Research Report Biomechanics of Submaximal Recumbent Cycling in Adolescents With and Without Cerebral Palsy Therese E Johnston, Ann E Barr, Samuel CK Lee TE lohnston, PT, PhD, MBA, is Research Specialist, Shriners Hospitals for Children, 3551 N Broad St, Philadelphia, PA 19140 (USA). Address all correspondence to Dr lohnston at: tjohnstonOshrinenet. org. AE Barr, PT, DPT, PhD, is Associate Professor, College of Health Professions, Temple University, Philadelphia, Pa, SCK Lee, PT, PhD, is Research Assistant Professor, Department of Physical Therapy, University of Delaware, Newark, Del, and Research Associate, Shriner's Hospitals for Children, [Johnston TE, Barr AE, Lee SCK. Biomechanics of submaximal recumbent cycling in adolescents with and without cerebral palsy. Phys Ther. 2007;87:572-585,] © 2007 American Physical Therapy Association Background and Purpose The purpose of tliis study was to compare the biomechanics of recumbent cyciing between adolescents with cerebral palsy (CP) classified at Gross Motor Function Classification System (GMFCS) levels III and IV and adolescents with typical development (TD). Subjects Twent)- subjects, ages (X±SD) 15,2±1.6 years (10 with TD, 10 with CP), participated. Methods Lower-extremity kinematics and muscle activity were measured at 30 and 60 rpm while subjects pedaled on a recumbent cycle. Energy expenditure and perceived exertion were measured during a 5-minute test, and efficiency was calculated, Noncircular data were analyzed with analyses of variance. Circular data were analyzed using circular t tests. Results Differences were found between groups for joint kinematics for all motions. Subjects with CP displayed earlier onsets and later offsets of muscle activity', increased co-contraction of agonist and antagonist muscles, and decreased efficiency compared with subjects with TD. There were no diffcretices in perceived exertion. Discussion and Conclusion Differences in cycling biomechanics between children with CP and children with TD may be due to decreased strengtb and motor control in the children with CP. Post a Rapid Response or find The Bottom Line: www.ptjournal.org 572 • Physical Therapy Volume 87 Number 5 May 2007 Biomechanics of Submaximai Recumbent Cycitng in Adolescents With and Wltiiout CP C hildren with cerebral palsy (CF) typically have progressive impairments that affect their function as children and later as attults. and they have decreased fitness levels versus children with typieal development (TD). Cycling has been stiggcsted as an inter\'ention to address common impairments and improve fitness levels in this population. However, little is known about the biomecUanics of cycling in children with CP. Ccjmpared with children with TD, children with spastic CP have decreased muscle strength (forcegenerating capacity),' muscle spasticity (hypertoniciry).- decreased joint range of motion (ROM),* altered motor and postural control,-* and gait deviations.^'* Several of these impairments are related to decreased function."" In addition, muscle co-contraction in children with CP bas received attention during isolated liml>segment movements as well as whole-hody activities such as gait''"' and is a contributor to decreased motor control." Fitness levels of people with disabUities recently have gained attention through Healtby People 2010.'^ '* Inactivity in people with disabilities can lead to a cycle of deconditioning, adversely affecting the cardio vascular system, bone density, and circulation and leading to social isolation and decreased .selfe s t e e m , " ' " Children with CP often decline in ambulator)' status as they become adults due to problems such as joint pain, joint deterioration, and overall fatigue.'" Adolescents and adults with CP experience secondar>- conditions, including fractures, osteoporosis. cardiova.scular system impairments, degcnenitive joint disease, obesity, pain, contractures, depression, decreased nKjbility. dependency on otber people for assistance, limited opport unit it's ftjr recreation, and st)ciai isolation.'*^ May 2007 However, most research on exercise interventions for individuals with C;F has focused on the younger age groups,^" with less research directed toward adolescents,-' a group particularly at risk for deconditioning and potential negative health effects due to decreasing mobility that continues into adultbood.''*-'-- In addition, adolescents with higher Ciross Motor Function Classification System-^ (CiMFCS) levels and therefore decreased mobilit)' are particularly at risk as they transition from adolescence to adulthood. Bicycling using a moving or stationary' bicycle is a potential intervention for cbildren with CP to address impairments while potentially minimizing joint stress,-' and studies have begun to examine otitcomes of a therapeutic cycling program in children with CP.^**-'' Only one study has examined the biomechanics of cycling in children with CP.-" A better understanding of how children with CP cycle may help to develop future interventions, such as volitional cycling programs or cycling assisted by functional eleetrical stimulation. Additionally, cycling may allow children witb CP more opportunities for exercise to enbance overall fitness, which is ciirrenth a fVicus of the Pediatric Section of the American Physical Therapy Association. Healthy People 2010. and the President s Council on Fitness.'^ The purpose of this study was to determine the 3-dimensional kinematics, electromyographic (EM(i) activity, gross mechanical efficiency (power output/metaholic inptit),-'** and perception of effort of constantload, low-intensity stationary recumbent cycling in adolescents with CP at GMFC:S levels III and IV compared with tho,se of adolescents witb TD. The hypotheses were that subjects with CP would show increased joint movement in the frontal and transverse planes, altered muscle activa- tion patterns, increased muscle cocontraction around the hip and knee, decreased gross mechanical efficiency, and greater perception of effort during cycling compared with subjects with TD. Method Subjects Twenty adolescents participated in the sttidy. Ten subjects (3 male, 7 female) had a diagnosis of spastic diplegic or quadriplegic CP (age [X±SD1 = 15,6± 1,8 years, body mass index=24.1±4.7), and 10 subjects (3 male, 7 female) were children with TD (age-14,9± 1.4 years, body mass index=22.6±5.4). Sixty percent of the subjects with CP and 40% of the subjects with TD were fnim minority poptilations. Subjects witb CP were recruited from Shriners Hospitals for Children, Philadelphia, Pa, and subjects with TD were recruited through advertisement. Subjects 18 years of