic indicators before (t1) and after
and after robot therapy (t2) are shown in Tables 1 and 2. Prior to
robot training (t2) are shown in Fig. 4A. For targets 1–8, execu-
robotic therapy the patient obtained a score of 11.9 in the MAUULF
tion time values were significantly shorter during the last session
scale, which improved to 26.6 after the three months training
(mean = 7.43 s, SD = 2.8) compared to the first session (mean =
period. MAUULF guidelines state a 14-point score change can be
22.67 s, SD = 2.8), (Tau − Urange = 0.64–0.92, 90% CIrange = −1.00
considered clinically significant, and as such the 14.8 difference
to −0.37, all p’s < 1.0). For target 9, Tau − U analysis indicated that
obtained in the present study is indicative of a clinically significant
execution time values were significantly shorter during the last
improvement in upper limb function. AHA scores also improved, (7.55 s, SD = 3.2) compared to the first session (4.60 s, SD = 3.06),
with a 15.9-points difference between pre- and post-assessment Tau − U = 0.68, 90% CI = 0.05 to 1.0, p = 0.076).
(t2−t1). This improvement exceeds the minimum change of points Improvements in lateral deviation were also found, with the
required to be considered clinically significant [37,38], indicating maximum distance between the actual and the ideal trajectories
that the patient had a noticeable reduction of motor impairments decreasing from 10.98◦ (SD = 7.8) at t1 to 2.92◦ (SD = 2.1)
during bimanual activities. at t2 (mean difference = 8.1◦ ), p < 0.001. Improvements
MAS scores of different upper extremity joints prior to (t1) and in lateral deviation was observed for all movement directions
after robot therapy (t2) are shown in Table 2. Prior to robot ther- (mean difference = 8.06◦ , SD = 7.31◦ , range = 1.68◦ –20.86◦ ),
apy (t1) the patient exhibited considerable spasticity in the wrist indicating that the subject regained mobility and isotropic RoM
flexors (MAS score of 3), and mild spasticity in the wrist extensors, despite the high level of spasticity. Tau − U analysis revealed
elbow and finger flexors (MAS score of 2: more marked increase significant differences in lateral deviation for targets 1–8 (Tau −
in tone, but affected parts are easily moved) and shoulder muscles Urange = −0.60–1.0, 90% CIrange = −1.00 to −0.37, all p’s < 1.0),
(MAS score of 1+: slightly increased tone). After the robotic train- but not target 9 (Tau − U = 0.02, 90% CI = −1.00 to −0.37,
ing program (t2), MAS score was reduced at all levels of the upper- p = 0.602).
limb, with greater improvements in the wrist extensors, elbow, The patient showed significant improvement (p < 0.001) in
wrist, and finger flexors (2-point change in score) compared to the linearity index, performing the movements with straighter trajec-
shoulder muscles, and elbow extensors (1-point change in score). tories in the last session (mean = 1.32, SD = 0.5) than the first
174 F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178

Fig. 3. (A) Mean active RoM values calculated prior (t1) and after robot training (t2) for the different tasks (FL, EX, AB, AD). Error bars indicate Standard Deviation evaluated
on the total number of trajectories requesting vertical or horizontal movements. (B) Representative trajectories during the first (left) and the last (right) training session.

Fig. 4. (A) Trend of performance’s indicators between first and last sessions. (B) Robotic assistance for the first five and the last five training sessions for flexion/extension (FE)
and abduction/adduction (AA), and trend line across sessions of total assistive torque and stiffness of the force field. Colors correspond to the different targets, as indicates
in Fig. 1C.

