Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review.

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RIDD-2289; No. of Pages 15 Research in Developmental Disabilities xxx (2014) xxx–xxx

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Review article

Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review B. Bonneche`re a,*, B. Jansen b,c, L. Omelina b, M. Degelaen d,e, V. Wermenbol f, M. Rooze a, S. Van Sint Jan a a

Laboratory of Anatomy, Biomechanics and Organogenesis (LABO), Universite´ Libre de Bruxelles, Belgium Department of Electronics and Informatics – ETRO, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium iMinds, Department of Future Media and Imaging (FMI), Gaston Crommenlaan 8 (Box 102), B-9050 Ghent, Belgium d Rehabilitation Hospital Inkendaal, Centrum voor bewegingsanalyse, Vlezenbeek, Belgium e Centre d’analyse du Mouvement, Hoˆpital Brugmann, Universite´ Libre de Bruxelles (ULB), Brussels, Belgium f Department of Paediatric Neurology – Hoˆpital Erasme, Belgium b c

A R T I C L E I N F O

A B S T R A C T

Article history: Received 14 January 2014 Received in revised form 3 April 2014 Accepted 8 April 2014 Available online xxx

The use of video games in rehabilitation is becoming more popular to clinicians. These games are embedded in off-the-shelf commercial entertainment applications or especially-developed for clinical purposes. Treatment of cerebral palsy (CP) children is a challenging task for clinicians. Lack of motivation and progress monitoring are two important factors clinicians need to deal with. The use of serious games (SG), sometimes referred to as Virtual Rehabilitation (VR), could therefore be an interesting adjuvant to conventional treatment for these patients. This is however a new discipline and many scientific issues remain to be solved. The aim of this paper is to describe available conventional treatment for CP children together with the level of evidence of each approach. A systematic review of the use of SG in rehabilitation is then conducted. 31 papers (7 randomized clinical trials, 16 cohort studies and 8 single-cases studies) were selected and analyzed, and their level of evidence compared to the conventional treatment. These studies reported outcomes for 352 patients. In summary, this review shows that it is difficult to compare those studies despite the large amount of patients. This is due to the lack of standardization in patient rehabilitation strategy and to the use of various clinical scales and scores. This non-standardization in patient follow-up between previously-published works make evidence-based conclusions difficult to obtain in order to support these techniques objectively. The use of SG for rehabilitation purposes currently meets similar issues. This paper proposes standardization strategies in order to improve treatment comparison and SG use in rehabilitation. ß 2014 Elsevier Ltd. All rights reserved.

Keywords: Cerebral palsy Rehabilitation Neurorehabilitation Treatment New technology

* Corresponding author. Tel.: +32 25556262. E-mail address: [email protected] (B. Bonneche`re). http://dx.doi.org/10.1016/j.ridd.2014.04.016 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

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Contents 1. 2.

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5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Data sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Data extraction . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Interventional treatment . . . . . . . . . . . . . . . . . . . 3.1.1. Chirurgical intervention . . . . . . . . . . . . 3.1.2. Oral medication . . . . . . . . . . . . . . . . . . . 3.1.3. Intrathecal baclofen . . . . . . . . . . . . . . . . 3.1.4. Intramuscular medication . . . . . . . . . . . 3.2. Rehabilitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1. Physiotherapy . . . . . . . . . . . . . . . . . . . . 3.2.2. Neurodevelopmental treatment (NDT) . 3.2.3. Therapeutic exercises . . . . . . . . . . . . . . 3.2.4. Orthoses . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.5. Conductive education (CE) . . . . . . . . . . 3.2.6. Occupational therapy (OT) . . . . . . . . . . 3.3. Serious games. . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Interventional treatment and rehabilitation . . . . 4.2. Serious games. . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Commercial video games . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction Cerebral palsy (CP) is a group of disorders that affect the development of movement and posture, resulting in limited activities. It is attributed to non-progressive disturbances that occurred in the developing fetal or infant brain (Rosenbaum et al., 2007). CP children present various motor control disorders. Depending on the form (hemiplegia, tetraplegia,. . .) upper and lower limbs can be affected. Motor and sensory impairment are responsible for difficulties during activities of daily life (e.g. gait (Ballaz, Plamondon, & Lemay, 2010), reaching – grasping and manipulating objects (McConnell, Johnston, & Kerr, 2011), posture (Slaboda, Lauer, & Keshner, 2013), etc.). Since there is currently no specific therapy available for children with CP, the treatment and management of these children is a complex task that requires frequent re-iterations (Papavasiliou, 2009) of rehabilitation schemes. The aim of the treatment is to increase patients’ participation and daily activities by improving functions and to minimize the development of secondary problems (e.g. skeletal deformations (Lee et al., 2010), (co)contractions of muscles (Pierce, Prosser, Lee, & Lauer, 2012), etc.). Since more than fifteen years rehabilitation schemes based on Serious Games (SG) have been developed and used in the treatment of various health conditions (Howeel, 2005) such as stroke (Sin & Lee, 2013), Parkinson’s disease (Pompeu et al., 2012), elderly (Verheijden Klompstra, Jaarsma, & Stro¨mberg, 2013). SG, also called virtual reality or exergames, are games whose primary focus (e.g., for education of rehabilitation) is not pure entertainment (Prensky, 2007). Commercial videogames can also be used in rehabilitation (Burdea, Jain, Rabin, Pellosie, & Golomb, 2011; Jelsma, Pronk, Ferguson, & JelsmaSmit, 2013; Winkels, Kottink, Temmink, Nijlant, & Buurke, 2013). That new approach offers various advantages in rehabilitation among which the most important is to fight against patient demotivation (Bonneche`re et al., 2013). Technological progress and cost reduction offer interesting perspectives for both patients and clinicians. However, the efficacy of such kind of interventions is still not known. The aim of this work is to summarize the works performed in SG for CP rehabilitation and to discuss these results with respect to conventional treatments. 2. Method Two methodologies have been used in this study. The first part of the paper is a bibliographic review related to interventional treatments and rehabilitation strategies, aiming to give a description of available treatments for the management of CP children. The concept of ‘‘current treatment’’ is obviously very large, extremely richly published in the literature and include aspects such as rehabilitation, drug intake, orthosis and casting, botox injection, various forms of surgeries, etc. In order to perform a literature analysis on current CP treatments, papers selected in our study only included meta-analysis published in peer-reviewed journals, systematic reviews and recent papers involving a relatively large Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