age and oldt-r and a parent of subjects who were less than 18 years of age signed an informed consent form approved by the governing institutional review board (IRB), Subjects who were less tban 18 years of age signed an IRB-approved assent form. All 20 screened subjects met the inclusion and exclusion criteria for the study (Tab. 1). Procedure Each subject was tested while cycling on a stationary bicycle,* The bicycle was a compact free-standing stationary' cycle consisting of a base, adjustable-length crank amis with adjustable pedals, handlebars, and a control pad (Fig, 1), The pedals differed from standard hicycle pedals by having a full footplate, atid they differed in the location of the pedal spindle in relation to the toot. The pedal spindle is the point of pedal rotation in relation to the crank arm. • RtslonilivL-Thcrjpics Inc. 907 S St, Builimorc, MI) 21224, Volume 87 Number 5 Physical Therapy • 573 Biomechanics of Submaximal Recumbent Cycling in Adolescents With and Without CP Table 1. Inclusion and Exclusion Criteria Inclusion Exclusion Ages 13-19 y Ability to maintain an upright sitting pusilion with minimal suppon Ability to commit to up to 4 sessions of training or testing Visuopcrceptiia] skills and cognitive and communication skills sufficient to follow multipk-step commands and to attend to tasks associated with data collection Diagnosis ol" spastic CP and classiJifd as level III or W using the Gross Motor Function Classification System'' Lower-extremity onhopcdic siirger) or traumatic fracture within the past 6 mo Lower-extremity joint pain during cycling Spinal fusion extending to the pelvis Hip. knee, or ankle joint instability or dislocation Lower-limb stress fracttjres in the past year Symptomatic or current diagnosis of cardiac disease as assessed hy the American Heart Association guidelines for cardiac history^ Uncontrolled .seizure disorder Current pulmonary disease or astlima and taking oral steroids or hospitalizeti for an acute episode in the past 6 mo Severe spasticity in legs (score of ^ 4 on the Modified Ashworth Scale)'' Severely limited joint range of motion or irreversible muscle contractures that prevented safe positioning on the cycle" Diagnosis of athetoid or ataxic CP'' " Maron B|, Thompson PD, Puffer )C, et al. Cardiovascular preparticipation screening of competitive athletes: a statement for health professionais from the Sudden Death Committee (clinical cardiology) and Congenital Cardiac Defects Committee (cardiovascular disease in the young), American Heart Association, Circulation. 1996;94:850-856. '' Subjects with cerebral palsy (CP) only. and the pedal spindle on a standani bicycle pedal is located at the plantar surface of the toot. In contrast, the pedal spindle on the stationary' hieycle used in this study was located closer to the lateral malleolus. The foot was placed on a footplate that was located 5.S cm distal to the pedal spindle and was attached to the pedal spindle through a metal frame. Because the free-standing hicyele had no seat, suhjects were seated on a therapy heneh^ attaehed to the hase of the hicyele through an adjustahle bar (Fig. 1). All suhjeets plaeet! their hands on handgrips mounted on the sides of the bench. The speeifie ranges for adjustability of the hack and the bar eonnecting the hieycle to the hench were determined hy reviewing reported anthropometric data for children with TD. ages 6 to 18 years. "^ Data on children younger than those in this study were ineluded because children with CP tend to be shorter and lighter than their age-matehed peers with TD.^" The bicycle was adjusted for each subject individually based upon anthropometric measurements (I ig. 2). The foot was positioned so that the second metatarsal head was aligned with the pedal spindle to maximi/:e ankle power.^' This position was set by manipulating the footplate fastened with Velero'' to the pedal. The position of the footplate also was manipulated on the pedal to aeeommodate any lower-extremity rotational deformities for the suhjeets with CP. The footplate was rotated until the knee was aligned statically in the sagittal plane. The footplate was positioned flush to the medial side of the pedal for subjeets with TD heeause Figure 1. Subject v^fith cerebral palsy using the cycle in the motion analysis laboratory. A therapy bench was attached to the cycle with an adjustable bar that was set based on subject anthropometries. The seat back was reclined 25 degrees from vertical and was heightadjustable. The reflective markers on the subject and the pedal were used for the kinematic analysis. 574 • Physical Therapy Volume 87 Number 5 ^ Kaye Pn>ducts, 555 Dimmwks Mill Rd, Hillshorough, NC 27278. ' Velcro tISA Inc, 406 Brown Ave, Manchester, NH 03103. May 2007 Biomechanics of Submaximai Recumbent Cyciing in Adolescents With and Without CP no subject with TD displayed atypical torsiona! alijinment. Subjects' feet were .secured to tbe footplate witb soft straps, Eacb subject was instructed to pedal at a cadence of 30 revolutions per minute (rpm) and 60 rpm tising tbe c>cle s tachometer for feedback. Subjects wiib ID required one sbort training session (less than !() minutes), and subjects witb CP required 1 or 2 training sessions witb a maxiiiiuni time of 20 minutes per sessiun. All subjects were permitted to rest as needed. Kinematic and KMG data were collected in a motion analysis laboratory. Three trials of 10 to lSsec(mds' duration were conducted for eacb subject for eacb cadence once tbe targeted cadence was reacbed. Six of the 10 subjects with CP were able to attain and maintain 60 rpm for sbortduration trials (up to approximately 30 seconds), Tbe 4 subjects witb CP who could not cycle at 60 rpm in the mt)tion laboratory' could cycle at 50 qim and were tested only at this lower cadence. The resistance load provided during cycling was based on each subject s weight and was calculated using the following formula adapted from Dore et al*-: Load (in newton-meters) = 0.49 N/kg X body weigbt (in kilograms) x crank arm length (in meters). Kinematic Evaiuation Three-tlimensional kinematics of the bilateral bip, knee, and ankle were collected using a 7-caniera Vicon .370 motion analysis system^ and a standard marker .set on tbe pelvis (bilateral anterior superior iliac spines and sacrum) and tbe bilateral lower extremities^* (Fig. 1). A rigid body marker setup was used, and joint centers were calculated. Data were collected at 60 Hz and digitally fil' Vicon Motion Systems. 