14
Provided for non-commercial research and educational use only. Not for reproduction, distribution or commercial use. This chapter was originally published in the book Progress in Brain Research, Vol. 192, published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who know you, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial From: Jan Kowalczewski and Arthur Prochazka, Technology improves upper extremity rehabilitation. In Andrea M. Green, C. Elaine Chapman, John F. Kalaska, Franco Lepore, editors: Progress in Brain Research, Vol. 192, Amsterdam: The Netherlands, 2011, pp. 147-159. ISBN: 978-0-444-53355-5 © Copyright 2011 Elsevier B.V. Elsevier

Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

  • Upload
    others

  • View
    0

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

Provided for non-commercial research and educational use only. Not for reproduction, distribution or commercial use.

This chapter was originally published in the book Progress in Brain Research, Vol. 192, published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who know you, and providing a copy to your institution’s administrator.

All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at:

http://www.elsevier.com/locate/permissionusematerial

From: Jan Kowalczewski and Arthur Prochazka, Technology improves upper extremity rehabilitation. In Andrea M. Green, C. Elaine Chapman, John F. Kalaska,

Franco Lepore, editors: Progress in Brain Research, Vol. 192, Amsterdam: The Netherlands, 2011, pp. 147-159.

ISBN: 978-0-444-53355-5 © Copyright 2011 Elsevier B.V.

Elsevier

Page 2: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

A. M. Green, C. E. Chapman, J. F. Kalaska and F. Lepore (Eds.)Progress in Brain Research, Vol. 192ISSN: 0079-6123Copyright � 2011 Elsevier B.V. All rights reserved.

Author's personal copy

CHAPTER 10

Technology improves upper extremity rehabilitation

Jan Kowalczewski and Arthur Prochazka*

Centre for Neuroscience, School of Molecular and Systems Medicine,University of Alberta, Edmonton, Alberta, Canada

Abstract: Stroke survivors with hemiparesis and spinal cord injury (SCI) survivors with tetraplegia find itdifficult or impossible to perform many activities of daily life. There is growing evidence that intensiveexercise therapy, especially when supplemented with functional electrical stimulation (FES), can improveupper extremity function, but delivering the treatment can be costly, particularly after recipients leaverehabilitation facilities. Recently, there has been a growing level of interest among researchers andhealthcare policymakers to deliver upper extremity treatments to people in their homes using in-hometeletherapy (IHT). The few studies that have been carried out so far have encountered a variety of logisticaland technical problems, not least the difficulty of conducting properly controlled and blinded protocols thatsatisfy the requirements of high-level evidence-based research. In most cases, the equipment andcommunications technology were not designed for individuals with upper extremity disability. It is clear thatexercise therapy combined with interventions such as FES, supervised over the Internet, will soon beadopted worldwide in one form or another. Therefore it is timely that researchers, clinicians, and healthcareplanners interested in assessing IHT be aware of the pros and cons of the new technology and the factorsinvolved in designing appropriate studies of it. It is crucial to understand the technical barriers, the role oftelesupervisors, the motor improvements that participants can reasonably expect and the process ofoptimizing IHT-exercise therapy protocols to maximize the benefits of the emerging technology.

Keywords: stroke; spinal cord injury; multiple sclerosis; upper extremity; telerehabilitation; in-hometeletherapy; functional electrical stimulation; upper extremity rehabilitation.

Introduction

Three million stroke survivors in North Americahave unilateral paresis of the upper extremity

*Corresponding author.Tel.: þ1-780-492-3783; Fax: þ1-780-492-1617E-mail: [email protected]

147DOI: 10.1016/B978-0-444-53355-5.00010-5

(Lloyd-Jones et al., 2009). Over 100,000 peopleliving with spinal cord injury (SCI) have bilateralparesis or paralysis (NSCISC, 2010). People withtetraplegia due to SCI often depend on caregiversto perform the simplest manual tasks. Recoveryof upper extremity function is their top priority,over all other disabilities (Anderson, 2004).

Page 3: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

148

Author's personal copy

A rigorous program of exercise therapy canimprove upper extremity function after strokeand SCI (Drolet et al., 1999), and smallimprovements can make a large difference(Beekhuizen and Field-Fote, 2005). However,ensuring compliance to a regular exercise therapyprogram after people leave rehabilitation facilitiesis challenging. Clients may be given lists of exe-rcises they should perform, but these tend to beboring and compliance drops off over time.Health-care systems cannot afford to pay forhome visits by therapists to supervise exercisetherapy. This unsatisfactory situation has givenrise over the last few years to some new methodsof delivering upper extremity rehabilitation.These include forced-use training, now known asconstraint-induced movement therapy (Taubet al., 2006), computerized exercise devices suchas the Nintendo Wii, robotic devices that applyforces to the arm to assist or resist movements(Volpe et al., 2009), therapeutic electrical stimula-tion and functional electrical stimulation (FES;Peckham and Knutson, 2005; Stein and Pro-chazka, 2009) and in-home teletherapy (IHT)supervised over the Internet (Gritsenko and Pro-chazka, 2004; Gritsenko et al., 2001;Kowalczewski et al., 2011; Krebs et al., 1998;Reinkensmeyer et al., 2011).

IHT delivered to participants, particularly whencombined with interventions such as FES, posesunique safety and legal challenges which must beresolved before the technology is made availableto the larger population (Cooper et al., 2001). Nev-ertheless, with an aging population and ever-decreasing technology costs, telesupervised reha-bilitation will most likely provide an importantalternative to traditional rehabilitation. Littleinformation has been published on the obstaclesthat may arise when implementing IHT and howthey can be overcome. In this chapter, we willdiscuss some of the technical problems we encoun-tered in a recent clinical trial involving IHTand FES.

The descriptions and opinions presented hereare based on the experiences acquired in a

randomized clinical trial (NCT00656149, www.clinicaltrials.gov). In this trial, we compared twolevels of FES-exercise therapy and IHT treatmentin people with SCI. The main results of this studyhave been published elsewhere (Ellaway et al.,2010; Kowalczewski and University of Alberta,Centre for Neuroscience, 2009; Kowalczewskiet al., 2011).

