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Interactive Computer Play as “Motor Therapy” for Individuals With Cerebral Palsy
Interactive Computer Play as “Motor Therapy” for Individuals With Cerebral Palsy Darcy Fehlings, MD, MSc, FRCPC,*,† Lauren Switzer, MSc,† Briar Findlay, BSc,† and Shannon Knights, MD* The aim of the study was to evaluate the quality of evidence for interactive computer play (ICP) to improve motor performance (including motor control, strength, or cardiovascular [CVS] fitness) in individuals with cerebral palsy. A computer-assisted literature search was completed, focusing on ICP as a therapeutic modality to improve motor outcomes in individuals of all ages with cerebral palsy with a specific focus on upper and lower extremity motor outcomes and promotion of CVS fitness. Articles were classified according to American Academy of Neurology guidelines and recommendation classifications were given based on the levels of evidence. Seventeen articles underwent full-text review including 6 on upper extremity motor function, 5 on lower extremity motor function, 1 on CVS fitness, and 5 on studies with a combination of upper or lower extremity or CVS fitness focus or both. Overall, there was level B (probable) evidence for ICP interventions to improve lower extremity motor control or function. However, there was inadequate evidence (level U) for ICP interventions improving upper limb motor control or function or CVS fitness. Although promising trends are apparent, the strongest level of evidence exists for the use of ICP to improve gross motor outcomes. Additional evidence is warranted especially when evaluating the effect of ICP on upper limb motor outcomes and CVS fitness. Semin Pediatr Neurol 20:127-138 C 2013 Elsevier Inc. All rights reserved.
Introduction Over the last 3 decades, there has been an increase in the number of individuals engaging in interactive computer play (ICP). ICP is defined as “any kind of computer game or virtual reality (VR) technology where the individual can interact and play with virtual objects in a computergenerated environment.”1 VR is defined as a “virtual environment that uses a range of computer technologies to present virtual or artificially generated sensory information in a format that enables the user to perceive experiences that are similar to real-life events and activities.”2 There are different types of VR that vary according to their degree of immersion and how the user interacts with the system. Immersion is defined as how much the user feels that they
*Department of Paediatrics, University of Toronto, Toronto, Ontario, Canada. †Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, Ontario, Canada. Address reprint requests to Darcy Fehlings, MD, MSc, FRCPC, Holland Bloorview Kids Rehabilitation Hospital, 150 Kilgour Rd, Toronto, Ontario, Canada M4G 1R8 E-mail: [email protected]
1071-9091/13/$-see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spen.2013.06.003
are in the computer-generated environment. For fully immersive systems, the individual wears a head-mounted display that brings the individual into a 3-dimensional virtual environment. Movement through the virtual world is controlled by head movement. In nonimmersive VR systems, the user views the virtual world through a 2-dimensional flat screen. These nonimmersive systems can capture total body movement or be controlled by a focused body movement where a mouse, joystick, keyboard, or cycling unit interacts with the computer to create an action. There is significant overlap between the terms ICP and VR. Rehabilitation specialists are becoming increasingly interested in ICP as a potential therapeutic modality and have started to develop and evaluate ICP for therapeutic purposes. Individuals with cerebral palsy (CP) have a motor disorder secondary to an injury or anomaly of the developing brain that causes activity limitations.3 Depending on the subtype of CP, they can have decreased selective motor control of both their arms and their legs. A diagnosis of CP is often associated with sedentary behavior and poor cardiovascular (CVS) fitness.4,5 Given these motor challenges, an opportunity exists for ICP to improve selective motor control in the upper and lower extremities by repetitive 127
D. Fehlings et al
128 motor practice or training and visual-spatial sensory feedback. There is also an opportunity to increase physical activity and fitness. A secondary potential benefit of ICP, if done through multiplayer games, is enhanced social interaction and well-being. There is a growing body of literature reporting on the development and evaluation of ICP as a therapeutic modality for individuals with CP. The objectives of this paper are to evaluate the quality of evidence for ICP to improve motor performance (including motor control, strength, or CVS fitness) in individuals with CP. A secondary objective is to report on the types of ICP being used for therapeutic purposes to improve motor function in individuals with CP.
Methods Computer-assisted literature searches were completed to find all studies published until December 2012 that focused on ICP used as a therapeutic modality to improve motor outcomes in individuals of all ages with CP. Specifically, MedLine, Cochrane, PsycINFO, and CINAHL databases were searched with a focus on ICP and CP using a combination of subject headings and key words that included the following: computer play, VR, exergames, gross motor, muscle strength, and manual ability. In addition, commercially available games (eg, Nintendo Wii) were integrated into the search strategy. The criteria for inclusion in the study were the following: (1) at least 5 participants (children, youth, or adults) with CP; (2) the intervention being evaluated was an ICP focused on improving some aspect of motor performance; (3) objective outcomes were included in the study design; and (4) English full-text studies. All eligible studies were then reviewed and the data were abstracted. The articles were then classified into 4 hierarchical classes of evidence developed by the American Academy of Neurology classification of evidence for therapeutic intervention and classification of recommendations.6 To summarize, class I studies included randomized controlled clinical trials, matched prospective cohort studies were class II, all other controlled trials were class III, and class IV articles included all other studies not meeting class I-III criteria. Recommendation level classifications for the effect of ICP to improve motor performance (including motor control, strength, or CVS fitness) in individuals with CP were generated based on the strength of evidence for all of the articles. To summarize the recommendation levels, level A (established as effective or ineffective) required at least 2 consistent class I studies, level B (probably effective or ineffective) required at least 1 class I study or at least 2 consistent class II studies, and level C (possibly effective or ineffective) required at least 1 class II study or at least 2 consistent class III studies. Level U (data inadequate or conflicting) resulted when studies did not meet class I-III requirements or when studies were conflicting. Evidence tables were created and summarized for 3 subgroups of
studies: upper extremity motor function, lower extremity motor function, and promotion of CVS fitness.
Results A total of 88 abstracts were initially identified through the search process. Of them, 25 abstracts met the screening criteria and underwent full-text review, and 17 articles fulfilled all the inclusion criteria and underwent data abstraction. The number of reviewed and abstracted studies for each of the 3 subgroups included 6 studies focused on upper extremity motor function; 5 studies focused on lower extremity motor function, and 1 study focused on promotion of CVS fitness. In addition, there were 5 studies that focused on a combination of upper or lower extremity motor function and promotion of CVS fitness and therefore were included.
Upper Extremity Studies The evidence table for upper extremity studies is outlined in Table 1. A series of different ICP have been developed, all with the goal of improving function or quality of movement or both in the upper limbs. These upper limb ICPs can be divided into 2 main types; the first where free movements are captured by the VR interface indicating a particular response7-13 and the other where a robot or device is integral to the computer interaction.14-16 Both types of ICP integrate shoulder, elbow, or wrist movements and pair these movements to response outcomes in a series of games. Although these interventions can be distilled into 2 broad types, there are some important features that differentiate the multiple ICPs. For instance, Jannink et al,10 Sandlund et al,17 Sharan et al,12 and Howcroft et al18 utilized commercially available systems such as the EyeToy for Sony PlayStation or the Nintendo Wii Sports or Fit; whereas Ritterband-Rosenbaum et al7 and Bilde et al11 utilized a home-based training program delivered through the internet. In contrast, Weightman et al,14 Mawase et al,15 Fluet et al,16 and Reid and Campbell9 customized their own VR interfaces, games, and experimental tasks. In addition, only a few of these interventions were amendable for use at home,7,11,14 with many being based in a treatment or research lab setting. Although there is generally positive engagement and participation19 and overall high enjoyment and satisfaction8,12 associated with ICPs, the results of these interventions on upper limb motor function are mixed. Significant kinematic analyses may provide evidence of improved speed and quality of movement;7,14,16 however, these results do not necessarily correlate or predict hand or upper limb motor function. Although upper limb functional improvement trends are apparent,9-12 only Weightman et al,14 Fluet et al,16 Bilde et al,11 and Rostami et al,13 show statistically significant functional improvements, as measured by the Canadian Occupational Performance Measure, the Melbourne Assessment of Unilateral Upper Limb Function, the Assessment
Level of Evidence on Improving Motor Outcomes Reference
Design
Reid and RCT Cambpell9
Jannink et al10
RCT
