level: locomotor training in children with cerebral palsy · locomotor training with an...

Gait

CME ARTICLE . 2011 SERIES . NUMBER 2

Improved Gait After RepetitiveLocomotor Training in Children withCerebral Palsy

ABSTRACTSmania N, Bonetti P, Gandolfi M, Cosentino A, Waldner A, Hesse S, Werner C,Bisoffi G, Geroin C, Munari D: Improved gait after repetitive locomotor training inchildren with cerebral palsy. Am J Phys Med Rehabil 2011;90:137Y149.

Objective: The aim of this study was to evaluate the effectiveness of repetitivelocomotor training with an electromechanical gait trainer in children with cerebralpalsy.

Design: In this randomized controlled trial, 18 ambulatory children withdiplegic or tetraplegic cerebral palsy were randomly assigned to an experimentalgroup or a control group. The experimental group received 30 mins of repetitivelocomotor training with an applied technology (Gait Trainer GT I) plus 10 mins ofpassive joint mobilization and stretching exercises. The control group received40 mins of conventional physiotherapy. Each subject underwent a total of 10treatment sessions over a 2-wk period. Performance on the 10-m walk test, 6-minwalk test, WeeFIM scale, and gait analysis was evaluated by a blinded rater beforeand after treatment and at 1-mo follow-up.

Results: The experimental group showed significant posttreatment improve-ment on the 10-m walk test, 6-min walk test, hip kinematics, gait speed, and steplength, all of which were maintained at the 1-mo follow-up assessment. No sig-nificant changes in performance parameters were observed in the control group.

Conclusions: Repetitive locomotor training with an electromechanical gaittrainer may improve gait velocity, endurance, spatiotemporal, and kinematic gaitparameters in patients with cerebral palsy.

Key Words: Development, Robotics, Rehabilitation, Brain Damage, Walking,Randomized Control Trial

CME Objectives:Upon completion of this article, thereader should be able to: 1) Identify theleading cause of gait impairments inchildren with Cerebral Palsy;2) Describe the potential benefits ofrepetitive locomotor training on gaitmechanics in children with CerebralPalsy; 3) Describe the potential effectsof repetitive locomotor training ondisability and energy expenditureduring gait in children with Cerebralpalsy.

Level: Advanced

Accreditation: The Association ofAcademic Physiatrists is accredited bythe Accreditation Council forContinuing Medical Education toprovide continuing medical educationfor physicians. The Association ofAcademic Physiatrists designates thisactivity for a maximum of 1.5 AMA PRACategory 1 Credit(s)TM. Physiciansshould only claim creditcommensurate with the extent of theirparticipation in the activity.

Authors:Nicola Smania, MDPaola Bonetti, MDMarialuisa Gandolfi, MDAlessandro Cosentino, MDAndreas Waldner, MDStefan Hesse, MDCordula Werner, MSCGiulia Bisoffi, STChristian Geroin, PTDaniele Munari, PT

Affiliations:From the Neuromotor and CognitiveRehabilitation Center, Department ofNeurological, Neuropsychological,Morphological and Motor Sciences,University of Verona, Italy (NS, PB, MG,CG, DM); Rehabilitation Unit ‘‘C.Santi,’’ Polyfunctional Centre DonCalabria, Verona, Italy (AC); VillaMelitta, Bolzano, Italy (AW); MedicalPark Berlin, Charite-UniversityMedicine, Berlin, Germany (SH, CW);and Statistics Unit, University Hospitalof Verona, Italy (GB).

0894-9115/11/9002-0137/0American Journal of PhysicalMedicine & RehabilitationCopyright * 2011 by LippincottWilliams & Wilkins

DOI: 10.1097/PHM.0b013e318201741e

www.ajpmr.com Locomotor Training in Cerebral Palsy 137

Copyright © 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Correspondence:All correspondence and requests for reprints shouldbe addressed to: Nicola Smania, MD, Neuromotorand Cognitive Rehabilitation Center, Department ofNeurological, Neuropsychological, Morphologicaland Motor Sciences, University of Verona, P.leLudovico Antonio Scuro, 10, 37134 Verona, Italy.

Disclosures:Financial disclosure statements have been obtained,and no conflicts of interest have been reported bythe authors or by any individuals in control of thecontent of this article. Supported by a grant fromthe CariVerona Fondation (PACIS), Verona, Italy.

Cerebral palsy (CP) describes a group ofchronic conditions affecting body movement andmuscle coordination caused by damage to one ormore areas of the brain, usually occurring duringfetal development or infancy.1 The motor disordersof CP are often accompanied by disturbances ofsensation, cognition, communication, perception,behavior, and/or a seizure disorder.2 One of themost disabling mobility impairments in CP is gaitimpairment, clinically characterized by reducedspeed and endurance, as well as reduced step, stridelength, and toe clearance during gait.3,4

Recently, gait rehabilitation methods inpatients with neurologic impairment have relied ontechnological devices, which drive the patient’s gaitin a body-weight support condition and emphasizethe beneficial role of repetitive practice.5 The ra-tionale for these approaches originates from animalstudies, which have shown that repetition of gaitmovements may enhance spinal and supraspinallocomotor circuits.6