General issues

Clinical studies of rehabilitation treatments, par-ticularly when these are telesupervised, differfrom clinical trials in other fields. First, mostresearchers planning randomized controlled trialsin rehabilitation, struggle with a suitable design,as in this field it is often difficult to provide quan-titative outcome measures, blinded assessments,control treatments that are not obvious to theparticipants and therapists and even suitable ran-domization, given the variability between peoplewith the same basic disability. It has been pointedout that in the whole field of rehabilitation, therehas been only a handful of studies that have ful-filled all the criteria of high-level, evidence-basedstudies (Johnston et al., 2006). Second, the equip-ment required for IHT has to be designed in sucha way as to withstand daily use for the duration ofthe trial, yet be intuitive and simple enough to beused by impaired participants without the con-stant presence of an able-bodied person to aid inthe rehabilitation process. Further, IHT equip-ment linking a therapist to a participant hasunique requirements compared to the commercialteleconferencing equipment primarily used forconference discussions. Third, if FES is involved,the FES equipment must be easy for the partici-pant to don, doff, and control, and be safe androbust enough to survive rough handling in thehome environment. Laboratory prototypes aregenerally not built with this in mind. Finally, ifthe therapy is performed at home in the absenceof daily supervision, compliance over days andweeks is a major issue, requiring careful attention

Page 4: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

149

Author's personal copy

to the entertainment value of the treatment.Therapists providing telesupervision shouldclosely monitor fatigue as this tends to demoralizeparticipants. Fatigue can easily be overlooked in atelerehabilitation setting.

Evidence-based rehabilitation

Only recently has the field of rehabilitation beenexamined according to the standards of evidence-based treatment through clinical meta-studies suchas Spinal Cord Injury Rehabilitation Evidence(www.icord.org/scire) and the Evidence-BasedReview of Stroke Rehabilitation (www.ebrsr.com). Rehabilitation therapists have been rela-tively slow in providing evidence-based care to cli-ents compared to practitioners in other medicalfields for a number of reasons. Rehabilitation reliesheavily on customization; therapists frequently arefaced with unique injuries and obstacles thatrequire patient-specific adaptation of protocolsand equipment. This customization is difficult tovalidate scientifically, unlike medical interventionsin conditions with fewer variables. It has generallybeen difficult in rehabilitation to reach a consensuson the best course of a particular treatment, as it isoften impossible to run properly blinded and con-trolled clinical trials. Unlike pharmacological trials,where placebos can be given to the control group ofpatients in a double-blind protocol, in rehabilita-tion trials, the rules of human experimentationrequire full disclosure to participants of thetreatments to be compared (Boutron et al., 2007).If a given treatment is compared to “standard care”or a “placebo treatment,” participants quickly rec-ognize whether they are in the treatment or controlgroup and adjust their expectations accordingly. Itis therefore preferable to compare differentintensities of a given treatment, where the relativeoutcomes are genuinely not predictable(Kowalczewski et al., 2007a) or to compare twoplausible treatments, for example, a novel interven-tion and a more conventional treatment that isadditional to normal care (Mangold et al., 2009).

It is clear from the above that to run properevidence-based rehabilitation trials, researchershave to be creative in designing and randomizingtheir trials (Komaroff and DeLisa, 2009). Reha-bilitation also usually takes a substantial amountof time, so treating enough participants to achievestatistical significance can be extremely costly.It is therefore vital for the field that researchersconcentrate on designing the best possiblerandomized controlled trials so as to maximizethe chance of influencing clinical practice.

Exercise equipment: efficacy, affordability,quantified outcomes

Conventional exercise therapy has focused on themanipulation of simple objects such as blocks,stacking cones, therapy putty, and so on. Exercisetherapy sessions are boring and in the absence ofsupervision, compliance falls off quickly, particu-larly at home. Performance is rarely if everquantified. This began to change with the devel-opment of robotic rehabilitation devicesinstrumented with sensors (Krebs et al., 1998;Volpe et al., 2009). The simplest rehabilitationrobots are motors that impose cyclical motion onextremities. They are commonly used in orthope-dics (Salter, 1996) and occasionally in stroke andSCI (Dirette and Hinojosa, 1994). The MIT-Manus (interactive-motion.com) is a robot thatsupports the arm and applies forces in the hori-zontal plane to assist or resist tracking of virtualobjects on a computer monitor (Aisen et al.,1997; Hogan et al., 2006). A recent randomizedcontrolled trial concluded that upper extremityfunction in chronic stroke subjects improved asmuch, though not more, after MIT-Manus roboticexercise therapy as after usual care by therapists(Lo et al., 2010). An editorial on the project con-cluded that the potential for robotic therapy afterstroke was enormous (Cramer, 2010). TheKINARM (bkintechnologies.com) is anotherexample of a planar robotic device that supportsthe arm. The Motorika ReoGo (motorika.com)

Page 5: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

150

Author's personal copy

is a telescopic device similar to a floor-shift gear-stick, which applies forces to the hand in 3Dspace. None of these robots exercise dexteroushand movements. The Inmotion 3.0 wrist robot,the Inmotion 5.0 hand robot, and some experi-mental robots address this deficiency to someextent (Hesse et al., 2006; Lambercy et al., 2007;Popescu et al., 2000). The above devices all costover $50,000 and so are unaffordable for IHT-exer-cise therapy. The only affordable robotic device, ataround $7000, is the Columbia Scientific “HandMentor.”However, this device only exercises wristand finger flexion–extension movements andignores range of motion of the whole arm.

Some groups have attempted to deliver motorrehabilitation in the home setting, with conven-tional exercises (Holden et al., 2007; Piron et al.,2004), therapeutic electrical stimulation (Alonet al., 2003; Sullivan and Hedman, 2007), or sim-ple robotic devices (Johnson et al., 2008; Rein-kensmeyer et al., 2002). It has become clear thatgreat efforts must be made in designing usablerehabilitation equipment, as participants in suchtrials are not able-bodied. In two previous trials,we set out to design and test instrumented work-stations suitable for in-home use (Gritsenko andProchazka, 2004; Gritsenko et al., 2001;Kowalczewski et al., 2007a,b) but we found thatthere were significant deficiencies in the devices.The first device (Fig. 1a) comprised a desk witha number of instrumented objects chosen to rep-resent household items: a spring-loaded door-knob, a handle attached via a cord and pulley toan adjustable set of weights, rectangular blocksand a cylinder designed to be transferred betweentwo docking bays. This workstation had looseitems that tended to be dropped, the layout madesome of the items hard to reach, the device wasbulky and not easily manufactured. In the nextversion (Fig. 1b), the items were mounted on a“Lazy Susan,” the idea being that the participantcould rotate the device to bring a given itemwithin easy reach. Unfortunately participantswere not strong enough to rotate the assembly,loose objects still fell and the structure was even

more bulky. We concluded from these attemptsthat any equipment destined for use in a homesetting would have to be of a size that suits thelimited amount of space in participants’ homes;the motor tasks would have to take into accountthe participant's disabilities and residual motorskills and all items should be in easy reach.