Fluet et al16 Prosp case series
Participants n ¼ 31 (20 males) tx ¼ 19 Control ¼ 12 CP (GMFCS I-V) Age: 8-10 y n ¼ 10 (9 males) tx ¼ 5 Control ¼ 5 CP (GMFCS I-IV; MACS II-IV) Age: 7-16 y n ¼ 9 (3 males) Hemiplegia CP Age: 5-18 y
Intervention tx: reaching VR intervention for 1 session/wk for 8 wk of roughly 1.5 h Control: typical therapy services
Outcome Measures
Motor Outcome Results
QUEST, COPM, and No significant findings Harter SPPC
tx: Sony PlayStation MAUULF EyeToy games in addition to regular PT Control: regular PT (30 min 2/wk for 6 wk) New Jersey Institute Active ROM, grip of technology Robot and pinch Assisted Virtual dynamometry, Rehabilitation (NJITMAUULF, and RAVR) system reaching mvmt Trained for 1 h 3/wk kinematic for 3 wk
n ¼ 9 (5 males) CP (GMFCS I-II; MACS I-II) Age: 9-13 y
Home-based, interac- AMPS, and AHA tive motor and cognitive training delivered through the internet 30 min/d for 20 wk
Sandlund et al17
Prosp case series
n ¼ 14 (8 males) CP (GMFCS I-III; MACS I-IV) Age: 6-16 y
Sony PlayStation mABC-2; subtest 5:6 EyeToy game Play3 of the BOTMP Recommended at least 20 min/d for 4 wk
Weightman et al14
Prosp case series
n ¼ 18 CP Age: 5-16 y
Home-based, UL COPM (personal care, adjustable assisproductivity, and tance device paired leisure) with gaming software Kinematic measureUse as much as they ment of voluntary UL wanted for 4 wk mvmt (to assess
For
Class I
Significant increase in social acceptance subscale of the Harter SPPC
Class I
No statistical change after intervention in either group
Statistically significant increase in MAUULF, a composite of 3 timed UL tasks of MAUULF, reaching kinematics, and active shoulder abduction, flexion and forearm supination Significant increase in AMPS No significant changes in AHA
Improvements in visual perception tests and combined score of the visual perception test Statistically significant When looking at increase in total mABC-2 subtests test score of the mABC-2, No changes in BOTMP 5:6 only “manual dexterity” reached significance Statistically increased COPM functional scores Kinematic analysis showed statistical improvements in speed and quality of mvmt
Against
Class III
Class III (AMPS)
Class III (AHA)
Class III (mABC-2)
Class III (BOTMP)
Class III
129
Bilde et al11 Prosp case series
Comments
Interactive computer play for individuals with cerebral palsy
Table 1 Upper Extremity Evidence Table
130
Table 1 (continued) Level of Evidence on Improving Motor Outcomes Reference
Design
Participants
Intervention
Outcome Measures
Motor Outcome Results
Comments
For
Against
quality of mvmt including speed and smoothness)
Crosssectional study
n ¼ 17 (10 males) CP (GMFCS I-II) Age: 9.68 ⫾ 1.69 y
Wii Bowling, Wii Tennis, Wii Boxing, and DDR Disney Dance Grooves 8 min each, in a random order
RitterbandRosenbaum et al7
Controlled longitudinal study
n ¼ 40 tx ¼ 20 Control ¼ 20 CP (GMFCS I-III; MACS I-II) Age: 8-16 y
tx: Move it to Improve Behavioral data conIt web-based training taining XY coordiprogram with cogninates resulting in tive and motor challine drawings prolenges for 30 min/d duced from for 20 wk completed mvmts Control: regular daily Subjective assessactivities in physical ments (yes vs no) of activity and being responsible computer habits for mvmt
No significant changes in ability to hit the target after the intervention in either group Time to complete mvmt decreased significantly in both groups and speed was faster in tx group
Rostami et al13
RCT
n ¼ 32 (14 males) VR þ mCIMT ¼ 8 VR ¼ 8 mCIMT ¼ 8 Control ¼ 8 Hemiplegic CP Age: 6-10 y
VR group: 18-h VR PMAL; speed and program; 1.5 h 3/ dexterity subtest of wk for 4 wk the BOTMP mCIMT group: unaffected hand immobilized for at least 5 waking hours; 18-h mCIMT program for 1.5 h 3/wk for 4 wk VR þ mCIMT group: 18-h VR program and unaffected hand immobilized Control group: conventional
Significant differences between preintervention and postintervention for the 3 groups VR þ CIMT had significant increase in speed and dexterity of BOTMP compared with VR and CIMT CIMT and VR groups had significantly increased scores than the control
UL muscle activations via surface electrodes; UL kinematics via optical motion capture system
Greatest muscle activation during boxing for the wrist extensors
A high level of Class IV enjoyment reported on PACES Angular velocities significantly increased in the dominant arm than the hemiplegic arm during bilateral play Significant increase Class II in tx group cor(speed) rectly reporting whether individual or computer was responsible for mvmt Significant increase in improved subjective reporting rate of agency between groups PMAL is a semiClass I structured interview adapted from the Adult Motor Activity Log PMAL was not blinded because it was completed by parents
Class II (accuracy)
D. Fehlings et al
Howcroft et al18
2, 2 times; 3, 3 times; AHA, Assisting Hand Assessment; BOTMP, Bruininks-Oseretsky Test of Motor Proficiency; COPM, Canadian Occupational Performance Measure; DDR, DanceDanceRevolution; g, grams; Harter SPPC, Harter self-perception profile for children; h, hour; mABC-2, movement Assessment Battery for Children-2; MACS, Manual Ability Classification System; MAUULF, Melbourne Assessment of Unilateral Upper Limb Function; mCIMT, modified constraint-induced movement therapy; min, minutes; mvmt, movement; n, number; PACES, Physical Activity Enjoyment Scale; PMAL, pediatric motor activity log; prosp, prospective; PT, physiotherapy; QUEST, Quality of Upper Extremity Test; ROM, range of motion; tx, treatment; UL, upper limb; VR, virtual reality; vs, versus; y, years.
Sharan et al12
RCT
n ¼ 16 tx ¼ 8 Control ¼ 8 CP post-surgery Age: tx ¼ 8.8 ⫾ 3.2 y Control ¼ 10.4 ⫾ 4.4 y
rehabilitation techniques; 1 h/wk tx: VR-based therapy MACS, levels of Nintendo Wii sports participation, and Wii fit – every motivation, 3 alternate d/wk for cooperation, and 3 wk and regular satisfaction rehabilitation modalities Control: regular rehabilitation modalities
Nonsignificant improvement in MACS scores after tx
MACS is not typically used as an outcome measure because of limited responsiveness to change Level of participation, motivation, cooperation, and satisfaction were higher among the tx group
Class I
Interactive computer play for individuals with cerebral palsy
131 of Motor and Process Skills, and the Bruinink-Oseretsky Performance Measure, respectively. With the exception of the randomized controlled trial (RCT) conducted by Rostami et al,13 several small RCTs did not support positive change following ICP. Therefore, based on this literature, ICP for the explicit improvement of upper limb motor function is inconsistent, resulting in a level U (inadequate or unproven) classification and warrants additional research in larger samples.
Lower Extremity Studies The effect of ICP on gross motor function in children and adults with CP has been investigated in numerous ways and is shown in Table 2. In some studies, commercially available virtual gaming systems like the Wii Fit and Wii Sports have been evaluated,12,17 whereas other researchers designed and implemented novel VR gaming consoles.20-22 VR simulations have also been evaluated as an additional dimension to more traditional training therapies including treadmill training,23 cycling training,22,24 and Lokomat training.25 Specific motions like ankle dorsiflexion21,22 and leaning movements20 have been targeted, whereas other ICPs take a more holistic, full-body approach.11 Despite the diverse ICP interventions studied, only a few studied gross motor function using RCTs. Sharan et al12 used a RCT to evaluate the effect of commercially available VR-based therapies, namely Wii Sports and Wii Fit, on balance in post-operative children with CP. The researchers found that after 3 weeks, the treatment group had significantly greater scores on the Pediatric Balance Scale. In a different RCT, Chen et al24 investigated whether VR cycling training could have motor benefits for ambulatory children with CP. Although they did find benefits for the treatment group, including increased knee flexor and extensor strength, the control group did not complete any cycling training and rather only participated in “general physical activity.” Therefore, it is unknown whether the VR aspect of the cycling was advantageous compared with traditional cycling. Wade and Porter20 investigated their interactive VR gaming system using a randomized crossover trial with the participants acting as their own controls. They discovered that with the intervention, the children improved their shoulder girdle position and spinal profile components of the Chailey Level of Ability specifically related to box sitting but they did not find significant changes in the overall score. They did find improvements in components of the Sitting Assessment for Children with Neuromotor Dysfunction. Likewise, several prospective case series studies have shown gross motor improvements in children with CP because of VR interventions.11,22,23 Wu et al22 found that their ICP for ankle rehabilitation resulted in improved passive and active range of motion of ankle dorsiflexion, joint stiffness, joint strength, balance, and gait symmetry, among other positive findings. Kott et al23 found that a VR treadmill training intervention resulted in increased treadmill walking speed and improved measures of Dimension E of the Gross Motor Function Measure-88. Similarly, Gordon et al26 determined
132
Table 2 Lower Extremity Evidence Table Level of Evidence on Improving Motor Outcomes Citation
Design
Participants
Bryanton et al21
Casecontrol study
n ¼ 10 (4 males) CP (GMFCS I-II) Age: 9-17 y n ¼ 6 children (2 male, 4 female) without CP; Age: 7-15 y
Wu et al22
Prosp case series
n ¼ 12 (6 males) CP (GMFCS I-II) MAS: 2-4 Age: 5-15 y
Prosp case series
n ¼ 5 (5 males) CP (GMFCS I-II) Age: 4-15 y
Bilde et al11
Prosp case series
n ¼ 9 (5 males) CP
Outcome Measures