Previous studies in gait rehabilitation inpatients with CP were carried out by using partialbody-weight support treadmill training (PBWSTT)and robotic-assisted treadmill therapy. Most ofthese studies consisted of single-case, small, orunselected patient samples and/or uncontrolledtrials.7Y11 In a recent randomized control trialstudy, Willoughby et al.12 showed that PBWSTT wasno more effective than overground walking forimproving walking speed and endurance in childrenwith CP. They concluded that the progressive re-duction of body-weight support along with the ad-dition of concurrent overground walking practice toa treadmill training protocol may increase the in-tensity of training and assist with carryover ofimprovements to overground walking.12 Despitetheir potential, these technologies have practicallimitations in their routine application: PBWSTTrequires the assistance of one or two physiothera-

pists to control the patient’s weight shift and lowerlimb position during training,13 and proper place-ment of the patient onto the machine (Lokomat;Hokoma Inc, Volketswill, Switzerland) for robotic-assisted treadmill training is time-consuming.14

More recently, several studies have focusedon the use of a new electromechanical gait trainer(Gait Trainer GT I; Reha-Stim, Berlin, Germany)15

in adult patients who have experienced a stroke.These studies have shown that training with thisdevice may significantly improve gait perfor-mance.16,17 Despite the clinical impact of thisnew rehabilitative procedure, to date, no studieshave been conducted on its use in childrenwith CP.

The primary aim of the present randomizedcontrolled trial was to evaluate whether repetitivelocomotor training with the Gait Trainer GT I canimprove walking speed and endurance in tetraple-gic or diplegic ambulatory children with CP. Thesecondary aim was to assess whether training canalso have a positive impact on kinematic and spa-tiotemporal gait parameters and on disability.

MATERIALS AND METHODSSubjects

Eighteen participants were recruited among31 children with CP attending the DevelopmentalAge Unit, ‘‘C. Santi,’’ Polyfunctional Centre DonCalabria, Verona, Italy, from January 2009 toOctober 2009.

Inclusion criteria were bilateral lower limb(diplegic or tetraplegic) CP, 10 to 18 yrs of age, andGross Motor Function Classification System18 levelsII to IV. The children needed to walk by themselvesor with the use of an assistance device for at least10 m, maintain a sitting position without assis-tance, follow instructions, and participate in therehabilitative program. Exclusion criteria werelower limb spasticity of 92 or higher on the Modi-fied Ashworth Scale,19 severe lower limb con-tractures, cardiovascular diseases, orthopedicsurgery or neurosurgery in the past 12 mos, orBotulinum toxin injections within 6 mos before thebeginning of the study. Before the start of the study,participants were allocated to the experimentalgroup or the control group via computerized ran-domization. The randomization sequence was gen-erated by a research assistant not involved with thestudy, and the group allocation was concealed usingsealed, numbered envelopes. The randomization listwas locked in a desk drawer accessible only to theprincipal investigator.20

138 Smania et al. Am. J. Phys. Med. Rehabil. & Vol. 90, No. 2, February 2011


Written informed consent was obtained fromthe children’s parents and the children themselves.The ethics committee of the Department of Neu-rological and Vision Sciences, University of Verona,approved the study protocol.

TrainingBefore the start of the study, the authors

designed experimental and control group treatmentprotocols and instructed two physiotherapists intheir use. One physiotherapist treated the experi-mental group and the other treated the controlgroup. The participants were treated individually onan outpatient basis in a rehabilitative gym at theC. Santi Medical Centre.

Both training programs consisted of ten40-min daily sessions for 2 wks (5 days/wk).

During the study period, participants receivedno physiotherapy other than that scheduled in thestudy protocol.

Experimental Group TrainingEach participant received 30 mins of repeti-

tive locomotor therapy on the Gait Trainer GT I,followed by 10 mins of passive joint mobilizationand stretching exercises by a physiotherapist.

The Gait Trainer GT IThe gait trainer consists of a double crank and

rocker gear system, composed of two footplatespositioned on two bars (coupler), two rockers, andtwo cranks that provide the propulsion. While usingthe gait trainer, individuals are secured in a harnessand positioned on two footplates, whose movementssimulate stance and swing phase, with a ratio of60% to 40% between the two phases.15 A servo-controlled motor assists gait movement by con-trolling the gear velocity and comparing it with thepreselected velocity. The rotation of the planetarygear system, equaling one gait cycle, controls themovement of the center of mass (CoM) in the ver-tical and horizontal directions. Two cranks, one forthe vertical and one for the horizontal movementCoM control, are attached to the planetary gearsystem. A transmission gear installed between theplanetary gear and the crank controlling the verticalCoM displacement provides a double frequency ofthe vertical CoM movement within one gait cycle. Arope attached to the crank controlling the verticalCoM displacement served as the central suspen-sion of the subject. A second rope connected tothe crank controlling the horizontal CoM dis-placement was attached to the left lateral aspect ofthe subject harness at the level of the pelvic crest(Fig. 1).15

Training ProceduresThe child was positioned on the gait trainer.

