Evaluation of Different Measures and Dimensions

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Clinical Assessment of Hemispatial Neglect: Evaluation of Different Measures and Dimensions Arja B. Lindell

a b

c

d

c

, Maarit J. Jalas , Olli Tenovuo , Teea Brunila , e

Marinus J. M. Voeten & Heikki Hämäläinen

c

a

Department of Rehabilitation , Turku University Central Hospital , Turku b

Department of Psychology , Åbo Akademi University , Åbo

c

Department of Psychology , Centre for Cognitive Neuroscience, University of Turku d

Department of Neurology , Turku University Central Hospital , Turku, Finland e

Department of Educational Sciences , Radboud University Nijmegen , Nijmegen, The Netherlands Published online: 13 Apr 2007.

To cite this article: Arja B. Lindell , Maarit J. Jalas , Olli Tenovuo , Teea Brunila , Marinus J. M. Voeten & Heikki Hämäläinen (2007) Clinical Assessment of Hemispatial Neglect: Evaluation of Different Measures and Dimensions, The Clinical Neuropsychologist, 21:3, 479-497, DOI: 10.1080/13854040600630061 To link to this article: http://dx.doi.org/10.1080/13854040600630061

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The Clinical Neuropsychologist, 21: 479–497, 2007 http://www.psypress.com/tcn ISSN: 1385-4046 print=1744-4144 online DOI: 10.1080/13854040600630061

CLINICAL ASSESSMENT OF HEMISPATIAL NEGLECT: EVALUATION OF DIFFERENT MEASURES AND DIMENSIONS Arja B. Lindell1,2, Maarit J. Jalas3, Olli Tenovuo4, Teea Brunila3, Marinus J. M. Voeten5, and Heikki Ha¨ma¨laïnen3 1

Department of Rehabilitation, Turku University Central Hospital, Turku, Department of Psychology, A˚bo Akademi University, A˚bo, 3Department of Psychology, Centre for Cognitive Neuroscience, University of Turku, 4 Department of Neurology, Turku University Central Hospital, Turku, Finland, and 5Department of Educational Sciences, Radboud University Nijmegen, Nijmegen, The Netherlands


2

The multidimensional nature of the neglect syndrome constitutes a challenge for clinical assessments. This study evaluates the sensitivity of different clinical measures to detect neglect and explores ways to evaluate the diversity of the syndrome in a clinical sample. An extensive battery of tests was used to examine aspects of visuospatial, representational, and personal neglect. A total of 31 normal control participants and 34 patients with right hemisphere stroke were examined 16.8 days post-stroke, on average. Of the patients, 24 showed neglect in at least one task. The Random shape cancellation test, Star cancellation, and two line bisection tasks appeared to be the most sensitive tests of visuospatial neglect. Personal neglect and neglect in far space occurred only together with extrapersonal neglect. Besides near space, other spatial aspects of neglect are important to consider in clinical assessments, but standardized methods are needed. In this patient group a minimum of 10 tests were needed to cover various aspects of detection, dissociations, and severity of neglect. A multifactorial approach in clinical testing of neglect is recommended.

INTRODUCTION Recent studies on the clinical manifestations and underlying mechanisms of spatial neglect have shown it to be a complex, and most likely a multifactorial, clinical syndrome (Halligan & Robertson, 1992; Kinsella, Packer, Ng, Olver, & Stark, 1995). Neglect has been shown to occur in several sensory modalities (Barbieri & De Renzi, 1989), but visuospatial neglect is the most extensively studied. Earlier studies have shown the different manifestations of neglect to dissociate in many ways, indicating possibly various underlying mechanisms. For example, on the level of single tests of visuospatial neglect, as well as reading performance, ˚ bo Akademi University, Address correspondence to: Arja Lindell, Department of Psychology, A ˚ bo, Finland. E-mail: [email protected] 20500 A Accepted for publication: January 30, 2006. First published online: October 12, 2006. # 2006 Psychology Press, an imprint of the Taylor & Francis group, an Informa business


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A. B. LINDELL ET AL.