The next attempt comprised a table-mounted“suitcase model” comprising a set of “taskmodules” attached by compliant cables to doc-king ports (Fig. 1c). Each module could be pulledout of its docking port, positioned, and stabilizedwith the less affected hand. This version was sig-nificantly cheaper to manufacture and it was rea-sonably successful in tests on a number of strokepatients; however, a major limitation was therestriction of tasks to a horizontal plane. Further,the device was not suitable for people withbimanual deficits as it depended on tasks beingstabilized with one hand while training the other.

By now it had become clear that a portabledevice was needed that would present the userwith tethered, instrumented objects that couldmove within the full 3D physiological workspaceof the hand. Further, the device would ideallyprovide interesting games that would make exer-cise sessions enjoyable. We decided to adoptand extend the approach of Reinkensmeyeret al. (2002) who used a commercially availablejoystick in a computer gaming environment. Therange of motion of consumer computer joysticksis very restricted. To extend the range, wefabricated a joystick that had a telescopic shaftand a gimble joint at its base (Fig. 1d). This com-bination allowed the top of the joystick, whichheld a number of manipulanda, to be movedthrough a larger volume. The joystick alsocontained a sliding card manipulandum designedto train lateral and palmar prehension andpush–pull movements like those involved ininserting credit cards into automatic bankmachines. Unfortunately, the volume of theworkspace was restricted by the lengths of thelower and upper segments of the telescopic shaft,and thus remained significantly smaller than the

Page 6: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

Handleloadingweight

(a)

(b) (c)

(d) (e) (f)

Blocks

Controlbox

Cylinder

FES push-buttons

Handle

Doorknob

Dockingbay

Fig. 1. Six versions of an exercise therapy workstation developed for in-home teletherapy. (a) The device used in our first study inchronic stroke (Gritsenko and Prochazka, 2004; Gritsenko et al., 2001); (b) The device used in a study of people with subacutestroke; (c) A table-top system with task modules; (d) A telescopic joystick with attachments; (e) Prototype ReJoyce workstationused in a recent IHT study of people with SCI (Kowalczewski et al., 2011); (f) Final version of the ReJoyce system.

151

Author's personal copy

full physiological range of the hand of an able-bodied person. It was difficult to maintain thesame grasp on the attachments at different shaftangles. Friction within the shaft at oblique anglesresisted movement. The only dexterous task onthis workstation was the card-sliding mechanism.Some users with restricted ROM could not reachthe manipulanda at the top of the joystick, whichat its shortest, was still 35 cm above the table sur-face. The main lesson learnt from this prototypewas the importance of positioning the easiesttasks closest to the user so that they were accessi-ble even to low-functioning users.

As a result of all these unsuccessful iterations, wefinally settled on a workstation comprising aspring-loaded, segmented arm that presents theuser with a variety of attachments representingactivities of daily life.We called this theRehabilita-tion Joystick for Computerized Exercise(“ReJoyce”). Ten prototypeReJoyceworkstationswere manufactured and used in our IHT study(Fig. 1e; Kowalczewski and Prochazka, 2010).

Sensors in the arm and attachments of theReJoyce provide signals that are used by the sys-tem's software to evaluate motor function and tocontrol video games that exercise specific types

Page 7: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

152

Author's personal copy

of hand movement. The device allows movementover the full physiological range of an able-bod-ied person. Each joint and attachment has a sen-sor that quantifies displacement or force. Signalsfrom these sensors are used to control a suite ofcomputer games which vary widely in subjectmatter and difficulty. They range from simplegames that exercise whole-arm range of motionto games requiring coordinated movements ofmultiple joints, for example, grasp and squeeze,pinch and lift, grasp and rotate.

The prototype was generally successful but notsurprisingly, a number of hardware problemsdeveloped over time, requiring home visits forrepairs or modifications. On two occasions, airfreight was required and this involved assurancesregarding the purpose and safety of the devices,which resulted in significant delivery delays.When devices were set up in participants’ homes,in some cases, the table clamps did not have a suf-ficient range of adjustment for different tables,finding space for the equipment could be prob-lematic in small rooms and connecting to theInternet was occasionally challenging.

The final implementation of the ReJoyce(Fig. 1f), its games and Internet software is theresult of 6 years of experimentation. The systemmay be used with or without telesupervision (seebelow).

FES equipment

Early studies showed that therapeutic electricalstimulation can significantly reduce hypertonusand improve motor function in stroke survivors(Baker et al., 1979; Taylor et al., 1996; Waterset al., 1981). EMG-triggered FES with hand exe-rcises has since been shown to have beneficialeffects (Cauraugh and Kim, 2002; Chae, 2003; deKroon et al., 2005; Francisco et al., 1998;Heckmann et al., 1997). FES-exercise therapyperformed daily for several weeks has beenshown to produce clinically significantimprovements in hand function in subacute and

chronic stroke participants (Alon et al., 2007;Gritsenko and Prochazka, 2004; Kowalczewskiet al., 2007a; Popovic et al., 2004, 2005). SeveralFES devices have been developed for foot-drop(Stein et al., 2006; Taylor et al., 1999; Vodovniket al., 1981) and some hand FES devices havebeen developed recently (Hansen, 1979; Nathan,1994; Prochazka, 1997; Prochazka et al., 1997;Weingarden et al., 1998). Currently, the onlycommercial FES hand stimulator is the BionessH200 (Nathan, 1994; Weingarden et al., 1998).It comprises a hinged splint containing padelectrodes, and a separate stimulator triggeredby push-button. It costs around $6000, which isout of the range of most potential IHT-exercisetherapy clients; however, more affordable handstimulators are on the horizon.

In the IHT study upon which this chapter isbased, two different stimulators were employed.The EMS 7500 surface stimulator was used fortherapeutic electrical stimulation. It is an afford-able, commercially available consumer devicedesigned to deliver stimuli via self-adhesive gelelectrodes placed over appropriate motor points.In our study, we found it necessary to mark thelocations of the electrodes on the participants’forearms to ensure accurate and repeatable place-ment. A permanent marker was used every2 weeks to refresh the locations of the electrodes.The placement of the electrodes was most oftenperformed by an aid or family member. Aftertwo or three sessions, the electrode gel lost itsadherence and so participants were provided withneoprene straps that helped keep the electrodesin place after this occurred.