9 Spfctnim Pointe Or, Lake Forest. CA 92630. May 2007 Figure 2. Bicycle setup. Ail components were adjusted based on subject anthropometries, (1) Seat-to-pedal distance = 85% of the distance from the greater trochanter to the base of the calcaneus. (2) Seat-to-greater trochanter distance=15% of the distance from the greater trochanter to the base of the calcaneus. (3) Crank arm length = 30% of tibial length. The seat back was placed comfortably behind the subject while maintaining the seat to greater trochanter distance. tered using a low-pass filter of 6 Hz, Eacb subject underwent a series of antbropometric measures, wbicb were required to process the kinematic data within tbe Vicon model. A rotary encoder" mounted on tbe crank axis recorded the crank position during eacb revolution in increments of 0.3 degree, Tbe crank arm was calibrated in a horizontal position prior lo data collection, and 0 degrees was defined as tbe point at wbich tbe left crank arm was borizontal and farthest trom tbe subject, as shown in Figure 2, All data were synchronized and processed witb customized software using Vicon Plug-in-Gait (Version 1.9, Build 051).^ All kinematic data were analyzed in 1-degree increments of tbe crank position using customized .software written in MATIJ\.B version 7.5.' Electro myog ra p hy Surface EMG data were collected from 8 lower-extremity muscles (glu"tJS Digital Corp, 14(H) NE 136th Ave, ViincoiiviT. WA 9S684. ' 'nil- M:iiliW.irks Inc, 3 Apple Hill Dr, Natick, MA 017(>()2(198. teus maximus, rectus femoris, vastus lateralis, medial ham.strings. biceps femoris. anterior tibialis. lateral ga.strocnemius, and soleus) bilaterally using standardized placement locations.^' Tbese muscles were selected beeause tbey are major contributors to cycling in adults.*<-'^' Tbe EMC. data were used only to determine muscle timing and co-contraction during cycling. Tbe EMG data were collected at 1,200 Hz using a Motion Lab Systems MA-30() surface EMCi recording system," Each EMG sensor (MA-310'*) consisted of 2 circular, stainless steel, dry button electrode ciintacts (12-mm diameter) tbat were preattacbed to double-differential preamplifiers IiKated witliin the electrode housing. The EMG data were normalized across subjects by establisbing a quiet ba.seline for each subject Ibr 6 seconds. Tbe EM(i data were digitally filtered using a band-pass filter of 20 to 350 Hz. To tletermine the otiset and offset of muscle activity, EMG data were rectified and then " Motion Lab Systems, i'i(i45 Old Hamnionil Hwy, Baton Rouge, LA 70816-1244, Volume 87 Number 5 Physical Therapy • 575 Biomechanics of Submaximai Recumbent Cyciing in Adolescents With and Without CP smoothed using a second-order lowpass Butterworth filter witb phase correction and a cutoff frequency of 10 Hz to create a linear envelope. The linear envelope tben was analyzed using 25-miIlisecond moving square windows. If the mean voltage witbin each 25-millisecond window was at least 3 standard deviations above tbe mean voltage during the quiet baseline, tbe muscle was identified as being active during that time period.^" ^" From the data, tbe crank positions for tbe onset and offset of muscle activity were determined in 0.3-degree increments for eacb muscle and eacb subject. Tbe duration of activity (in degrees) also was calculated. Periods of co-contraction around each joint were identified based on tbe percentage of the cycling revolution in wbich each of 6 agonist and antagonist pairings around the biiateral hip and knee and tbe atikle were co-contracting. These pairings were the rectus femoris and biceps femoris muscles, tbe rectus femoris and medial bam.string muscles, the vastus lateralis and biceps femoris muscles, tbe vastus lateralis and medial bamstring muscles, the anterior tibialis and gastrocncmius muscles, and the anterior tibialis and soleus muscles. Energy Expenditure and Gross Mechanicai Efficiency Energy expenditure data were collected via tbe breath-by-breatb method utilizing a SensorMedics Vmax29 metabolic cart^^ witb subjects fasting for at least 2 bours prior to testmg. Subjects wore a small airtigbt facemask** over tbe mouth and nose that beld tbe flow sensor used to measured tbe volume of oxygen consumed (in milliliters per kilogram of body weigbt) (Voykg) for each breath. A gel liner** was placed inside the edges of the mask to ensure that air passed through tbe flow sensor and did not escape around tbe edges of the mask. The Vo2/kg measurements were obtained under 4 consecutive conditions: (1) sitting quietly for S minutes to establisb resting values, (2) cycling at the desired cadence for 1 minute to allow the body to warm up. (3) cycling at the desired cadence for 5 minutes, and (4) sitting quietly to establisb 3 minutes of recovery values. Power output data recorded once per second were dow^nloaded from customized software on a pocket personal computer linked to the bicycle's electronics. Following tbe test, gross mechanical efficiency was calctilated by dividing tbe average power output (in watts) by the average metabolic input (in volume of oxygen consumed per kilogram of body weigbt) across the entire 5-niinute cycling test. Perception of Effort Following eacb energy expenditure testing session, subjects were asked to rate their perception of effort using the c:bildren s OMNI Scale of Perceived Exertion.^'' There are multiple versions of the OMNI scale depicting children doing a variety of activities. The version used in tbis study sbows a cbild riding a bicycle upbill witb a score of 0 ("not tired at all ) at the bottom of the hill and a score of 10 ("very, very tired") at tbe top of tbe bill and has tbe child rate tbe exercise based on bow tired he or sbe feels.^'-* Tbe Children's OMNI Scale of Perceived Exertion bas been shown to yield reliable data in a study witb adolescent girls'" and vahd data for cbildren ages 8 to 12 years of mixed sexes and races." matic data were selected for analysis for each cadence for eacb subject. All data for the left ;md right sides were analyzed separately, and leftand right-side data were not c<jmpared. For brevity, only the left-side data are presented. For all data, rank transformations usiiig normalized ranks were performed prior to analysis secondary to a nonnormal distribution.'