Step length and gait speed were individually setaccording to the gait parameters recorded at thepretreatment gait analysis. Walking speed wasgradually increased over the course of the 2 wks ifthe children completed the last previous trainingsession without discomfort or complaints of fatigue.The partial body-weight support was progressivelydecreased from 30% to 0% over the duration of thesessions. The criterion for the reduction was thechild’s ability to avoid his/her knee collapsing intoflexion during the stance phase because of theincreased load of body weight. Each participantwas supervised during therapy sessions by onlyone physiotherapist who corrected knee motionmanually, when needed. No patients required theassistance of two physiotherapists. The machine wasstopped if pain or other problems such as musclecramps occurred.

Control Group TrainingConventional training consisted of the repeti-

tion of three different sets of exercises: (1) passivejoint mobilization and stretching of the lower limbmuscles with the patient lying on a physiother-apy mat in the supine position; (2) strengtheningexercises, including leg-press exercises and sit-to-stand and stand-to-sit exercises. In the first session,

FIGURE 1 Training of a 6-yr-old on the GangtrainerGT I.



the correct performance of the leg-press exerciserequired strict supervision by the physiotherapist:the participants lay in the supine position and wereasked to slowly push their feet against the phys-iotherapist’s chest and to slowly bend them backagain; in the subsequent sessions, these exerciseswere performed by using a leg-press machine withresistance specifically adapted for the child’s ability;(3) balance and gait exercises. The balance exerciseswere carried out with the participant sitting on abench and in the standing position, with a frontsupport or against a wall. Gait exercises consisted ofguided ground walking (e.g., side stepping) withthe assistance of the physiotherapist. Each set ofexercises lasted 10, 15, and 15 mins, respectively.During the entire sessions, the physiotherapiststood near the children to ensure safety and preventpotential falls.

TestingBefore and after treatment and at 1-mo follow-

up, the participants were evaluated by the sameexaminer who was unaware of treatment allocation.The assessment procedures, consisting of clinicaland instrumental evaluations, were carried out atthe C. Santi Medical Centre: the clinical tests tookplace in a spacious and silent environment to avoidthe child potentially becoming distracted, whereasthe instrumented evaluations were conducted in theGait Analysis Laboratory. All the assessments wereadministered in the same sequence (clinical andinstrumented evaluations) and at the same time ofday, in the afternoon, around 3 p.m. During testing,the participants were allowed to wear their usualfootwear and orthoses and use their gait-assistivedevices.

Primary Outcomes10-m Walk Test:

This is a validated test for the clinical evalua-tion of walking speed.21 The subject was asked towalk at her/his self-selected walking speed along thecentral 10 m of a 14-m linoleum-covered walkway.A digital stopwatch was used to time the walks.

6-Min Walk Test:This is a validated test for the clinical evalua-

tion of walking endurance that involves respiratory,cardiovascular, skeletal, nervous, and muscularsystem competences/skills.22 The subject was askedto walk at her/his self-selected walking speed in thegym along an oval track 20 m in length marked outwith masking tape. The distance walked during thetest was calculated with a tape measure.

Secondary OutcomesFunctional Independence Measure forChildren (WeeFIM):

This widely used scale for the evaluation ofdisability in children with CP23 investigates threemain domains: self-care, mobility, and cognition(score, 18Y126; high, best performance).

Gait Analysis:Three-dimensional gait analysis (Vicon; Oxford

Metrics, Oxford, UK) by means of a motion capturesystem consisting of six infrared cameras was carriedout according to a standard marker placement pro-tocol.24 The participants were required to walk attheir self-selected speeds. The data from at least fourtrials were collected. The gait parameters were sag-ittal plane kinematics (joint angles of the hip, knee,and ankle at initial contact; middle stance; and initialswing and middle swing) and spatiotemporal gaitparameters (speed, cadence, and step length).

Statistical AnalysisWe calculated effect sizes between the two in-

dependent groups (Cohen d) and used 95% confi-dence intervals. Because our data were not normallydistributed (after visual and descriptive inspection),we used nonparametric tests for inferential statistics.The Mann-Whitney U test was used for testing dif-ferences between groups at baseline, the Friedmantest was used to analyze changes in performancewithin groups, and Wilcoxon’s signed rank testswere used to compare changes between groupsfrom pretreatment/posttreatment and pretreatment/follow-up measures. The Mann-Whitney U test wasused for between-group comparisons. For this pur-pose, we computed the differences ($) betweenpretreatment and posttreatment performance andbetween pretreatment and follow-up performancefor all outcome measures. We set the alpha levelfor significance at 0.05; however, to adjust for mul-tiple comparison, we used a Bonferroni25 correction(> = 0.025). All statistical analysis was carried outusing the SPSS for Macintosh statistical package,version 16.0.

RESULTSNo children withdrew from the study. Partici-

pant demographics and clinical characteristics arereported in Table 1.

