What does the Ashworth scale really measure and are instrumented measures more valid and precise?

Transcription

1 Wht does the Ashworth scle relly mesure nd re instrumented mesures more vlid nd precise? Dine L Dmino* PhD PT; Jeffrey M Quinlivn ME; Bryn F Owen MS; Ptrici Pyne BS PT; Kren C Nelson MD; Mrk F Ael MD, University of Virgini, Deprtment of Orthopedics, Chrlottesville, VA, USA. *Correspondence to first uthor t Wshington University, Humn Performnce Lortory/Brnes-Jewish Hospitls, 4555 Forest Prk Prkwy, St. Louis, MO 6318, USA. E-mil: dld683@jc.org This study imed to explore the limittions of the Ashworth scle for mesuring spsticity. An isokinetic dynmometer to quntify resistnce to pssive stretch nd surfce EMG ws used to verify if stretch response occurred nd, if so, t wht joint ngle. The uthors sought to determine which components of pssive resistnce (mgnitude, rte of chnge, onset ngle of stretch, or velocity dependence) were most relted to Ashworth scores nd which were relted to motor function in cererl plsy (CP). Twenty-two individuls with spstic CP (11 mles, 11 femles; men ge 11.9 yers, SD 4.3) nd comprison group of nine children without CP (four mles, five femles; men ge 11.3 yers, SD 2.5)prticipted in the study. The group with CP included those with dignosis of spstic diplegi, hemiplegi, or qudriplegi, distriuted cross Gross Motor Functionl Clssifiction Levels. Procedures included: (1) clinicl ssessment t the knee joint, (2) functionl ssessments, nd (3) isokinetic ssessment of pssive resistnce torque in hmstrings nd qudriceps t three velocities. EMG dt were recorded simultneously to identify stretch responses. Detecting stretch responses using the Ashworth scle compred with instrumented mesures showed ner complete greement t extremes of the scle, with mrked inconsistencies in midrnge vlues. Ashworth scores were correlted with instrumented mesures, prticulrly for the qudriceps, with higher correltions to the rte of chnge in resistnce (stiffness) nd onset ngle of stretch thn to pek resistnce torque. Those with greter resistnce tended to hve poorer function with isokinetic reltions typiclly stronger. The Ashworth scle (Ashworth 1964) hs gined widespred clinicl cceptnce s mesure of spsticity of centrl or peripherl origin. Its use is lso reported frequently in clinicl trils documenting chnges in spsticity throughout the course of disese or s result of n intervention. The clssic description hd the exminer rte the mount of tone felt s lim ws moved pssively through its rc of motion (Tle I). Lter modifictions incorported n estimtion of how soon in the motion, nd how much during the motion, the resistnce ws felt (Bohnnon nd Smith 1987). To our knowledge, how this dded specifiction my hve ffected the vlidity of the scle for mesuring spsticity hs not een ddressed. An oserved tendency for scores to cluster in the mid-rnges hs led some uthors to spred out the middle portion of the scle (Bohnnon nd Smith 1987). However, poorer reliility my ccompny the greter discrimintory ility of this modifiction (Pndyn et l. 1999). Despite its shortcomings nd lck of consensus in the exct scoring, the Ashworth scle with ll of its vrints remins the stndrd with which other mesures of spsticity re compred. The clinicl import of the Ashworth scle hs not een well estlished nd is, in prt, enmeshed in the controversy s to whether spsticity hs significnt or cusl reltionship with motor performnce (Shrmnn 1977). Ashworth scores re consistently reduced in cererl plsy (CP) fter surgicl interventions designed specificlly to reduce spsticity (McLughlin et l. 1998, Butler et l. 2). However, ordinl scles such s the Ashworth my lck precision nd sensitivity for mesuring nd detecting smller degrees of, or chnges in spsticity. Even though the Ashworth scle purportedly guges the degree of spsticity, which y definition is heightened response to stretch tht is velocity dependent (Lnce 198), the test is performed t single, lthough modertely risk, speed. Even more importntly, the Ashworth scle does not quntify spsticity exclusively, if t ll; rther, it mesures pssive resistnce to motion tht my or my not e cused y heightened stretch response. In order to develop more vlid nd quntittive mesure of spsticity, or to identify components of spsticity or resistnce more precisely, multiple iomechnicl nd electrophysiologicl methods hve een developed. These methods include, ut re not limited to, H-reflex testing (Angel nd Hoffmn 1963), quntifiction of deep tendon reflexes (Zhng et l. 2) nd clonus (Hidler nd Rymer 1999), resonnt frequency tests (Price et l. 1991), rmp nd hold tests (Ktz nd Rymer 1989), pendulum tests (Bjd nd Vodonik 1984, Fowler et l. 2), nd instrumented torque mesurements during pssive motion t preset velocities (Broerg nd Grimy 1983, Firoozkhsh et l. 1993, Engserg et l. 1996, Perell et l. 1996, LMontgne et l. 1998, Akmn et l. 1999, Dmino et l. 21). Ech of these methods vries in the degree of expertise nd specil equipment required, the neurl or peripherl component mesured, the joints tht cn e tested, the reliility of the mesurements, nd the correltion of the prmeters otined with clinicl nd functionl mesures. Multiple reports hve een pulished descriing, vlidting, nd compring these mesures in vriety of ptient popultions (Ktz et l. 1992, Skinner 1992, Sehgl nd McGuire 1998). In this investigtion, the gol ws to determine the vlidity of the Ashworth scle y using n isokinetic dynmometer to quntify resistnce to pssive stretch in knee flexion nd extension, nd EMG recording to verify if stretch response 112 Developmentl Medicine & Child Neurology 22, 44:

2 occurred nd, if so, t wht joint ngle. Furthermore, we wnted to compre the multiple prmeters quntified through instrumenttion, such s mgnitude of resistnce, chnge in resistnce with ngle, onset ngle of stretch, nd velocity dependency of ech of these prmeters, with those otined y the Ashworth scle, nd lso to relte ech of these impirment mesures to vlidted functionl scles. We chose to employ n isokinetic device insted of other instrumented Angle mesures ecuse this method closely simultes the Ashworth scle; its use hs een reported s relile nd vlid in severl popultions nd it is cliniclly ccessile (Broerg nd Grimy 1983, Firoozkhsh et l. 1993, Perell et l. 1996, Dmino et l. 21). In this protocol, the isokinetic device ws used to move the knee joint pssively t three preset velocities through the rc of motion in flexion nd extension while resistnce torque ws mesured nd EMG dt were lso recorded to verify the stte of muscle ctivtion including the presence or sence of stretch responses. We hypothesized tht the severity of the Ashworth scores would e directly relted to the mgnitude nd rte of chnge in resistnce torque nd to n erlier ngle of onset of the stretch response. We further projected tht oth clinicl nd instrumented mesures would e relted to functionl severity in CP. Method PARTICIPANTS A totl of 31 individuls gve their consent to prticipte in this study including 22 (11 mles, 11 femles) ptients with spstic CP nd comprison group of nine (four mles, five femles) normlly developing children. The men ge for the children included here with CP ws 11.9 yers (SD 4.3 ) nd EMG Tle I: Originl Ashworth scle Score Description No increse in tone 1 Slight increse in tone giving ctch when the lim is moved in flexion or extension 2 More mrked increse in tone ut lim esily flexed 3 Considerle increse in tone, pssive movement difficult 4 Lim rigid in flexion or extension Angle Tle II: Numer of prticipnts with CP per Gross Motor Functionl Clssifiction System (GMFCS) level GMFCS level Numer of children I 1 II 1 III 8 IV V 3 EMG Figure 1: () sence nd () presence of hmstring stretch response. Top portion of ech figure shows position (uppermost lines) dt from pssive knee trils. Up-slope of position grph = flexion; down-slope = extension. Lower portion is EMG dt for hmstrings which shows no ctivity in (), ut in () consistent nd prolonged stretch response tht egins during extension is seen. Tle III: Numer of muscle groups with or without identified stretch responses listed y Ashworth score Ashworth score (+) Stretch ( ) Stretch Bold, result inconsistent with isokinetic/emg ssessment. Precision of Ashworth Scle nd Instrumented Mesures Dine L Dmino et l. 113