VR exercises for Starting and finishing ankle motor ankle position for each control repetition, time to 90 min exercise complete each session: repetition, and the Ankle exercises number of repetitions completed in 10completed for each min blocks where 2-min bout each block consisted of a set of conventional and VR exercises (counterbalanced) Rehabilitation robot SCALE, MAS, laboratory for treatment of evaluation (ie, passive or ankle impairments active ROM, joint 3 sessions/wk for stiffness, and strength), 6 wk PBS, TUG, and gait Session ¼ approxipatterns mately 20 min of passive stretching; 15 min of assisted active mvmt; 15 min of resistance mvmt; 10 min of passive stretching VR system with SWOC, GMFM-88 treadmill training Dimension E, speed on A total of 9 h over treadmill 3-4 wk (11-12 sessions)
Home-based interactive motor and
Isometric muscle strength of knee extensors and
Motor Outcome Results
Comments
Ankle ROM and hold-time VR was rated more were in the stretched fun position increased during VR compared with conventional exercises More repetitions of the conventional were completed than the VR exercises in both groups
For
Against
Class III
Significant improvements Assisted active mvmt Class III Class III in passive and active (TUG) involves playing the (passive or ROM of ankle dorsiflex- interactive active ROM, ion, joint stiffness, dorstiffness, computer game siflexor strength, strength, SCALE at ankle, hip and SCALE, foot, MAS, balance, MAS, dynamic steadiness balance, and during gait, gait symCOF metry, COF trajectory
trajectory)
SWOC: increased speed for 1 condition of obstacle walk; no significant changes for the other 2 conditions; Significant increases in Dimension E of GMFM-88 Significant increase in treadmill speed from initial to final speed Significant increase in Improvements in Figfrontal and lateral stepure ground test of
Class III (GMFM-88; treadmill speed)
Class III (SWOC)
Class III (balance,
D. Fehlings et al
Kott et al23
Intervention
cognitive training delivered through the internet 30 min/d for 20 wk
flexors; Sit-to-stand, unloaded; Sit-to-stand, loaded; Lateral and frontal step-up; Romberg 30 s, eyes open balance test
n ¼ 14 (8 males) CP (GMFCS I-III; MACS I-IV) Age: 6-16 y
Sony PlayStation mABC-2 EyeToy game Play3 recommended at least 20 min/d for 4 wk
Chen et al24
RCT
n ¼ 28 (19 males) tx ¼ 13 Control ¼ 15 Ambulatory CP Age: 6-12 y
Gordon et al26
Prosp case series
n ¼ 7 (4 males) CP (4 wheelchair dependent, 2 ambulant) Age: 9-12 y
Home-based virtual Gross motor function of cycling training: the BOTMP, muscle 40 min, 3/wk for strength (isokinetic 12 wk torque of knee extensor 5-min warm-up, 20 and flexor muscle) sit-to-stand mvmts, cycling for 20-min, and 5-min cool-down Control group: general physical activity at home Nintendo Wii GMFM-88 Sports Resort 2 d/wk for 6 wk for 45 min
Sharan et al12
RCT
n ¼ 16 CP postoperation tx ¼ 8 Control ¼ 8 Age: tx ¼ 8.88 ⫾ 3.23 y Control ¼ 10.38 ⫾ 4.41 y
Nintendo Wii sports PBS and Wii fit Study group played VR games every 3 alternate days in a week for 3 wk Both groups received their conventional rehabilitation modalities
the visual perception tests and combined score of a visual perception test Long intervention (20 wk)
Significant increase in overall score of the mABC-2 When looking at the subtests of the mABC2, the gross motor balance subtest did not reach significance tx group showed increase Control group isokinetic torque in knee completed general extensor and flexor physical activity muscles and so it is tx group showed unknown what increased isokinetic effect the VR strength improvement in aspect of the the knee flexor cycling had on compared with knee muscle strength extensor No differences in the BOTMP Total GMFM score 1 Child dropped out increased by 7% (n ¼ 6 for data (1% ¼ clinically analysis) important difference) Sitting section showed largest increase of 12% and Lying and Rolling section showed smallest increase of 2%
Class III (stepup tests, sitto-stand)
isometric muscle strength)
Class III (balance subtest)
Class I (strength)
Class I (BOTMP)
Class III (GMFM-88)
Level of participation, Class I tx group had motivation, significantly increased cooperation, and improvement in PBS than the control group satisfaction were increased among the tx group
133
Sandlund Prosp case et al17 series
up tests and sit-tostand test No changes in balance tests or isometric muscle strength
Interactive computer play for individuals with cerebral palsy
(GMFCS I-II; MACS I-II) Age: 9-13 y
134
Table 2 (continued) Level of Evidence on Improving Motor Outcomes Citation
Design
Wade and Crossover Porter20 RCT
Participants n ¼ 13 CP (GMFCS level IV or V; Chailey Scale of sitting ability Level 3 or higher) Age: 5-16 y
Intervention
Outcome Measures
Computer games Chailey Levels of Ability operated by lean(levels related to box ing in different sitting), SACND directions in a seated position 3-5/wk for 3 mo then 3 mo of general physical activity (counterbalanced)
Motor Outcome Results Chailey level of box sitting ability: no differences for overall score SACND: statistically significant increase for overall scores for rest and reach, for components of associated postural reaction during rest phase, proximal stability rating, and leg extension during the reach phase
Comments
For
Parent-report for Class III amount of time (SACND) spent playing Statistically significant changes in girdle position and spinal profile for the Chailey level of box sitting ability
Against Class III (Chailey level of box sitting)
3-5, 3-5 times; 3, 3 times; approx, approximate; BOTMP, Bruininks-Oseretsky Test of Motor Proficiency; COF, center of force; GMFCS, Gross Motor Functional Classification System; GMFM-88, Gross Motor Function Measure (88 items); grp, group; min, minutes; mABC-2, movement Assessment Battery for Children-2; MACS, Manual Ability Classification System; MAS, Modified Ashworth Scale; mvmt, movement; n, number; PBS, Pediatric Balance Scale; prosp, prospective; ROM, range of motion; SACND, Sitting Assessment for Children with Neuromotor Dysfunction; SCALE, selective control assessment of motor control; SWOC, Standardized Walking Obstacle Course; TUG, Timed up and go; tx, treatment; VR, virtual reality; y, years.
D. Fehlings et al
Interactive computer play for individuals with cerebral palsy that their intervention resulted in clinically significant improvements in all dimensions of the Gross Motor Function Measure-88. Additionally, Bilde et al11 found improvements in functional motor tests, like the sit-tostand test and frontal and lateral step-up tests, as a result of 20 weeks of their home-based interactive motor and cognitive virtual gaming; however, they failed to see improvements in the Romberg eyes open balance test or isometric muscle strength tests. Therefore, based on the findings of a diverse range of ICP interventions on gross motor function, ICP can be considered probably effective (level B classification) in improving gross motor function in the lower extremities.
CVS Fitness Active video games, also called exergames, require participants to engage in physical activity beyond that of traditional hand-controlled video games.27 Exergames include rhythmic dancing games, virtual cycling, and virtual sports simulators.28 Two popular commercial examples are Nintendo’s Wii Sports and Konami’s DanceDanceRevolution. Researchers are also developing customized one-player and multiplayer exergames. Usually, these consist of cycling on a stationary bicycle where the speed of cycling is linked to controlling an avatar in a computer game.29,30 Exergames are gaining popularity in our increasingly technologycentered society. A recent population-based study revealed that 24% of adolescents played exergames and 73% of exergamers played at a moderate or vigorous intensity.28 Although active video games have been shown to be an enjoyable activity for youth with CP,8,18 the prevalence of exergaming in individuals with CP or other physical disabilities is currently unknown. Individuals with CP have lower levels of physical activity and fitness than their typically developing peers.4,5 This puts them at increased risk of developing obesity and its related complications, such as diabetes, CVS disease, and musculoskeletal pain.31 Exergames have the potential to promote increased physical activity and enhanced CVS fitness for individuals with CP. Exergames that provide positive reinforcement and opportunities for social interaction may enhance motivation to play.32 In addition to being readily available through inexpensive commercial systems, active video games have the advantage of being able to be played at home. This reduces barriers to participation such as transportation and accessibility.18 The effect of exergames on CVS fitness in individuals with CP has been summarized in Table 3. Many of the studies use metabolic equivalent for tasks (METs) to describe the physical activity intensity elicited by the ICPs.17,18,33 Moderate-intensity exercise is described as 3-5.9 METs and vigorous activity is described as greater than 6 METs.34 In a study by Hurkmans et al,33 ambulatory adults with CP were able to achieve moderate levels of energy expenditure while playing Wii tennis and boxing, with METs of 4.5 and 5.0, respectively. Howcroft et al18 showed that children with
135 CP could achieve moderate levels of physical activity during games that involved full-body movements, such as DanceDanceRevolution (MET ¼ 3.2) and Wii boxing (MET ¼ 3.36). Moderate levels of physical activity have been associated with enhanced CVS fitness if sustained over a sufficient period of time;35 however, both of the above studies did not include a formal assessment of CVS fitness at baseline and after the intervention. Sandlund et al17 found that children with CP increased their time at more than 3 METs by roughly 1.5 hours per day and significantly increased their time spent in the “vigorous” levels of activity (6-9 METs) as a result of their interactive gaming intervention. However, they did not significantly improve in the 1-minute walk test after the 4-week intervention. A study by Wu et al22 evaluated the use of a robot-assisted ankle movement in ambulatory children with CP. A significant improvement was found in the 6-minute walk test (a secondary outcome measure). However, another study by Bilde et al11 did not find an improvement on the 6-minute walk test. Therefore, based on a review of the current literature, there is conflicting evidence, and hence a level U (inadequate/unproven) grade is given for the use of ICP to enhance CVS fitness.