dissociations or double dissociations have been reported (Binder, Marshall, Lazar, Benjamin, & Mohr, 1992; Ellis, Young, & Flude, 1993; Marshall & Halligan, 1995). Within distances of space, neglect has been reported to dissociate between personal, near, and far space (Bisiach, Perani, Vallar, & Berti, 1986; Guariglia & Antonucci, 1992; Halligan & Marshall, 1991; Vuilleumier, Valenza, Mayer, Reverdin, & Landis, 1998; Zoccolotti & Judica, 1991). Besides difficulties in orienting in external space, neglect may also be confined to an internally generated imaginal or representational dimension (Vallar, 1998). Studies comparing individual tests have shown that the tests can differ substantially in their sensitivity to detect neglect (Agrell, Dehlin, & Dahlgren, 1997; Halligan, Marshall, & Wade, 1989; Jehkonen, Ahonen, Dastidar, Koivisto, Laippala, & Vilkki, 1998; Marsh & Kersel, 1993; Stone et al., 1991). The Star cancellation test from the Behavioral Inattention Test (BIT) (Wilson, Cockburn, & Halligan, 1987) has been shown to be one of the most sensitive tests in many studies, but also other types of tasks have shown high detection rates (Halligan et al., 1989; Kinsella et al., 1995; Stone et al., 1991). The limitation in earlier studies is that they have mainly compared a rather limited number of tasks or focused on the subtests from the BIT. The different clinical tasks may also differ in how severely neglect is exhibited (total or partial neglect) (Halligan, Robertson, Pizzamiglio, Holmberg, Weber, & Bergego, 1991b). From a clinical point of view it would be important to know if some commonly used tasks tend to give biased information of the severity of the syndrome. The available clinical assessment procedures have been claimed not to sufficiently acknowledge the diversity of the disorder (Kinsella et al., 1995). Most researchers agree that more than one test should be used when wanting to assess neglect more comprehensively (Agrell et al., 1997; Halligan et al., 1989), but many tasks are not standardized or commercially available, apart from standard batteries like the BIT (Wilson et al., 1987). There is also as yet no commercially available test of neglect in far space that we know of. This phenomenon may therefore easily remain undetected. Furthermore, a clinical impression is that the milder forms of neglect may just appear in a very subtle way on tests, and that some measures may be too easy for a patient, even in cases where neglect is clearly observable in other situations. Although in these situations other diagnostic indicators, such as the tendency to start a clinical task on the right side (Jalas, Lindell, Brunila, Tenovuo, & Ha¨ma¨laïnen, 2002), can be used, further comparisons between different tests are needed. In this study we focused (a) on further exploring the sensitivity and utility of different measures to detect neglect, (b) on how severely neglect is manifested in different types of tasks, and (c) on providing data for clinical use when selecting a compact, yet comprehensive, test battery on neglect. An extensive clinical battery was used including, besides subtests from the BIT, other known, modified, or self-constructed neglect tasks. The tasks were chosen to allow description of the patient performances at the level of personal, near, and far space, and at the level of mental representational imagery. For practical purposes (duration of clinical examination, personnel resources) motor neglect or extinction phenomena were not included in our study.

CLINICAL ASSESSMENT OF NEGLECT

481

METHOD


Participants A total of 34 patients with a first single unilateral stroke in the right cerebral hemisphere were examined. The patients were recruited from the Department of Rehabilitation and the Department of Neurology at the Turku University Central Hospital during three consecutive years. Patients with previous psychiatric or neurological disorder, other serious systemic diseases, or a history of significant alcohol abuse were excluded. The clinical diagnosis of stroke was confirmed with CT in all cases and with MRI in 25 cases. The lesions were located mainly in the following brain regions: six parietal (patients 7, 13, 22, 24, 26, 36), one parieto-occipital (patient 8), one parieto-temporal (patient 15), two frontal (patients 21, 28), seven fronto-parietal (patients 3, 4, 10, 12, 20, 25, 30), two fronto-temporal (patients 11, 14), two temporal (patients 1, 19), one occipital (patient 16), one occipito-temporal (patient 27), and eleven subcortical (patients 5, 6, 9, 17, 18, 29, 31–35). Patients with large or multiple lesions were classified according the main lesion site. The NIH stroke scale (Brott et al., 1989) was used to assess the severity of stroke. A total of 14 patients had stroke-related visual field defects. A total of 31 controls with no history of neurological deficits, alcoholism, or psychiatric illnesses were included in the study. Of all participants, 62 were righthanded. Two patients and one control were classified as ambidextral according to the Edinburgh Handedness Inventory (Oldfield, 1971), but reported to be subjectively right-handed. Informed consent was obtained from all participants. The study was approved by the Turku University Central Hospital Ethics Committee. Demographic variables of the study groups are presented together with patient characteristics in Table 1.

Neuropsychological Tasks The neglect tests included mainly conventional paper-and-pencil type of neglect tasks or non-conventional (behavioral) tasks reflecting aspects of daily life functioning

Table 1 Demographic and clinical data of the study groups RCVA patients (N ¼ 34) Demographic variables Sex Age (years) Education (years) Patient characteristics Days post-onset Visual field defects

Male 24, female 10 58.6 8.02 (46–73) 8.9 3.7 (4–16) 16.8 8.9 (3–36) 6 partial hemianopia 8 total hemianopia

Mean SD (range). RCVA ¼ Right hemisphere cerebrovascular accident.

Controls (N ¼ 31)

p

Male 15, female 16 55.2 13.4 (25–74) 9.5 3.4 (4–17)