At baseline, there were no statically significantdifferences between the two groups in age, perfor-mance on the 10-m walk test and the 6-min walktest, or WeeFIM scores (age, Z = j0.13, P = 0.89;10-m walk test, Z = j0.08, P = 0.93; 6-min walk



TABLE 1 Patients’ demographics and pretreatment, posttreatment, and 1-mo FU performance in the 6-min walk test, the 10-m walk test, and WeeFIM

Patient no. Sex Age, yr/mo Diagnosis GMFCS Walking Aids

10-m Walk Test, m/sec 6-Min Walk Test, m WeeFIM

Pre Post FU Pre Post FU Pre Post FU

Experimental group1 F 11 ST I None 0.99 1.05 1.18 308 393 395 115 116 1162 F 11/1 SD IV Walker 0.76 0.77 0.75 205 262 288 85 85 853 M 14/4 ST I None 1.35 1.54 1.59 451 590 550 94 94 944 M 14/4 SD I None 1.12 1.16 1.18 400 462 462 117 117 1175 M 17/6 ST II None 1.10 1.32 1.45 368 412 423 84 84 846 F 13/2 SD IV Walker 0.82 0.85 0.96 302 362 378 112 116 1167 F 10/1 SD IV Walker 0.53 0.68 0.60 144 208 186 62 62 628 F 15/8 SD II None 0.74 0.76 0.77 360 378 380 63 63 639 M 17/8 ST IV Walker, AFO 0.61 0.63 0.64 90 180 190 102 104 104

5F/4MMean 13/88 0.89 0.97 1.01 292 360 361 92.66 93.44 93.44SD 2.83 0.27 0.31 0.36 121.44 128.71 120.81 20.94 21.68 21.68Range (min-max) 0.53Y1.35 0.63Y1.54 0.60Y1.59 90Y451 180Y590 186Y550 62Y117 62Y117 62Y117

Control group10 M 10/4 SD IV Walker, AFO 0.39 0.38 0.39 321 403 400 86 86 8611 M 14/1 SD III Walker, AFO 0.91 0.89 0.88 322 312 314 111 112 11212 F 8/9 SD III None 0.83 0.84 0.84 319 350 347 85 85 8513 F 15/4 SD I None 1.00 0.92 0.92 317 284 281 94 94 9414 M 12/1 SD I Walker 1.12 1.11 1.10 403 290 300 117 117 11715 F 15/8 SD III Walker, AFO 1.11 1.02 1.02 259 322 318 84 84 8416 M 10/7 ST IV Walker, AFO 1.00 0.91 0.85 350 319 318 112 113 11317 M 10 ST IV Walker, AFO 0.57 0.63 0.62 284 270 272 62 62 6218 M 17/8 ST I None 0.69 0.72 0.72 290 321 320 83 83 83

3F/6MMean 12/79 0.85 0.82 0.82 318 319 319 92.67 92.89 92.89SD 3.08 0.25 0.22 0.21 41.3 39.60 37.73 17.73 18 18Range (min-max) 0.39Y1.12 0.38Y1.11 0.39Y1.10 259Y403 270Y403 272Y400 62Y117 62Y117 62Y117

GMFCS, Gross Motor Function Classification System; Pre, baseline; Post, posttreatment; FU, follow-up; ST, spastic tetraparesis; SD, spastic diplegic; AFO, ankle-foot orthosis.

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TABLE 2 Patients’ performance and treatment effects in all outcome measures

Group

Pre-Post Pre-1 Mo FU

95% CI, Mean (LB; UB) Effect Size (BG) P (Z ) 95% CI, Mean (LB; UB) Effect Size (BG) P (Z )

10-m WT Experimental j0.08 (j0.14; j0.02) 0.558 0.008 (j2.67)a j0.12 (j0.21; j0.02) 0.644 0.011 (j2.54)a

Control 0.02 (0.01; j0.06) 0.214 (j1.24) 0.03 (0.01; 0.08) 0.314 (j1.00)6-min WT Experimental j68.78 (j94.73; j42.82) 0.438 0.008 (j2.66)a j69.33 (j90.04; j48.63) 0.474 0.008 (j2.66)a

Control j0.67 (j45.92; 44.59) 0.095 (j0.59) j0.56 (j43.13; 42.02) 0.095 (j0.59)WeeFIM Experimental j0.78 (j1.85; 0.29) 0.027 0.109 (j1.60) j0.78 (j1.85; 0.29) 0.027 0.109 (j1.60)

Control j0.22 (j0.56; 0.12) 0.157 (j1.4) j0.22 (j0.56; 0.12) 0.157 (j1.4)Hip

Initial contact Experimental 0.78 (j0.62; 2.20) 0.192 0.109 (j1.60) 2.71 (j1.88; j3.53) j0.12 0.008 (j2.66)a

Control 0.05 (j2.12; 2.22) 0.214 (j1.24) 0.15 (j2.03; 2.34) 0.139 (j1.48)Middle stance Experimental 2.02 (0.94; 3.1) j0.023 0.011 (j2.54)a 3.18 (1.11; 5.27) j0.210 0.008 (j2.66)a

Control 0.22 (j0.03; 0.49) 0.008 (j1.71) 0.091 (j0.21; 0.39) 0.441 (j0.77)Initial swing Experimental 0.93 (0.03; 1.84) 0.025 0.024 (j2.24)a 2.25 (0.92; 3.4) 0.114 0.008 (j2.66)a