Discussion Promising trends on upper limb motor function in individuals with CP are evident as motivating, enjoyable, and barrier-free options for engagement, participation, and therapy. However, additional research with larger samples is necessary, especially as many of these studies are underpowered to appropriately investigate significant functional changes. Although trends in functional improvement are evident, the results of these studies are not conclusively statistically or clinically significant. Therefore, it would be advantageous for future research to investigate if improved performance on clinical outcome measures confers improvement on activities of daily living and participation. In addition, no recommendations exist with respect to dose and duration of ICP interventions and as to whether these interventions should be administered alone or as cointerventions to regular occupational therapy, constraint-induced movement therapy, etc for optimal success. It is encouraging that the body of literature evaluating ICP to improve gross motor function in individuals with CP shows probable effectiveness (level B) evidence. Although ICP appears to have the potential to produce gross motor improvements in terms of strength, balance, coordination, and gait for individuals with CP, more research is needed. Specifically, more RCTs are necessary to determine the effect and potential added benefit of ICP compared with traditional therapies. Furthermore, larger sample sizes and longer duration studies would more effectively identify the benefits of ICP. Ultimately, ICP may have important clinical applications in terms of rehabilitation, gait training, and strength training for individuals with CP.
136
Table 3 Cardiovascular Fitness Evidence Table Level of Evidence on Improving CVS Fitness Outcomes Citation
Design
Hurkmans Cross-sectional et al33 study
Wu et al22
Prosp case series
Bilde et al11
Prosp case series
Sandlund et al17
Prosp case series
Howcroft et al18
Cross-sectional study
Participants n ¼ 8; (5 males) GMFCS I-II Age: 36 ⫾ 7 y n ¼ 12 (6 males) CP (GMFCS I-II; MAS: II-IV) Age: 5-15 y
n¼9 (5 males) CP (GMFCS I-II; MACS I-II) Age: 9-13 y n ¼ 14 (8 males) CP (GMFCS I-III; MACS I-IV) Age: 6-16 y
Wii Sports tennis and boxing 15 min each in a random order
Outcome Measures
Cardiovascular Fitness Results
Energy expenditure All participants attained energy expenditures 43 by oxygen uptake METs and 2 participants while sitting and attained energy while playing Wii expenditures 46 METS sports 6 MWT Significant improvements in 6 MWT
Rehabilitation robot for treatment of ankle impairments 3 sessions/wk for 6 wk Session ¼ approx 20 min of passive stretching; 15 min of assisted active mvmt; 15 min of resistance mvmt; 10 min of passive stretching Home-based interactive Bruce Fitness motor and cognitive treadmill test, training delivered 6 MWT through the internet 30 min/d for 20 wk
Significant increase in Bruce Fitness Treadmill Test No changes in 6 MWT
Comments Adult population
For
Against
Class IV
Class III
Class III (Bruce test)
Class III (6 MWT)
Sony PlayStation EyeToy TEE, number of steps, time spent game Play3 as “physically recommended active” (43 at least 20 min/d for METs), 1 MWT 4 wk
Significant increase in Only 10 children were Class III TEE/d during the (TEE, included in the gaming weeks; METs) analysis for TEE, Significant increase in steps steps and measures during the gaming weeks of METs Significant increase in time 43 METs and in time between 6 and 9 METs (vigorous activity)
Class III (1 MWT)
Wii Bowling, Wii Tennis, Energy expenditure via a portable Wii Boxing, and DDR cardiopulmonary Disney Dance testing unit Grooves 8 min each in random order
Moderate level of physical activity during the dance (43 METs)
Long intervention (20 wk)
A high level of enjoy- Class IV ment reported on PACES
1 MWT, 1-min walk test; approx, approximate; DDR, DanceDanceRevolution; GMFCS, Gross Motor Functional Classification System; MACS, Manual Ability Classification System; MAS, Modified Ashworth Scale; min, minutes; mvmt, movement; n, number; PACES, Physical Activity Enjoyment Scale; prosp, prospective; 6 MWT, 6-min walk test; TEE, Total Energy Expenditure; y, years.
D. Fehlings et al
n ¼ 17 (10 males) CP (GMFCS I-II) Age: 9.68 ⫾ 1.69 y
Intervention
Interactive computer play for individuals with cerebral palsy Exergames have also been used in a limited number of studies to enhance CVS fitness for individuals with CP, but there is limited evidence to date to support their use for this purpose. Exergames provide a promising approach in engaging individuals with CP in social interaction and physical activity to improve CVS fitness and therefore warrant further study. This review of the evidence adds to 3 other excellent reviews (with literature searches completed in 2008 and 2009) published on ICP or VR therapy (VRT) use in individuals with CP36-38 in the following ways: (1) by updating the literature search to 2012, (2) by focusing exclusively on CP, including a broad age range of pediatric and adult participants, and (3) by reviewing the evidence according to interventions for upper extremities, lower extremities, and CVS fitness. In addition, our review of the evidence utilized the American Academy of Neurology scoring system that generates an overall grade of evidence. All the previous reviews reported poor to fair evidence but with positive trends supporting VRT or ICP. In our review, we have found an evolution in the evidence with enhanced support for positive gross motor outcomes in individuals with CP receiving ICP or VRT interventions. We continue to support the recommendation to continue research in this promising area with larger samples and stronger study designs (ie, RCTs). In summary, research into innovating and evaluating ICP for individuals with CP is starting to appear in the literature. Both customized and commercially available systems are being evaluated. The strongest level of evidence exists for the use of ICP in CP to improve gross motor outcomes that had a level of B (probably effective). Although there are some promising trends, evidence was unproven (level U) for improvements in upper extremity motor function and CVS fitness with ICP interventions.
Acknowledgments We would like to acknowledge the contribution from Pui Ying Wong, research librarian at Holland Bloorview Kids Rehabilitation Hospital, who assisted in the literature review search. We would also like to acknowledge NeuroDevNet Networks Centre of Excellence for their support in funding this project.
References 1. Sandlund M, Dock K, Hager CK, et al: Motion interactive video games in home training for children with cerebral palsy: Parents' perceptions. Disabil Rehabil 34:925-933, 2012 2. Wilson PN, Foreman N, Stanton D: Virtual reality, disability and rehabilitation. Disabil Rehabil 19:213-220, 1997 3. Rosenbaum P, Paneth N, Leviton A, et al: A report: The definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl 109:8-14, 2007 4. Maher CA, Williams MT, Olds T, et al: Physical and sedentary activity in adolescents with cerebral palsy. Dev Med Child Neurol 49:450-457, 2007 5. Rimmer JH: Physical fitness levels of persons with cerebral palsy. Dev Med Child Neurol 43:208-212, 2001
137 6. Edlund W, Gronseth G, So Y, et al: Clinical Practice Guideline Process Manual. St Paul, MN, American Academy of Neurology, 2004 7. Ritterband-Rosenbaum A, Christensen MS, Nielsen JB: Twenty weeks of computer-training improves sense of agency in children with spastic cerebral palsy. Res Dev Disabil 33:1227-1234, 2012 8. Li W, Lam-Damji S, Chau T, et al: The development of a home-based virtual reality therapy system to promote upper extremity movement for children with hemiplegic cerebral palsy. Technol Disabil 21:107-113, 2009 9. Reid D, Campbell K: The use of virtual reality with children with cerebral palsy: A pilot randomized trial. Ther Recreation J 40:255-268, 2006 10. Jannink MJ, van der Wilden GJ, Navis DW, et al: A low-cost video game applied for training of upper extremity function in children with cerebral palsy: A pilot study. Cyberpsychol Behav 11:27-32, 2008 11. Bilde PE, Kliim-Due M, Rasmussen B, et al: Individualized, home-based interactive training of cerebral palsy children delivered through the Internet. BMC Neurol 11:32, 2011 12. Sharan D, Ajeesh PS, Rameshkumar R, et al: Virtual reality based therapy for post operative rehabilitation of children with cerebral palsy. Work 41:3612-3615, 2012 13. Rostami HR, Arastoo AA, Nejad SJ, et al: Effects of modified constraintinduced movement therapy in virtual environment on upper-limb function in children with spastic hemiparetic cerebral palsy: A randomised controlled trial. Neurorehabil 31:357-365, 2012 14. Weightman A, Preston N, Levesley M, et al: Home based computerassisted upper limb exercise for young children with cerebral palsy: A feasibility study investigating impact on motor control and functional outcome. J Rehabil Med 43:359-363, 2011 15. Mawase F, Bar-Haim S, Karniel A: Lack of predictive control in lifting series of virtual objects by individuals with diplegic cerebral palsy. IEEE Trans Neural Syst Rehabil Eng 19:686-695, 2011 16. Fluet GG, Qiu Q, Kelly D, et al: Interfacing a haptic robotic system with complex virtual environments to treat impaired upper extremity motor function in children with cerebral palsy. Dev Neurorehabil 13:335-345, 2010 17. Sandlund M, Waterworth EL, Hager C: Using motion interactive games to promote physical activity and enhance motor performance in children with cerebral palsy. Dev Neurorehabil 14:15-21, 2011 18. Howcroft J, Klejman S, Fehlings D, et al: Active video game play in children with cerebral palsy: Potential for physical activity promotion