- A P value of less tban ,05 was accepted for significance. For variables witb multiple measures (ie. 16 muscles), tbe accepted P value was determined by dividing .05 by tbat ntimber. Kinematic data were analyzed using 3-way mixed-model analyses of variance (ANOVAs) witb crank position used as a random factor to determine differences in the position of tbe joint (in degrees) based on grotip, cadence, and crank position in 1-degree increments. The inclusion of crank position in tbe analysis allows tbe comparison of the kinematic curves as a wbole, accotinting for differences in joint excursions and timing simultaneously. For FMG data, circular / tests using t>riana 2.0^^ were performed to determine differences in tbe crank position (in ().3-degree increments) at wbicb onset and offset of muscle activity occurred based on group and cadence. A Mardia-Watson-Wbeeler test tising rank transformations was used due to tbe nonnormal distribtition of the data,^^ A 2-way ANOVA for onset and offset data was not performed because a model for this statistic has not yet been developed for circulac data. To analyze tbe duration of muscle activity\ a 2-way ANOVA basetl on grotip and cadence was performed. Finally, an analysis of covariance (ANCOVA) based on grotip and targeted cadence with actual cadence as a covariate was used for the Data Anaiysis " SensorMedics Corp, 22745 Savi Ranch Pk\, Yorha Linda, CA 92887. ** Hans Rudolph Inc, 7200 Wyandotte, Kansas, MO 64114. 576 • Physical Therapy Volume 87 For kinematic and EMG analysis, 5 cycling revolutions closest to tbe targeted cadence witb complete kine- Number 5 '* Compiiiinji Scr\'ices, 8S Nant-y-Felin Pcntnifth, Isk- of Anglesey, LL75 8tIV, Wales, tinited Kingdom. May 2007 Biomechanics of Submaximal Recumbent Cyciing in Adoiescents With and Without CP Tabie 2. Statistical Results (P Values) for the Kinematic Data" Variable Croup Cadence Crank Position Croup X Cadence Croup X Crank Position Croup X Crank Position x Cadence Ix.'lt hip tiexion ami exteniiion .8767 <.OOO1 <.OOO1 .0009 <.OOO1 ,().-4()0 I.c-ri hip addticiion and ahdiiciion .7649 <.OOO1 .8664 .0035 <.OOO1 ,6809 l.eli hip nicdial (internal) and lateral (external) rotaiion .1040 <.OOO1 <.OOO1 <.32O2 <.0O01 <.OOO1 Ij;ft knee llexion and extension .S121 <.OOO1 <.OOO1 .1722 <.OOO1 ,2217 U'fl knee varus and valgus . 1570 <.OOO1 <.OOO1 <.OOO1 <.OOO1 <.OOO1 Lffi ankle dorsitlexion and plantar flexion . 1697 <.OOO1 <.OOO1 <.OOO1 <.OOO1 <.OOO1 " The vdlues in bold type were significant (P<.004 for significance due to 12 joint motions being studied overall). The results that include the crank position (in degrees) reflect the comparison of the kinematic curves as a whole. analysis of efficiency and perception of effort due to differences in cadences achieved between groups tluring the attempted (lO-rpm energy expenditttre test, Tliere were no differences in achieved cadences hetween groups for tbe sborterdtiration (10-15 seconds) trials for assessing joint kinematics and EMG activity in tbe motion laboratory, so an AN<X)VA was not needed for analyzing those data. action). In tbat case, there were differences in all joint motions, indicating tbat kinematic curves were different. There also were differences in 3 of 6 joint motions wbcn looking at the interaction of group, crank position, and .speed. Post hoc analyses were not performed for the interactions involving the crank position dtie to tbe large numbers of comparisons tbat would be required, greatly reducing tbe P value needed for significance. Resuits Ditlerences were seen between groups and cadences for joint kinematics, muscle activity, and energy expenditure dtiring cycling. As compared with subjects with TD, subjects with CV bad increased joint movement in tbe frontal and transverse planes and altered sagittal pUuie kinematics, Electn)m) (jgraphic activity W;LS prolonged, cocontraction was increased, iuid efficiency was k)wer for the subjects witb CP. Kinematics Figures 3 and 4 display tbe joint angles of the left lower extremity throughout the c-ycling revolution for each group and eacb cadence. In additi<}n, tbere were differences between groups in the position of tbe foot in tbe transverse plane, witb an average of 18,8±10.'> degrees of lateral (external) rotation for subjects with TD and 31.0± 18.0 degrees of lateral rotation for subjects witb CP iP=.0l5). Because the foot was fixed to tbe footplate, minimal mcjtion was permitted in this plane. joint kinematics of tbe left lower extremit) differed based on cadence and crank position and interactions involving gnjup. crank position, and cadence (Tab. 2). No differences were seen between groups unless crank position was taken into account (group X crank position inter- Subjects with CP had earlier onsets, later offsets, and longer durations of muscle activity for some muscles of tbe left lower extremity compared witb subjects witb TD (Tab. 3). Onset, offset, and duration of muscle May 2007 E i ect ro myog ra p hy activity for some muscles were affected by increasing cadence, witb more activity seen at 60 rpm as compared witb 30 r^im. 1 igtire S displays the patterns for tbe onsets and offsets of EMG activity for eacb muscle for eacb group at eacli cadence. For subjects witb CP cycling at 60 rpm, average crank positions for tbe onsets and offsets of activity for tlie left lateral gastrocnemius muscle indicate that tbe muscle was working only briefly (Tab, 3). However, in looking at the data for each subject, tbe lateral gastrocnemius mtiscle was active for most of the cycling revolution. Therefore, the average values do not represent the activity of this muscie. F-igure 5 displays a more accurate representation of tbe activity of the lateral gaslrocnemius muscle for the subjects with CP at 60 rpm. In the analysis of agonist and antagonist muscle ccx'ontraction of tbe left lower extremity, subjects with CP had increased ct>contraction for 4 out of tbe 6 agonist and antagonist pairings compared with subjects with TD, atid co-contraction was greater wben cycling at 60 rpm compared witb 30 rjim for all subjects for 4 out of the 6 pairings (Fig, 6). Stibjects with CP also had a greater increase in co-contraction witb in- Volume 87 Number 5 Physical Therapy • 577 Biomechanics of Submaximal Recumbent Cycling in Adoiescents With and Without CP creasing cadence (group X cadence interaction) compared with subjects with TD for all 6 pairings, Bonferroni post hoc testing showed dilfcrences (P<.0042) in co-contraction percentage between tbe subjects witb TD and the sttbjects witb C:P wben cyciing at 60 rpm for all 6 significant pairings. Left Hip Sagittai Piane Flex 90 85 S 80 75 70 65 0 Energy Expenditure and Cross iVlechanicai Efficiency 30 60 90 120 150 180 210 240 270 300 330 360 Degrees Left Hip Frontai Piane Add — -12 Abd -16 1 ^_^^^ i 1— 1 1 1 r——1 1 1 -TD30 CP30 TD60 CP60 1 ' 1 0 30 60 90 120 150 180 210 240 270 300 330 360 Degrees Left Hip Transverse Plane MR — TD30 -CP30 TD60 CP60 Using cadence as a covariate, efficiency was greater for tbe subjects witb TD tban for the subjects witb CP (F=7.