(mean = 6.31, SD = 4.5). Trajectories were found to be straighter was higher in the first training session than the last session for FE
after robotic training for targets 1–8 (mean difference = 5.4, (14.16 m N m vs 2.08 m N m, , Tau − U = −0.84, 90% I = −1.0
SD = 4.5, range = 1.09–11.23), which was confirmed by Tau − U to −0.210 , p = 0.0283) and AA (29.35 m N m vs 5.45 m N m),
analysis (Tau − Urange = −0.76–1.0, 90% CIrange = −1.00 to Tau − U = −1, 90% CI = −1.0 to −0.370 , p = 0.0090, both
−0.37, all p’s < 1.0). In contrast, linearity values did not differ p values < 0.001. As can be seen in Fig. 4B (third and fourth
significantly between the first and last session for target 9 (2.92 panels), there was a decreasing trend in the total amount of re-
and 1.60 respectively), Tau − U = 0.02, 90% CI = −0.43 to 0.83, quired robotic assistance (exponential fit, r 2 = 0.52) and stiffness
p = 0.602. (exponential fit, r 2 = 0.59), indicating that the patient needed less
Movement smoothness significantly changed over the course robotic assistance after completing the robotic training program.
of therapy, such that trajectories in the last training session were Important information can be gleaned by examining the unique
smoother (0.180e4, SD = 0.033e04) when compared to the first contributions of the separate FE and AA DoFs. The directional
training session (2.405e4, SD = 0.537e4). Tau−U analysis revealed representation of the assistance at the beginning (t1) and end (t2)
significant differences in lateral deviation for targets 1–3 and 5–8 of the therapy is shown in the first and second panels of Fig. 4B. It
(Tau − Urange = −0.68–1.0, 90% CIrange = 0.05 to 1.0, all p’s < 1.0), is clear that the amount of torque provided by the device is higher
but not target 4 (Tau − U = 0.52, 90% CI = −0.031 to 1.0, in directions in which the subject was initially unable to move or
p = 0.175). had a limited range of motion. Prior to robotic therapy the patient
required a greater amount of robotic assistance for wrist extension
3.2.2. Robot assistance measures and adduction than wrist flexion and abduction (Fig. 5). However,
The level of assistance provided by the robotic device was also the patient was not only able to perform the task with an overall
evaluated (Figs. 4B and 5). In general, the amount of assistive force lower level of assistance after the three-month robotic training
F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178 175