and rehabilitation therapies. Arch Phys Med Rehabil 93:1448-1456, 2012 19. Green D, Wilson PH: Use of virtual reality in rehabilitation of movement in children with hemiplegia—A multiple case study evaluation. Disabil Rehabil 34:593-604, 2012 20. Wade W, Porter D: Sitting playfully: Does the use of a centre of gravity computer game controller influence the sitting ability of young people with cerebral palsy? Disabil Rehabil Assist Technol 7:122-129, 2012 21. Bryanton C, Bosse J, Brien M, et al: Feasibility, motivation, and selective motor control: Virtual reality compared to conventional home exercise in children with cerebral palsy. Cyberpsychol Behav 9:123-128, 2006 22. Wu YN, Ren Y, Hwang M, et al: Efficacy of robotic rehabilitation of ankle impairments in children with cerebral palsy. In: 32nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society; 2010; Buenos Aires, Argentina; 2010. p. 4481-4484 23. Kott K, Lesher K, DeLeo G: Combining a virtual reality system with treadmill training for children with cerebral palsy. J Cyberther Rehabil 2:35-42, 2009 24. Chen CL, Hong WH, Cheng HY, et al: Muscle strength enhancement following home-based virtual cycling training in ambulatory children with cerebral palsy. Res Dev Disabil 33:1087-1094, 2012 25. Brutsch K, Koenig A, Zimmerli L, et al: Virtual reality for enhancement of robot-assisted gait training in children with central gait disorders. J Rehabil Med 43:493-499, 2011 26. Gordon C, Roopchand-Martin S, Gregg A: Potential of the Nintendo Wii as a rehabilitation tool for children with cerebral palsy in a developing country: A pilot study. Physiotherapy 98:238-242, 2012
138 27. Mears D, Hansen L: Active gaming: Definitions, options and implementation. Strategies 23:26-29, 2009 28. O'Loughlin EK, Dugas EN, Sabiston CM, et al: Prevalence and correlates of exergaming in youth. Pediatrics 130:806-814, 2012 29. Rhodes RE, Warburton DE, Bredin SS: Predicting the effect of interactive video bikes on exercise adherence: An efficacy trial. Psychol Health Med 14:631-640, 2009 30. Warburton DE, Bredin SS, Horita LT, et al: The health benefits of interactive video game exercise. Appl Physiol Nutr Metab 32:655-663, 2007 31. Yamaki K, Rimmer JH, Lowry BD, et al: Prevalence of obesity-related chronic health conditions in overweight adolescents with disabilities. Res Dev Disabil 32:280-288, 2011 32. Biddiss E, Irwin J: Active video games to promote physical activity in children and youth: A systematic review. Arch Pediatr Adolesc Med 164:664-672, 2010
D. Fehlings et al 33. Hurkmans HL, van den Berg-Emons RJ, Stam HJ: Energy expenditure in adults with cerebral palsy playing Wii sports. Arch Phys Med Rehabil 91:1577-1581, 2010 34. Ainsworth BE, Haskell WL, Herrmann SD, et al: 2011 Compendium of physical activities: A second update of codes and MET values. Med Sci Sports Exerc 43:1575-1581, 2011 35. Tremblay MS, Warburton DE, Janssen I, et al: New Canadian physical activity guidelines. Appl Physiol Nutr Metab 36:36-46, 2011. 47-58 36. Sandlund M, McDonough S, Hager-Ross C: Interactive computer play in rehabilitation of children with sensorimotor disorders: A systematic review. Dev Med Child Neurol 51:173-179, 2009 37. Laufer Y, Weiss PL: Virtual reality in the assessment and treatment of children with motor impairment: A systematic review. J Phys Ther Educ 25:59-71, 2011 38. Snider L, Majnemer A, Darsaklis V: Virtual reality as a therapeutic modality for children with cerebral palsy. Dev Neurorehabil 13:120-128, 2010
Introduction Over the last 3 decades, there has been an increase in the number of individuals engaging in interactive computer play (ICP). ICP is defined as “any kind of computer game or virtual reality (VR) technology where the individual can interact and play with virtual objects in a computergenerated environment.”1 VR is defined as a “virtual environment that uses a range of computer technologies to present virtual or artificially generated sensory information in a format that enables the user to perceive experiences that are similar to real-life events and activities.”2 There are different types of VR that vary according to their degree of immersion and how the user interacts with the system. Immersion is defined as how much the user feels that they
*Department of Paediatrics, University of Toronto, Toronto, Ontario, Canada. †Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, Ontario, Canada. Address reprint requests to Darcy Fehlings, MD, MSc, FRCPC, Holland Bloorview Kids Rehabilitation Hospital, 150 Kilgour Rd, Toronto, Ontario, Canada M4G 1R8 E-mail: [email protected]
1071-9091/13/$-see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spen.2013.06.003
are in the computer-generated environment. For fully immersive systems, the individual wears a head-mounted display that brings the individual into a 3-dimensional virtual environment. Movement through the virtual world is controlled by head movement. In nonimmersive VR systems, the user views the virtual world through a 2-dimensional flat screen. These nonimmersive systems can capture total body movement or be controlled by a focused body movement where a mouse, joystick, keyboard, or cycling unit interacts with the computer to create an action. There is significant overlap between the terms ICP and VR. Rehabilitation specialists are becoming increasingly interested in ICP as a potential therapeutic modality and have started to develop and evaluate ICP for therapeutic purposes. Individuals with cerebral palsy (CP) have a motor disorder secondary to an injury or anomaly of the developing brain that causes activity limitations.3 Depending on the subtype of CP, they can have decreased selective motor control of both their arms and their legs. A diagnosis of CP is often associated with sedentary behavior and poor cardiovascular (CVS) fitness.4,5 Given these motor challenges, an opportunity exists for ICP to improve selective motor control in the upper and lower extremities by repetitive 127
D. Fehlings et al
128 motor practice or training and visual-spatial sensory feedback. There is also an opportunity to increase physical activity and fitness. A secondary potential benefit of ICP, if done through multiplayer games, is enhanced social interaction and well-being. There is a growing body of literature reporting on the development and evaluation of ICP as a therapeutic modality for individuals with CP. The objectives of this paper are to evaluate the quality of evidence for ICP to improve motor performance (including motor control, strength, or CVS fitness) in individuals with CP. A secondary objective is to report on the types of ICP being used for therapeutic purposes to improve motor function in individuals with CP.
Methods Computer-assisted literature searches were completed to find all studies published until December 2012 that focused on ICP used as a therapeutic modality to improve motor outcomes in individuals of all ages with CP. Specifically, MedLine, Cochrane, PsycINFO, and CINAHL databases were searched with a focus on ICP and CP using a combination of subject headings and key words that included the following: computer play, VR, exergames, gross motor, muscle strength, and manual ability. In addition, commercially available games (eg, Nintendo Wii) were integrated into the search strategy. The criteria for inclusion in the study were the following: (1) at least 5 participants (children, youth, or adults) with CP; (2) the intervention being evaluated was an ICP focused on improving some aspect of motor performance; (3) objective outcomes were included in the study design; and (4) English full-text studies. All eligible studies were then reviewed and the data were abstracted. The articles were then classified into 4 hierarchical classes of evidence developed by the American Academy of Neurology classification of evidence for therapeutic intervention and classification of recommendations.6 To summarize, class I studies included randomized controlled clinical trials, matched prospective cohort studies were class II, all other controlled trials were class III, and class IV articles included all other studies not meeting class I-III criteria. Recommendation level classifications for the effect of ICP to improve motor performance (including motor control, strength, or CVS fitness) in individuals with CP were generated based on the strength of evidence for all of the articles. To summarize the recommendation levels, level A (established as effective or ineffective) required at least 2 consistent class I studies, level B (probably effective or ineffective) required at least 1 class I study or at least 2 consistent class II studies, and level C (possibly effective or ineffective) required at least 1 class II study or at least 2 consistent class III studies. Level U (data inadequate or conflicting) resulted when studies did not meet class I-III requirements or when studies were conflicting. Evidence tables were created and summarized for 3 subgroups of
studies: upper extremity motor function, lower extremity motor function, and promotion of CVS fitness.
Results A total of 88 abstracts were initially identified through the search process. Of them, 25 abstracts met the screening criteria and underwent full-text review, and 17 articles fulfilled all the inclusion criteria and underwent data abstraction. The number of reviewed and abstracted studies for each of the 3 subgroups included 6 studies focused on upper extremity motor function; 5 studies focused on lower extremity motor function, and 1 study focused on promotion of CVS fitness. In addition, there were 5 studies that focused on a combination of upper or lower extremity motor function and promotion of CVS fitness and therefore were included.