ns ns ns

482



such as picture scanning, reading, writing, and object finding. A test of visuo-spatial neglect in far space, a blindfold searching task, and a task for evaluating personal neglect were used to tap further aspects of neglect. The six conventional subtests and two picture-scanning tasks from the BIT were included. Since the BIT was not available in Finnish at the time of the study, the direct use of the behavioral subtests was limited. Other conventional or behavioral types of tasks were chosen if they had shown themselves clinically relevant, or were thought to be more demanding than the tasks in the BIT. The participants were seated during the testing situation and all testing material was presented facing the participant’s midline. Neglect tests given in near extrapersonal space were presented at table level. In far space the participants were presented with a slide displayed at a distance of 2.50 m. All tests were given in the same order within a clinical neuropsychological examination. The number after each test description indicates the presentation order of this test. Scanning of targets and pictures. Line-crossing, Letter cancellation, and Star cancellation tests from BIT were administered according to the BIT manual, except for the Line-crossing task where four instead of two of the lines in the central column lines were crossed for demonstration (order of presentation 2, 14, 15). In the Random shape cancellation test (Weintraub & Mesulam, 1988) the A3-sized stimulus sheet contained 60 target shapes located pseudorandomly among distracter shapes. The participants were asked to cross over all the targets. Four of the most central targets were used for demonstration and therefore not scored. The maximum score in each task was 56, and there was an equal number of targets on each side of the midline (18). The Random letter cancellation test (Weintraub & Mesulam, 1988) had the letter A as a target item and the distracters were other letters. Otherwise the task was identical to the previous test and was administered in a similar way (4). The Object-finding test was renamed from the Object Memory test (Portin, Saarija¨rvi, Joukamaa, & Salokangas, 1995), where 20 common objects were attached in a random order to an A2-sized board, 10 on each side. The participant was asked to point to and name each object. The number of objects found by pointing was scored, but correct naming was not required. The maximum score was 20 (1). In the Picture scanning, Meal and Washbasin test (BIT) A3-sized photographs were presented one at a time to the participant, first Meal and then Washbasin. The task was to name and to point out the main items seen in the picture. The maximum number of target items was eight in the Meal (three lateral and two central items) and nine in the Washbasin (three in each vertical section) (16,17). In the Two Part Picture (TPP) test (Brunila, Jalas, Lindell, Tenovuo, & Ha¨ma¨laïnen, 2003) the A3-sized picture presented two room interiors, separated by a thin gap. The number of items in each interior was 10. The participant was instructed to point and name all major items seen in the whole picture (3). In the Slide (far space) test the participant was presented at eye level with a slide-projection of 1.5 1.0 m showing a scene from a lobby, with three target items on each lateral side and three in the central part of the picture. The selection of target items was based on the most frequent responses from the control participants for each section of the picture. The participants were asked to name all items they saw on the slide (7).


483


Line bisection. In the Line bisection test (BIT) the participant had to estimate the center of three lines (each 20.4 mm) presented horizontally and in a staircase fashion on a page (12). The Complex line bisection test was a modification of a task described by Butter, Mark, and Heilman (1988). Twelve horizontal lines were spaced in a mirror image on A3 paper, six lines on each half of the paper. In the upper half of the paper three pairs of lines of equal length (63 mm) were placed in a pyramid-like fashion, with the upper pair placed closest to the center of the paper. In the lower half of the stimulus sheet three pairs of lines started from the same distance from the central line. The lengths of the lower half line-pairs from top down were 63 mm, 123 mm, and 185 mm. The participant had to estimate and mark the center of each line. A deviation from the true center in each line was scored (13). Copying. In the Figure and shape copying test (BIT) the tasks were presented and scored according to the BIT manual (10). In the Complex flower copying task (modified from Marshall & Halligan, 1993) the stimulus picture represented two mirror-image flowers unified by a common stem. The total number of details was 21, with 10 on each side and 1 for the common stem. The score for the stem was split in two, making 10.5 the total score for each side (11). In the Sentence copying test the participants were asked to copy a 10-word sentence written across a white paper. The number of letters omitted on each side was recorded (9). Representational Imagery In the Representational drawing test (BIT) the participant was instructed to draw from memory a clock face with numbers, a simple drawing of a man or woman, and a butterfly (5). The blindfold Tactuo-Motor search (TMS) task consisted of searching for wooden cylinders (height 3.6 cm diameter 2 cm) semi-randomly attached among wooden cubes (height 3.6 cm width 2 cm length 2 cm) on an A3-sized search board. The cubes and the cylinders protruded 2 cm above the surface of the board. Beforehand it was confirmed that the participant could tangibly differentiate between the two forms. The blindfolded participants performed the search with their right hand. In the starting position the participant’s hand was placed in the midline of the board (on the two example items) and he or she was instructed to search for all cylinder-shaped targets and to report them. The starting position of the search was verbalized: ‘‘your hand is placed in the middle of a square board.’’ There was no time limit. The maximum score was 12, six on each side (6). Article reading. A Finnish folk story was selected and presented in a similar way as in the original BIT Article reading subtest. Each of the three columns included 58 words. Both the number of words partially or wholly omitted across all three columns irrespective of the position on each line and the number of words consecutively omitted from the beginning of each line were scored (8). Personal neglect. The Personal neglect evaluation included a combination of tasks introduced by Bisiach et al. (1986) and Cutting (1978), and two tasks (using a

484


comb, putting on a pair of sunglasses) from the personal neglect scale by Zoccolotti and Judica (1991). In the first tasks the examiner pointed to the participant’s right hand saying: ‘‘With this hand touch your ear on the opposite side.’’ This instruction was followed by others to touch the opposite little finger, thumb, and finally elbow. The task was done with the participant’s upper limbs placed at the side of the trunk. Scoring: 0 ¼ the participant promptly reaches for the target; 1 ¼ the target is reached with hesitation and search; 2 ¼ the search is interrupted before the target is reached; 3 ¼ no movement is performed towards the target. In the tasks by Zoccolotti and Judica the original scoring 0–3 was used. The largest score 3 indicated a severe deficit and 0 a normal symmetric performance. The assessment was done by a physical therapist (19).