3 for the comprison group of nine children without CP the men ge ws 11.3 yers (SD 2.5). Prticipnts were recruited s prt of preopertive protocol for ptients undergoing orthopedic or neurosurgicl procedures. Inclusion criteri were: no mjor surgery within the pst 6 months, the ility to fit ntomiclly on the isokinetic device, nd the ility to comply with instructions. Any prticipnt who ssisted the pssive motion (determined y EMG) in t lest one direction ws lso eliminted from the study, s this would distort the resistnce torque clcultions. PROCEDURES Clinicl nd functionl ssessments All individuls prticipted in clinicl ssessment of spsticity Tle IV: Correltion of knee extensor (KE) nd knee flexor (KF) Ashworth scores with isokinetic prmeters in prticipnts with CP Correltions /s n KE Ashworth (rho) KF Ashworth (rho) Resistnce torque ns Resistnce torque ns Resistnce torque ns Stiffness ns Stiffness ns Stiffness Onset ngle 3 1Q/14H.8 ns Onset ngle 6 1Q/14H ns ns Onset ngle 12 1Q/14H ns.58 Q, qudricep stretch response; H, hmstring stretch response. Resistnce torque in ft-ls/ls Comprison ASH1 ASH4 Slope of torque y ngle Comprison ASH1 ASH Resistnce torque in ft-ls/ls Slope of torque y ngle Figure 2: Resistnce torque in ft-ls/ls plotted y Ashworth scores for () qudriceps during knee flexion nd () hmstrings during knee extension t 12 /s. Figure 3: Rte of chnge in resistnce or slope of resistnce torque y ngle (TXA) curve plotted y Ashworth scores for () qudriceps during knee flexion nd () hmstrings during knee extension t 12 /s. 114 Developmentl Medicine & Child Neurology 22, 44:

4 including Ashworth score, Ely test (or Duncn-Ely; Gge 1992), nd deep tendon reflexes. The Ashworth scle used ws similr to the clssic one (Ashworth 1964; see Tle I) with the exception here tht scores were shifted so tht score indicted when resistnce ws less thn norml. The Ely test is used to ssess rectus spsticity during rpid pssive knee flexion while the ptient is prone. For those in the CP group, knee joint rnge of motion, selective control of knee flexion nd extension, nd the Gross Motor Function Mesure (GMFM; Russell et l. 1989) were lso ssessed. The prent/cregiver ccompnying the child or dolescent completed the Prent Bseline Form of the Peditric Outcomes Dt Collection Instrument (Dltroy 1998). Pssive isokinetic nd EMG ssessments Surfce EMG electrodes (Norxon USA Inc, Scottsdle, AZ, USA) were plced over the qudriceps nd hmstrings muscles. The child ws seted on the isokinetic device (System 3 Pro; Biodex Medicl Systems, Shirley, NY, USA) in semireclining position with the hip joint ngle t 6 of flexion. The left leg ws the tested leg, except for three ptients with right hemiplegi on whom the right leg ws tested. Pssive isokinetic testing of the knee t 3, 6, nd 12 /s ws performed. EMG nd resistnce torque dt were collected simultneously t smpling rte of 12 Hz (Dtpc 2; RUN Technologies, Lgun Hills, CA, USA). DATA ANALYSIS For clrifiction, knee extensor Ashworth scores indicte resistnce from the qudriceps during knee flexion nd knee flexor Ashworth scores indicte resistnce from the hmstrings during knee extension. Similrly, resistnce torque nd stiffness in the qudriceps refers to isokinetic mesurements during pssive knee flexion nd during knee extension for the hmstring vlues. Resistnce joint torque ws mesured in ft-l/ls, the lim weight ws removed nd the torque ws normlized y ody weight. Pek resistnce torque ws the mesure of