Upper Extremity Studies The evidence table for upper extremity studies is outlined in Table 1. A series of different ICP have been developed, all with the goal of improving function or quality of movement or both in the upper limbs. These upper limb ICPs can be divided into 2 main types; the first where free movements are captured by the VR interface indicating a particular response7-13 and the other where a robot or device is integral to the computer interaction.14-16 Both types of ICP integrate shoulder, elbow, or wrist movements and pair these movements to response outcomes in a series of games. Although these interventions can be distilled into 2 broad types, there are some important features that differentiate the multiple ICPs. For instance, Jannink et al,10 Sandlund et al,17 Sharan et al,12 and Howcroft et al18 utilized commercially available systems such as the EyeToy for Sony PlayStation or the Nintendo Wii Sports or Fit; whereas Ritterband-Rosenbaum et al7 and Bilde et al11 utilized a home-based training program delivered through the internet. In contrast, Weightman et al,14 Mawase et al,15 Fluet et al,16 and Reid and Campbell9 customized their own VR interfaces, games, and experimental tasks. In addition, only a few of these interventions were amendable for use at home,7,11,14 with many being based in a treatment or research lab setting. Although there is generally positive engagement and participation19 and overall high enjoyment and satisfaction8,12 associated with ICPs, the results of these interventions on upper limb motor function are mixed. Significant kinematic analyses may provide evidence of improved speed and quality of movement;7,14,16 however, these results do not necessarily correlate or predict hand or upper limb motor function. Although upper limb functional improvement trends are apparent,9-12 only Weightman et al,14 Fluet et al,16 Bilde et al,11 and Rostami et al,13 show statistically significant functional improvements, as measured by the Canadian Occupational Performance Measure, the Melbourne Assessment of Unilateral Upper Limb Function, the Assessment
Level of Evidence on Improving Motor Outcomes Reference
Design
Reid and RCT Cambpell9
Jannink et al10
RCT
Fluet et al16 Prosp case series
Participants n ¼ 31 (20 males) tx ¼ 19 Control ¼ 12 CP (GMFCS I-V) Age: 8-10 y n ¼ 10 (9 males) tx ¼ 5 Control ¼ 5 CP (GMFCS I-IV; MACS II-IV) Age: 7-16 y n ¼ 9 (3 males) Hemiplegia CP Age: 5-18 y
Intervention tx: reaching VR intervention for 1 session/wk for 8 wk of roughly 1.5 h Control: typical therapy services
Outcome Measures
Motor Outcome Results
QUEST, COPM, and No significant findings Harter SPPC
tx: Sony PlayStation MAUULF EyeToy games in addition to regular PT Control: regular PT (30 min 2/wk for 6 wk) New Jersey Institute Active ROM, grip of technology Robot and pinch Assisted Virtual dynamometry, Rehabilitation (NJITMAUULF, and RAVR) system reaching mvmt Trained for 1 h 3/wk kinematic for 3 wk
n ¼ 9 (5 males) CP (GMFCS I-II; MACS I-II) Age: 9-13 y
Home-based, interac- AMPS, and AHA tive motor and cognitive training delivered through the internet 30 min/d for 20 wk
Sandlund et al17
Prosp case series
n ¼ 14 (8 males) CP (GMFCS I-III; MACS I-IV) Age: 6-16 y
Sony PlayStation mABC-2; subtest 5:6 EyeToy game Play3 of the BOTMP Recommended at least 20 min/d for 4 wk
Weightman et al14
Prosp case series
n ¼ 18 CP Age: 5-16 y
Home-based, UL COPM (personal care, adjustable assisproductivity, and tance device paired leisure) with gaming software Kinematic measureUse as much as they ment of voluntary UL wanted for 4 wk mvmt (to assess
For
Class I
Significant increase in social acceptance subscale of the Harter SPPC
Class I
No statistical change after intervention in either group
Statistically significant increase in MAUULF, a composite of 3 timed UL tasks of MAUULF, reaching kinematics, and active shoulder abduction, flexion and forearm supination Significant increase in AMPS No significant changes in AHA
Improvements in visual perception tests and combined score of the visual perception test Statistically significant When looking at increase in total mABC-2 subtests test score of the mABC-2, No changes in BOTMP 5:6 only “manual dexterity” reached significance Statistically increased COPM functional scores Kinematic analysis showed statistical improvements in speed and quality of mvmt
Against
Class III
Class III (AMPS)
Class III (AHA)
Class III (mABC-2)
Class III (BOTMP)
Class III
129
Bilde et al11 Prosp case series
Comments
Interactive computer play for individuals with cerebral palsy
Table 1 Upper Extremity Evidence Table
130
Table 1 (continued) Level of Evidence on Improving Motor Outcomes Reference
Design
Participants
Intervention
Outcome Measures
Motor Outcome Results
Comments
For
Against
quality of mvmt including speed and smoothness)
Crosssectional study
n ¼ 17 (10 males) CP (GMFCS I-II) Age: 9.68 ⫾ 1.69 y
Wii Bowling, Wii Tennis, Wii Boxing, and DDR Disney Dance Grooves 8 min each, in a random order
RitterbandRosenbaum et al7
Controlled longitudinal study
n ¼ 40 tx ¼ 20 Control ¼ 20 CP (GMFCS I-III; MACS I-II) Age: 8-16 y
tx: Move it to Improve Behavioral data conIt web-based training taining XY coordiprogram with cogninates resulting in tive and motor challine drawings prolenges for 30 min/d duced from for 20 wk completed mvmts Control: regular daily Subjective assessactivities in physical ments (yes vs no) of activity and being responsible computer habits for mvmt
No significant changes in ability to hit the target after the intervention in either group Time to complete mvmt decreased significantly in both groups and speed was faster in tx group
Rostami et al13
RCT
n ¼ 32 (14 males) VR þ mCIMT ¼ 8 VR ¼ 8 mCIMT ¼ 8 Control ¼ 8 Hemiplegic CP Age: 6-10 y
VR group: 18-h VR PMAL; speed and program; 1.5 h 3/ dexterity subtest of wk for 4 wk the BOTMP mCIMT group: unaffected hand immobilized for at least 5 waking hours; 18-h mCIMT program for 1.5 h 3/wk for 4 wk VR þ mCIMT group: 18-h VR program and unaffected hand immobilized Control group: conventional
Significant differences between preintervention and postintervention for the 3 groups VR þ CIMT had significant increase in speed and dexterity of BOTMP compared with VR and CIMT CIMT and VR groups had significantly increased scores than the control
UL muscle activations via surface electrodes; UL kinematics via optical motion capture system
Greatest muscle activation during boxing for the wrist extensors
A high level of Class IV enjoyment reported on PACES Angular velocities significantly increased in the dominant arm than the hemiplegic arm during bilateral play Significant increase Class II in tx group cor(speed) rectly reporting whether individual or computer was responsible for mvmt Significant increase in improved subjective reporting rate of agency between groups PMAL is a semiClass I structured interview adapted from the Adult Motor Activity Log PMAL was not blinded because it was completed by parents
Class II (accuracy)
D. Fehlings et al
Howcroft et al18
2, 2 times; 3, 3 times; AHA, Assisting Hand Assessment; BOTMP, Bruininks-Oseretsky Test of Motor Proficiency; COPM, Canadian Occupational Performance Measure; DDR, DanceDanceRevolution; g, grams; Harter SPPC, Harter self-perception profile for children; h, hour; mABC-2, movement Assessment Battery for Children-2; MACS, Manual Ability Classification System; MAUULF, Melbourne Assessment of Unilateral Upper Limb Function; mCIMT, modified constraint-induced movement therapy; min, minutes; mvmt, movement; n, number; PACES, Physical Activity Enjoyment Scale; PMAL, pediatric motor activity log; prosp, prospective; PT, physiotherapy; QUEST, Quality of Upper Extremity Test; ROM, range of motion; tx, treatment; UL, upper limb; VR, virtual reality; vs, versus; y, years.
Sharan et al12
RCT
n ¼ 16 tx ¼ 8 Control ¼ 8 CP post-surgery Age: tx ¼ 8.8 ⫾ 3.2 y Control ¼ 10.4 ⫾ 4.4 y
rehabilitation techniques; 1 h/wk tx: VR-based therapy MACS, levels of Nintendo Wii sports participation, and Wii fit – every motivation, 3 alternate d/wk for cooperation, and 3 wk and regular satisfaction rehabilitation modalities Control: regular rehabilitation modalities
Nonsignificant improvement in MACS scores after tx
MACS is not typically used as an outcome measure because of limited responsiveness to change Level of participation, motivation, cooperation, and satisfaction were higher among the tx group
Class I
Interactive computer play for individuals with cerebral palsy
131 of Motor and Process Skills, and the Bruinink-Oseretsky Performance Measure, respectively. With the exception of the randomized controlled trial (RCT) conducted by Rostami et al,13 several small RCTs did not support positive change following ICP. Therefore, based on this literature, ICP for the explicit improvement of upper limb motor function is inconsistent, resulting in a level U (inadequate or unproven) classification and warrants additional research in larger samples.