Procedures Cut-off values for impaired performances and the criteria for neglect. Cut-off scores have been commonly used in establishing the limits of normal performance in tests of neglect (Halligan, Cockburn, & Wilson, 1991a; Samuelsson, 1997). In the present study, a cut-off score indicative of impaired performance was set for each test separately at one point below that of the lowest score achieved by the controls (Table 2). In order to obtain a measure of the distribution of omissions, an asymmetry score was calculated for each test separately according to the procedure described by Halligan et al. (1991b): the number of detected or correctly drawn items on the left side was divided by the total number of correctly found or produced items Table 2 Performance of the control group and cut-off scores for defective performance in each task

Clinical tasks Line crossing (BIT) Letter cancellation (BIT) Star cancellation (BIT) Line bisection (BIT) Figure and shape copying (BIT) Representational drawing (BIT) Shape cancellation A3 – random Letter cancellation A3 – random Complex line bisection Complex flower copying Picture scanning (BIT) – Meal – Washbasin Two Part picture Slide Article reading – omissions total – left-side omissions Sentence copying Object finding Tactuo-motor search Personal neglect

Maximum score 36 40 54 4 3 56 56 21 8 9 20 9 174 174 58 20 12

Normal range: total score (asymmetry score)

Cut-off scores: total score (asymmetry score)

36 (0.50) 36–40 (0.47–0.56) 53–54 (0.49–0.51) 33 to þ 18 3–4 (0.48–0.52) 3 (0.44–0.53) 54–56 (0.48–0.51) 48–56 (0.44–0.53) 31 to þ 28 20–21 (0.50) 7–8 (0.50–0.60) 5–9 (0.50–0.60) 18–20 (0.47–0.50) 6–9 (0.40–0.50) 0–1 0 0–7 (0.50–0.59) 18–20 (0.47–0.53) 10–12 (0.45–0.55) 0–3

35 (0.49, 0.51) 35 (0.46, 0.57) 52 (0.48, 0.52) 34, þ 19 2 (0.47, 0.53) 2 (0.43, 0.54) 53 (0.47, 0.52) 47 (0.43, 0.54) 32, þ29 19 (0.49, 0.51) 6 (0.49, 0.61) 4 (0.49, 0.61) 17 (0.46, 0.51) 5 (0.39, 0.51) 4 1 8 (0.49, 0.60) 17 (0.46, 0.54) 9 (0.44, 0.56) 2 in any 6 subtasks

Asymmetry based on lateral omissions, only. More centrally located omissions were left out. Cut-off level was set at 2% omissions of the total amount of words to match the criteria used in the BIT.



485

in the test. In pictures, the asymmetry score was based on the correctly detected items in the lateral sections (targets in the center were not counted). In other cancellation, search, and copying tasks including the TPP the entire left and right halves were included in counting the asymmetry score. A value of 0.50 indicated that an equal number of targets had been detected on each half of the test. A decreased value (lower limit 0.0), indicated left-sided omissions, and an increased asymmetry score (upper limit 1.0) indicated neglect for the right hemispace. Cut-off scores for asymmetry were set at one point from the greatest level of lateralized omissions performed by the controls in each test (Table 2). Both the total performance and the asymmetry scores had to reach the set cut-off level in the same test in order to designate the test performance as neglect, whether contra- or ipsilateral. In the line bisection tasks, deviations from the true center were calculated in mm and prefixed with a () (to the left) or with a (þ) (to the right). The values from each line were added together and a mean value was obtained. Thus, positive mean indicated contralateral and negative mean ipsilateral neglect. In the article-reading task, a performance was designated as contralateral neglect if both the number of words consecutively omitted from the beginning of each line, and the number of whole or partial omissions of words, was at or above the cut-off score. Personal neglect was classified only when the patient received a score of two or more in any of the subtasks. A performance was not scored as personal neglect if the target was reached with hesitation and search, even if performed in such a way in several tasks. The severity of neglect. In the performances showing neglect the degree of the lateralized omissions was classified for each test separately. The classification was modified from Halligan et al. (1991b) and based on the scores showing the extent of these omissions (an asymmetry score, and in line bisection and article-reading tasks the degree of neglect). In partial contralateral inattention the asymmetry score of a test ranged between the obtained cut-off value and 0.1, and in partial ipsilateral inattention between the cut-off point and 0.99. If the asymmetry score of a test was 0.0 the performance was classified as total contralateral neglect, and in total ipsilateral neglect the asymmetry score was 1.0 (all ipsilateral items omitted). In the line bisection tests, standard deviations (SD) were used to determine the severity of biased inattention. Partial contra- or ipsilateral inattentions were scored for values up to 6 SD from the cut-off levels, and deviations of more than 6 SD were regarded as total contra- or ipsilateral inattention. In the article-reading test, up to 57 neglect omissions counted from the beginning of each line, were classified as partial contralateral inattention, and > 57 omissions as total neglect. In the personal neglect test the scoring already included an estimate of the severity. A second, more traditional, severity rating of neglect, based on the number of subtests showing neglect, was also calculated for each patient. Neglect in one to three tests was chosen to indicate mild neglect, and neglect in four or more tests was classified as moderate to severe neglect. Statistical Analyses In group comparisons of the demographic variables the t-test and chi-square were used. The sensitivity of the neglect tests was analyzed descriptively (frequency

486


counts and percentages). Cohen’s kappa was used for measuring agreement between personal neglect measures. In order to describe the relationships between the tests and the patients’ performances a principal components analysis (PRINCALS) for categorical data was applied (SPSS Categories 8.0, 1998). Neglect was either present or absent on a test, thus dichotomous data were analyzed. The method of analysis aimed at making a low-dimensional representation of the patients’ score patterns and of the relationships between the tests. In nine tests there were one or more missing values. The missing values were treated as passive, meaning that all available data were used, deleting only the missing data.