The other stimulator was a new version of the“Bionic Glove” (Prochazka et al., 1997). Theoriginal device was a fingerless glove-like gar-ment containing a built-in stimulator and wettableelectrodes. It was controlled by wrist movements.The new version was controlled by the partici-pant, who generated small tooth-clicks to advancethe stimulator through a cyclical sequence ofthree states corresponding to hand opening,grasp, and relaxation (Simpson et al., 2008).

Page 8: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

153

Author's personal copy

The tooth-clicks were detected by a wireless ear-piece similar to a hearing aid. The hanger portionof the earpiece was looped over the ear and helda three-axis accelerometer that rested on the tra-gus, the small cartilage in front of the ear. Whena tooth-click occurred, the earpiece sent a codedtransmission to the stimulator in the participant'sgarment. This caused the stimulator to advanceto the next state in the stimulation sequence.Initially the garment portion of the device was

the same as in the Bionic Glove, covering thewrist, palm, and dorsal part of the hand. How-ever, we found that even though the wrist sectionwas compliant, it restricted hand movements.Because we had replaced the wrist movementsensor of the Bionic Glove with the earpiece con-troller, the palmar portion of the garment was nolonger necessary and was replaced with a neo-prene loop over the webspace between thumband index finger which held the thumb adductorelectrode in place. This was an improvement, aswe have found that covering the palm, even withthe use of high-friction materials, increases thelikelihood of slip, for example, when graspingand pushing wheelchair rims.The electrodes were secured by Velcro to the

inner surface of the garment, so that when thegarment was donned, they were pressed on orclose to the desired motor points. The electrodepositions within the garment were reevaluated atevery laboratory visit. The correct donning ofthe device required some practice as inappropri-ate positioning could lead to inadequate or inef-fective stimulation. Unlike the adhesiveelectrodes used in the EMS 7500, the electrodesin the garment needed to be moistened with tapwater before each use. Wetting and reconnectingthe electrodes to the glove was most often per-formed by an aid or family member, especiallyin very low-functioning SCI participants. In con-trast, most stroke participants have adequatefunction of their less affected hand to don anddoff stimulator cuffs unaided. Some failures ofthe hand stimulator occurred initially becausethe connector between the stimulator and wristlet

was exposed and unreliable. This was solved byrecessing the connector within a rubberized shoeor “galosh” attached to the wristlet.

Teleconferencing equipment and software

We found that one-on-one telesupervision usingthe Internet was possible with relatively modestsoftware requirements on the supervisors’ and par-ticipants’ computers and recurring costs were negli-gible. Internet-based telerehabilitation requires aminimum of two computers connected reliably tothe Internet, webcams, speakers, and microphonesor headsets consisting of headphones and a micro-phone (recommended for echo-cancelation). Stan-dard desktop or laptop computers were used in ourstudy and they had sufficient processing power tohandle the large video and audio streams and thecustom processor-intensive games that were sup-plied with the ReJoyce system.

We found that it was crucial to maintain arobust Internet connection. Most participantshad a wireless router system in their homes.Remote access from the laboratory to these wire-less routers was useful, as electrical storms, routerresets and modem resets corrupted the wirelesslinks on several occasions. Remote access gener-ally allowed these problems to be overcomequickly, though on a few occasions a home visitwas required. The majority of Internet-relateddifficulties emerged in the first few days oftreatment.

In our trial, we used two types of Virtual Net-work Computing software. The first, RealVNCÒ

(realvnc.com), implemented a direct computer-to-computer link. The second, LogmeinÒ (www.logmein.com), used a third party server to accessthe participant's computer, which was more con-venient as it did not require the use and configu-ration of an Internet protocol address, nor thesetting up of the participant's router to establisha connection. The drawback to using a third partyserver is the greater potential for a breach ofsecurity (see below).

Page 9: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

154

Author's personal copy

Various teleconferencing software programswere available prior to this trial, but they wereall designed for group interactions. None alloweda therapist to monitor a group of participants andto select particular participants for briefindividualized discussions which the other par-ticipants did not hear. Software that did providethis ability was developed specifically for theReJoyce system. It also allowed the therapistremotely to choose games, difficulty levels andthe manipulanda involved, for each participantindividually. It also allowed an automated, quan-titative hand function test to be performedremotely and the data to be downloaded.

Though data and audiovisual streams wereencrypted, as with any telecommunication system,it was impossible completely to exclude the possi-bility of intruders intercepting audiovisual anddata transmissions. However, because the customsoftware was very specialized, restricted to smallgroups and password-protected, the risk of inter-ception was probably far less than that of publicInternet telecommunications protocols, such asSkype, which is used by over 100 million peopleworldwide. Users and therapists alike wererequired to accept this risk. Precautions such asavoiding the use of names and places during tel-etherapy sessions were taken, and will probablyremain advisable in all future systems.

Not all computer games were of equal value inour rehabilitation trial. The types of computergames used in upper extremity rehabilitation varyfrom very simple games (Reinkensmeyer et al.,2002) to virtual reality simulation of real-worldtasks with force feedback from haptic devicessuch as the Phantom robot (Adamovich et al.,2004; Boian et al., 2002). The primary role of acomputer game in upper extremity rehabilitationis to increase compliance. Therefore, the gamesneed to be entertaining. They also should ensurethat the types of movements involved are benefi-cial and ideally the games should provide feed-back to both the participants and therapists onperformance. This feedback can be in the formof an overall score or the time taken to perform

a given task. An example of a successful devicethat provides numerous entertaining games isthe Nintendo Wii, which has become popular inrehabilitation clinics for providing range ofmotion exercises of the whole upper body (Allen,2007; Graves et al., 2008). However, the Wii wasnot designed for rehabilitation and its controllerdoes not require or exercise manual dexterity.Nor are the movement signals that control thegames available for analysis, though someresearchers are working to change this.

Games that provided this type of feedback tothe users were among the most utilized by ourtelesupervisors and the most requested by theparticipants. Feedback on performance evidentlyprovides a “hook” that plays on the user's com-petitive nature. Participants are more inclined toimprove on their previous performance whenthey are provided with a measure of this perfor-mance and rewarded for a better outcome.Games that incorporated a reward mechanismhad the highest rate of acceptance and usage.

