Assessment of apraxia: inter-rater reliability of anew apraxia test, association between apraxia andother cognitive deficits and prevalence of apraxia ina rehabilitation settingAngeliek Zwinkels Rehabilitation Centre Blixembosch, Chantal Geusgens Institute for Rehabilitation Research and InstituteBrain and Behaviour, University of Maastricht, Peter van de Sande Rehabilitation Centre Hoensbroek and Caroline vanHeugten Rehabilitation Centre Hoensbroek, Institute for Rehabilitation Research and Institute Brain and Behaviour, Universityof Maastricht, The Netherlands
Received 14th June 2003; returned for revisions 21st August 2003; revised manuscript accepted 10th January 2004.
Objective: To investigate the inter-rater reliability of a new apraxia test. Furthermoreto examine the association of apraxia with other neuropsychological impairments andthe prevalence of apraxia in a rehabilitation setting on the basis of the new test.Design: Cross-sectional cohort study, involving 100 patients with a first strokeadmitted to a rehabilitation centre in the Netherlands.Measures: General patient characteristics and stroke-related aspects. Cognitivescreening involving apraxia, visuospatial scanning, abstract thinking and reasoning,memory, attention, planning and aphasia.Results: The indices for inter-rater agreement range from excellent to poor.Significant correlations are found between apraxia and visuospatial scanning,memory, attention, planning and aphasia. The patients with apraxia performsignificantly worse than the patients without apraxia on memory, the time needed tocomplete the tests for scanning and attention, and aphasia. The prevalence of apraxiais 25.3% in the total group, 51.3% in the left hemisphere stroke patients and 6.0% inthe right hemisphere stroke patients. Patients with and without apraxia do not differsignificantly concerning age, gender and type of stroke.Conclusion: The apraxia test has been shown to be a reliable instrument. Apraxia isoften associated with aphasia, memory problems and mental slowness. This studyshows that on the basis of the apraxia test, the prevalence of apraxia among patientsin the rehabilitation centre is high, especially among patients with left hemispherelesions.
Introduction covers a spectrum of disorders affecting thepurposeful execution of learned and meaningful
Apraxia is one of the more frequent consequences skills.2 It is mostly found in stroke patients, butfollowing brain damage and can lead to severe the deficit is also seen in patients with Alzheimer'sdisabilities in daily life.' -3 The term apraxia disease,4'5 cortico-basal degeneration and Hun-
apraxic, while none of the right hemispherepatients had apraxia. Liepmann concluded thatthe left hemisphere is dominant for the organiza-tion of motor control. Later studies confirmedthis claim. In a study conducted by De Renzi andhis colleagues,9 50% of the left brain-damagedpatients and 20% of the right brain-damagedpatients were classified as apraxic. Apraxia canbe associated with aphasia, for which the lefthemisphere is also dominant. A correlation of0.40 between apraxia and aphasia has beenfound.'0"' This association is most likely to bea result of the fact that contiguous structures areinvolved.2"2
Despite the fact that apraxia seems to be oneof the more frequent impairments after stroke,the exact prevalence is not known. The studiesmentioned above are some of the rare studiesfound in the literature on the occurrence ofapraxia. In a paper by Donkervoort et al.13 areview on the prevalence of apraxia yielded only10 studies, which mainly concerned heterogeneousand selected, rather small, patient groups. Don-kervoort and her colleagues conclude that thereliability and validity of the prevalence estimatesare limited and therefore present a new study onthe prevalence of apraxia. The rates they foundwere 28% among patients with a left hemispherestroke in rehabilitation centres and 37% in nur-sing homes. As in most studies, however, thediagnosis of apraxia relied on clinical judgement,in the absence of standardized tests. The presenceof apraxia was examined by the treating medicalteam based on a clear definition of apraxia. Thevalidity of this clinical diagnosis can be ques-tioned as the team can overestimate the caseswith apraxia, or cases can be missed.
Recently a test for apraxia was developed thatcan be used to objectify and support the clinicaldiagnosis. In an earlier study the internal con-sistency and diagnostic value of this new apraxiatest were investigated and shown to be good.'4 Inthe present study the inter-rater reliability of thisnew test will be reported, because this is animportant aspect of the quality of the test for usein clinical practice. In addition, the association ofapraxia with other cognitive functions will beexplored in order to gain more insight intopotential cognitive profiles. Finally, the prevalence
of apraxia in a rehabilitation setting is investi-gated on the basis of the new test.