mgnitude. In ddition, resistnce torque ws plotted ginst joint ngle for the isokinetic prt of the rnge nd the slope of this line ws computed nd used s mesure of stiffness (see Glossry in Appendix). EMG dt were used to identify the stte of muscle ctivtion during the pssive trils, i.e. whether the muscles were quiescent or whether stretch response ws consistently evident in the ntgonist. Figure 1 illustrtes the EMG response to pssive knee motion for child without stretch response in either muscle (Fig. 1) nd child with stretch response in the hmstrings muscles during knee extension (Fig.1). Prticipnts were ctegorized y whether or not they demonstrted hmstrings or qudriceps stretch responses. Onset ngle ws lso recorded for ech tril where stretch response ws identified y finding the ngle equivlent of the EMG onset. Chnges in stiffness, pek resistnce, nd onset ngle with velocity (vlues from 12 /s trils vlues from 3 /s trils) were lso quntified to evlute the velocity dependency of ech prmeter. Spermn s rho nd Person s r procedures were used to exmine correltions etween vrile pirs ASH Results The group with CP included those with dignosis of spstic diplegi, hemiplegi, or qudriplegi, with the distriution cross Gross Motor Functionl Clssifiction Levels (Plisno et l. 1997) shown in Tle II. No individul in the comprison group showed stretch response t ny of the velocities tested. Of the 22 children with CP, 14 demonstrted stretch responses in the hmstrings, 1 hd stretch responses in the qudriceps, seven hd these in oth muscles, nd five hd these in neither muscle. We first exmined the predictive vlue of the Ashworth scle in detecting or filing to detect stretch responses compred with the isokinetic exmintion (Tle III). Of the 1 muscles ssigned grde of 1 in either the knee flexor or extensor Ashworth ASH1 ASH4 Figure 4: Onset ngle in degrees of knee flexion plotted y Ashworth scores for () qudriceps during knee flexion nd () hmstrings during knee extension t 12 /s. Tle V: Spermn s correltion of knee extensor (KE) Ashworth scores nd functionl mesures in those with CP Correltions KE Ashworth (rho) POSNA Glol Function Scle.48 Upper Extremity.52 Trnsfers nd Bsic Moility.61 Gross Motor Function Mesure TOTAL.68 Lying nd Rolling.63 Sitting.66 Crwling nd Kneeling.63 Stnding.58 Wlk, Run nd Jump.57 Precision of Ashworth Scle nd Instrumented Mesures Dine L Dmino et l. 115

5 score, only one child ws shown to hve stretch response in the hmstrings during the isokinetic/emg tests. Tht sme child hd een ssigned for the qudriceps Ashworth score, yet hd lso demonstrted stretch response in tht muscle. Of the 13 muscles ssigned n Ashworth score of 2, six hd identifile stretch responses. Of the 13 muscles ssigned Ashworth scores of 3, nine hd stretch responses. Finlly, of the seven muscles ssigned scores of 4 or 5, ll seven hd evidence of stretch responses on the isokinetic/emg evlution. RESISTANCE TORQUE, STIFFNESS, AND ONSET ANGLE BY ASHWORTH A cler grdient ws pprent in the men resistnce (Figs 2 nd ) nd stiffness vlues (Figs 3 nd ) s Ashworth scores incresed. Onset ngle of the stretch response tended to occur sooner in the motion in those with higher Ashworth scores (Figs 4 nd ). In ll ptients, the EMG response, once initited, continued throughout the motion. RELATIONS BETWEEN ASHWORTH SCORES AND QUANTITATIVE MEASURES Significnt correltions tended to e in the wek to moderte rnge with the qudriceps mesurements showing typiclly higher nd more consistent reltions (see Tle IV). CORRELATION WITH FUNCTION Knee extensor Ashworth scores were significntly relted to the functionl scores (Tle V) while knee flexor Ashworth scores were not. Instrumented mesures for oth muscle groups hd significnt reltionships with the functionl mesures s shown in Tles VI nd VII. However, the correltions with the hmstrings tended to e lower nd/or more spordic thn those seen for the qudriceps. An inverse