RESULTS Detection of Neglect The percentages of neglect performances detected by each test are shown in Table 3. All of the most sensitive tests were typical conventional measures of visual neglect. Among the picture-scanning tasks the TPP test ranked the highest in detection rate. The lowest number of cases detected was seen in the Representational drawing test; 13% of the patients showed neglect in far space (Slide); and 29% met the criteria for personal neglect. Ipsilateral neglect performances were observed 13 times in total. The occurrence of detected neglect seemed to be influenced by the complexity of the task, with the more complex visual cancellation tests ranking the highest. The age or years of education of the patients did not correlate significantly with any of the tests. In the whole patient group a total of 24 (71%) patients showed contralateral neglect in at least one test. Two patients showed only mild ipsilateral neglect performance and eight (24%) were identified as not showing any form of neglect. Specificity values for each test were calculated and are presented in percentages in Table 3, i.e., the percentage of people without contralateral neglect showing normal (nonlateralized) performance in each test. Ipsilateral performances were treated as false positives for the contralateral neglect condition in this calculation.

Determination of the Severity of Neglect The severity of the biased attention is also shown in Table 3. In some tests only partial contralateral inattention was observed, whereas in one test (Washbasin) only total neglect was detected. Interestingly, the number of cases with total contralateral inattention performances was highest in the Two-part picture (N ¼ 9) and Articlereading (N ¼ 7) tasks. However, the overall sensitivity of these tests was only moderate. In the Shape and Star cancellation tests and Complex line bisection, the number of cases with partial contralateral inattention was clearly higher than that of total inattention. No cases of total contralateral inattention were seen in Figure and Shape copying, Complex flower copying, TMS, or in Representational drawing tests. All ipsilateral neglect performances were partial in severity. Although the analysis shows the variability of the severity of neglect in the patients, it does also suggest that the nature of the task may influence how the neglect is manifested.

487 10 (29%) 7 (21%)

34 33

(52%) (48%) (41%) (38%) (36%) (36%) (36%) (35%) (32%) (29%) (26%) (21%) (21%) (18%) (13%) (9%) (6%)

17 13 14 13 12 12 9 12 11 10 9 7 7 5 4 3 2

33 27 34 34 33 33 25 34 34 34 34 34 34 28 30 33 34

0

5 2 2 6 5 7 0 9 3 0 4 1 3 1 2 3 0

Total

7

12 11 12 7 7 5 9 3 8 10 5 6 4 4 2 0 2

Partial

Testwise total and partial contralateral inattention performances1

1

3 1 1 1 0 0 0 1 0 0 1 0 0 0 0 0 1

Number of ipsilateral neglect performances Total

1

1

1

1

3 1 1 1

Partial

Testwise total and partial ipsilateral inattention performances2

100 100

89 100 90 100 100 100 100 90 100 100 100 100 100 100 100 100 100

Percent of patients without neglect showing normal performance3 (%)

Rank ordered by percentages detecting contralateral neglect. 1 Total contralateral inattention performance (asymmetry score 0.0), partial contralateral inattention performance (asymmetry score cut-off to 0.1). 2 Total ipsilateral inattention performance (asymmetry score 1.0), partial ipsilateral inattention performance (asymmetry score cut-off to 0.9). 3 Percentages calculated from patients without contralateral neglect.

Conventional and behavioral tests Shape cancellation=random Complex line bisection Star cancellation Line bisection Letter cancellation=random Article reading Complex flower copying Two part picture Letter cancellation Figure and Shape copying Line crossing Object finding Picture scanning – Meal Sentence copying Slide Picture scanning – Washbasin Representational drawing Other tests of neglect Personal neglect Tactuo-motor search

Clinical tasks

Number of contralateral neglect Number of performances patients (% positive tested performances)

Table 3 Number and percentages of positive neglect performances detected by each test and testwise distribution of total and partial inattention performances


488


The six tests reported to be the most sensitive were evenly distributed across the battery (beginning, middle, end) and total neglect omissions occurred also throughout the battery. Already in the first three tasks (Object finding, Line crossing, TPP) patients made total neglect omissions (Table 3). This contrasts the thought that tasks employed in the end of the battery would have been potentially prone to more errors due to fatigue effects. Among the contralateral neglect patients, nine were classified as having mild neglect (in one to three tests) and the rest moderate to severe neglect.


Profiles of Test Performances of Individual Patients The tests were grouped according to type, and presented in performance profiles of individual patients. These groupings are presented in Table 4. Neglect in line bisection and cancellation tasks dissociated in three patients. One patient (8) showed neglect in only line bisection, and one patient (33) in only paper and pen cancellation tests. Two patients (31, 35) showed neglect in only picture scanning or object finding (behavioral tasks). Neglect in reading alone was not present in any patients, but in one patient (3) it occurred with personal neglect only. Neglect in far space was detected in four (12%) patients, but only in combination with neglect in near space. Likewise, personal neglect occurred only together with visual neglect in near or far space. Of all the patients with neglect, 13 (54%) showed neglect in only near extrapersonal space and not in Slide or Personal neglect. A majority (83%) of the patients with neglect showed neglect across two or more types of tests. Comparison between the Different Groups of Tests The present test battery included visual tests that were either self-constructed modifications, single tests of neglect, or tests that have not earlier been used for detecting neglect. To ascertain the validity of these tests (called SET 2) the number of all neglect cases detected by them was compared with the number of cases detected by the eight subtests from the BIT including ipsilateral cases (Table 5). The tests in SET 2 were more sensitive to the presence of neglect, detecting eight cases that were not detected by the BIT, while one case detected by BIT was negative according to SET 2. Classifications according to the two groups of tests were in agreement for 73.5% of the patients. In the personal neglect task the usefulness of the task selection (pointing to parts on ones own body vs the use of two common objects) was evaluated. The Cohen’s kappa showed that measurement of agreement was low between these two types of tasks (kappa ¼ 0.09). Nine patients with personal neglect were identified by the sunglasses and comb subtasks, and only one patient was identified by the pointing task. Dimensions of Visuospatial Neglect Performances In order to investigate possible associations between the tests more closely, a Principal components analysis (PRINCALS) for categorical data was applied to