(>6, /'=.O127) and greater for all subjects when cycling at 30 rpm compared with tbe attempts at 60 rpm (F=6,5I, /^=.0068) (Fig. 7), 1 here was no interaction effect of group and cadence (F=0.41, P=.5288). All subjects could all cycle at 30 rpm (subjects with TD at 3O.6±l.l rpm and subjects witb f.P at 29.4±3,O rpm) throtigbout tbe energy expenditure test. However, during tbe attempted 60-rpm test, .subjects witb CP were unalilc to maintain tbis cadence tbrotigbout tbe test. The S .subjects witb CP who attempted Cbe energy expenditure test at 60 rpm cycled at 46.5±5.8 rptn, wbereas tbe subjects witb TI^ cycled at 57,9:^1,2 rpm. Tliere were no differences between groups (F=2.88, P=A605) or between cadences (F=5,O6, P=.U86) 180 210 240 270 300 330 360 0 30 60 90 120 150 for perceived effort as measured Degrees witb the Cliildren s OMNI Scale of Figure 3. Joint kinematics of the left hip for all subjects. Zero degrees is the point at which the left Perceived Exertion, and tbere was (F=36.4, crank arm was horizontal and farthest from the subject, as shown in Figure 2, Qualitative no interaction effect differences are evident, demonstrating the differences in magnitude and timing be- /'=.3694). Subjects witb TD retween groups and cadences. Subjects with cerebral palsy (CP) had greater excursions ported median OMNI scores of 0 of motion in the frontal and transverse planes, greater hip flexion, greater knee exten- (range=0-1) and 1 (r.mge=0-6) at sion, and greater dorsiflexion compared with the subjects with typical development 30 rpm and 60 rpm, respectively, (TD). The positive direction indicates flexion, adduction, and medial (internal) rotation for sagittal, frontal, and transverse planes, respectively, Flex=flexion, Add=adduction, and subjects with CP reported meAbd = abduction, MR^medial rotation, LR^Iateral (external) rotation, TD30^subjects dian (")MNI scores of 1 (range=0-6) with TD at cadence of 30 rpm, CP30=subjects with CP at cadence of 30 rpm, and S (range=2-10) at 30 rpm and TD60=subjects with TD at cadence of 60 rpm, CP60=subjects with CP at cadence of tbe attempted 60 rpm. respectively. 60 rpm. With the sample size and standard deviations in this study and witb alpha=.O5 (2-tailed) and 80% power, a mean score of 4.48 in tbe subjects 578 • Physical Therapy Volume 87 Number 5 May 2007 Biomechanics of Submaximal Recumbent Cycling in Adoiescents With and Without CP with CP (effect size=2.38) would bave been necessary' to attain statistical significance in OMNI scores between groups. Left Knee Sagittal Plane -7D30 Discussion Differences were seen in cycling biomecbanics between adolescents witb CP and adolescents witb TD. Subjects were successful with short botits of cycling at 30 or 60 rpm in tbis study, and no subjects were excluded from tbe study due to failure to leam to cycle. It should be noted that the cycle design used in tbis study is diiferent from tbat t}'pically used in cycling studies, and tbe results may reflect tbis specific design, Altbougb only tbe left-side data are presented, results for tbe right iower extremity were overall similar to those of the left lower extremity. -CP30 TD60 CP60 30 60 90 120 150 180 210 240 270 300 330 360 Degrees Left Knee Frontal Plane Var -TO30 -CP30 —TD60 —CP60 1 Kinematics 30 60 1 1 1 i T 90 120 150 180 210 240 270 300 330 360 Subjects witb CP displayed differences in joint kinematics around the bip, knee, and ankle in all 3 planes of motion compared witb the subjects witb TD. Altbougb tbe findings of differences in the frotital and transverse planes were anticipated due to differences in gait kinematics in tbese planes,*'-^'^* differences in tbe sagittal plane of increased hip flexion and increased knee extension for tbe subjects with CP were unanticipated because the positioning on the bicycle was based on antbropometrics. However, ankle dorsiflexion was increased, tbus effectively shortening the limb, and therefore might bave affected tbe position of tbe bip and knee in tbe sagittal plane. Tbe subjects with ('P may bave bad tbis increased ankle dorsiflexion due to decrea.sed strengtb and motor control of tbe plantar flexors, Joint kinematics of the left knee and ankle for all subjects. Zero degrees is the point at which the left crank arm was horizontal and farthest from the subject, as shown in Figure 2. Qualitative differences are evident, demonstrating the differences in magnitude and timing between groups and cadences. The positive direction indicates flexion (dorsiflexion) and varus for sagittal and frontal planes, respectively, Flex^flexion, Var=varus, Val=valgus, Df=dorsifiexion, Pf = plantar flexion. TD30=subjects with TD at cadence of 30 rpm, CP30=subjects with CP at cadence of 30 rpm, TD60=subjects with TD at cadence of 60 rpm, CP60=subjects with CP at cadence of 60 rpm. Tbe differences in joint kinematics may have been due to decreased strengtb and motor control for tbe subjects witb ("P. Interestingly, tbe stibjects with CP could physically attain tbe degree of bip lateral rotation achieved by tbe subjects witb TD, demonstrating that ROM was not limiting tbe ability to reach tliis joint position. Therefore, issues sucb as motor control and strengtb may be May 2007 Degrees Left Ankle Sagittai Plane -7D30 -CP30 —TD60 —CP60 1 i 1 r 30 60 90 120 150 180 210 240 270 300 330 360 Degrees Figure 4. more relevant factors. Muscles can increase or decrease the amouni of rotation observed during functional movements in people witb bony rotational deformities,** Thus, muscle Volume 87 Number 5 Physical Therapy • 579 Biomecbanics of Submaximal Recumbent Cyciing in Adoiescents With and Witbout CP Q _ M » u i „ ~ •v -i fl fl fl 0 fO "J 5 fj • 1 76.4 tl tl r- •0 s tl -?• If d i~i r-i IN f. c 0 fi tl o i rr, tf l I^ I f -o ^ ^ rf\ 0 *^ *. tn e Q E Xi • 0 tl tl fl rr. M >H I ; *J y 5 P ** ^ a 0t a-. IM 2; "^. oc 5. -n 03 fl rTJ T j 0 •r, fl t-- r-t tl OS rr. =0 ir ir> tl •r. ft p -o ~ _^ tl up^ l-i tl M "T' OJ _0j d fl ti t- CO ff. ad if •T I f X tl - tl \r- - • .™m in u. o a. 0 Q. 5 £ ^j 0 ago. '4—J Off! V "0 « :ion J 31 fi. U M fl ir n-^ OS •r 0 •-r ^ • IN fl tl fl „ t- 30 3t l +1 eu? 1--. tl s tl M. 0 rr. r- 307. "> 83.7 tl •!- I I f tl 1 • i• t 1 t-. -r •ri ir tl •s tl 1 cv r^ u- =>? tl fl fl I f 0 a. E § 1^ £• 0 w s 0 " 0 U .. 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IJ ^ 0 H cro 92,0 1 -sfl £•0 T3 1^ !r 'Z if- CC 27.6 & ^ c a 5* ft S •r, — Q M "5: If - 0 ?• o> 75.9 n tl 1-; tl <* fl O; h- •'•. •'*: ?: •• "r U tl tfl 74.0 S 199 ' ^ tj 50,8 c "^ 180, 11 28. ^ ^ B"1 0 J! 62.1 ro <u u S II ^• P •u • c u > 9 3 "^ 'tj F "ra -T ~T ii: IN tl p ~ •0 Z -n I f 85. 