Lower Extremity Studies The effect of ICP on gross motor function in children and adults with CP has been investigated in numerous ways and is shown in Table 2. In some studies, commercially available virtual gaming systems like the Wii Fit and Wii Sports have been evaluated,12,17 whereas other researchers designed and implemented novel VR gaming consoles.20-22 VR simulations have also been evaluated as an additional dimension to more traditional training therapies including treadmill training,23 cycling training,22,24 and Lokomat training.25 Specific motions like ankle dorsiflexion21,22 and leaning movements20 have been targeted, whereas other ICPs take a more holistic, full-body approach.11 Despite the diverse ICP interventions studied, only a few studied gross motor function using RCTs. Sharan et al12 used a RCT to evaluate the effect of commercially available VR-based therapies, namely Wii Sports and Wii Fit, on balance in post-operative children with CP. The researchers found that after 3 weeks, the treatment group had significantly greater scores on the Pediatric Balance Scale. In a different RCT, Chen et al24 investigated whether VR cycling training could have motor benefits for ambulatory children with CP. Although they did find benefits for the treatment group, including increased knee flexor and extensor strength, the control group did not complete any cycling training and rather only participated in “general physical activity.” Therefore, it is unknown whether the VR aspect of the cycling was advantageous compared with traditional cycling. Wade and Porter20 investigated their interactive VR gaming system using a randomized crossover trial with the participants acting as their own controls. They discovered that with the intervention, the children improved their shoulder girdle position and spinal profile components of the Chailey Level of Ability specifically related to box sitting but they did not find significant changes in the overall score. They did find improvements in components of the Sitting Assessment for Children with Neuromotor Dysfunction. Likewise, several prospective case series studies have shown gross motor improvements in children with CP because of VR interventions.11,22,23 Wu et al22 found that their ICP for ankle rehabilitation resulted in improved passive and active range of motion of ankle dorsiflexion, joint stiffness, joint strength, balance, and gait symmetry, among other positive findings. Kott et al23 found that a VR treadmill training intervention resulted in increased treadmill walking speed and improved measures of Dimension E of the Gross Motor Function Measure-88. Similarly, Gordon et al26 determined
132
Table 2 Lower Extremity Evidence Table Level of Evidence on Improving Motor Outcomes Citation
Design
Participants
Bryanton et al21
Casecontrol study
n ¼ 10 (4 males) CP (GMFCS I-II) Age: 9-17 y n ¼ 6 children (2 male, 4 female) without CP; Age: 7-15 y
Wu et al22
Prosp case series
n ¼ 12 (6 males) CP (GMFCS I-II) MAS: 2-4 Age: 5-15 y
Prosp case series
n ¼ 5 (5 males) CP (GMFCS I-II) Age: 4-15 y
Bilde et al11
Prosp case series
n ¼ 9 (5 males) CP
Outcome Measures
VR exercises for Starting and finishing ankle motor ankle position for each control repetition, time to 90 min exercise complete each session: repetition, and the Ankle exercises number of repetitions completed in 10completed for each min blocks where 2-min bout each block consisted of a set of conventional and VR exercises (counterbalanced) Rehabilitation robot SCALE, MAS, laboratory for treatment of evaluation (ie, passive or ankle impairments active ROM, joint 3 sessions/wk for stiffness, and strength), 6 wk PBS, TUG, and gait Session ¼ approxipatterns mately 20 min of passive stretching; 15 min of assisted active mvmt; 15 min of resistance mvmt; 10 min of passive stretching VR system with SWOC, GMFM-88 treadmill training Dimension E, speed on A total of 9 h over treadmill 3-4 wk (11-12 sessions)
Home-based interactive motor and
Isometric muscle strength of knee extensors and
Motor Outcome Results
Comments
Ankle ROM and hold-time VR was rated more were in the stretched fun position increased during VR compared with conventional exercises More repetitions of the conventional were completed than the VR exercises in both groups
For
Against
Class III
Significant improvements Assisted active mvmt Class III Class III in passive and active (TUG) involves playing the (passive or ROM of ankle dorsiflex- interactive active ROM, ion, joint stiffness, dorstiffness, computer game siflexor strength, strength, SCALE at ankle, hip and SCALE, foot, MAS, balance, MAS, dynamic steadiness balance, and during gait, gait symCOF metry, COF trajectory
trajectory)
SWOC: increased speed for 1 condition of obstacle walk; no significant changes for the other 2 conditions; Significant increases in Dimension E of GMFM-88 Significant increase in treadmill speed from initial to final speed Significant increase in Improvements in Figfrontal and lateral stepure ground test of
Class III (GMFM-88; treadmill speed)
Class III (SWOC)
Class III (balance,
D. Fehlings et al
Kott et al23
Intervention
cognitive training delivered through the internet 30 min/d for 20 wk
flexors; Sit-to-stand, unloaded; Sit-to-stand, loaded; Lateral and frontal step-up; Romberg 30 s, eyes open balance test
n ¼ 14 (8 males) CP (GMFCS I-III; MACS I-IV) Age: 6-16 y
Sony PlayStation mABC-2 EyeToy game Play3 recommended at least 20 min/d for 4 wk
Chen et al24
RCT
n ¼ 28 (19 males) tx ¼ 13 Control ¼ 15 Ambulatory CP Age: 6-12 y
Gordon et al26
Prosp case series
n ¼ 7 (4 males) CP (4 wheelchair dependent, 2 ambulant) Age: 9-12 y
Home-based virtual Gross motor function of cycling training: the BOTMP, muscle 40 min, 3/wk for strength (isokinetic 12 wk torque of knee extensor 5-min warm-up, 20 and flexor muscle) sit-to-stand mvmts, cycling for 20-min, and 5-min cool-down Control group: general physical activity at home Nintendo Wii GMFM-88 Sports Resort 2 d/wk for 6 wk for 45 min
Sharan et al12
RCT
n ¼ 16 CP postoperation tx ¼ 8 Control ¼ 8 Age: tx ¼ 8.88 ⫾ 3.23 y Control ¼ 10.38 ⫾ 4.41 y
Nintendo Wii sports PBS and Wii fit Study group played VR games every 3 alternate days in a week for 3 wk Both groups received their conventional rehabilitation modalities
the visual perception tests and combined score of a visual perception test Long intervention (20 wk)
Significant increase in overall score of the mABC-2 When looking at the subtests of the mABC2, the gross motor balance subtest did not reach significance tx group showed increase Control group isokinetic torque in knee completed general extensor and flexor physical activity muscles and so it is tx group showed unknown what increased isokinetic effect the VR strength improvement in aspect of the the knee flexor cycling had on compared with knee muscle strength extensor No differences in the BOTMP Total GMFM score 1 Child dropped out increased by 7% (n ¼ 6 for data (1% ¼ clinically analysis) important difference) Sitting section showed largest increase of 12% and Lying and Rolling section showed smallest increase of 2%
Class III (stepup tests, sitto-stand)
isometric muscle strength)
Class III (balance subtest)
Class I (strength)
Class I (BOTMP)
Class III (GMFM-88)
Level of participation, Class I tx group had motivation, significantly increased cooperation, and improvement in PBS than the control group satisfaction were increased among the tx group
133
Sandlund Prosp case et al17 series
up tests and sit-tostand test No changes in balance tests or isometric muscle strength
Interactive computer play for individuals with cerebral palsy
(GMFCS I-II; MACS I-II) Age: 9-13 y
134
Table 2 (continued) Level of Evidence on Improving Motor Outcomes Citation
Design
Wade and Crossover Porter20 RCT
Participants n ¼ 13 CP (GMFCS level IV or V; Chailey Scale of sitting ability Level 3 or higher) Age: 5-16 y
Intervention
Outcome Measures
Computer games Chailey Levels of Ability operated by lean(levels related to box ing in different sitting), SACND directions in a seated position 3-5/wk for 3 mo then 3 mo of general physical activity (counterbalanced)
Motor Outcome Results Chailey level of box sitting ability: no differences for overall score SACND: statistically significant increase for overall scores for rest and reach, for components of associated postural reaction during rest phase, proximal stability rating, and leg extension during the reach phase
Comments
For
Parent-report for Class III amount of time (SACND) spent playing Statistically significant changes in girdle position and spinal profile for the Chailey level of box sitting ability
Against Class III (Chailey level of box sitting)
3-5, 3-5 times; 3, 3 times; approx, approximate; BOTMP, Bruininks-Oseretsky Test of Motor Proficiency; COF, center of force; GMFCS, Gross Motor Functional Classification System; GMFM-88, Gross Motor Function Measure (88 items); grp, group; min, minutes; mABC-2, movement Assessment Battery for Children-2; MACS, Manual Ability Classification System; MAS, Modified Ashworth Scale; mvmt, movement; n, number; PBS, Pediatric Balance Scale; prosp, prospective; ROM, range of motion; SACND, Sitting Assessment for Children with Neuromotor Dysfunction; SCALE, selective control assessment of motor control; SWOC, Standardized Walking Obstacle Course; TUG, Timed up and go; tx, treatment; VR, virtual reality; y, years.