Methods
PatientsAll patients admitted consecutively to the
stroke unit of a rehabilitation centre with a firststroke were eligible for the study, starting May2000. Stroke patients were excluded on the basisof the following criteria: presence of other centralneurological lesions or dementia before thecurrent stroke, addiction to alcohol, drugs ormedication, insufficient physical fitness to performthe cognitive screening, psychiatric disturbancesinterfering with neuropsychological testing, insuffi-cient knowledge of the Dutch language or severeaphasia.
All patients received verbal and written informa-tion about the study and gave written consent toparticipate. The research protocol was approved bythe local medical ethical committee.
AssessmentsThe presence of apraxia was established on the
basis of an apraxia test.14 This short and simpletest consists of two subtests. The first subtest wasdesigned to evaluate the use of objects, therebyassessing ideational apraxia. Three sets of objectsare presented to the patient with the same instruc-tion: 'Show me how you would use...'. Each setcontains three objects used in daily activities. Thefirst set (key, saw and toothbrush) is presented onlyby verbal request, without the object present. Thesecond set (spoon, hammer and scissors) is pre-sented visually, with the object present. The thirdset (eraser, comb and screwdriver) can actually beused by the patient. The second subtest involvesthe assessment of the ability to imitate gestures,aiming at ideomotor apraxia. This part of the testconsists of the following six gestures which have tobe imitated immediately upon demonstration bythe testing assistant: sticking out one's tongue,blowing out a candle, closing one's eyes, wavinggoodbye, saluting and making a fist. To avoidinterference of motor or sensory impairments, thepatients used their healthy (i.e., nonaffected) hand.The scoring procedure was as follows: 3 points fora correct and appropriate performance, 2 points
Assessment of apraxia 821
for a performance that resembles the correct onebut is imprecise or involves a body part as object, 1point for only weak resemblance to the correct oneor executed in the wrong place, and 0 points for aperformance which is incorrect or not recognizable.If the performance is correct at the first trial, 6points are given; if the performance was notcorrect, a second attempt was offered and thetwo scores are added. This way a maximum of 6per item, 54 for the subtest demonstration, 36 forthe subtest imitation, and a maximum of 90 for thetotal test is generated. The quality of the apraxiatest was good in terms of the internal consistency(Cronbach's alpha = 0.96; Mokken coefficient ofscalability H=0.72; Mokken coefficient of relia-bility rho=0.96) and the diagnostic value: theapraxia test is sufficiently discriminative to allowa differentiation between people with apraxia andpeople without apraxia (sensitivity and specificityhigher than 80%). 14A Dutch letter cancellation test is used to
investigate the visuospatial scanning ability of thepatient.15 These tests are the most sensitive inmeasuring the presence of neglect.'6 A piece ofpaper with many letters in an unstructured, chaoticpattern is presented. The patient has to locate andmark the letter 0. The number of omissions in eachvisual field is scored, as well as the time needed tocomplete the test.
Raven's Coloured Progressive Matrices (RCPM)is a nonverbal visual test which can be used toassess the ability of abstract thinking and reason-ing. The test consists of a set of 36 visual patternsof which one part is missing. The patient has tochoose the correct piece of pattern from a set ofsix alternatives. The scorerange of the RCPM is0 to 36.Memory performance was evaluated using the
Rivermead Behavioural Memory Test(RBMT).'8-20 The RBMT is an ecologically validmemory test providing information about theeffect of the memory impairment on a patient'sdaily life. The test consists of tasks such asremembering an appointment or a name, findinga route, and orientation in time and place. Theperformance of the patient can be scored on adichotomous scale or on a three-point scale; thisrespectively counts up to a screening score (max-imum 12) or a profile score (maximum 24).
Attention was assessed using the Trail MakingTest, part A and B (TMT).2' Performance on thistest generates information about the motor speed,visual scanning and flexibility/capacity of atten-tion. In part A the patient has to connect 25numbers by drawing lines between the numberscounting forward. In part B numbers and letters(in alphabetical order) have to be connectedpairwise. The time the patient needs to completethe task is scored in seconds.The Tower of London Test (TLT) was deve-
loped to assess the ability of planning.2223 Thepatient receives a little board with three sticks andthree coloured dice, placed in a starting position. Apicture of a new configuration is shown and thepatient has to replace the dice in the new position;the number of steps needed is told beforehand. Intotal 12 configurations are tested, each being moredifficult. The number of attempts is scored in areverse order (fewer attempts gives a higher scorerepresenting better performance); the maximumscore is 36.The Token Test was used to measure language
impairments; it is a subtest of the Aachen AphasiaTest.24 The test consists of a series of pictures withtriangles and squares of different colours and sizes,which have to be selected by the patient uponverbal request by the examiner. The test is one ofthe most sensitive in differentiating between brain-damaged patients with and without aphasia. Ascore of 5 or lower denotes the presence of aphasiain our study.