Our trial also suggested that improvements inupper extremity function did not require fullyimmersive 3D games. All the games developedfor the ReJoyce were built with 2D game technol-ogy which avoids the need for 3D graphic acceler-ation, virtual reality displays, or haptics. It wasclear, however, that variety in games was crucial.The more games the participant and supervisorcould choose from, the higher the chance of thegames continuing to appeal to the participants inmany repeated sessions. Although preference incomputer games has been related to gender inyoung adults (Lucas and Sherry, 2004) and chil-dren (Blumberg and Sokol, 2004), in our trial thiswas not an obvious outcome, though it would beinteresting to study this more rigorously.

Unlike many games designed only for enter-tainment, the games used in our trial were specif-ically designed for rehabilitating and retrainingupper extremity movements. The advantages ofusing custom games included the ability to (1)train unique movements that could not be trainedon preexisting consumer-oriented games; (2)

Page 10: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

155

Author's personal copy

modify difficulty settings during the training pro-cess in order to optimize the therapy; (3) auto-matically compute difficulty settings on the basisof a hand function test score; (4) embed thegames in the telerehabilitation software suite,minimizing the need to learn how to use non-customized games; (5) design the games to beplayed with the various manipulanda on theworkstation. Six games were developed and usedin the trial: a car racing game, a gardening game,a boxing game, a timing game, a target shootinggame, and a catching game.It has become clear in the course of our work

that different treatment regimes are needed fordifferent motor disorders. Thus, stroke survivorsseemed to benefit most from the training ofwhole-arm range of motion and finger extension(hand opening) movements, whereas SCI par-ticipants benefitted most from training hand graspand tenodesis pinch-grip.

Outcome evaluation, effect of fatigue

The results of the IHT study have been reportedin detail elsewhere (Kowalczewski et al., 2011).The primary outcome measure was the widelyused Action Research Arm Test (Lyle, 1981;Yozbatiran et al., 2008). Secondary outcomemeasures included (1) The ReJoyce AutomatedHand Function Test; (2) Pinch force betweenthumb and fingers measured with a pinch gauge(B&L Engineering, Santa Ana, CA); (3) Graspforce measured with a rubberized, instrumentedcylinder on the workstation. The ReJoyceAutomated Hand Function Test was performedon the ReJoyce workstation with audiovisualprompts and reminders generated by interactivesoftware. Sensors in the workstation providedsignals that allowed quantitative scoring of thefollowing variables: range of motion of the handalong three axes (in–out, up–down, left–right),the force of grasp and the amount of pronationand supination during grasp and key-grip. Thesevariables were scored as a percentage of the mean

ranges achieved by able-bodied individuals. Inaddition, there were two functional placementtasks involving grasping, transferring, and releas-ing two manipulanda on the workstation, onemimicking a soft-drink can and the other a peg.The mean times taken to do several repetitionsof these functional tasks were used to obtain apercentage score related to the performance ofable-bodied individuals. The mean of all thescores obtained in the above tasks was computed,providing a single overall outcome score. TheReJoyce Automated Hand Function Test tookabout 5 min to perform.

The scores from both the Action ResearchArm Test and the ReJoyce Automated HandFunction Test improved significantly more duringand after ReJoyce exercise therapy with FES thanafter conventional exercise therapy with thera-peutic electrical stimulation (Fig. 2). Bothprotocols involved 6 weeks of 1 h/day IHT. Graspforce also increased more in the ReJoyce group.We concluded that FES-assisted exercise therapyon a ReJoyce workstation, supervised over theInternet with IHT, was feasible and effective.The improvements exceeded the minimal clini-cally important difference, which is often used asa criterion to introduce a treatment into bestpractice.

We found that during IHT therapists had to becareful not to overexert participants involved inIHT-exercise therapy. In one case, a participantdeveloped proximal muscle strain that requireda rest period of 2 weeks for recovery. Fatiguecan potentially aggravate preexisting pain andspasticity as well as cognitive and emotional dis-orders (Hammell et al., 2009). On the other hand,moderate physical activity in SCI has been shownto lower pain, fatigue, and depression (Tawashyet al., 2009). Therefore, it is important to judgethe appropriate amount of exercise on an individ-ual basis.

Muscle fatigue was commented upon by all ofthe participants in our study. It is known thatmuscles lose fatigue resistance following SCI(Shields et al., 1997). The loss occurs fairly

Page 11: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

Conventional (postexercise)ReJoyce (postexercise)ConventionalReJoyce

25(a)

(b)

20

AR

AT

impr

ovem

ent (

%)

15

10

5

0

−5Baseline Week 2 Week 4

TimeWeek 6

25

30

20

RA

HFT

impr

ovem

ent (

%)

15

10

5

0

−5Baseline Week 2 Week 4

TimeWeek 6

Conventional (postexercise)ReJoyce (postexercise)ConventionalReJoyce

Fig. 2. Hand function tests performed during biweeklylaboratory visits by participants taking part in the IHT study(Kowalczewski et al., 2011). (a) Mean improvements overbaseline in the Action Research Arm Test (ARAT). Solidand dashed lines: scores before and after 1-h of FES-ETperformed in the laboratory. Notice that at 2 weeks, therewas a significant difference (asterisk) between the pre-ETand post-ET scores, which we attribute to muscle fatigue.This was not seen in subsequent sessions at 4 and 6 weeks.(b) Mean improvements in the ReJoyce automated handfunction test (RAHFT), showing a similar difference in pre-and post-ET scores at 2 weeks.

156

Author's personal copy

rapidly, is generally complete within 2 years ofinjury but is apparently not age-dependent(Shields et al., 2006). Loss of fatigue resistancecan be reversed to some extent with repeatedelectrical stimulation commencing soon afterinjury (Shields and Dudley-Javoroski, 2006).

Traditionally, muscle fatigability is quantified bymeasuring the torque generated by an electricallystimulated muscle or group of muscles (Steinet al., 1992). In our IHT trial, no such quantitativemeasure was available, but it was commonlyobserved that most participants were unable tocomplete a full hour of FES-assisted exercise inthe first week of ReJoyce training sessions. Ini-tially, muscles would only respond to stimulationfor a few minutes. This improved as the treatmentprogressed and by the second week all par-ticipants were able to generate functional move-ments with FES for the entire 1 h session.