489

14 15 13 4 17 11 29 25 24 16 12 10 27 36 30 18 20 3 21 28

1

1 1 1 1 1 1 ip 1

1 1 1 1 1 1 1 1

1 1

1 1 1 1 1 1 1 1 1 1 1 ip 1 1 1 1 ip

1 1 1 1 1 1 1 1 1 1 1 1 ip 1 1 1 1

1 1 1

1 1 1 1 1 1 1 1 1

1

1 1 1 1 1 1 1 1 1 1 1 1

1

1

1 1 1 1 1 1 1 1 1 1

1

1

1 1

1 1

1

1 1 1 1

1

ip

1

1

1 1 1 1

1

ip

1

1

1

1

1

1 1

1

1 1 1 1

1 1 1

(Continued)

9 9 9 9 9 9 8 8 8 7 6 5 5 4 4 2 3 2 2 2

Line Letter BIT Picture Number of Patient bisection and Shape cancellation scanning Copying Article Object Sentence TMS Representational Personal contralateral neglect number tasks cancellations tasks tasks tasks reading finding copying search drawing Slide neglect by type of task

Table 4 Performance profiles of individual patients according to the test type


490

8 33 31 35 19 32 6 1 5 7 9 22 26 34 N %

17 14%

–

ip

ip

ip ¼ ipsilateral neglect.

17 14%

1

16 13%

ip

1

14 11%

ip

1

13 10%

12 10%

7 6%

1

5 4%

7 6%

2 2%

4 3%

10 8%

1 1 1 1 0 0 0 0 0 0 0 0 0 0 124

Line Letter BIT Picture Number of Patient bisection and Shape cancellation scanning Copying Article Object Sentence TMS Representational Personal contralateral neglect number tasks cancellations tasks tasks tasks reading finding copying search drawing Slide neglect by type of task

Table 4 Continued



491

Table 5 Comparison between 8 subtests from the BIT and a selection of 11 other visual neglect tasks (SET 2) SET 2 BIT


No neglect % count within BIT neglect % count within BIT Total

No neglect

Neglect

Total

8 50.0% 1 5.6% 9

8 50.0% 17 94.4.% 25

16 100% 18 100% 34

the data (neglect=no-neglect performance) obtained in every test for each patient. In this analysis all 19 tasks were used. Two dimensions emerged in this analysis. The first dimension explained a rather large proportion of the variance (50%). The second dimension explained only 9% of the variance, which is however still above the percentage of variance that a single test can explain on average (100=19 ¼ 5.3). The first dimension indicated the severity of neglect, while the second dimension was related to different types of neglect performances. Most tests loaded positively and high on the first dimension; only two tests, Slide and Representational drawing, loaded on the second dimension. In the second dimension the results showed neglect in Representational drawing (high positive value) to be associated with non-neglect in Slide (low negative value) and vice versa. Three of the patients with severe neglect (cases 16, 17, and 29) did not show neglect in far space (Slide), but in Representational drawing and many other visual neglect tasks in near space. One severe case (4) and two cases with moderate neglect (25, 10) showed neglect in both far space (Slide) and near space tasks, but not in Representational drawing. Tactuo-motor search seemed more related to the other tests than Representational drawing in this analysis, although both are considered tasks of representational imagery. The results suggest that most of our selected tests measured the severity of neglect in near extrapersonal space, but that other aspects contributing to the symptomatology may be present. However, with 34 participants the results of the analysis must be interpreted with caution. Selection of Tests for a Clinical Battery When selecting the most useful tests from the present set we emphasized the following aspects: test sensitivity, important dissociations, and severity of neglect. The selected tests should detect all cases, not leave out important dissociations between test types, and keep severity classification of neglect stable. The three most sensitive tests (Random Shape cancellation, Complex Line bisection, Star cancellation) together detected 88% of the 24 neglect cases. In order to catch all neglect cases, Two Part picture, Article reading, and Object finding had to be added. Article reading was preferred above Personal neglect because of higher sensitivity. When dissociations between types of neglect performances were also considered, the same six tests could still be selected. In order to keep the severity classification for each patient unaffected, Letter cancellation, Line bisection, Random

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Letter cancellation, and Picture scanning (Meal) had to be added to the battery. Thus the final selection included a total of 10 visual neglect tests. Although Slide (far space), Representational drawing, and Personal neglect did not detect any additional cases of neglect or clearly dissociated from other types of tests, these could be included to cover separate spatial aspects. Finally, the new combination of 10 visual neglect tests was contrasted with the eight subtests of BIT. No cases detected by the BIT went undetected by the new battery. On the other hand, the new battery detected seven more cases. Agreement between BIT and the new, partially overlapping battery reached 79.4%.