5 Tl ai 1." i*^ rt. 6.6 ^ +1 il ... tl' 52. t 3.9 -gi '8.8 x_ •p 0 III). •0 2.7 viati( "i activity rather than rotational deformities may have led to some of the differences seen. In addition, it is possible tbat foot position altered tbe kinematics at the more proximal joints. The goal was to position the foot to accommodate deformities to allow the hip and knee to be better aligned in the sagittal plane. Because cycling occurs primarily in the sagittal plane, motion out of this plane may place additional stresses on the liip and knee joints. Further study is needed to detennine the forces to which these joint are exposed. si rf-. r- tl nj ™ •I- ^ V a 1E •o h: t X tl pn • U a e Q tl • --t (L 1-1 IN fi -T m I f C * ^o w u * "c" +1 tl T t- J a. W « n ^.0 & a 1 5,3 3 a f 1' 15. 10 •": ^1 100,1 c •£ n U fT. >- 3 S & ® "D ' " 1^ « f-i 'I If 1 IL S "5 0 5 g E: 08. «• 0 98. M a 19.6 a. W fl 1)9 irtl ^^ 0 ,3 S ±41.7 V i% 1^ ^ TO ^ II 'j 2^ •= £ — "D Electromyography Tlie EMG patterns differed for some muscles between groups. In general, subjects witb CP displayed earlier onset and later offset of muscle activity within the cycling revolution than did subjects with TD (Tab. 3, Fig. 5). Tbese results are similar to those of Kaplan,^" who performed a more limited biomechanical study comparing cycling between children with and without C\*. Again, subjects with CP may have experienced differences due to decreased strengtb and motor control and therefore activated as many muscles as possible to both stabilize the joints anti allow movement. This pattem of increased activity may contribute to decreased efficiency' and greater effort during cycling and may help to explain why some cbildren with CP may have difficulty witb the task. Tbere appeared to be differences in bow subjects with TD and subjects with CP used their muscles while cycling. For tbe subjects witb TD, the rectus femoris and vastus lateralis muscles appeared to act mainly as knee extensors, whereas the subjects witb CP appeared to use tbe rectus femoris muscle for hip flexion in addition to using both muscles for knee extension. Both groups appeared to use the medial hamstring and biceps femoris muscles for a combination of hip extension and May 2007 Biomechanics of Submaximal Recumbent Cycling in Adolescents With and Without CP ^ 1 Extensors ^ 1 Flexors I I No Activity Figure 5. Polar plots of nnean onsets and offsets of muscle activity of the left lower extremity for all subjects. Zero degrees occurred when the left crank arnn was horizontal and farthest from the subject (Fig. 2). Muscles other than the gluteus maximus were labeled as primary extensors and flexors based on their actions at the knee and at the ankle. The duration of activity may differ from those shown in Table 3 because the durations here represent the difference between mean onset and mean offset. From these plots, the relationship of activity of muscles, including co-contraction, can be seen. The innermost circle represents when hip flexion and extension occurred in order to identify the phase. The stick figures show the approximate position of the lower extremities at that point in the revolution, and the arrow indicates forward movement of the crank when viewed from the right side of the cycle. 1 =gluteus maximus muscle, 2 = rectus femoris muscle, 3=vastus lateralis muscle, 4^medial hamstring muscle, 5 = biceps femoris muscle, 6=anterior tibialis muscle, 7^lateral gastrocnemius muscle, 8=soleus muscle. TD30=subjects with typical development (TD) at cadence of 30 rpm, CP30=subjects with cerebral palsy (CP) at cadence of 30 rpm, TD60=subjects with TD at cadence of 60 rpm, CP60=subjects with CP at cadence of 60 rpm. hip deceleration; however, for knee flexion, subjects with TD appeared to use the medial hamstring muscles, whereas the subjects w^ith CP used the hiceps femoris muscle. May 2007 Around the ankle, subjects with TD used the anterior tibialis muscle only during flexion, but the subjects with CP used tliis muscle throughout the revolution except for a brief period near the end ofthe extension phase. Subjects with TD used the gastrocneniius and soleus muscles primarily during the extension phase and into the flexion phase at the higher ca- Volume 87 Number 5 Physical Therapy 581 Biomechanics of Submaximal Recumbent Cycling in Adolescents With and Without CP Percentage of Co-contraction a,b,c rectus/biceps rectus/mham viat/biceps vtat/mham TA/gastroc TA/sol Figure 6. Percentage (mean and standard deviation) of the cycling revolution in which co-contraction occurred for each agonist and antagonist pairing around the left knee and ankle for each subject. Subjects with cerebral palsy had increased co-contraction compared with the subjects with typical development, and all subjects displayed increased co-contraction when cycling at 60 rpm compared with 30 rpm. Rectus=rectus femoris muscle, biceps^biceps femoris muscle, vlat=vastus lateralis muscle, mham = medial hamstring muscle, TA=anterior tibialis muscle, gastroc^gastrocnemius muscle, sol^soleus muscle. "Significant main effect of group, ^Significant main effect of cadence. 'Interaction of group and cadence. Significance defined as P<.004 due to 12 agonist and antagonist pairings being studied (6 per side). TD30=subjects with TD at cadence of 30 rpm, CP30 = subjects with CP at cadence of 30 rpm, TD60^subjects with TD at cadence of 60 rpm, CP60^subjects with CP at cadence of 60 rpm. dence, potentially as a decelerator or a knee flexor. Subjects with C;P used these muscles primarily during the extension phase at 30 rpm but increased the activity to nearly continuous at 60 rpm. These differences may bave been due to poor motor planning and the inability to dissociate the activity of some muscles, resulting in ct>contraction of muscles around a joint. For the suhjects with CP, it was difficult to determine which muscle was contributing primarily to the motion observed. In order to determine tbis, future work would need to examine the magnitude of EMG activity.