D. Fehlings et al
Interactive computer play for individuals with cerebral palsy that their intervention resulted in clinically significant improvements in all dimensions of the Gross Motor Function Measure-88. Additionally, Bilde et al11 found improvements in functional motor tests, like the sit-tostand test and frontal and lateral step-up tests, as a result of 20 weeks of their home-based interactive motor and cognitive virtual gaming; however, they failed to see improvements in the Romberg eyes open balance test or isometric muscle strength tests. Therefore, based on the findings of a diverse range of ICP interventions on gross motor function, ICP can be considered probably effective (level B classification) in improving gross motor function in the lower extremities.
CVS Fitness Active video games, also called exergames, require participants to engage in physical activity beyond that of traditional hand-controlled video games.27 Exergames include rhythmic dancing games, virtual cycling, and virtual sports simulators.28 Two popular commercial examples are Nintendo’s Wii Sports and Konami’s DanceDanceRevolution. Researchers are also developing customized one-player and multiplayer exergames. Usually, these consist of cycling on a stationary bicycle where the speed of cycling is linked to controlling an avatar in a computer game.29,30 Exergames are gaining popularity in our increasingly technologycentered society. A recent population-based study revealed that 24% of adolescents played exergames and 73% of exergamers played at a moderate or vigorous intensity.28 Although active video games have been shown to be an enjoyable activity for youth with CP,8,18 the prevalence of exergaming in individuals with CP or other physical disabilities is currently unknown. Individuals with CP have lower levels of physical activity and fitness than their typically developing peers.4,5 This puts them at increased risk of developing obesity and its related complications, such as diabetes, CVS disease, and musculoskeletal pain.31 Exergames have the potential to promote increased physical activity and enhanced CVS fitness for individuals with CP. Exergames that provide positive reinforcement and opportunities for social interaction may enhance motivation to play.32 In addition to being readily available through inexpensive commercial systems, active video games have the advantage of being able to be played at home. This reduces barriers to participation such as transportation and accessibility.18 The effect of exergames on CVS fitness in individuals with CP has been summarized in Table 3. Many of the studies use metabolic equivalent for tasks (METs) to describe the physical activity intensity elicited by the ICPs.17,18,33 Moderate-intensity exercise is described as 3-5.9 METs and vigorous activity is described as greater than 6 METs.34 In a study by Hurkmans et al,33 ambulatory adults with CP were able to achieve moderate levels of energy expenditure while playing Wii tennis and boxing, with METs of 4.5 and 5.0, respectively. Howcroft et al18 showed that children with
135 CP could achieve moderate levels of physical activity during games that involved full-body movements, such as DanceDanceRevolution (MET ¼ 3.2) and Wii boxing (MET ¼ 3.36). Moderate levels of physical activity have been associated with enhanced CVS fitness if sustained over a sufficient period of time;35 however, both of the above studies did not include a formal assessment of CVS fitness at baseline and after the intervention. Sandlund et al17 found that children with CP increased their time at more than 3 METs by roughly 1.5 hours per day and significantly increased their time spent in the “vigorous” levels of activity (6-9 METs) as a result of their interactive gaming intervention. However, they did not significantly improve in the 1-minute walk test after the 4-week intervention. A study by Wu et al22 evaluated the use of a robot-assisted ankle movement in ambulatory children with CP. A significant improvement was found in the 6-minute walk test (a secondary outcome measure). However, another study by Bilde et al11 did not find an improvement on the 6-minute walk test. Therefore, based on a review of the current literature, there is conflicting evidence, and hence a level U (inadequate/unproven) grade is given for the use of ICP to enhance CVS fitness.
Discussion Promising trends on upper limb motor function in individuals with CP are evident as motivating, enjoyable, and barrier-free options for engagement, participation, and therapy. However, additional research with larger samples is necessary, especially as many of these studies are underpowered to appropriately investigate significant functional changes. Although trends in functional improvement are evident, the results of these studies are not conclusively statistically or clinically significant. Therefore, it would be advantageous for future research to investigate if improved performance on clinical outcome measures confers improvement on activities of daily living and participation. In addition, no recommendations exist with respect to dose and duration of ICP interventions and as to whether these interventions should be administered alone or as cointerventions to regular occupational therapy, constraint-induced movement therapy, etc for optimal success. It is encouraging that the body of literature evaluating ICP to improve gross motor function in individuals with CP shows probable effectiveness (level B) evidence. Although ICP appears to have the potential to produce gross motor improvements in terms of strength, balance, coordination, and gait for individuals with CP, more research is needed. Specifically, more RCTs are necessary to determine the effect and potential added benefit of ICP compared with traditional therapies. Furthermore, larger sample sizes and longer duration studies would more effectively identify the benefits of ICP. Ultimately, ICP may have important clinical applications in terms of rehabilitation, gait training, and strength training for individuals with CP.
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Table 3 Cardiovascular Fitness Evidence Table Level of Evidence on Improving CVS Fitness Outcomes Citation
Design
Hurkmans Cross-sectional et al33 study
Wu et al22
Prosp case series
Bilde et al11
Prosp case series
Sandlund et al17
Prosp case series
Howcroft et al18
Cross-sectional study
Participants n ¼ 8; (5 males) GMFCS I-II Age: 36 ⫾ 7 y n ¼ 12 (6 males) CP (GMFCS I-II; MAS: II-IV) Age: 5-15 y
n¼9 (5 males) CP (GMFCS I-II; MACS I-II) Age: 9-13 y n ¼ 14 (8 males) CP (GMFCS I-III; MACS I-IV) Age: 6-16 y
Wii Sports tennis and boxing 15 min each in a random order
Outcome Measures
Cardiovascular Fitness Results
Energy expenditure All participants attained energy expenditures 43 by oxygen uptake METs and 2 participants while sitting and attained energy while playing Wii expenditures 46 METS sports 6 MWT Significant improvements in 6 MWT
Rehabilitation robot for treatment of ankle impairments 3 sessions/wk for 6 wk Session ¼ approx 20 min of passive stretching; 15 min of assisted active mvmt; 15 min of resistance mvmt; 10 min of passive stretching Home-based interactive Bruce Fitness motor and cognitive treadmill test, training delivered 6 MWT through the internet 30 min/d for 20 wk
Significant increase in Bruce Fitness Treadmill Test No changes in 6 MWT
Comments Adult population
For
Against
Class IV
Class III
Class III (Bruce test)
Class III (6 MWT)
Sony PlayStation EyeToy TEE, number of steps, time spent game Play3 as “physically recommended active” (43 at least 20 min/d for METs), 1 MWT 4 wk
Significant increase in Only 10 children were Class III TEE/d during the (TEE, included in the gaming weeks; METs) analysis for TEE, Significant increase in steps steps and measures during the gaming weeks of METs Significant increase in time 43 METs and in time between 6 and 9 METs (vigorous activity)
Class III (1 MWT)
Wii Bowling, Wii Tennis, Energy expenditure via a portable Wii Boxing, and DDR cardiopulmonary Disney Dance testing unit Grooves 8 min each in random order
Moderate level of physical activity during the dance (43 METs)
Long intervention (20 wk)
A high level of enjoy- Class IV ment reported on PACES
1 MWT, 1-min walk test; approx, approximate; DDR, DanceDanceRevolution; GMFCS, Gross Motor Functional Classification System; MACS, Manual Ability Classification System; MAS, Modified Ashworth Scale; min, minutes; mvmt, movement; n, number; PACES, Physical Activity Enjoyment Scale; prosp, prospective; 6 MWT, 6-min walk test; TEE, Total Energy Expenditure; y, years.
D. Fehlings et al
n ¼ 17 (10 males) CP (GMFCS I-II) Age: 9.68 ⫾ 1.69 y
Intervention
Interactive computer play for individuals with cerebral palsy Exergames have also been used in a limited number of studies to enhance CVS fitness for individuals with CP, but there is limited evidence to date to support their use for this purpose. Exergames provide a promising approach in engaging individuals with CP in social interaction and physical activity to improve CVS fitness and therefore warrant further study. This review of the evidence adds to 3 other excellent reviews (with literature searches completed in 2008 and 2009) published on ICP or VR therapy (VRT) use in individuals with CP36-38 in the following ways: (1) by updating the literature search to 2012, (2) by focusing exclusively on CP, including a broad age range of pediatric and adult participants, and (3) by reviewing the evidence according to interventions for upper extremities, lower extremities, and CVS fitness. In addition, our review of the evidence utilized the American Academy of Neurology scoring system that generates an overall grade of evidence. All the previous reviews reported poor to fair evidence but with positive trends supporting VRT or ICP. In our review, we have found an evolution in the evidence with enhanced support for positive gross motor outcomes in individuals with CP receiving ICP or VRT interventions. We continue to support the recommendation to continue research in this promising area with larger samples and stronger study designs (ie, RCTs). In summary, research into innovating and evaluating ICP for individuals with CP is starting to appear in the literature. Both customized and commercially available systems are being evaluated. The strongest level of evidence exists for the use of ICP in CP to improve gross motor outcomes that had a level of B (probably effective). Although there are some promising trends, evidence was unproven (level U) for improvements in upper extremity motor function and CVS fitness with ICP interventions.
Acknowledgments We would like to acknowledge the contribution from Pui Ying Wong, research librarian at Holland Bloorview Kids Rehabilitation Hospital, who assisted in the literature review search. We would also like to acknowledge NeuroDevNet Networks Centre of Excellence for their support in funding this project.
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