by the robotic device at the end of the robotic training program was
similar between the two DoFs.
Considering results from both the clinical and robotic assess-
ments, this case study provides preliminary evidence that partic-
ipation in intensive distal upper extremity robotic therapy that
features an adaptive control strategy can lead to positive changes
in active wrist RoM, wrist kinematics and dynamics. They also
show, for the first time, that distal upper extremity training can
lead to improvements in both the proximal and distal segments
of the upper limb in a pediatric stroke patient. This finding is
congruent with prior research in adult populations on robotic
rehabilitation of stroke [44,45] and incomplete spinal cord injury
in adult populations [46], and can be attributed to central and
peripheral mechanisms [43,47]. Examination of human upper ex-
tremity skeletal muscles [48] has revealed that distal movements
activate nerves and muscles that control the entire upper limb,
Fig. 5. Representative maximum assistive force provided by the robot during the
first (light gray) and last training sessions (dark gray) for flexion/extension (FE, and as such wrist training results in muscle activity at the distal
horizontal axis) and abduction/adduction (AA, vertical axis) movements. as well as the proximal segments of the limb. The improvements
in spasticity and motor performance brought about by distal upper
extremity robotic rehabilitation in turn lead to profound changes
program, but the reduced robotic intervention was delivered in a in neural plasticity within the cerebral cortex [49–51]. In contrast
more isotropic way (Fig. 5). to post-stroke proximal upper extremity robotic therapy, in which
improvements in function are limited to the elbow and shoul-
4. Discussion der [52], there is emerging evidence that rehabilitation of the distal
portion of the paretic limb leads to positive changes in the function
In this paper the effects of a three-month distal upper extremity of the entire limb even in the non-exercised joints. As such, it is
robotic training program that featured an online adaptive control recommended that bioengineering groups continue to focus their
algorithm was evaluated on a 14-year-old patient affected by up- efforts on the development of devices and control algorithms for
per extremity hemiparesis and spasticity after stroke. In contrast distal upper extremity rehabilitation.
to previous control algorithms in which the level of assistance is The results reported in this case study demonstrate that the
adjusted at the end of each trial or training session, the present on- proposed adaptive control strategy is robust (in terms of patient
line adaptive control algorithm provided assistance continuously response), is well accepted by the patient, and is able to smoothly
throughout the trial, so that the level of assistance was always adapt to the specific impairments of the patient without fine ad-
tailored to the participant’s capabilities. justments of the controller gains. The robust control architecture
The use of our online adaptive control algorithm lead to a allows for the introduction of a haptic robotic rehabilitation system
reduction in upper extremity spasticity after the three-month that features tuneable assistance and a user friendly interface to
robotic training program that extended throughout the entire limb, a clinical environment. Haptic robotic rehabilitation systems can
with greater improvements observed in the upper arm flexors, complement conventional physical therapy protocols by allowing
forearm/wrist flexors and extensors, and finger flexors compared the patient to perform a greater number of trials per training
to the shoulder and upper arm extensor muscles. In addition, session, and providing kinematic and dynamic feedback to the
clinical scores of upper extremity unimanual and bimanual limb clinician and patient. The proposed controller strategy is an autom-
function increased after the three-month robotic training program atized robotic version of the established wrist splinting technique,
(14.8-point and 15.9-point difference for the MAUULF and AHA, which many clinicians are familiar with. It is hypothesized that
respectively). The improvement in scores between the pre- and the similarities between the established manual technique and
post-test assessments exceeded the minimum change for both as- the robotic device will assuage any concerns that medical staff
sessments [42,43], suggesting a clinically significant improvement have regarding robotic rehabilitation, and consequently allow for
in arm function during unimanual and bimanual activities. technological based solutions to become more accessible to neuro-
There were also noticeable improvements in kinematic and logical populations who require specialized rehabilitation.
robot-based measures. Improvements in the quality of wrist In the future, it would be worthwhile comparing the effects
movement could be observed post-training: path lengths were obtained using our adaptive control strategy to different adap-
smoother, shorter, and featured fewer corrective movements in the tive control algorithms [20,53]. For example, Pehlivan et al., [54]
last training session than the first training session. Improvements presented an assist-as-needed controller featuring a feedback
in wrist joint angular RoM as a consequence of robotic training gain modification algorithm (which estimates only the position-
differed between DoFs. While there were no substantial changes dependent elements) and a real-time trajectory generation algo-
in wrist extension and abduction, active flexion RoM and adduc- rithm (used to modify the amount of permissible error based on
tion improved as a consequence of robotic training. In addition, user performance). Results demonstrated that the AAN adapted to
the amount of torque generated by the robot to help the patient the behavior of the (neurologically healthy) participants by provid-
complete the trial (assistive torque) was significantly lower in the ing varying levels of mechanical assistance and adapts the feedback
last training session than the first session, indicating that the pa- gains based on task performance. In a more recent study, the same
tient required less robotic assistance after completing the robotic research group [55] developed a minimal assist-as-needed (mAAN)
training program. We also found pre-training differences between controller that uses a Kalman filter and Lyapunov stability analysis
FE and AA DoFs, such that the amount of torque generated by the to accurately determine state estimation, a modification algorithm
robot to help the patient complete the trial (assistive torque) was that alters the degree of allowable error, and a disturbance re-
higher for wrist extension and adduction than for wrist flexion and jection decay algorithm that decreases resistive forces when able
abduction. However, this anisotropy in impairment decreased after subject movement desirably exceeds some given trajectory. Re-
the robotic training program, as the amount of assistance delivered sults from ten neurologically healthy individuals indicate that error
176 F. Marini et al. / Robotics and Autonomous Systems 91 (2017) 169–178

bound modification is capable of responding to changes in partic- References


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00182-2.
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347–351. URL http://www.ncbi.nlm.nih.gov/pubmed/2771177. ests include, neural control of movement, motor learning,
robot therapy, and robot cognition.
Francesca Marini graduated in Biomedical Engineering
at the University of Rome. Since January 2014, she has
been following a Ph.D. program in Cognitive Robotics,
Interaction and Rehabilitation Technologies at the Italian I
nstitute of Technology. Her Ph.D. project is mainly focused
on robotic rehabilitation in children with neurological in-
juries.
Lorenzo Masia, Assistant Professor at the Nanyang Techn
ological University (NTU) of Singapore was formerly post-
doctoral researcher at Italian Institute of Technology (IIT).
He graduated as Ph.D. in ‘‘Mechanical Measurement for
Dr Charmayne Hughes is now Associate Professor at the Engineering’’ at the University of Padua and was Ph.D. vis-
Department of Kinesiology of San Francisco State Univ iting student at the Massachusetts Institute of Technology
ersity and she was a senior post-doctoral fellow in the (MIT).
Robotics Research Centre in the Department of Mechanical
and Aerospace Engineering at Nanyang Technological Uni-
versity (NTU). Charmayne joined NTU in December 2013
following a Ph.D. in Motor Control at Purdue University,
and postdoctoral fellowships at Bielefeld University and
the Technical University of Munich.

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