-''-^^'^^ Greater co-contraction of muscles around the hip, knee, and ankle was seen in subjects with CP compared with subjects with TD. Cocontraction has been reported to occur normally during cycling in hoth children^" and adults^' who are healthy. The increase in cocontraction for the subjects with CP may reflect an attempt to stabilize 582 Efficiency n=10 n=5 TD30 CP30 TD60 CP60 Figure 7. Cycling efficiency (mean and standard deviation) for all subjects. When actual cadence (rather than targeted cadence) was used as a covariate, there were significant main effects of group (P=.O127) and cadence (P=.OO68); however, the interaction was nol significant, Vo2=volume of oxygen consumed, TD30=subjects with typical development (TD) at cadence of 30 rpm, CP30^subjects with cerebral palsy (CP) at cadence of 30 rpm, TD60^subjects with TD at cadence of 60 rpm, CP60=subjects with CP at cadence of 60 rpm. Physical Therapy Volume 87 Number 5 May 2007 Biomechanics of Submaximal Recumbent Cycling in Adolescents With and Without CP the joints wbile allowing movement to occur. In addition, co-contraction increased for subjects with CP when cycling at (>() rpm compared with cycling at 30 rpm to a greater extent than was seen for the subjects with ID, indicating a greater task demand and the potential need for greater stabilization of joints at the higher cadence. In this study, onset of muscle activity was determined by EMC; amplitude being at least 3 standard deviations above a c|iiiet baseline. For most subjects, obtaining a quiei baseline was not problematic; however, a quiet baseline was unobtainable for every muscle for every subject, which may have undere.stimated muscle activity, hi addition, subjects with CP often showed constant or almost constant activity that was 3 standard deviations above the baseline tbroughout tlie c)cling revolution. In some of these subjects, phasic increases in muscle activity could be visually identified above this level of activity, I'herefore. the muscle activity likely represented a combination of postural demands as well as tbe demands required for cycling. Future work should determine tbe differences between postunil demands on muscles versus demands for activity. In contrast, some subjects with CP displayed continuous, nonphasic activity throughout the cycling revolution. This finding is similar to what was described by Kaplan,^'' who suggested Ihat the coordination of the cycling pattern may be less affected by continuous activit>' of some muscles due to the strength and timing of the muscles that are acting phasically. However, this pattern may be relatively inefficient for cycling. In addition, subjects witb CP in ihe present study displayed cocontraction around joints almost continuously for some muscle combinations, especially around the anMay 2007 kle, with a greater effect at the higher cadence. The subjects with CP may have been using cocontraction to stabilize the foot and ankle. Minimal dorsiflexion and plantar-fiexion movement was noted tor both groups. It is possible that the pedal design used in this study affected ankle motion, as it was a full-length pedal in which the entire foot maintained contact with the surface. In addition, the pedal weight favored movement toward dorsiflexion, and the location of the pedal spindle in relation to the foot differed. Perhaps greater stabilization ofthe foot and ankle was required by all subjects due to tbis pedal design, because subjects with TD displayed greater co-contraction around the ankle than that reported in the literature for cycling in adults who are healthy.*^ However, Kaplan-" reported similar percentages of cocontraction around the ankle in children with TD, as was seen with the suhjects with TD in this study. Subjects in tbis study were adolescents, so it is unknown whether cocontraction is related to an immature system or to pedal design. As gait matures hefore adolescence,^*' it would be anticipated that adolescents would bebave more like adults while c-ycling, which recjuires a similar repetitive task but witb more constraints to movement than with gait. Efficiency Suhjects with TD cycled more efficiently than did the suhjects with CP, and all subjects were more efficient when cycling at 30 rpm compared with cycling when attempting 60 rpm, hicreased viscous resi.stance to motion of contracting muscle filaments'^ as well as failure of a muscle to relax between contractions could potentially contribute to an increased metabolic cost of cycling.'" These issues may have contributed to a decreased efficiency for the subjects with CP due to increased met- abolic demand. In addition, spasticity can iticrease the energy demand due to involuntary movements, the need to fight the spasticity in order to move, and the need to stabilize the hody on a cycle.'** Subjects with CP in the present study displayed greater muscle co-contraction than subjects with TD, which may have contributed to the decrease in efficiency seen in the suhjects with CP. When attempting the 60 rpm cadence, subjects with (JP and with TD cycled with fairly comparable efficiency (1.4±0.9 and 1.6±0.8 WM>,, respectively) when directly comparing the values. However, although tlie targeted cadence for each group was the same (ie, 60 rpm), subjects with CP had difficulty attaining and maintaining this cadence during the 5-minute cycling test, despite heing able to achieve this cadence during the short trials in the motion analysis laboratory. In addition, efficiency declines with increasing cycling cadence due to the linearly or exponentially increased demand for oxygen.-'"'-'^' Therefore, subjects with CP in the present study may have cycled less efficiently if they had been able to cycle at 60 rpm during the S-minute cycling test. No differences were seen between groups or cadences in the perce(> tion of effort as measured by the Children's OMNI Scale of Perceived Exertion. Unexpectedly, several subjects with CP reported a low perception of effort using the OMNI scale during the S-minute cycling test. Seven of the 10 subjects with CP reported an OMNI score of 2 or less ( a little tired" or less) for the 30 rpm test, and 1 out of 6 subjects reported this score for the attempted 60 rpm test. There was variability- among tbe other subjects, with scores of 3, *), and 6 for the remaining 3 subjects at the 30 rpm test and scores of 5, 6, and 10 for the remaining i subjects during the attempted 60 rpm test. Volume 87 Number 5 Physical Therapy • 583 Biomechanics of Submaximal Recumbent Cycling in Adolescents With and Without CP This variability was unanticipated due to the similar task demand among subjects. As the resistance provided was based on body weight, basing the resistance on lean body mass or muscle volume may have been more appropriate due to potential differences in the proportion of fat and lean tissue among subjects. All subjects with TD reported OMNI scores of 0 or I at 30 rpm. There was greater variability at 60 rpm, with 6 of the 10 .subjects reporting scores of 0 or 1, and the remaining suhjeets reporting scores of 3, 4, 5, and 6. Further research is needed to study lead to improvements in strength specific outcomes, including strength- and cardiovascular conditioning in ening and cardiovjLscular improve- adolescents with CP, ments. Based on the results of this study, adolescents with CP may not This work was completed in partial fulfillbe able to cycle for