Control 0.08 (j0.01; 0.18) 0.86 (j1.71) 0.01 (j0.40; 0.40) 0.767 (j0.29)Middle swing Experimental 3.23 (0.13; 6.33) j0.356 0.051 (j1.95) 3.32 (0.12; 6.76) j0.335 0.066 (j1.83)

Control 0.23 (j0.43; 0.89) 0.484 (j0.70) j0.09 (j0.54; 0.36) 0.374 (j0.89)Knee

Initial contact Experimental 1.66 (j2.35; 5.68) j0.356 0.249 (j1.15) j0.46 (j6.47; 5.54) 0.043 0.917 (j0.10)Control j0.02 (j0.25; 0.21) 0.714 (j0.36) j0.07 (j0.32; 0.16) 0.131 (j1.51)

Middle stance Experimental 1.82 (j0.47; 4.12) j0.169 0.43 (j2.02) j0.17 (j3.30; 2.953) 0.019 0.893 (j0.13)Control j0.12 (j0.30; 0.05) 0.130 (j1.51) j0.01 (j0.18; 0.15) 0.20 (j2.33)

Initial swing Experimental 1.27 (j1.78; 4.34) j0.045 0.917 (j0.10) 2.38 (j3.91; 8.67) j0.158 0.735 (j0.33)Control 0.07 (j0.11; 0.27) 0.339 (j0.95) 0.11 (j0.06; 0.28) 0.174 (j1.36)

Middle swing Experimental 2.06 (j1.50; 5.61) j0.116 0.172 (j1.36) 2.07 (j3.89; 8.05) j0.124 0.31 (j1.01)Control j0.08 (j0.25; 0.09) 0.349 (j0.93) j0.03 (j0.20; 0.14) 0.776 (j0.28)

AnkleInitial contact Experimental 2.83 (j1.64; 7.31) j0.371 0.285 (j1.06) 3.04 (j1.8; 7.88) j0.404 0.285 (j1.06)

Control j0.06 (j0.41; 0.28) 0.888 (j0.141) j0.14 (j0.46; 0.17) 0.497 (j0.67)Middle stance Experimental 2.82 (j2.82; j8.46) j0.363 0.273 (j1.09) 3.30 (j3.43; 10.03) j0.449 0.273 (j1.09)

Control j0.08 (j0.21; 0.04) 0.167 (j1.38) j0.21 (j0.32; j0.09) 0.178 (j1.45)Initial swing Experimental 1.88 (2.72; j6.47) j0.182 1.00 (0.00) 1.98 (j2.96; 6.92) 0.066 1.00 (0.00)

Control j0.17 (j0.48; 0.15) 0.231 (j1.19) j0.17 (j0.43; 0.10) 0.182 (j1.33)Middle swing Experimental 2.69 (j2.90; 8.28) j0.250 0.109 (j1.60) 2.71 (j2.87; 8.29) j0.244 0.144 (j1.461)

Control j0.13 (j0.25; j0.02) 0.036 (j2.10) j0.03 (j0.17; 0.10) 0.570 (j0.56)Gait speed Experimental j0.05 (j0.09; j0.01) 0.905 0.028 (j2.19)a j0.11 (j0.16; j0.05) 1.058 0.008 (j2.26)a

Control 0.10 (0.07; 0.13) 0.347 (j2.66) 0.10 (0.07; 0.14) 0.198 (j2.66)Cadence Experimental 0.76 (j4.38; 5.91) j0.201 0.575 (j0.56) j1.53 (j6.90; 3.84) j0.055 0.515 (j0.65)

Control j4.49 (j11.16; 2.18) 0.173 (j1.36) j4.49 (j11.16; 2.18) 0.173 (j1.36)Step length Experimental 0.02 (0.4; 0.00) 0.555 0.024 (j2.25)a 0.02 (0.04; 0.00) 0.630 0.011 (j2.53)a

Control j0.0.1 (j0.02; 0.00) 1 (0.00) j0.01 (j0.03 j0.00) 1 (0.00)

P and Z values were identified from the Wilcoxon’s test.Pre, baseline; Post, posttreatment; FU, follow-up; CI, confidence interval; LB, lower bound; UB, upper bound; BG, between groups; WT, walk test.aStatistically significant.

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test: Z = j0.13, P = 0.89; WeeFIM, Z = j0.22,P = 0.82) (Table 1).

Primary OutcomesIn the experimental group, overall significant

changes in performance in the different evaluationsessions were found in regard to all primary out-come measures (10-m walk test, df = 2, X = 11.56,P = 0.003; 6-min walk test, df = 2, X = 12.51,P = 0.001). Within-group comparisons showedthat changes in performance were significant atboth the posttreatment and follow-up evaluations(see Table 2 for details). In the control group, nosignificant changes in the primary outcome mea-sures were found at any of the evaluation sessions(statistics in Table 2).

A between-group comparison showed that theeffects of the experimental and the control treat-ments were significantly different in all primaryoutcome measures (see Table 3 for details).

Secondary OutcomesNo significant changes in WeeFIM scores were

found in either group (see Table 2 for details).In regard to gait analysis, the experimental

group showed significant changes in the joint anglesof the hip during initial contact, middle stance, andinitial swing, as well as in gait speed and step length

at all assessments (hip kinematicsYinitial contact,df = 2, X = 14.222, P = 0.001; middle stance, df = 2,X = 11.556, P = 0.003; initial swing, df = 2,X = 13.886, P = 0.001; spatiotemporal parametersYgait speed, df = 2, X = 13,771, P = 0.001; step length,df = 2, X = 9.188, P = 0.010).