Interestingly, this effect was discernible in thescores of the Action Research Arm Test andReJoyce Automated Hand Function Test whenthese were performed before and after 1 h exer-cise sessions (Fig. 2, solid lines: scores just beforeexercise therapy, dashed lines: scores just afterexercise therapy). Paired Student's t-tests showedsignificant differences at week 2, but not thereafter,suggesting that the muscles had become morefatigue resistant by week 4. This correlated withspontaneous comments from the ReJoyce group inearly training sessions that the games distractedthem to the point that at the end of a session theyfelt that they had had a very vigorous workout.The control group rarelymade this sort of comment.

Experiencing rapid muscle fatigue followingelectrical stimulation in the initial period was dis-couraging for the participants. During the first2 weeks, it is therefore important that participantsbe made aware that electrical stimulation can rap-idly fatigue muscles but that with training themuscles build fatigue resistance.

Conclusion

Many recent studies have shown that exercisetherapy can significantly improve upper extremityfunction after a stroke or SCI, which implies thatcurrently the duration and intensity of exercisetherapy provided to these individuals are insuffi-cient. This is because of the cost and logistical

Page 12: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

157

Author's personal copy

difficulties of providing such treatment, particu-larly after people rejoin their communities. Fur-ther, because of time and budgetary constraints,the main focus of many therapists is to teach basicadaptive strategies, self-care, and hygiene and toprovide assistive devices and techniques for lifeat home. Improving hand function is often treatedas a desirable but secondary aim. This state ofaffairs is driven by the increased pressure onhealthcare systems and third-party payers to pro-vide patients with only the most elementary cop-ing skills to contain costs and allow for a largethroughput. But as suggested by Dr. KimberleyAnderson in a study of SCI priorities (Anderson,2004), this may be a false economy. The use ofaffordable technology that allows upper extremityrehabilitation to be performed at home withInternet-based telesupervision provides apromising solution to this dilemma.

Acknowledgments

This work was funded by the Canadian Institutesfor Health Research, the Alberta Heritage forMedical Research (now Alberta Innovates HealthSolutions), and the International Spinal ResearchTrust.

References

Adamovich, S. V., Merians, A. S., Boian, R., Tremaine, M.,Burdea, G. S., Recce, M., et al. (2004). A virtual realitybased exercise system for hand rehabilitation post-stroke:Transfer to function. Conference Proceedings: Annul Inter-national Conference of the IEEE Engineering in Medicineand Biology Society, 7, 4936–4939.

Aisen, M. L., Krebs, H. I., Hogan, N., Mcdowell, F., &Volpe, B. T. (1997). The effect of robot-assisted therapyand rehabilitative training on motor recovery followingstroke. Archives of Neurology, 54, 443–446.

Allen, D. (2007). You're never too old for a Wii. NursingOlder People, 19, 8.

Alon, G., Levitt, A. F., & Mccarthy, P. A. (2007). Functionalelectrical stimulation enhancement of upper extremity func-tional recovery during stroke rehabilitation: A pilot study.Neurorehabilitation and Neural Repair, 21, 207–215.

Alon, G., Sunnerhagen, K. S., Geurts, A. C., & Ohry, A.(2003). A home-based, self-administered stimulation pro-gram to improve selected hand functions of chronic stroke.Neuro Rehabilitation, 18, 215–225.

Anderson, K. D. (2004). Targeting recovery: Priorities of thespinal cord-injured population. Journal of Neurotrauma,21, 1371–1383.

Baker, L. L., Yeh, C., Wilson, D., & Waters, R. L. (1979).Electrical stimulation of wrist and fingers for hemiplegicpatients. Physical Therapy, 59, 1495–1499.

Beekhuizen, K. S., & Field-Fote, E. C. (2005). Massed practiceversus massed practice with stimulation: Effects on upperextremity function and cortical plasticity in individuals withincomplete cervical spinal cord injury. Neurorehabilitationand Neural Repair, 19, 33–45.

Blumberg, F. C., & Sokol, L. M. (2004). Boys’ and girls’ use ofcognitive strategy when learning to play video games. TheJournal of General Psychology, 131, 151–158.

Boian, R., Sharma, A., Han, C., Merians, A., Burdea, G.,Adamovich, S., et al. (2002). Virtual reality-based post-stroke hand rehabilitation. Studies in Health Technologyand Informatics, 85, 64–70.

Boutron, I., Guittet, L., Estellat, C., Moher, D.,Hrobjartsson, A., & Ravaud, P. (2007). Reporting methodsof blinding in randomized trials assessing non-pharmacological treatments. PLoS Medicine, 4, e61.

Cauraugh, J. H., & Kim, S. (2002). Two coupled motor recov-ery protocols are better than one: Electromyogram-trig-gered neuromuscular stimulation and bilateral movements.Stroke, 33, 1589–1594.

Chae, J. (2003). Neuromuscular electrical stimulation formotor relearning in hemiparesis. Physical Medicine andRehabilitation Clinics of North America, 14, S93–S109.

Cooper, R. A., Fitzgerald, S. G., Boninger, M. L.,Brienza, D. M., Shapcott, N., Cooper, R., et al. (2001).Telerehabilitation: Expanding access to rehabilitation exper-tise. Proceedings of the IEEE, 89, 1174–1193.

Cramer, S. C. (2010). Brain repair after stroke. The NewEngland Journal of Medicine, 362, 1827–1829.

De Kroon, J. R., Ijzerman, M. J., Chae, J., Lankhorst, G. J., &Zilvold, G. (2005). Relation between stimulation cha-racteristics and clinical outcome in studies using electricalstimulation to improve motor control of the upper extremityin stroke. Journal of Rehabilitation Medicine, 37, 65–74.

Dirette, D., & Hinojosa, J. (1994). Effects of continuous pas-sive motion on the edematous hands of two persons withflaccid hemiplegia. The American Journal of OccupationalTherapy, 48, 403–409.

Drolet, M., Noreau, L., Vachon, J., & Moffet, H. (1999). Mus-cle strength changes as measured by dynamometry followingfunctional rehabilitation in individuals with spinal cordinjury. Archives of Physical Medicine and Rehabilitation,80, 791–800.

Page 13: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

158

Author's personal copy

Ellaway, P. H., Kuppuswamy, A., Balasubramaniam, A. V.,Maksimovic, R., Gall, A., Craggs, M. D., et al. (2010).Development of quantitative and sensitive assessments ofphysiological and functional outcome during recovery fromspinal cord injury: A clinical initiative. Brain Research Bulle-tin, 84, 343–357.