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amount of patients. The list of interventions aims to be as exhaustive as possible. The first part of the paper aims to give a description of level of evidence of available treatments for the management of CP children. The second part of this article focuses on the available studies related to the use of SG with CP children. The review of the SG literature has been performed according to a search methodology as described in the next section. 2.1. Data sources The following electronic scientific and medical library databases (Academic OneFile, ERIC, PubMed, ScienceDirect and Scopus) were searched. Different search terms (‘‘serious gaming’’, ‘‘serious games’’, ‘‘virtual reality’’, ‘‘tele-rehabilitation’’, ‘‘virtual environment’’, ‘‘computer game’’, ‘‘exergaming’’) were used to select a primary list of papers related to the topics. This list was then shortened to focus on articles showing a direct relationship with the topic of the current paper (Fig. 1). There was no time restriction (research paper ended 1st December 2013).

[(Fig._1)TD$IG]

Fig. 1. Flow diagram of study selection.


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2.2. Study selection Inclusion and exclusion criteria were as follows: due to the relatively small amount of studies related to CP and serious gaming, all study designs were included. No time period threshold was used because serious gaming is a fairly recent paradigm. A PICOS approach (Population, Intervention, Control, Outcome and Study design) was used (Liberati et al., 2009): Population: Children with cerebral palsy. Intervention: At least one session of serious gaming included in the study. Control: None taken into account. Outcome: All measurements before and after interventions were included (such as satisfaction, functional motor skills, self-evaluation). Study design: RCT, cohort studies, single case studies. A flow diagram of study selection with the screened articles and the selection process is shown in Fig. 1. 2.3. Data extraction Each selected paper was rated for methodological quality using the Downs and Black rating scale (Downs & Black, 1998). This scale is used to assess the quality of both randomized and non-randomized studies. The test is divided into five subscales: reporting – which assessed whether the information provided in the paper was sufficient to allow a reader to make an unbiased assessment of the findings of the study, external validity – which addressed the extent to which the findings from the study could be generalized to the population from which the study subjects were derived, bias – which addressed biases in the measurement of the intervention and the outcome, confounding – which addressed bias in the selection of study subjects, power – which attempted to assess whether the negative finding from a study could be due to chance (Downs & Black, 1998). From the selected studies various data were extracted: type of study, number of children involved in the study and, if present, the number of children in the control group, whether serious gaming is used in complement of other treatments, what type of treatment, frequency of serious gaming, which parameters are studied and finally, results of the study. 3. Results 3.1. Interventional treatment 3.1.1. Chirurgical intervention Previously, chirurgical intervention for CP children usually only focused on one particular aspect of the pathology (e.g. tendon lengthening, derotation osteotomy or bone fusions) followed by intensive rehabilitation (Rang, Silver, & de la Garza, 1986). These interventions were frequently repeated yearly, and have been gradually replaced by multilevel surgery (Nene, Evan, & Patrick, 1993). In order to obtain adequate results, multilevel surgery must be based on comprehensive gait analysis and clinical examination. A recent review of the efficacy of multilevel surgery concluded that evidence is not sufficient at the moment to support this technic (McGinley et al., 2012). Another interventional option is selective dorsal rhizotomy; this intervention helps decreasing spasticity, but there is however no consensus in the literature about long term effects on patient functioning (Grunt, Becher, & Vermeulen, 2011; MacWilliams, Johnson, Shuckra, & D’Astous, 2011). 3.1.2. Oral medication Various oral medications are available to control spasticity: baclofen, sodium dantrolene, tizanidine, benzodiazepines, tiagabine and gabapentin. Statistical evidence on the long term efficacy of oral medication is poor (Chung, Chen, & Wong, 2011; Verrotti, Greco, Spalice, Chiarelli, & Iannetti, 2006), and adverse drug reactions are common. 3.1.3. Intrathecal baclofen Baclofen (derivative of gamma-aminobutyric acid (GABA)) can be delivered intrathecally (ITB) to obtain a greater effect. A decade ago, a review performed by the American Academy for Cerebral Palsy and Developmental Medicine (AACPDM) could not confirm any treatment effect because of the poor methodological quality of the studies available in the literature (Butler & Campbell, 2000). A more recent review shows some more benefits (Kolaski & Logan, 2008). Because adverse effects might occur (Kolaski & Logan, 2007), it is important to carefully select patients who could benefit from ITB (Murphy, Irwin, & Hoff, 2002). Despite high complication rates, most of the parents of CP children treated with ITB agreed that it was beneficial for their children (Zdolsek, Olesch, Antolovich, & Reddihough, 2011). 3.1.4. Intramuscular medication The aim of an intramuscular injection is to produce a neuromuscular block (to stop the propagation of the action potential within the injected muscle). The most used pharmacological agent for CP children is the Botulinum toxin Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