DISCUSSION The heterogenous and multifactorial nature of neglect is not a new finding, but most of the former studies have inadequately described its multiplicity. Indeed, instead of ‘‘neglect’’ one should use the term ‘‘neglect syndrome,’’ because there are both multiple clinical presentations as well as apparently a variety of underlying lesions. This wide variability makes it difficult to cover the whole syndrome within one study, e.g., simply by patient compliance as a limiting factor. In this study we concentrated on the visuospatial, representational, and personal aspects of neglect, omitting, for example, motor neglect and extinction. However, these phenomena are obvious parts of the neglect syndrome, and their relationships to the results of this work are worth studying. The location of the lesion within the right hemisphere is undoubtedly a likely explanation for the variable dissociations of the clinical tasks. These clinical–anatomical connections in our study material are a subject of a separate report. Choosing a Test Battery for Neglect The results of this study showed that on the level of single tests, symbol cancellations and line bisection ranked highest in sensitivity. Otherwise, great differences occurred in the detection rate of neglect between different types of tests. Thus, we confirmed many earlier findings of test sensitivity and dissociations, but also provided data for comparing how neglect is manifested in several clinical measures, and to what extent neglect in the personal–extrapersonal domain occurred in a small clinical sample. Our study supports the former conclusion that several tests are more likely to reveal neglect than a single test (Agrell et al., 1997; Halligan et al., 1989). A selection of 10 tests from the original battery of 19 tests was needed to detect most cases with neglect performance and also to keep ratings of severity and neglect dissociations unchanged. In contrast to earlier studies where the focus has been merely on the sensitivity of tests, or combination of tests, to detect neglect (Agrell et al., 1997; Halligan et al., 1989; Jehkonen et al., 1998; Marsh & Kersel, 1993), in the present study the focus was extended to aspects of severity and dissociations when analyzing the usefulness of selected tests. In cases where only one neglect performance is observed there is always the possibility of a false diagnosis. Therefore we emphasize the use of several tasks, and in ambiguous cases taking into consideration also the qualitative aspects of the performance (total vs. partial inattention). In clinical decision making, one partial inattention performance is seldom enough for a neglect diagnosis, but one total may be. Even if not addressed in this study, other


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indicators, such as the tendency to start a clinical task on the right side (Jalas et al., 2002), or behavioral observations (Appelros, Nydevik, Karlsson, Thorvwalls & Seiger, 2003), can give additional information about the possible underlying orienting bias. Furthermore, the results support earlier findings that spatial aspects (at least near and far) deserve attention when examining neglect.


Neglect Manifestations in Single Tests In the present study Shape and Star cancellations and Line bisection tasks provided the most sensitive estimates of neglect, ranging from 38% to 52%. This confirms earlier findings of these tasks being sensitive indicators of neglect (Halligan & Robertson, 1992, Kinsella et al., 1995). Our results were also in line with earlier findings by Weintraub and Mesulam (1985, 1988), who showed that shapes were more sensitive than letters in detecting neglect. Our result on Random Shape cancellation being the most sensitive task is supported by previous findings of Kinsella and colleagues (1995). In their study the Random Shape cancellation was the most sensitive test of neglect, providing a 43% detection rate of neglect out of a battery of six tests, applied on a patient group of 40 patients with right cerebral accident on average 2 months post-stroke. Our somewhat higher rate of 52% may be due to differences in scoring the laterality of omissions and the somewhat more acute stage. The asymmetry scoring used in the present study, in combination with the use of cut-off levels in determining neglect, has been shown to have the advantage of giving a reasonably homogenous estimate of the laterality of the defective performance (Samuelsson, 1995), while also catching cases with mild inattention. Placing the stimulus in the contralesional hemispace might have added the sensitivity in some tests (Heilman & Valenstein, 1979, Mennemeier, Vezey, Chatterjee, Rapcsak, & Heilman, 1997), but would also have caused one more confounding factor, which would disturb the evaluation, for example in laterality comparisons to other studies and controls. The percentages of detected neglect in line bisection tasks (38% to 48%) are somewhat lower than what has been reported earlier (Agrell et al., 1997, Halligan et al., 1989). However, the percentages in these studies were calculated from the number of detected neglect participants, and not from the total number of participants studied as in the present study. The Complex Line bisection gave a somewhat higher percentage (48%) of detected neglect than the Line bisection task of BIT (38%), which, on the other hand, was close to what has been reported in line bisection earlier (Kinsella et al., 1995; Marsh & Kersel, 1993). The difference may partly be due to the lower number of participants examined with the former test, but also to the higher complexity of the task. The two line bisection tasks used differ with respect to the number and length of lines and structure of the display. In contrast to the stimulus material used in the study by Butter et al. (1988), from which the idea for the Complex Line bisection was applied, the present lines were shorter and displayed at the same time on one sheet. In their study the patients’ errors were significantly related to the length of lines, but also to the increasing distance of the short lines from the mid-central line into the left hemispace. Although this distance (gap) was not analyzed as a separate variable in the present study, this aspect may have contributed to the high detection of neglect performances in this test.