Francisco, G., Chae, J., Chawla, H., Kirshblum, S., Zorowitz, R.,Lewis, G., et al. (1998). Electromyogram-triggered neuromus-cular stimulation for improving the arm function of acutestroke survivors: A randomized pilot study.Archives of Physi-cal Medicine and Rehabilitation, 79, 570–575.

Graves, L. E., Ridgers, N. D., & Stratton, G. (2008). The con-tribution of upper limb and total body movement toadolescents’ energy expenditure whilst playing NintendoWii. European Journal of Applied Physiology, 104, 617–623.

Gritsenko, V., Chhibber, S., & Prochazka, A. (2001). AutomatedFES-assisted exercise therapy for hemiplegic hand function.Society for Neuroscience Abstracts, 27, 210–220.

Gritsenko, V., & Prochazka, A. (2004). A functional electricstimulation-assisted exercise therapy system for hemiplegichand function. Archives of Physical Medicine and Rehabili-tation, 85, 881–885.

Hammell, K. W., Miller, W. C., Forwell, S. J., Forman, B. E.,& Jacobsen, B. A. (2009). Fatigue and spinal cord injury:A qualitative analysis. Spinal Cord, 47, 44–49.

Hansen, G. V. O. (1979). EMG-controlled functional electricalstimulation of the paretic hand. Scandinavian Journal ofRehabilitation Medicine, 11, 189–193.

Heckmann, J., Mokrusch, T., Kroeckel, A., Warnke, S., VonStockert, T., & Neundoerfer, B. (1997). Electromyogram-triggered neuromuscular stimulation for improving the armfunction of acute stroke survivors: A randomized pilotstudy. European Journal of Physical Medicine and Rehabili-tation, 7, 138–141.

Hesse, S., Schmidt, H., & Werner, C. (2006). Machines to sup-port motor rehabilitation after stroke: 10 years of experi-ence in Berlin. Journal of Rehabilitation Research andDevelopment, 43, 671–678.

Hogan, N., Krebs, H. I., Rohrer, B., Palazzolo, J. J.,Dipietro, L., Fasoli, S. E., et al. (2006). Motions or muscles?Some behavioral factors underlying robotic assistance ofmotor recovery. Journal of Rehabilitation Research andDevelopment, 43, 605–618.

Holden, M. K., Dyar, T. A., & Dayan-Cimadoro, L. (2007).Tele-rehabilitation using avirtual environment improvesupperextremity function in patients with stroke. IEEE Transactionson Neural Systems and Rehabilitation Engineering, 15, 36–42.

Johnson, M. J., Loureiro, R. C., & Harwin, W. S. (2008). Col-laborative tele-rehabilitation and robot-mediated therapyfor stroke rehabilitation at home or clinic. Intelligent ServiceRobotics, 1, 109–121.

Johnston, M. V., Sherer, M., & Whyte, J. (2006). Applying evi-dence standards to rehabilitation research. American Jour-nal of Physical Medicine and Rehabilitation, 85, 292–309.

Komaroff, E., & Delisa, J. A. (2009). Best research evidencefor physical medicine and rehabilitation. The Journal of Spi-nal Cord Medicine, 32, 3–5.

Kowalczewski, J., Chong, S. L., Galea, M., & Prochazka, A.(2011). In-home tele-rehabilitation improves tetraplegichand function. Neurorehabilitation and Neural Repair, 25,412–422.

Kowalczewski, J., Gritsenko, V., Ashworth, N., Ellaway, P., &Prochazka, A. (2007). Upper-extremity functional electricstimulation-assisted exercises on a workstation in the sub-acute phase of stroke recovery. Archives of Physical Medi-cine and Rehabilitation, 88, 833–839.

Kowalczewski, J., & Prochazka, A. (2010). Method and appa-ratus for automated delivery of therapeutic exercises of theupper extremity. USA patent application US2007265146.

Kowalczewski, J. A., Prochazka, A., & Chong, S. L. (2007b).Home based upper extremity rehabilitation in spinal cordinjured patients. In Society for Neuroscience Abstracts. SanDiego, USA: 75.71/GG71.

Kowalczewski, J.University of Alberta, Centre for Neurosci-ence. Upper extremity neurorehabilitation. (2009). [Online].Available:http://hdl.handle.net/10048/755 (Accessed).

Krebs, H. I., Hogan, N., Aisen, M. L., & Volpe, B. T. (1998).Robot-aided neurorehabilitation. IEEE Transactions onRehabilitation Engineering, 6, 75–87.

Lambercy, O., Dovat, L., Gassert, R., Burdet, E., Teo, C. L., &Milner, T. (2007). A haptic knob for rehabilitation of handfunction. IEEE Transactions on Neural Systems and Reha-bilitation Engineering, 15, 356–366.

Lloyd-Jones, D., Adams, R. J., Brown, T. M., Carnethon, M.,Dai, S., De Simone, G., et al. (2009). Heart disease andstroke statistics–2010 update. A report from the AmericanHeart Association. Circulation, 121, e46–e215.

Lo, A. C., Guarino, P. D., Richards, L. G., Haselkorn, J. K.,Wittenberg, G. F., Federman, D. G., et al. (2010). Robot-assisted therapy for long-term upper-limb impairment afterstroke.The NewEngland Journal ofMedicine, 362, 1772–1783.

Lucas, K., & Sherry, J. L. (2004). Sex differences in videogame play: A communication-based explanation. Communi-cation Research, 31, 499–523.

Lyle, R. C. (1981). A performance test for assessment of upperlimb function in physical rehabilitation treatment andresearch. International Journal of Rehabilitation Research,4, 483–492.

Mangold, S., Schuster, C., Keller, T., Zimmermann-Schlatter, A.,& Ettlin, T. (2009). Motor training of upper extremity withfunctional electrical stimulation in early stroke rehabilitation.Neurorehabilitation and Neural Repair, 23, 184–190.

Nathan, R. H. (1994). Device for generating hand function. USPatent #5,330,516 US Patent Office, 15 claims, 6 drawingsheets.

NSCISC. (2010). Spinal cord injury facts and figures at a glanceBirmingham. Alabama: National Spinal Cord Injury Statisti-cal Center.