Before-after comparisons showed improved hipextension at middle stance, initial swing, gait speed,and step length (see Table 2 for details). Before-follow-up comparisons showed increased hip ex-tension at different phases of the gait cycle andincreased gait speed and step length. No changes inperformance of the control group were seen (seeTable 2 for details).

Between-groups analysis showed a significantdifference in the rate of hip extension at differentphases of the gait cycle, in gait speed, and in steplength (see Table 2 for details).

DISCUSSIONOur results demonstrate that repetitive locomo-

tor gait training with an electromechanical body-weight support machine can significantly improvegait velocity and endurance in ambulatory childrenwith diplegic and tetraplegic CP and that the im-provements can be maintained for at least 1 mo post-treatment. Improvements were also seen in proximallower limb gait kinematics and in spatiotemporalparameters (gait speed and step length). The resultsobtained displayed that the magnitude of treatmenteffect was small to medium among the primary out-comes, further supporting the value of our experi-mental approach. No changes were seen in disability.There was no adverse event that led to a missedtraining session. No joint pain ormuscle spasms werereported during or after the GT I training program.

Our study showed that the children in the ex-perimental group significantly improved their gaitvelocity after treatment (10-m walk test and gaitanalysis). There are several reasons for this effect oftreatment. First, children showed significant post-treatment changes in hip kinematics in the sagittalplane, with increased hip extension during middlestance and initial swing. This may have been be-cause of the fact that during training with the GT Imachine, the footplates forced the children toextend their hips.15 The leg movement imposed bythe machine has a maximal fulcrum at the hip level,and backward pelvis displacements are blocked bya rear bar, thus forcing the patient to extend thehip joint. As a result, training might have progres-sively enhanced the extensibility of the hip flexormuscles and periarticular hip joint tissues, leadingto increased hip movement. Another possible

TABLE 3 Comparison of treatment effectsbetween the experimental andcontrol groups

Pre-Post Pre-1 Mo FU

P (Z ) P (Z )

10-m WT 0.007 (j2.69)a 0.004 (j2.87)a

6-min WT 0.015 (j2.43)a 0.007 (j2.669)a

WeeFIM 0.466 (j0.72) 0.466 (j0.72)Hip

Initial contact 0.58 (j1.89) 0.005 (j2.78)a

Middle stance 0.009 (j2.60)a 0.000 (j3.40)a

Initial swing 0.03 (j2.16) 0.004 (j2.87)a

Middle swing 0.85 (j1.72) 0.035 (j2.42)a

KneeInitial contact 0.120 (j1.55) 0.351 (j0.93)Middle stance 0.529 (j2.90) 0.855 (j0.18)Initial swing 0.329 (j0.97) 0.559 (j0.58)Middle swing 0.045 (j2.00) 0.184 (j1.33)

AnkleInitial contact 1.00 (0.00) 0.380 (j0.87)Middle stance 0.096 (j1.66) 0.018 (j2.37)Initial swing 0.236 (j1.18) 0.466 (j0.72)Middle swing 0.113 (j2.48) 0.279 (j1.08)

Gait speed 0.000 (j3.58)a 0.000 (j3.58)a

Cadence 0.145 (j1.45) 0.757 (j0.30)Step length 0.004 (j2.89)a 0.001 (j3.51)a

The P value and the corresponding Z value were identifiedfrom the Mann-Whitney U test.

Pre, baseline; Post, posttreatment; FU, follow-up.aStatistically significant.



explanation for the improvement in gait velocitymay have been the increased muscle strengthpresent after training.26 It has been demonstratedthat muscle weakness is a primary limiting factor inambulation in children with CP.26Y28 Althoughmuscle strength was not specifically tested in thisstudy, previous studies have shown that adult strokepatients trained with the GT I machine significantlyincreased their performance on the Motricity IndexTest (lower limb section).13 This effect on musclestrength is further confirmed by the fact thattrained patients in previous studies usually expe-rience a feeling of muscle fatigue after treatment,indicating that training on the GT I machine notonly acts as a passive guide for movements butalso requires active involvement of the lower limbmuscles.15

A second main result of the present studywas that the children in the experimental grouphad improved gait endurance after training. Thisimprovement could have resulted from the previ-ously described effects on gait kinematics andstrength. However, a reduction in energy expen-diture29 related to the decrease in co-contractionmuscle30,31 and the improvement in movementefficacy during gait29 may have also contributed tothis improvement. This may lead to an optimizationof cardiovascular performance. To date, no studieshave investigated the effect of body-weight supportgait-training approaches on energy expenditure inchildren with CP. Future research on this topic inthe neuromotor rehabilitation of children with CPis needed.

The question arises as to the possible delayedeffects of training. It is worth noting that at the1-mo follow-up, the participants in the experimen-tal group showed a trend toward continued im-provement in gait kinematics and gait velocity. Aftertraining, the children may have been more moti-vated to practice gait during daily life activities. Thishypothesis was supported by informal interviewsconducted with the children’s parents.