ProcedureUpon admission to the stroke unit of the
rehabilitation centre, all stroke patients werescreened for cognitive, emotional and behaviouralproblems within the first three weeks. This cogni-tive screening consists of performance on a set ofneuropsychological tests, behavioural observationsby the therapists and nurses of the rehabilitationteam, and an interview by the psychologist, alsoinvolving the caregiver. In this paper only theneuropsychological screening is considered. Onproviding consent to participate in the study,patients were screened on all cognitive assessments.Each patient was assessed by a neuropsychologicalassistant and a speech therapist (for the TokenTest) in a quiet room. On average, it took one anda half hours to complete.
822 A Zwinkels et al.
The first 45 patients agreed to have two ob-servers during the performance on the apraxia test.In total five different raters conducted the pairwiseobservations; all of these raters were neuropsycho-logical assistants working at the stroke unit. Thetwo raters observed simultaneously, but scoredtheir findings independently in order to establishthe inter-rater reliability of the apraxia test. One ofthe two raters had access to the medical recordsbeforehand because this assistant performed thecomplete cognitive screening.
Statistical analysesBeforehand, a calculation was conducted to
establish the number of patients needed for thereliability study: based on an expected correlationcoefficient of 0.8 to be reliable, a significance levelof 0.05 and a power of 0.90, at least 30 patientswere needed. The inter-rater reliability is expressedin three ways. First, the percentage of agreementwas calculated which equals the number of casesfor which the observers fully agree, proportional tothe total number of cases. Second, Cohen's kappa25is calculated to account for agreement by chance.The intraclass correlation coefficient (ICC) iscalculated because it is more appropriate fordetermining the reliability of sumscores. The ICCis defined as the ratio of the variance amongsubjects over the total variance. A kappa or ICCbelow 0.40 is considered to indicate little agree-ment, between 0.41 and 0.60 indicates moderateagreement, between 0.61 and 0.80 indicates goodagreement, and a kappa or ICC higher than 0.81indicates almost perfect agreement. 6-29The performance on the test of apraxia and the
other cognitive tests is presented by mean scoresand standard deviations. Bivariate relationshipsbetween apraxia and the other cognitive functionsare expressed by means of Pearson's productmoment correlation coefficients.On the basis of a cut-off point of 86, the total
group is divided into a group of patients withapraxia and a group of patients without apraxia.This cut-off point was based on earlier researchconcerning the diagnostic value of the test. 14 Next,the differences on the cognitive tests between thegroups are determined using t-tests for indepen-dent samples. Significance was set at 0.05. Analyseswere performed using SPSS 11.0 for Windows.
Results
PatientsIn total, 100 stroke patients were included in the
study on the basis of the criteria over a periodof two years; the first 45 patients were enrolledin the study of the inter-rater reliability of theapraxia test. Thirty patients were excluded onthe basis of other neurological disorders (8),insufficient physical fitness (6), insufficient knowl-edge of the Dutch language (4), severe aphasia (5),or refusal to participate (7). The characteristics ofthe patients are shown in Table 1. The twosubgroups of patients are comparable on allcharacteristics.
Inter-rater reliabilityIn Table 2 the level of agreement between two
observers, as indicated by percentages of agree-ment, Cohen's kappa and intraclass correlationcoefficients, is shown. These data are based on thesubgroup of 45 pairwise observations.
All percentages of agreement for the separateitems of the test are above 60%, indicatingsatisfactory to good agreement. Correcting forchance, it appears that three items have a kappavalue indicating poor reliability: demonstrating atoothbrush, blowing out a candle and saluting.One item has a kappa between 0.41 and 0.60; theother items have a kappa above 0.60. Looking atthe ICC values, two items show moderate agree-ment. The ICC for the sumscores are satisfactoryto very good: 0.97 for the demonstration sumscore,0.64 for the imitation sumscore and 0.96 for thetotal scale.
Association with other cognitive impairmentsCorrelations between apraxia and the other
cognitive domains on the basis of the total groupof patients are shown in Table 3. Significantrelationships are found between apraxia and thescores on the Token Test, the letter cancellationtest (omissions right and time), the RBMT, theTower of London, and the TMT, part A.