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type A (BOT). BOT acts on the neuromuscular junction by inhibiting the release of acetylcholine. This chemodenervation lasts between 8 and 12 weeks (Gracies, 2004). During this period intensive physiotherapy work must be performed (motor learning, balance, stretching. . .) in order to get maximal benefits. BOT provides a time window to improve the outcomes for physical management of the focal and multi-focal problems of spasticity (Ward, 2008). Castings can be combined with BOT injection to enhance the benefits of the injection (Hayek, Gershon, Wientroub, & Yizhar, 2010; Park et al., 2010). 3.2. Rehabilitation 3.2.1. Physiotherapy Management of CP children requires a team of medical specialists (doctors, physiotherapists, occupational therapists, orthotist. . .). Physiotherapy is however a central component of any CP treatment scheme. Physiotherapy mainly includes rehabilitation exercises (see Section 3.2.2) and orthosis design (see Section 3.2.4) (Papavasiliou, 2009). Evaluation of the effectiveness of physiotherapy is difficult as there are no standardized treatments or standardized outcomes during trials (Anttila, Malmivaara, Kunz, Autti-Ra¨mo¨, & Ma¨kela¨, 2006). Thus, research evidence supporting the effectiveness of physiotherapy is inconclusive (Papavasiliou, 2009). 3.2.2. Neurodevelopmental treatment (NDT) Physiotherapy includes the so-called neuro-developmental treatment. Bobath developed this method during the sixties (Bobath, 1967). The aim of this method is to facilitate the movement by reducing muscle tone and inhibiting primitive and abnormal reflexes. Another important aspect of the NDT approach is to allow the children to have a greater independence and to be able to focus on the movement scheme planned by the therapist. Although NDT is one of the most widely used techniques in rehabilitation, a review of AACPDM concluded that ‘‘The preponderance of results in the evidence table did not confer any advantage to NDT over the alternatives to which it was compared. With the exception of immediate improvement in dynamic range of motion (. . .) More intensive therapy did not seem to confer a greater benefit.’’ (Butler & Darrah, 2001). 3.2.3. Therapeutic exercises Children can perform different kinds of exercises at home or during physiotherapy sessions, for example strength training of the antagonist muscles. In a systematic review from 2002 (23 selected articles, 11 accepted), Dodd et al. concluded that training can increase strength and may improve motor activity in CP children without adverse effect (Dodd, Taylor, & Damiano, 2002). In a meta-analysis from 2009 (6 selected articles, 5 accepted), Scianni et al. concluded that in children and adolescents with cerebral palsy who are walking, the current evidence suggests that strengthening interventions are neither effective nor worthwhile. Static weight-bearing exercises are used to reinforce antigravity muscles, prevent hip dislocation, improve bone mineral density, improve self-esteem, improve feeding, assist bowel and urinary functions, reduce spasticity, and improve hand function (Scianni, Butler, Ada, & Teixeira-Salmela, 2009). A review of ten studies concluded that evidence for static weight bearing is still limited except for an increase of bone density and temporary reduction of spasticity (Pin, 2007). Exercise training, typically performed on a static bicycle or a treadmill, is another method to increase aerobic (oxygen consumption) capacity. One study showed that a six-week program of static bicycle training improves gait and motor functions without adverse effect (Williams & Pountney, 2007). Another study using treadmill training (body partially supported) showed an increase of walking speed and endurance (Dodd & Foley, 2007). Passive stretching is another approach used to increase the range of motion and to reduce spasticity (muscle tone). There are different techniques of passive stretching, but there is currently still a lack of evidence for the efficacy of passive stretching in CP children (Wiart, Darrah, & Kembhavi, 2008). 3.2.4. Orthoses Orthoses are external devices that attempt to correct body segment alignment and posture abnormalities. For the lower limbs most orthoses focus on controlling the ankle position and kinematic motion during the gait (McNee et al., 2007). For the upper limbs the final objective is to improve functioning by increasing the range of motion and limiting deformations. Unfortunately, for both lower (Autti-Ra¨mo¨, Suoranta, Anttila, Malmivaara, & Ma¨kela¨, 2006; Figueiredo, Ferreira, Maia Moreira, Kirkwood, & Fetters, 2008) and upper limbs (Autti-Ra¨mo¨ et al., 2006), there is no statistically significant evidence that orthoses could help CP children. 3.2.5. Conductive education (CE) This method was developed by Dr Peto¨ in order to assist children with impaired motor function to attain what the author calls ‘‘orthofunction’’ – defined as the capacity of individuals to respond to biological and social demands made upon them – in other words, to give children maximum independence. The AACPDM concluded, ‘‘The limited number of studies and their weak quality makes it impossible for the literature alone to guide decision-making regarding CE’’ (Darrah, Watkins, Chen, & Bonin, 2004). Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

Population

Intervention

Control

Outcomes

Conclusion

Reporting 7/11 External validity 3/3 Bias 5/7 Confounding 6/6 Power 5/5 Total 26/32 Reporting 5/11 External validity 3/3 Bias 5/7 Confounding 6/6 Power 5/5 Total 24/32 Reporting 7/11 External validity 3/3 Bias 5/7 Confounding 6/6 Power 5/5 Total 26/32