Page 14: Provided for non-commercial research and …...of delivering upper extremity rehabilitation. These include forced-use training, now known as constraint-induced movement therapy (Taub

159

Author's personal copy

Peckham, P. H., & Knutson, J. S. (2005). Functional electricalstimulation for neuromuscular applications. Annual Reviewof Biomedical Engineering, 7, 327–360.

Piron, L., Tonin, P., Trivello, E., Battistin, L., & Dam, M.(2004). Motor tele-rehabilitation in post-stroke patients.Medical Informatics and the Internet in Medicine, 29,119–125.

Popescu, V. G., Burdea, G. C., Bouzit, M., & Hentz, V. R.(2000). A virtual-reality-based telerehabilitation system withforce feedback. IEEE Transactions on Information Technol-ogy in Biomedicine, 4, 45–51.

Popovic, D., Popovic, M., Sinkjaer, T., Stefanovic, A., &Schwirtlich, L. (2004). Therapy of paretic arm in hemiplegicsubjects augmented with a neural prosthesis: A cross-overstudy. Canadian Journal of Physiology and Pharmacology,82, 749–756.

Popovic, M., Thrasher, T., Zivanovic, V., Takaki, J., &Hajek, V. (2005). Neuroprosthesis for retraining reachingand grasping functions in severe hemiplegic patients.Neuromodulation, 8, 58–72.

Prochazka, A. (1997). Garment having controller that isactivated by mechanical impact. Canada, WO 99/19019 pat-ent application.

Prochazka, A., Gauthier, M., Wieler, M., & Kenwell, Z.(1997). The bionic glove: An electrical stimulator garmentthat provides controlled grasp and hand opening in quadri-plegia. Archives of Physical Medicine and Rehabilitation,78, 608–614.

Reinkensmeyer, D. J., Pang, C. T., Nessler, J. A., &Painter, C. C. (2002). Web-based telerehabilitation for theupper extremity after stroke. IEEE Transactions on NeuralSystems and Rehabilitation Engineering, 10, 102–108.

Salter, R. B. (1996). History of rest and motion and the scien-tific basis for early continuous passive motion. Hand Clinics,12, 1–11.

Shields, R. K., Chang, Y. J., Dudley-Javoroski, S., & Lin, C. H.(2006). Predictive model of muscle fatigue after spinal cordinjury in humans. Muscle & Nerve, 34, 84–91.

Shields, R. K., & Dudley-Javoroski, S. (2006). Musculoskeletalplasticity after acute spinal cord injury: Effects of long-termneuromuscular electrical stimulation training. Journal ofNeurophysiology, 95, 2380–2390.

Shields, R. K., Law, L. F., Reiling, B., Sass, K., & Wilwert, J.(1997). Effects of electrically induced fatigue on the twitchand tetanus of paralyzed soleus muscle in humans. Journalof Applied Physiology, 82, 1499–1507.

Simpson, T., Broughton, C., Gauthier, M. J., & Prochazka, A.(2008). Tooth-click control of a hands-free computer interface.IEEETransactions onBiomedical Engineering, 55, 2050–2056.

Stein, R. B., Chong, S., Everaert, D. G., Rolf, R.,Thompson, A. K., Whittaker, M., et al. (2006). A multicen-ter trial of a footdrop stimulator controlled by a tilt sensor.Neurorehabilitation and Neural Repair, 20, 371–379.

Stein, R. B., Gordon, T., Jefferson, J., Sharfenberger, A.,Yang, J. F., De Zepetnek, J. T., et al. (1992). Optimal stim-ulation of paralyzed muscle after human spinal cord injury.Journal of Applied Physiology, 72, 1393–1400.

Stein, R. B., & Prochazka, A. (2009). Impaired motor function:Functional electrical stimulation. In A. M. Lozano, P. L.Gildenberg & R. R. Tasker (Eds.), Textbook of stereotacticand functional neurosurgery. Berlin: Springer.

Sullivan, J. E., & Hedman, L. D. (2007). Effects of home-based sensory and motor amplitude electrical stimulationon arm dysfunction in chronic stroke. Clinical Rehabilitation,21, 142–150.

Taub, E., Uswatte, G., King, D. K., Morris, D., Crago, J. E., &Chatterjee, A. (2006). A placebo-controlled trial of con-straint-induced movement therapy for upper extremity afterstroke. Stroke, 37, 1045–1049.

Tawashy, A. E., Eng, J. J., Lin, K. H., Tang, P. F., & Hung, C.(2009). Physical activity is related to lower levels of pain,fatigue and depression in individuals with spinal-cord injury:A correlational study. Spinal Cord, 47, 301–306.

Taylor, P., Burridge, J., Dunkerley, A., Wood, D., Norton, J.,Singleton, C., et al. (1999). Clinical audit of 5 years provisionof the Odstock dropped foot stimulator. Artificial Organs,23, 440–442.

Taylor, P. N., Burridge, J. H., Hagan, S. A., Chapple, P., &Swain, I. D. (1996). Improvement in hand function and sen-sation in chronic stroke patients following electrical stimula-tion exercises. A retrospective clinical audit. In P. HunterPeckham (Ed.), 1st Annual Conference of the InternationalFES Society. Cleveland, OH.

Vodovnik, L., Bajd, T., Kralj, A., Gracanin, F., & Strojnik, P.(1981). Functional electrical stimulation for control of loco-motor systems. CRC Critical Reviews in Bioengineering, 6,63–131.

Volpe, B. T., Huerta, P. T., Zipse, J. L., Rykman, A.,Edwards, D., Dipietro, L., et al. (2009). Robotic devices astherapeutic and diagnostic tools for stroke recovery. Arc-hives of Neurology, 66, 1086–1090.

Waters, R., Bowman, B., Baker, L., Benton, L., &Meadows, P. (1981). Treatment of hemiplegic upper extrem-ity using electrical stimulation and biofeedback training.In D. Popovic (Ed.), Advances in external control of humanextremities. Belgrade: Yugoslav Committee for Electronicsand Automation.

Weingarden, H. P., Zeilig, G., Heruti, R., Shemesh, Y.,Ohry, A., Dar, A., et al. (1998). Hybrid functional electricalstimulation orthosis system for the upper limb: Effects onspasticity in chronic stable hemiplegia. American Journalof Physical Medicine and Rehabilitation, 77, 276–281.

Yozbatiran, N., Der-Yeghiaian, L., & Cramer, S. C. (2008).A standardized approach to performing the action researcharm test. Neurorehabilitation and Neural Repair, 22, 78–90.