correltion etween chnge in hmstring stiffness nd the Glol Function Scle score ws found (r=.51) with greter chnge cross velocity relted to poorer ility. OTHER INTERIMPAIRMENT CORRELATIONS Knee extensor Ashworth scores nd qudriceps stiffness t ll three velocities were relted to the Ely test (r=.45 for Ashworth; r=.67 to.77 for stiffness). The knee flexor Ashworth score nd hmstring stiffness were inversely relted to pssive knee extension (r=.48 for Ashworth; r=.51 to.59 for stiffness) indicting tht greter resistnce in the hmstrings is ssocited with more restricted muscle lengths. Only three children with CP demonstrted incresed knee jerk responses (greter thn 3/5) on tendon tp. Ech of those children lso demonstrted stretch response during the knee extension isokinetic tests with knee flexor Ashworth score of 4 in two children nd 3 in one child, despite the fct tht no correltion ws found etween tendon reflexes nd Ashworth scores. Isolted control of the hmstrings (grded from for no control, 1 if they could initite the movement with the hip in extension or complete it while flexing the hip, nd 2 if they could complete the movement without flexion t the hip) ws inversely relted to resistnce torque in the qudriceps (rho=.48), indicting tht greter ctive control in the hmstrings ws ssocited with lower pssive resistnce in the ntgonist. Discussion Lnce (1981) descried spsticity in clinicl sense s, the senstion of resistnce felt s one mnipultes joint through rnge of motion, with the suject ttempting to relx (p 128). However, our investigtion corroorted previous reports showing tht incresed resistnce in CP cn e from intrinsic stiffness, or ltered muscle properties in the sence of EMG ctivity, from stretch responses tht cuse n involuntry muscle ctivtion, or from oth fctors comined (Ktz nd Rymer 1989, Dietz nd Berger 1995). Severl of the children with CP showed no stretch responses in one or more of the muscle groups nd no one in the control group showed stretch response t either joint t ny of the ngulr velocities tested. While stretch responses cn e detected in norml muscles, the threshold velocity needed to elicit these is much greter thn those employed here (Fellows et l. 1994). A protocol designed to increse the ngulr velocity incrementlly until stretch response cn e elicited in ll prticipnts my more clerly differentite responses in CP versus non-cp muscles. It ws pprent in this smple tht the mgnitude of resistnce in ptients with identifile stretch responses cn rech much higher levels, prticulrly t fster velocities, thn typiclly seen in those without stretch responses. Tle VI: Person s correltion of Gross Motor Function Mesure (GMFM) totl nd Glol Function Scle Score (GLOBAL) of Peditrics Outcomes Dt Collection Instrument with instrumented pssive motion tests for qudriceps muscle group Correltion /s GMFM (r) GLOBAL (r) Resistnce torque Resistnce torque Resistnce torque 12 ns ns Stiffness Stiffness Stiffness 12.7 ns Onset ngle 3.85 ns Onset ngle 6 ns ns Onset ngle 12 ns ns Tle VII: Person s correltion of Gross Motor Function Mesure (GMFM) totl nd Glol Function Scle Score (GLOBAL) of Peditrics Outcomes Dt Collection Instrument with prmeters from instrumented tests for hmstrings muscle group Correltions /s GMFM (r) GLOBAL (r) Resistnce torque 3 ns ns Resistnce torque 6 ns ns Resistnce torque 12 ns ns Stiffness 3.6 ns Stiffness 6.57 ns Stiffness ns Onset ngle 3 ns ns Onset ngle 6 ns ns Onset ngle 12 ns ns ns, not sttisticlly significnt t p< Developmentl Medicine & Child Neurology 22, 44:

6 However, ptients my exist in whom the mgnitude of the spstic response is very smll or the mgnitude of pssive stiffness lone is firly high. Ptients ssigned Ashworth scores in the mid-rnges of resistnce yet who hd pssive stiffness lone could e incorrectly judged to hve mild to moderte spsticity nd, consequently, my e treted inppropritely. It is lso possile tht the degree of spsticity could e overestimted, even when present, which could lso dversely ffect tretment outcomes. In the sence of EMG verifiction, evluting ptients t different velocities my help to distinguish pssive stiffness lone from reflex stiffness (spsticity); however, the Ashworth scle is only performed t single velocity. Therefore, instrumented devices or other clinicl methods, such s the newly revised Trdieu Scle (Boyd nd Grhm 1999) tht guge resistnce t severl speeds my e more useful, especilly in more equivocl cses. As Ashworth scores nd isokinetic tests oth mesure resistnce to pssive stretch, it is logicl to ssume tht they would e correlted. Stiffness, rther thn the mgnitude of resistnce, ppered to hve higher, more consistent correltions with the Ashworth scores. Fctors such s differences in the position of the ptient during the tests (supine versus sitting), position of djcent lims (hip flexing nd extending throughout versus eing in stticlly flexed position of 6 ), differences in velocities, nd potentilly different levels of nxiety or ftigue cross conditions my explin why these reltions were not stronger thn those shown here. The Ashworth scle, s well s more quntittive mesures of spsticity or resistnce, hs vlue eyond the impirment level if scores re shown to relte to functionl performnce. As CP is multifceted disorder nd s evidence disputes the primcy of spsticity in disrupting voluntry motor function, reltionships etween spsticity indictors nd function in this investigtion were hypothesized to e wek. An erlier multicenter investigtion on the reltionships etween impirment function nd disility in multory children with CP showed tht Ashworth scores were wekly correlted with functionl mesures (Dmino nd Ael 2). Correltions reported here in different dt set support the previous finding ut re even higher. This difference is most likely due to the greter vrition in this smple which lso included children with qudriplegi. Correltion procedures re very sensitive to the rnge of vlues, nd if the smple is firly homogeneous quite different results my e found from those reported in more vrile smples. We elieve tht smpling differences cross studies my explin mny of the discrepncies reported in the literture on whether or not spsticity is relted to function in CP or in other CNS disorders. It is lso possile tht spsticity, like cocontrction, must rech certin level efore it egins to impir function (Dmino 1993); therefore, the fct tht this study included those with higher levels of resistnce my help to explin these results. Instrumented mesures tended to hve greter correltions with function thn the Ashworth scle, which my e due to greter ojectivity, precision, or rnge of vlues resulting from this method. Future investigtions will focus on the reltive sensitivity of isokinetic mesures compred with the Ashworth scores in detecting chnge in pssive resistnce s result of interventions. We will lso continue to explore other confounding or coliner fctors tht my e distorting the correltions reported here, such s restrictions in muscle length, nd uncovering the mechnism y which spsticity, pssive phenomenon, disrupts voluntry muscle ctivtion (Dmino et l. 21,) nd motor performnce. Conclusions A stndrd rehilittion device, n isokinetic dynmometer, cn e used to quntify vlidly resistnce torque during pssive joint motion. In this investigtion, the instrumented mesures tended to hve stronger reltionships with function thn the current clinicl stndrd, the Ashworth scle. Pssive resistnce to motion, s mesured cliniclly nd with instrumenttion, shows consistent direct reltionship with vlidted mesures of function in CP. Accepted for puliction 1st August 21. Acknowledgements This work ws supported y funding from the Ntionl Institutes of Helth (R29HD36516), United Cererl Plsy Eductionl nd Reserch Foundtion, nd Medtronics Neurologicl. 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