21 CP children (7–14 years old)

6 to 8 sessions of 30–60 min during one month

Non-specific rehabilitative training

2 computer based tests and 2 non-computer tasks

No difference was observed between groups

45 CP children (unknown age)

6 to 8 sessions of 30–60 min during one month

Supporting tasks

Benton Judgment of Line Orientation test, arrows subtest of the Nepsy, Roads test

Treatment group improved more than control group

31 CP children (8–10 years old) GMFCS levels I–V

One session of 90 min of SG per week during 8 weeks (soccer, volleyball, music)

‘‘Standard of care’’ (occupational and physical therapy)

Canadian Occupational Performance Measure (COPM), the Self-Perception Profile for children (SPPC), Quality of Upper extremity Skills Test (QUEST)

40 min of training (The program consisted of a 5-min warm-up exercise, twenty repetitions of sitting-tostanding movements, cycling for 20 min, and a cool-down exercise for 5 min.) a day 3 times per week for 12 weeks SG (Nintendo1 Wii sportsTM and Wii fitTM) in every three alternates days in a week along the conventional rehabilitation during three weeks

Control group was encouraged to perform general physical activity at home under parental supervision

Gross motor function, Bruininks-Oseretsky Test of Motor Proficiency (BOTMP), Muscle strength (knee flexion-extension) measured with Cybex

No statistically significant results were found except for the social acceptance (subscale of the SelfPerception Profile for children showing a significant improvement in SG intervention group) Significant and large effect on knee muscle strength after the treatment compared to control. Both groups did not significantly differ in BOTMP and gross motor function after intervention

Conventional rehabilitation

Manual ability classification system (MACS), pediatric balance score (PBS), the level of participation, satisfaction, cooperation and motivation

30 min daily training using an internet-based home training system for CP children (MiTii, MiTii development)

Normal habits in relation to their physical activity level and computer habits

Reaching task by moving an object on a pen-tablet (subjective reporting and trajectory)

40 min of cycling on a virtual cycling system, three time a week during 12 weeks

Control group was encouraged to perform general physical activity (walking, running. . .) for 40 min a day three time a week during 12 weeks at home under parental supervision

GMFM-66, muscle strength, areal bone mineral density for lumbar spine and femur

Akhutina et al. (2003, Part 2)

Reid and Campbell (2006)

Chen et al. (2012)

Reporting 9/11 External validity 2/3 Bias 5/7 Confounding 6/6 Power 5/5 Total 27/32

28 children with hemiplegic CP (6–12 years old) GMFCS levels I–II

Sharan et al. (2012)


16 CP children (9 3 years old)

Ritterband-Rosenbaum et al. (2012)

Reporting 9/11 External validity 3/3 Bias 6/7 Confounding 6/6 Power 5/5 Total 30/32 Reporting 9/11 External validity 3/3 Bias 6/7 Confounding 6/6 Power 5/5 Total 30/32

40 children with hemiplegic CP (12 2 years old) GMFCS levels I–II and a healthy age-matched group of 65 children 27 CP children (age 6–12 years old) GMFCS levels I–II

Chen et al. (2013)

The SG group shows significant improve for balance but no effect for manual ability. Participation, satisfaction, cooperation and motivation were all significantly higher in the SG group Significantly larger increase in the number of correct subjective reporting and a decrease of compensatory motions CP in the intervention group had greater femoral bone mineral density and isokinetics torques of knee muscles. Muscle strengthening program is more specific than general activity

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Study Akhutina et al. (2003, Part 1)

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Table 1 Summary of Randomized Controlled Trial (RCT) studies included in the review.