In Table 4 the scores on the neuropsychologicaltests are shown for the total group and for thegroups of patients with and without apraxiaseparately. From the table it can be seen that thepatients with apraxia perform worse on most testsin comparison to the patients without apraxia and
Assessment of apraxia 823
Table 1 Characteristics of patients
Total group
N(%l
NumberGenderMaleFemale
Type of strokeHaemorrhageInfarction
Location of strokeLeft hemisphereRight hemisphereOtherwisea
Hand of preferenceRightLeft
AgebTime since strokeb,C
100
63 (63)37 (37)
25 (25)75 (75)
40 (40)50 (50)10 (10)
95 (95)5 (5)
57.1 (10.6; 23-75)34.0 (14.9; 12-83)
SubgroupReliability studyN (%
45
29 (64.4)16 (35.6)
11 (24.4)34 (75.6)
17 (37.8)23 (51.1)5 (11.1)
42 (93.3)3 (6.7)
58.0 (10.9; 31 -75)32.9 (14.2; 13-83)
Other participantsN(%
55
34 (61.8)21 (38.2)
14 (25.5)41 (74.5)
23 (41.8)27 (49.1)5 (9.1)
53 (96.4)2 (3.6)
56.4 (10.3; 23-73)34.9 (15.5; 12-81)
aOtherwise: basal ganglia, brainstem or both hemispheres.bFor age and time since stroke, the mean, standard deviation and range are presented.CTime since stroke: number of days between stroke and admission ot the rehabilitation centre.
the total group. The differences between patientswith and without apraxia are significant for theamount of time needed to complete the lettercancellation test (t=2.13; p=0.04), the RBMT
ImitationBlow out candleClosing eyesWaving goodbyeSticking outtongueSalutingMaking a fist
Sumscoredemonstration
Sumscoreimitation
Total scale
screening and profile scores (t =4.12; p<0.01 andt=4.79; p<0.01, respectively), the TMT part A(t=2.38; p=0.03) and the Token Test (t=5.07;P<O.01).
eliability Prevalence of apraxia
% agreement Kappa ICC The mean score on the apraxia test for the totalgroup (n=99; one patient could not complete thetest) is 86.1 (SD 7.8; range 47-90). The patients
97.884.480.088.982.2
10010097.8
93.397.810097.8
91.1100
U.Uz0.900.330.420.610.661.001.000.82
0.360.711.000.71
0.31100
U.zi/0.970.870.790.770.881.001.000.99
0.330.801.000.80
0.591.000.97
0.64
0.96
Table 3 Correlations between apraxia and the other cogni-tive tests
N Apraxia test
Letter cancellationOmissions left 96 -0.03Omissions right 95 -0.270**Time 97 -0.232*
RCPM, Raven's Coloured Progressive Matrices; RBMT, Rivermead Behavioural Memory Test; TMT, Trail Making Test; TLT,Tower of London Test.
with a stroke in the left hemisphere (n = 39) have amean of 82.1 (SD 11.0; range 47-90), while theright hemisphere stroke patients (n = 50) have amean of 88.9 (SD 2.1; range 79-90). This differ-ence is significant (t =4.29; p< 0.01).The prevalence of apraxia was based on the
number of patients scoring below the cut-off pointof 86. In total 99 patients performed the apraxiatest: 25 of them scored below 86. This equals25.3%. When the patients with apraxia (n =25) andwithout apraxia (n = 74) are compared, there areno significant differences in age, gender or type ofstroke.
Considering the patients with a stroke in the lefthemisphere (n = 39), it appears that 51.3% (n = 20)have apraxia. In the group of patients with a righthemisphere stroke (n = 50), only three scored belowthe cut-off point (6.0%). The group of patientswith a stroke in both hemispheres, or in other areasof the brain (n =10) demonstrates a prevalence rateof 20%.
Discussion
In the present study the inter-rater reliability of anew apraxia test was determined. Furthermore, theassociation between apraxia and other cognitiveimpairments and the prevalence of apraxia in arehabilitation setting was examined.
The apraxia test has proved to be a reliableinstrument; the indices for agreement of the sum-scores are satisfactory to very good. The kappavalues, however, ranged from excellent to poor.Three items of the test had a low kappa value:demonstrating the use of a toothbrush, blowingout a candle, and saluting. For these items theinstructions for observation are now supplementedwith additional observational cues. For instance,the way the hand has to positioned on the foreheadwhen saluting, is described in more detail. Theseadditions were provided by the neuropsychologicalassistants who used the test in this study.