As shown by the WeeFIM results, the childrenin the experimental group showed no reduction inactivities of daily life after training. Although gait isan important activity of daily life, this result maybe explained by the fact that the WeeFIM is notsensitive enough to point out significant changes inthe overall performance of activities of daily life.Furthermore, a potential ceiling effect may be anadditional explanation of the small changes in scoreseen in children with higher scores in the WeeFIM.

No improvements in the primary and second-ary outcomes were obtained in the control group.

This could be because of the different level in theGross Motor Function Classification System and inthe gait-assistive devices required in the experi-mental and control group.

Most studies on body-weight support gait-training techniques discuss the effects of PBWSTTand Lokomat robotic training. PBWSTT differs inseveral ways from the GT machine approach. Themajor disadvantage of PBWSST is that the trunkand the lower limbs are difficult to control duringexercise. Hence, the more severe the mobility im-pairment, the more physical effort is demandedfrom the child. In addition, at least two physio-therapists are needed to assist trunk and limbmovements during the gait cycle.13 Two reviews7,8

on the limited studies investigating the effect ofPBWSTT on gait parameters in children with CPconcluded that, currently, there is no evidence thatchildren with CP benefit from PBWSTT. This lack ofevidence was attributed to small sample size, dis-parate ability levels of participants, and low-qualityexperimental design.

A recently developed pediatric version of theLokomat consists of a robotic-driven exoskeleton11

that moves the lower limbs to reproduce normalwalking. Lower limb movements are synchronizedwith a treadmill. The few studies examining theeffect of this device on children with CP demon-strated positive effects on gait velocity and endur-ance in clinical tests.9Y11 However, these studieswere limited because of small sample size, lack ofa randomized control trial design, and lack ofinstrumental evaluations.

Some limitations of the present study mustbe acknowledged. First, no measure of musclestrength, energy expenditure, or quality-of-life wasperformed. Second, a longer session time (1 mo)could have led to a more significant improvementin children performances. Third, the fact that onlyone physiotherapist treated the control group andonly one physiotherapist treated the treatmentgroup makes it difficult to determine if groupdifferences are related to the interventions or ratherto a characteristic of the assigned therapist. Fourth,a great variability in the Gross Motor FunctionClassification System scores was evident in oursample of patients. Finally, a longer follow-upperiod (3Y6 mos) is needed to determine the long-term effects of a gait-training program with thisdevice. Nonetheless, our results strongly sug-gest that repetitive locomotor training on a body-weight support electromechanical machine mayimprove gait speed and endurance in childrenwith CP.



ACKNOWLEDGMENTSWe thank the participants and their family for

their dedication to and participation in this study.Also, we are grateful to the staff of the Develop-mental Age Unit, C. Santi Medical Centre, DonCalabria Institute, Verona, Italy, for their helpfulcollaboration.

REFERENCES

1. Rosenbaum P, Paneth N, Leviton A, et al: A report:the definition and classification of cerebral palsy.2006. Dev Med Child Neurol 2007;109:S8Y14

2. Bax M, Goldstein M, Rosenbaum M, et al: ExecutiveCommittee for the Definition of Cerebral Palsy. Pro-posed definition and classification of cerebral palsy.Dev Med Child Neurol 2005;47:571Y6

3. Pirpiris M, Wilkinson AJ, Rodda J, et al: Walkingspeed in children and young adults with neuromus-cular disease: comparison between two assessmentmethods. J Pediatr Orthop 2003;23:302Y7

4. Jean L. Gait: development and analysis. In: CampbellKS, Vander Linden DW, Palisano RJ, eds. PhysicalTherapy for Children. Elsevier Health Sciences,2006:161Y90

5. Hesse S: Locomotor therapy in neurorehabilitation.NeuroRehabilitation 2001;16:133Y9

6. Scivoletto G, Ivanenko Y, Morganti B, et al: Plasticityof spinal centers in spinal cord injury patients: newconcepts for gait evaluation and training. Neuro-rehabil Neural Repair 2007;21:358Y65

7. Mutlu A, Krosschell K, Spira DG: Treadmill trainingwith partial body-weight support in children withcerebral palsy: a systematic review. Dev Med ChildNeurol 2009;51:268Y75

8. Damiano DL, DeJong SL: A systematic review of theeffectiveness of treadmill training and body weightsupport in pediatric rehabilitation. J Neurol PhysTher 2009;33:27Y44

9. Meyer-Heim A, Borggraefe I, Ammann-Reiffer C,et al: Feasibility of robotic-assisted locomotor train-ing in children with central gait impairment. Dev MedChild Neurol 2007;49:900Y6

10. Borggraefe I, Meyer-Heim A, Kumar A, et al: Im-proved gait parameters after robotic-assisted loco-motor treadmill therapy in a 6-year-old child withcerebral palsy. Mov Disord 2008;23:280Y3

11. Meyer-Heim A, Ammann-Reiffer C, Schmartz A, et al:Improvement of walking abilities after robotic-assisted locomotion training in children with cerebralpalsy. Arch Dis Child 2009;94:615Y20