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3.2.6. Occupational therapy (OT) OT focuses on fine motor control and particular skills needed for activities of daily living (eating, bathing, dressing, etc.). Like physiotherapy it is important to integrate OT in the treatment after Botox injection (Russo et al., 2007). As therapeutic exercises are also included in some exercises of OT, some can be performed at home under parent supervision. Home programs consisting of eight weeks of occupational therapy resulted in statistically significant improvement in function (level of independence), and parental satisfaction related with function, compared with no treatment (Novak, Cusick, & Lannin, 2009). 3.3. Serious games The first attempts to introduce serious gaming within a rehabilitation program for CP children were performed about fifteen years ago (Grealy & Heffernan, 2000; McComas, Pivik, & Laflamme, 1998; Stanton, Foreman, & Wilson, 1998). These first studies focused on the feasibility of SG for rehabilitation and the new applications that SG technology could address (Bryanton et al., 2006). For example, the lack of therapists in some emerging countries could be compensated by the developments of rehabilitation schemes based on SG; a pilot-study on this topic has been successfully conducted in Jamaica (Gordon, Roopchand-Martin, & Gregg, 2012). Fig. 1 presents the flow diagram of the bibliographic SG search leading to 31 relevant papers. Table 1 summarizes the Randomized Controlled Trials or RCT (7 papers) included in this review, Table 2 the cohort studies (16 papers) and Table 3 the single-case studies (8 papers). The included papers represent a total of 352 patients distributed as follows: 142 patients in RCTs, 201 patients in cohort studies and 9 patients in single case studies. Concerning the quality of the studies, we used the Downs and Black rating scale (Downs & Black, 1998). The mean rating scale (maximal scale value = 32) was 26.7 (2.5), 21.9 (2.5) and 11.6 (1.3) for RCTs, cohort studies and single case studies, respectively. Eighteen studies (4/7 for RCTs [Akhutina et al., 2003, part 1 & 2; Chen et al., 2012; Reid & Campbell, 2006], 7/16 for cohortstudies [Chen et al., 2007; Golomb et al., 2010; Green & Wilson, 2012; Harris & Reid, 2005; Kirshner, Weiss, & Tirosh, 2011; Reid, 2004; Wu, Hwang, Ren, Gaebler-Spira, & Zhang, 2011] and 7/8 for single case studies [Barton, Holmes, Hawken, Lees, & Vanrenteghem, 2006; Barton, Hawken, Foster, Holmes, & Butler, 2013; Chang, Chen, & Huang, 2011; Chang, Han, & Tsai, 2013; Golomb et al., 2011; Qiu et al., 2009; You et al., 2005]) used specially-developed games, while the other 13 relied on commercially available solutions (Chen et al., 2013; Deutsch, Borbely, Filler, Huhn, & Guarrera-Bowlby, 2008; Howcroft et al., 2012; Jelsma et al., 2013; Luna-Oliva et al., 2013; Ramstrand & Lygnega˚rd, 2012; Ritterband-Rosenbaum, Christensen, & Nielsen, 2012; Robert, Ballaz, Hart, & Lemay, 2013; Sandlund, Waterworth, & Ha¨ger, 2011; Sandlund, Domello¨f, Grip, Ro¨nnqvist, & Ha¨ger, 2013; Sharan et al., 2012; Tarakci, Ozdincler, Tarakci, Tutuncuoglu, & Ozmen, 2013; Winkels et al., 2013). 4. Discussion 4.1. Interventional treatment and rehabilitation The first part of this paper focused on the most widely-available treatments for CP children. Surprisingly, while these treatments are administered daily, none of them is supported by strong scientific evidence. For example, even widely used techniques such as passive stretching (Wiart et al., 2008) or strength training (Scianni et al., 2009) lack quantitative facts supporting their efficiency. The main reason for this lack of quantitative data is probably related to the practical methodological issues to organize a statistical evaluation of the efficacy of CP treatment (limited amount of available patients to perform statistics on large patient cohorts, highly heterogeneous clinical signs in patients diagnosed with similar disorders, variable individual response to treatment, limited possibility of double-blinded trials, etc.). On the other hand, many CP-related interventions are either invasive or can show side-effects (multilevel surgery [McGinley et al., 2012], rhizotomy [Grunt et al., 2011; MacWilliams et al., 2011], botulinic toxin [Gracies, 2004; Ward, 2008]). From an ethical point-of-view, the clinical field should aim to improve standardization of patient follow-up to allow clinical decision based on evidence-based conclusions rather than on empirical knowledge. 4.2. Serious games The use of SG in CP rehabilitation programs has been tested over the last decade. A number of such studies are now available. From a methodological point-of-view, Tables 1–3 show that 26 papers reported the outcome of efficacy assessment of SG interventions. These papers included all together more than 35 different tests. Unfortunately, the limited amount of wellorganized trials (the 7 RCTs found in this study) does not allow to draw objective conclusions related to the efficacy of SG use during CP rehabilitation. Furthermore, no similar studies adopted the same methodological approaches and the studies only included a limited number of participants. Several studies evaluated whether SG can be used to increase CP children’s motivation (Harris & Reid, 2005; Reid, 2004), with promising results. These works were mainly psychologically-oriented and focusing only on the motivation. Unfortunately, these studies do not appear to have been followed by clinical studies. A questionnaire evaluating the Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

Population

Intervention

Outcomes

Conclusion



8 sessions of 60 min of SG

Test of playfulness (motivation, internal control)

SG environment stimulated playfulness of CP children

16 CP children (8–12 years old) GMFCS levels I–V

8 sessions of 90 min of SG play interventions

Pediatric Volitional Questionnaire (motivation)

SG seems to be a promising medium for the delivery of a motivating rehabilitation program

4 CP children (6.3 years old) 3 with spastic quadriplegia and one with spastic hemiplegia

4 week intervention program (2 or 3 session per week for a total of 120 min of treatment per week) added to regular therapies programs. The SG was focused on hand rehabilitation training system

Kinematic measurements (reaching performance), fine motor assessment tool

Forearm bones density, functional MRI (fMRI), hand grip, pince grip, hand function (BruininksOseretsky Test of Motor Proficiency and the Jebsen Hand Function Test), fingers’ range of motion Short feedback questionnaire for children (SFQ-Child), Borg Scale of Perceived Exertion, performance during the game

3 of the 4 children showed improvement in the quality of reaching performance, training effect were partially maintained 4 weeks after the intervention. Increase in the fine motor domain Improvement in function of the plegic hand, and in bones’ density. fMRI show spatial extent of activation relative to baseline in brain motor circuitry Both groups enjoyed playing the games (no difference between groups). CP children have lower score (performance) during the games The games promote physical activity and enhance motor performance

Harris and Reid (2005)

Chen et al. (2007)

Golomb et al. (2010)


3 children with hemiplegic CP (13–15 years old)

At least 30 min of SG a day five days a week during 3 months

Kirshner et al. (2011)


Two 60 min sessions in two weeks, 4 different games were tested

Sandlund et al. (2011)


16 CP children (9 2 years old) 6 with hemiplegia, 5 with diplegia, 1 with monoplegia and 4 with quadriplegia. GMFCS levels I–IV and a control group of 16 typically developing children (9 2 years old) 15 CP children (6–16 years old) GMCS levels I–III

20 minute/day of commercial video games (Sony PlayStation 2TM Eye Toy game play3) during 4 weeks

Total energy expenditure, number of steps, time spend to play. The movement assessment battery for children-2, BruininksOseretsky test of Motor Proficiency

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Downs & Black


Study Reid (2004)


8


Table 2 Summaries of cohort study included in the review.