longer periods of ment of the requirements for Dr )ofinston's time due to inefficiency of tbe task. doctoral degree at Temple University, Altbough Uiis may lead to liigher heart authors provided concept/idea/research rates, which are desirahle for cardio- All design and project management. Dr vascular benefits, it may lead to early lohnston and Dr Earr provided writing and fatigue as well as dissatisfaction with data analysis, Dr Johnston and Dr Lee provided data collection and fund procurement, cycling as a mode of exercise. Dr Johnston provided subjects. Dr Lee provided facilities/equipment, Dr Barr and Dr Lee provided institutional liaisons and consultation (including review of manuscript before submission), Dr Johnston acknowledges her doctoral dissertation committee members Kim Nixon-Cave, PT, PhD, and Brian Clark, PhD, as well as the following people from Shriners Hospitals for Children who assisted in many different ways: Carrie Stackhouse, MS, Emily Slater, MS, Richard Lauer, PhD, Brian Smith, MS, )ames McCarthy, MD, Kyle Watson, PT, DPT, and Patricia Shewokis, PhD (also at Drexel University). The authors also acknowledge |ohn Caughan, PhD, of Temple University, who assisted with the statistical analysis. In addition, some adolescents in this study were not able to achieve cadences higher than 30 rpm. Cycling at this low cadence may prevent the Training and Resistance In this study, all subjects received attainment of a heart rate high enough sbort training sessions, with a maxi- to achieve the cardiovascular l>enemum of 2 sessions required to ac- fits of exercise. Altered kinematics, complish the task demands. Because pn>longed muscle activity, and cothe task and cycle design were contraction likely interfered witii tlie novel, increased practice may have ability to cycle efficiently, and metlv led to differences in cycling patterns, ods to encourage appropriate muscle including joint kinematics, muscle activity may be beneficial. Extended activity, co-contniction, and effi- training and cues such as "push out" at ciency. With practice, co-contraction the appropriate time may lead to im- This project received funding from Shriners may have decreased in all subjects, provements in cycling. Another pos- Hospitals for Children (grant 8530) and from potentially leading to increased effi- sibility' is the tise of electrical stimula- a Clinical Research Grant from the Pediatric ciency, Future work should examine tion botb as a way of providing Section of the American Physical Therapy the changes seen with increased information on appropriate muscle Association, Dr Lee also was supported by Institutes of Health grant timing as well as to activate mus- National practice. HD043859. cles to acbieve a higher cadence. This article was received September 5, 2006, Resistance In this study w^as based on Further research is needed to de- arid was accepted January 4, 2007. termine whether techniques such eacb subject's body weight in order DOI: 10.2522/pti.20060261 to allow comparison between groups. as these can be successful However, this resistance may have been too great for tbe subjects witb Conclusions CP. Future work should examine cy- During cycling, adolescents witb CP References 1 Daniiimo DL, Martcllotta TL. Quintivan JM. cling biomechanics at differing levels displayed differences in joint kineAlx-I MF, Dfficitfi in eccentric versus conof resistance to determine Its effects. matics in all 3 planes, altered muscle centric torque in children with spiisiie (.erebral palsy, Med Sci .Sports lixetc. 201)1: Literature on cycling in adults who activation patterns, and increased co33:117-122, contraction compared with thei r are healthy has shown differences in 2 Burtner PA, Quails C, Woollacott MH. IVfuscycling efficiency'^" and EMG pat- peers with TD, all of which may have ele aciivaiLon characteristics of stance balcontrihuted to the decreased cycling terns'*^ with differing workloads, and ance control in children with spa,stic cerebral palsy, Cail Pasture. 1998:H:163-174, similar effects may be seen in sub- efficiency seen In the subjects witb 3 Uleck EK Orthopedic MuHcificiiietit in CeCP, Many of the differences seen jects witb CP. rebnii Paisy. London, I'nitei-I Kingdom: may be due to issues such as deMacKeith Press; \9H'^. creased strength and motor control 4 Woollacott MH, Runner P, Neural and Clinical Relevance musculoskeletal eontribiilions to the deAs diiferences were seen in kinemat- for the subjects with CP. The inforvelopment of stance balance control in typical children and in children with cea'ics, EMG, and efficiency, cycling in- mation from this study can assist in bral palsy, Aclii PcietiiatiSit/j/tl. I W6:416: the development of future interventerventions may provide different 18-62, benefits for adolescents with CP tion studies, which should examine compared with adolescents with TD. whether a cyciing intervention can 584 • Physical Therapy Volume 87 Number 5 May 2007 Biomechanics of Submaximai Recumbent Cyciing in Adolescents With and Without CP 5 Snssman Ml>. Cmuched gait consensus. In: Siiisni.in Ml>. t-d. llw Di[)U'^ic Child: hi'tjlniitioti utid Mtiriiififim-nt. Rost-mont, 111: AmtTkan Aciidt-my of Drthopacdic Sur6 Wren TA. Retliklsen S. Kay RM. Prevalence of specific gait abnomiiiliiics in chiltla'ii with txTchnil palsy: inllut-ncc of ceri'hral palsy siibiypc, age. and previitus surHfry.y PeiluitrOrtlMi/). 2(K)S:25:79-83. 7 Damiano DL, Quinlivan J, Owen BF, ct al. Spasticity versu.s strength in ccrebnil palsy: relationships anionj; involuntar>' resistance, voluntar)' torque, and motor function, liitrj Neuntl. 2()<)l;8(.suppl 20 Damiano DL, Vaughan CL, Abel MF. Mtiscle response to heavy resistance f xercise in children with spastic cerebral palsy. Der Med Chiid Neurol. 1995:37:731-739. 37 Di Fabio RP. Reliability of computerized surface electromyogniphy for determining the onset of mu.scle acti\ity. i'bys Wer. 1987:67:43-48. 21 Bell KJ, Oimpuu S, DeLiica PA, Romness MJ. Natural progression of gait in children with cerebral pals). J Pediatr Orthop. 2002:22:677-682. 38 Hodges PW, Bui IJH. A comparison of computer-ba.sed methods for the determination of onsc-t of muscle contraction using elect romyogniphj. l-tectroencephalo^r Clin Netirophysiol. 19*X.: 101:511-519. 22 Bottos M. heliciangeli A, Sciuto L, ft al. Functional status of adults with cerebntl palsy and implications for treatment of children. Dev Med Child Neurol. 2OO1;43: 516-528. 23 Palisano R, Kosenbaum P. Walter S, et al. Development and reliability' of a system to classify gross motor function in childa'n with cerfbral palsy. 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