12. Willoughby KL, Dodd KJ, Shields N, Foley S: Efficacyof partial body weight-supported treadmill trainingcompared with overground walking practice forchildren with cerebral palsy: a randomized controlledtrial. Arch Phys Med Rehabil 2010;91:333Y9

13. Dias D, Lains J, Pereira A, et al: Can we improve gaitskills in chronic hemiplegics? A randomised controltrial with gait trainer. Eura Medicophys 2007;43:499Y504

14. Colombo G, Joerg M, Schreier R, Dietz V: Treadmilltraining of paraplegic patients using a robotic or-thosis. J Rehabil Res Dev 2000;37:693Y700

15. Hesse S, Uhlenbrock D: A mechanized gait trainer forrestoration of gait. J Rehabil Res Dev 2000;37:701Y8

16. Pohl M, Werner C, Holzgraefe M, et al: Repetitivelocomotor training and physiotherapy improvewalking and basic activities of daily living after stroke:a single-blind, randomizedmulticentre trial (DEutscheGAngtrainerStudie, DEGAS). Clin Rehabil 2007;21:17Y27

17. Mehrholz J, Werner C, Kugler J, et al:Electromechanical-assisted training for walking afterstroke. Cochrane Database Syst Rev 2007;17:CD006185

18. Palisano RJ, Hanna SE, Rosenbaum PL, et al: Vali-dation of a model of gross motor function for childrenwith cerebral palsy. Phys Ther 2000;80:974Y85

19. Bohannon RW, Smith MB: Interrater reliability of aModified Ashworth Scale of muscle spasticity. PhysTher 1987;67:206Y7

20. Bryant TN, Machin D: Statistical methods. In: WilsonBA, McLellan DL, eds. Rehabilitation StudiesHandbook. Cambridge, United Kingdom: CambridgeUniversity Press; 1997:189Y204

21. Wade DT: Measurement in Neurological Rehabilita-tion. Oxford, United Kingdom: Oxford UniversityPress; 1992

22. Maher CA, Williams MT, Olds TS: The six-minutewalk test for children with cerebral palsy. Int JRehabil Res 2008;31:185Y8

23. Ottenbacher KJ, Taylor ET, Msall ME, et al: Thestability and equivalence reliability of the functionalindependence measure for children (WeeFIM). DevMed Child Neurol 1996;38:907Y16

24. Davis RB, Ounpuu S, Tyburski DJ: A gait analysis datacollection and reduction technique. Hum Mov Sci1991;10:575Y87

25. Shaffer JP: Multiple hypothesis testing. Annu RevPsychol 1995;46:561Y84

26. Bottos M, Gericke C: Ambulatory capacity in cerebralpalsy: prognostic criteria and consequences for in-tervention. Dev Med Child Neurol 2003;45:786Y90

27. Gormley ME Jr: Treatment of neuromuscular andmusculoskeletal problems in cerebral palsy. PediatrRehabil 2001;4:5Y16

28. Eagleton M, Iams A, McDowell J, et al: The effects ofstrength training on gait in adolescents with cerebralpalsy. Pediatr Phys Ther 2004;16:22Y30

29. Waters RL, Mulroy S: The energy expenditure of nor-mal and pathologic gait. Gait Posture 1999;9:207Y31

30. Unnithan VB, Dowling JJ, Frost G, et al: Role of co-contraction in the O2 cost of walking in children withcerebral palsy. Med Sci Sports Exerc 1996;28:1498Y504

31. Piccinini L, Cimolin V, Galli M, Berti M, Crivellini M,Turconi AC: Quantification of energy expenditureduring gait in children affected by cerebral palsy.Eura Medicophys 2007;43:7Y12



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CME SELF-ASSESSMENT EXAM

CME Article 2011 Series Number 2: N. Smania, et al.

1. In this study, which was used for repetitive locomotortraining in children with Cerebral Palsy?A. A robotic-driven exoskeletonB. A treadmill deviceC. An electromechanical body-weight support gait trainerD. Lower limbs orthoses

2. In this study, which of the following may explainthe velocity improvements after repetitive locomotortraining?A. Increased hip extension during the middle stance

and initial swingB. Increased knee flexion during swing phaseC. Decreased ankle dorsiflexion during swing phaseD. Increased ankle dorsiflexion during stance phase

3. Which of the following represent the scientific rationalefor repetitive locomotor training in gait rehabilitation?A. Repetition of gait movements may enhance

supraspinal circuitsB. Repetition of gait movements may enhance spinal

and supraspinal locomotor circuits

C. Repetition of gait movements may increase theprimary motor cortex excitability

D. Repetition of gait movements may decrease lowerlimb spasticity

4. Which of the following represent gait impairment inchildren with Cerebral Palsy?A. Increased step, stride length, toe clearance, gait

speed and endurance.B. Increased ankle dorsiflexion during phases of gaitC. Reduced step and stride length, toe clearance, gait

speed and endurance.D. Increase hip flexion, stride length, toe cleareance

and endurance

5. In this study the improvement in gait endurance seenin the experimental group may result fromA. Improved gait mechanicsB. Improved strengthC. Improved movement efficiency and reduction of

energy expenditureD. All of the above.

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