Population

Intervention

Outcomes

Conclusion


12 CP children (8.5 years old) 6 with hemiplegia and 6 with diplegia GMFCS levels I–III

18 sessions of 60 min training (20 min of warm-up and passive stretching, 15 min of assisted-active movement, 15 min of resisted-active movement, 110 min of cool down passive-stretching)

Increase in AROM and PROM. Improvement in joint biomechanical properties, motor control performance and functional capability in balance and mobility

Green and Wilson (2012)


8 children with hemiparetic upper limb motor disorders (from 4 to 15 years old)

30 min of daily training using RE-ACTION system during 3 or 4 weeks

Howcroft et al. (2012)


17 CP children (9 2 years old) 15 with hemiplegia and 2 with diplegia GMFCS level I

One single session of games (Nintendo WiiTM), 4 games were played during 8 min with 5 min rest between games

Modified Ashworth Scale, Modified Tardieu Scale, Pediatric Balance Scale, Selective Control Assessment of the Lower Extremity, 6minute walk test, Timed Upand-Go, Passive Range of Motion (PROM), Active Range of Motion (AROM), Muscle Strength System-generated measures, standardized measures of activities and activity limitation, functional grasp and release (box and blocks test), Jebsen-Taylor Test of Hand function, ABILHANDKids, questionnaire on engagement and participation Energy expenditure, upper limb muscle activations, upper limb kinematics, selfreported enjoyment (Physical Activity Enjoyment Scale)

18 hemiplegic or diplegic CP children (8–16 years old) GMFCS levels I–II

5 weeks of commercial games (Wii FitTM) a minimum of 30 min a day 5 days a week

Balance evaluation: Modified sensory organization test, reactive balance, rhythmic weight shift

No significant difference

14 spastic hemiplegic CP children (7–14 years old) GMFCS levels I–II

3 weeks of commercial games (Wii fitTM) instead of the conventional therapy

Modified balance and running speed and agility (RSA) scales of the BruininksOserestky test of Motor Performance and the timed up and down stairs (TUDS)



12 sessions of commercial Wii sessions of play (twice a week during 6 weeks)

The Melbourne Assessment of Upper Limb Function and ABILHAND-Kids. Satisfaction questionnaire

Balances score improved significantly. Most of the children prefers SG compared to conventional treatment The quality of upper extremity movements did not change. Significant increase of convenience in using hands/arms during performance of daily activities

Ramstrand and Lygnega˚rd (2012)

Jelsma et al. (2013)

Winkels et al. (2013)

Improvement of upper limb function and activity participation after rehabilitation

Light to moderate physical activity level were achieved during the games

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Downs & Black



Study Wu et al. (2011)


Table 2 (Continued )

9

Population

Intervention

Outcomes

Conclusion

Reporting 8/11 External validity 2/3 Bias 5/7 Confounding 3/6 Power 5/5 Total 23/32 Reporting 9/11 External validity 2/3 Bias 4/7 Confounding 3/6 Power 5/5 Total 23/32 Reporting 9/11 External validity 2/3 Bias 5/7 Confounding 3/6 Power 5/5 Total 24/32 Reporting 10/11 External validity 2/3 Bias 6/7 Confounding 4/6 Power 5/5 Total 27/32


8 weeks of commercial video games (Kinect Xbox 360TM) treatment added to conventional physiotherapy treatment

Motor skills (balance, gait speed, running and jumping) and dexterity (fine motor control and finger dexterity)

Significant statistical difference pre and post-treatment for each variables

15 CP children (6–16 years old) GMFCS levels I–III

4 weeks of commercial video games (Sony PlayStation 2 EyeToyTM) for at least 20 min a day

Precision and movement control is increasing after SG

10 CP children (7–12 years old) with spastic diplegia and 10 healthy control children

1 session of 40 min of commercial video games: jogging, cycling, snowboarding and skiing (Nintendo WiiTM)

Kinematics of the subjects during goal-directed movement (mean velocity, peak velocity, timing of peak velocity and movement straightness) Exercise intensity (heart rate)

14 CP children (5–17 years old) GMFCS levels I–III

24 sessions of 40 min (twice a week for 12 weeks) of commercial games (Nintendo Wii FitTM)

Sandlund et al. (2013)

Robert et al. (2013)

Tarakci et al. (2013)

Balances functions: one leg standing test, functional reach test, timed-up and go test, 6-min walking test

Similar intensity for the 4 games, no difference between CP and control

Statistically significant improve for each balance tests

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Downs & Black


Study Luna-Oliva et al. (2013)



10

Table 2 (Continued )

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Table 3 Summaries of single-case study included in the review. Study

Downs & Black

Population

Intervention

Outcome

Conclusion

You et al. (2005)


8 years old child with hemiplegia

20 sessions of 60 min of SG. Three virtual environments were interfaced with the bird-ball, conveyor and a soccer game