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For clinical purposes it would be important to know how patients in general perform in commonly used tasks, and if these tests differ in exhibiting partial or total neglect. Halligan et al. (1991b) have described this aspect in a large study using the six conventional subtests from the BIT. In the present study no patients made total contralateral omissions in the BIT Figure and Shape copying and Representational drawing tasks, which is in line with their findings. Besides, this lack of total neglect was also seen in another copying task (Complex Flower) and the blindfold TMS. In general, an increase of partial inattention performances in most sensitive tests was exhibited in both studies. The present study also extends these earlier findings, by providing descriptions of neglect severity for several other tests, too. In the present study both Article reading and Two Part picture were the tasks in which the most total contralesional omissions occurred. Although the reason for this finding could not be directly addressed in this study, there seem to be some similar characteristics in the tasks. Both tasks are clearly characterized by discontinuity in stimulus display in contrast to all the other tests, except for the Complex line bisection. The Two-Part picture is divided by a gap, and the text in the Article is divided in columns. In experimental studies discontinuity has been observed to be important in the exhibition of neglect deficits (Kartsounis & Warrington, 1989) and to the allocation of attention (Farah, Wallace, & Vecera, 1993). Observed Dissociations and Dimensions in Test Performance The dissociation between neglect in line bisection tasks as opposed to visual scanning tasks, observed in some patients, confirms earlier notions of separate components of neglect (Binder et al., 1992; McGlinchey-Berroth, Bullis, Milberg, Verfaillie, Alexander, & D’Esposito, 1996; Shinichiro et al., 2001) and the importance of these types of tasks to be included in neglect batteries. Of the neglect patients, 54% (N ¼ 13) showed neglect only in near extrapersonal space (not personal neglect), which is in line with findings from single case studies that peripersonal neglect can occur in isolation (Halligan & Marshall, 1991). Neglect in far space measured with the Slide occurred in four patients, co-existing always with near extrapersonal neglect. Although no clear evidence for independent neglect in far space occurred in this patient group, the results showed that the phenomenon is clinically present in some patients, and therefore important to consider in evaluations. Neglect of far space can easily lead to spatial misjudgments, and further increase the risk for accidents in daily living and traffic situations. Earlier notions of neglect being more severe in far space than near space (Cowey, Small, & Ellis, 1994; Vuilleumier et al., 1998) were not supported in the present study. Of course, the fact that only one task measured neglect in far space limits the conclusions. The PRINCALS results showed that the Slide test, but also Representational drawing, seemed to distinguish itself from the other tests. In the present study the PRINCALS analysis clearly has its limits due to the small participants-to-variables ratio. The results can mostly be considered preliminary, but seem to be in line with earlier findings of more than one underlying aspect related to the neglect phenomena (Kinsella et al., 1995, McGlinchey-Berroth et al., 1996). In earlier studies using factorial models, no measure of neglect in far space has been included, as far as we know. Representational drawing, however, has been reported to load on a



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separate factor called spatial representation and imagery in a study by Kinsella and colleagues (1995), together with a Tactile Maze task. In the study by Halligan et al. (1989), where the conventional subtests of the BIT loaded on only one factor, the Representational drawing had the lowest loading and was also the least sensitive test in their study. Clearly, further studies for clinical evaluation of the underlying aspects of neglect are needed. Although personal neglect did not emerge as an independent disorder in any patient, its amount was comparable to what Zoccolotti, Antonucci, and Judica (1992) reported in their hemi-inattentive patient group. In their study about half of the neglect patients displayed asymmetric performance in a personal neglect measure. In our study 10 out of 24 (42%) patients with contralateral visual neglect also showed personal neglect. Our results support the use of common objects in the personal neglect evaluation rather than pointing to parts of one’s body. Since the start of the present study, new promising techniques of testing aspects of personal neglect have been reported, and thus their possible influence on our results cannot be evaluated (Beschin & Robertson, 1997; Cocchini, Beschin, and Jehkonen, 2001). It seems, though, that the reported incidence of personal neglect is on the level of earlier studies. SUMMARY In the present study different types of neglect manifestations were explored in a patient group examined on average 2–3 weeks after right hemisphere stroke. Although the present results support many previous findings of test sensitivity and dissociations, they also demonstrate the need for further studies concerning the structure of common clinical batteries and tasks. Especially, there is a need to develop clinical methods to study the spatial aspects other than near space in the neglect syndrome. We underline the importance of including several types of measures in a comprehensive assessment of neglect. In this study a minimum of 10 tests was needed to cover all the various aspects of detection, dissociations, and severity of neglect. Clearly, more than one test is needed, also for screening purposes. ACKNOWLEDGMENT This study was supported by the Academy of Finland (Grant # 37873 for Heikki Ha¨ma¨laïnen), University of Turku, and Turku University Central Hospital. We are grateful to Dr. Matti Haataja and the personnel at the Department of Rehabilitation and Department of Neurology at the University Central Hospital of Turku for the help and encouragement we have received during this study. REFERENCES Agrell, B. M., Dehlin, O. I., & Dahlgren, C. J. (1997). Neglect in elderly stroke patients: A comparison of five tests. Psychiatry and Clinical Neurosciences, 51, 295–300. ˚ . (2003). Assessing uniAppelros, P., Nydevik, I., Karlsson, G. M., Thorwalls, A., & Seiger, A lateral neglect: Shortcomings of standard methods. Disability and Rehabilitation, 25(9), 473–479.


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