Furthermore, the association of apraxia withother cognitive impairments was examined. Con-cerning the cognitive measurements, it should benoted that on some of the tests, motor perfor-mance is requested (i.e., drawing lines, replacingdice). Since apraxia involves motor behaviour,these results can be confounded. However, one ofour earlier studies on the apraxia test showed onlyweak relationships with motor functioning.37Apraxia was found to be correlated with aphasia,memory and mental speed. The strong relationshipof apraxia with aphasia has been shown in otherstudies before, albeit not as strong as wefound. JU,11,32 The association between the twoimpairments is most probably due to the fact thatcontiguous structures are involved.2"2 The rela-tionship with memory and mental speed is less
Assessment of apraxia 825
obvious from the literature. However, both impair-ments occur frequently in stroke patients.33'34 In arecent study concerning patients with traumaticbrain injury, it was found that mental speeddetermines the performance on attention tests;35in other words, it can be argued that speed ofinformation processing is a more global impair-ment which frequently occurs and interferes withtest performance.The prevalence of apraxia was high among
patients with a left hemisphere stroke: more thanhalf of the patients in this study has apraxia. Theprevalence among right hemisphere patients was
considerably less. This finding confirms earlierresults.8- 10.9,30,31 In comparison to the study byDonkervoort et al.'3 we found higher rates, whichmight be an indication of an underestimation ofapraxia on the basis of clinical judgement in theirstudy. Parallel to the study of Donkervoort andcolleagues, we also did not find a relationshipbetween the prevalence of apraxia and patientcharacteristics such as gender, age and type ofstoke.
This study has some limitations. One of themore evident limitations is the selected group ofstroke patients recruited in only one rehabilitationcentre. This design limits the generalizibility ofthe results on the one hand; on the other hand, thecharacteristics of the patients in this study showthat we did consider a rather representativepopulation of stroke patients in rehabilitation.The prevalence rates are however potentiallyspecific to the stroke unit because local admissioncriteria were used. A second limitation concerns
the design of the study: we did not assess apraxiaon the basis of different tests, which could have
given us more information on the validity of our
test. In a recent study Butler36 found poor relation-ships between several tests of apraxia, suggestingthat not all apraxia tests are of comparable quality.These results were based on a very small number ofpatients (n =17). In an earlier study however,we did examine the diagnostic value of the apraxiatest, which was good.14 In addition, the relation-ship between the apraxia test and standardizedADLobservations, measuring disabilities due toapraxia, was investigated in another study.37Correlational and multivariate analyses showedthat there was a strong association betweenthese two measures as opposed to motor function-ing and general measures of disabilities (i.e.,Barthel Index). On the basis of these findingswe recommended that apraxia should be diag-nosed not solely on the use of neuropsychologicaltests, but also on the basis of observation ofthe consequences of apraxia for daily life. Inaccordance, Butler36 argues that functional andbehavioural indices in ADL tasks should beconsidered as more clinically relevant than pure
test scores.Future research concerning the course of
apraxia can now be initiated with this new test,whereby the patients are followed for a periodof time, starting in the acute phase. This isimportant since apraxia has shown to be a
persistent disorder which has negative conse-
quences on ADL recovery.30'38-40 Prognostic fac-tors should be identified.
Conclusions
A short and simple, reliable bedside test hasbecome available to test the presence of apraxia.This test can be used to differentiate betweenpatients with and without apraxia. Cliniciansshould be alert to the presence of apraxia afterstroke since the prevalence rates have shown tobe rather high, especially after left brain damage.Ideally, diagnosing apraxia should be doneby combining the results of the apraxia testwith observations of functioning in daily lifetasks.
Clinical messages
* Clinicians should be alert to the presence ofapraxia after left hemisphere stroke.
* A short and simple, reliable bedside test forapraxia is now available and is recom-mended for use in clinical practice.
* Test scores should be combined with beha-vioural observations for a proper evaluationof apraxia and its consequences in daily life.
826 A Zwinkels et al.
AcknowledgementsThe authors would like to thank the psycholo-
gical assistants Mieke Ploum, Marij Eussen, HenkMeurders and Basje Roberts, and the speechtherapists Virginie Pielanen, Marie-Jeanne teMeij and Carine Crijns for helping with the datacollection.
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