Barton et al. (2006)

Reporting 7/11 External validity 1/3 Bias 3/7 Confounding 1/6 Power 0/5 Total 12/32 Reporting 6/11 External validity 1/3 Bias 3/7 Confounding 1/6 Power 0/5 Total 11/32

16 years old child with asymmetrical CP diplegia and 1 healthy subject

One session of SG game

Functional MRI (fMRI), Bruininks-Oseretsky Test of Motor Proficiency (BOTMP), modified Pediatric Motor Activity Log (PMAL), upper limb subtest of the Fugl-Meyer assessment (FMA) ROM of spine and hip joint

SG enhanced functional motor skills and increased amount of use and quality of movement in the affected limb. SG did not influence any observable or meaningful change in fMRI Motion pattern can be analyzed during SG session. Differences were found between healthy control 0 and CP child

13 years old with spastic diplegia

Visual Perceptual Skills, Wechsler Intelligence Scale for Children, Posture Scale Analyzer, functional mobility

Improvement for all studied parameters

Qiu et al. (2009)


7 and 10 years old with spastic hemiplegia

11 sessions of 60 to 90 min of WiiTM games (golfing, bowling, baseball, tennis, and boxing) associated with normal physical therapy program (3 times a week) and occupational therapy (twice a week) Assisted SG for upper limb: 60 min a day, three days a week for three weeks

One subjects shows improvement in the MAUULF score. Increase in supination AROM and in strength

Chang et al. (2011)

Reporting 6/11 External validity 1/3 Bias 2/7 Confounding 1/6 Power 0/5 Total 10/32 Reporting 8/11 External validity 1/3 Bias 2/7 Confounding 1/6 Power 0/5 Total 12/32 Reporting 9/11 External validity 1/3 Bias 2/7 Confounding 2/6 Power 0/5 Total 14/32 Reporting 6/11 External validity 1/3 Bias 2/7 Confounding 1/6 Power 1/5 Total 10/32

17 years old boy with severe cerebral palsy

Two phases of interventions (11 and 12 days, 2 sessions a day) of rehabilitation using Kinerehab

Upper extremity ROM (AROM) and strength, Melbourne Assessment of Unilateral Upper Limb Function (MAUULF), specific parameters recorded during the game (mainly smoothness of motion) Number of correct movement

15 years old CP children

14-month SG hand telerehabilitation intervention

Hand function and forearm bone density

Increasing of the hand function and the mineralization of forearm’s bones

10 years old CP children

13 sessions of 30 min (twice a week)

Range of motion of pelvis and trunk during the games, coupling between pelvis and trunk

Increasing of the coupling during the games appearing to be a better control of the trunk

2 CP children (14 years old)

Two phases of interventions (11 and 12 days, 2 sessions a day) of rehabilitation using Kinerehab

Number of correct movement

Statistical improvement of the number of correct motion, considerable interest for the games

Deutsch et al. (2008)

Golomb et al. (2011)

Barton et al. (2013)

Chang et al. (2013)

Statistical improvement of the number of correct motion

satisfaction of children using serious games has recently been developed (Chia & Li, 2012), but this questionnaire does not seem to be widely adopted yet since no reference in the literature could be found. Of the seven RCTs found in literature, five of them did find a difference between a SG intervention compared to a control group for muscle strength (Chen et al., 2012, 2013), balance (Sharan et al., 2012), motivation and participation in the treatment (Sharan et al., 2012), performance (Akhutina et al., 2003, part 2; Ritterband-Rosenbaum et al., 2012) and bone density (Chen et al., 2013). The two others RCTs (Akhutina et al., 2003, part 1; Reid & Campbell, 2006) did not find significant improvement for the SG intervention group compared to conventional therapy. 16 patient cohorts were included representing a total of 201 CP children. Due to the relatively small number of patients involved in each independent study, Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

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and to the lack of protocol standardization to assess intervention outcomes, results and conclusions should be interpreted with caution. Three studies were assessing if SG could be used as a complement for traditional physical rehabilitation by focusing on the level of activity reached during SG. One of these studies focuses on the estimation of energy expenditure and muscle activation outcome (Howcroft et al., 2012), another one on the exercise intensity reach during the game (Robert et al., 2013), while the last one estimated if it is possible to provide a live feedback to patients during SG (Barton et al., 2013). Despite interesting aims, these studies unfortunately included one unique SG session with no long term assessment. Not surprisingly, all single case-studies present results in favor of SG. These studies concluded that SG schemes need to be adapted for the specific needs and disabilities of each individual patient. 58% of the studies included in this review tested the use of games, which are explicitly described in the papers as specially developed and adapted for CP children. This patient customization seems however limited. Indeed, CP patients might show a large spectrum of clinical signs and impairments (Odding, Roebroeck, & Stam, 2006). Highly configurable SG scenarios must be developed to take into consideration the very specific needs and disabilities of each individual patient, and to answer the therapists’ expectations. Adapted SG should include features such as plain background for patients with visual impairment, adapting speed of games, possibility to play in a wheelchair, etc. (Omelina, Jansen, Bonneche`re, Van Sint Jan, & Cornelis, 2012; Perez, Benitez, & Reinkensmeyer, 2011). Specific games should be developed to focus on one particular aspect of the rehabilitation for one particular group of patients (e.g. increase upper limb coordination with hemiplegic patients, increase balance with diplegic patients, etc.). 4.3. Commercial video games Most studies focusing on commercial video games used the Nintendo Wii FitTM (Deutsch et al., 2008; Howcroft et al., 2012; Jelsma et al., 2013; Luna-Oliva et al., 2013; Ramstrand & Lygnega˚rd, 2012; Robert et al., 2013; Sharan et al., 2012; Tarakci et al., 2013; Winkels et al., 2013). These games have been specifically developed for normal individuals from the general public to motivate them to increase physical activities by proposing fitness-like exercises. One of the studies had shown that the use of Wii FitTM games by CP children corresponds to a light to moderate level of physical activity (Howcroft et al., 2012). Aerobic training (walking, cycling. . .) is beneficial to CP children (Dodd & Foley, 2007; Williams & Pountney, 2007). If movements performed during fitness activities remain slow (i.e., to avoid spasticity firing), these games’ efficacy is probably due to the increase of aerobic capacity induced by the training in the games. The same results (increase of energy expenditure and exercises intensity) were found with the Eye Toy Games (Sony PlayStationTM) (Sandlund et al., 2011). While specially developed games are focusing on a particular aspect of the rehabilitation, the use of commercial video games seems to be broader. It has already been above-mentioned that protocols were different from one study to the other. More specifically, next to different methods for outcome measurement, other methodological differences were found such as frequency (variable from twice to week to daily), number of sessions (variable from a single session to 150 sessions), duration of the session (variable from 30 to 90 min per session) and types of interventions (types of game). Although some particular studies pinpoint the fact that the more the patient is playing, the more benefit they observe (Golomb et al., 2010), this review does not allow to determine the best frequency and duration for rehabilitation based on SG. Generally speaking there is a lack of details about the patient population: CP is a generic term including many categories (hemiplegia, diplegia, quadriplegia. . .) and the interventions (i.e., the description of the games is often quite poor). Therefore comparison between different studies is even more difficult due to this lack of clarification. There is not enough information in the available papers to summarize the population characteristics. Although it is not clearly stated in the analyzed papers, it seems that the majority of patients included in the studies were hemiplegic patients with GMFCS levels I and II (moderate form of CP). 5. Conclusion In most papers found in the literature about the efficacy assessment of a particular intervention, the intervention is standardized without taking into account patients’ specific clinical signs. It is probably one of the major reasons why it is difficult to find statistically-meaningful evidence-based conclusions for many clinical interventions while most of them are used daily in clinics (Autti-Ra¨mo¨ et al., 2006; Chung et al., 2011; Figueiredo et al., 2008; Papavasiliou, 2009; Scianni et al., 2009; Verrotti et al., 2006; Wiart et al., 2008). Management and treatment of CP children is a complex, multidisciplinary and multidimensional task with lots of parameters that must be taken into account. Such complexity and heterogeneous clinical presentation made it difficult to find scientific evidence for treatments and interventions. Currently, there is no clear evidence found in the literature that SG could help CP children. Nevertheless, it has been underlined that most of the current treatments for CP children used in daily practice are not based on scientific evidence. In this particular context, despite the fact that large studies are still needed to investigate the efficacy of serious games, SG is emerging as an interesting tool for both patients and clinicians. One might expect that, due to the highly heterogeneous clinical signs in CP, there is no one and only one effective treatment. Therefore, SG shows enough evidence to be included within conventional treatment of CP children since it proved to be efficient for increasing patients’ motivation. However, in order to increase the level of evidence, it is important to adopt standardized Please cite this article in press as: Bonneche`re, B., et al. Can serious games be incorporated with conventional treatment of children with cerebral palsy? A review. Research in Developmental Disabilities (2014), http://dx.doi.org/10.1016/ j.ridd.2014.04.016

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Evaluation of cervical posture improvement of children with cerebral palsy after physical therapy based on head movements and serious games.

Digital Posturography Games Correlate with Gross Motor Function in Children with Cerebral Palsy.

Protocol for a prospective observational study of conventional treatment and traditional Korean medicine combination treatment for children with cerebral palsy.

Assessment and treatment of children with cerebral palsy.

Pes planovalgus deformity in children with cerebral palsy: review article.

Nutritional management of children with cerebral palsy.

School readiness of children with cerebral palsy.

Dental health of children with cerebral palsy.

Rehabilitation outcomes of children with cerebral palsy.

Hand functioning in children with cerebral palsy.

Should children with cerebral palsy exercise?

Children with cerebral palsy. Introductory paragraph.

Intrauterine growth in children with cerebral palsy.

Fractures in children with cerebral palsy.

Nutritional management of children with cerebral palsy: a practical guide.

Swallowing disorders in a population of children with cerebral palsy.

A systematic review of interventions for children with cerebral palsy: the state of the evidence.

Can walking ability enhance the effectiveness of breathing exercise in children with spastic cerebral palsy?

Relevance of intraglandular injections of Botulinum toxin for the treatment of sialorrhea in children with cerebral palsy: a review.

Efficacy of upper limb strengthening in children with Cerebral Palsy: A critical review.

Effect of functional electrical stimulation on activity in children with cerebral palsy: a systematic review.

Onabotulinumtoxin A Treatment of Drooling in Children with Cerebral Palsy: A Prospective, Longitudinal Open-Label Study.

Evaluation and characterization of manual reaching in children with cerebral palsy: A systematic review.

Sleep and Children with Cerebral Palsy: A Review of Current Evidence and Environmental Non-Pharmacological Interventions.