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The ecological assessment of unilateral neglect
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The ecological assessment of unilateral neglect Philippe Azouvi a,*,b a
AP–HP, hoˆpital Raymond-Poincare´, service de me´decine physique et de re´adaptation, 92380 Garches, France EA 4047 HANDIReSP, universite´ Versailles – Saint-Quentin, UFR des sciences de la sante´ – Simone-Veil, 2, avenue de la Source-de-la-Bie`vre, 78180 Montigny-Le-Bretonneux, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 May 2015 Accepted 23 December 2015
Conventional paper-and-pencil tests of unilateral neglect are of limited ecological validity. To address this issue, a number of assessment procedures have been proposed to provide clinicians and researchers with more ecologically valid assessments of unilateral neglect, which may be useful to plan rehabilitation and to measure the generalization of the effects of rehabilitation to daily life. We present here an overview of the different assessment measures available in the literature. The most widely used scales are the Behavioural Inattention Test (BIT), the semi-structured scales for assessment of personal and extra-personal neglect, the Subjective Neglect Questionnaire, the Baking Tray Task, the wheelchair obstacle course, the ADL-based neglect battery, and the Catherine Bergego Scale (CBS). The CBS is probably, to date, the most widely used behavioural assessment instrument for unilateral neglect. It has been found to be reliable, valid, and sensitive to change during rehabilitation. It also enables the assessment of awareness of the consequences of unilateral neglect in daily life skills. ß 2016 Elsevier Masson SAS. All rights reserved.
Keywords: Unilateral neglect Stroke Assessment Ecological validity
1. Introduction Unilateral neglect is defined as the ‘‘failure to report, respond, or orient to novel or meaningful stimuli presented to the side opposite a brain lesion, when this failure cannot be attributed to either sensory or motor defects’’ [1]. This complex disorder of spatial cognition can have an impact on numerous daily living activities. Patients affected behave as if they were oblivious of half of the space around them, or even of their own body. In the most severe cases, the patient presents permanent deviation of the head and gaze towards the right, and ignores any solicitations from the side opposite to the brain lesion. During meals, the patient may upset plates located to their left, or fail to eat the food on the left side of their plate. They omit the left-hand page in a book, or they miss details situated on the left of drawings or photographs. Paterson and Zangwill [2] also noted that one of their patients could not get his left leg into his trousers, and sometimes even tried to put both legs in the same trouser leg. Unilateral neglect can also appear in other elementary activities, such as writing, drawing or games. A tendency for the patients to systematically turn right when they should be turning left, leading sometimes to erratic circular movements, was noted in the early observations [3], as
* Correspondence. E-mail address: [email protected].
well as the occurrence of collisions with objects located to the left. Neglect can also affect the use of the body, with some patients losing motor spontaneity in their left hand, despite normal strength (motor neglect) [4]. Numerous clinical tests, whether pencil-and-paper or computerised, have been proposed to assess unilateral neglect, but they sometime lack sensitivity. A large body of research has shown the possibility of discrepancies between performance on classic clinical tests and patient functioning in everyday life, in particular among patients in the chronic phase. These discrepancies could be due to a retest effect, or to the differing nature of mechanisms involved in clinical tests and in daily life. Indeed, the administration of a test, like rehabilitation programmes, could rely essentially on mechanisms requiring the voluntary orienting of attention. In contrast, in daily life, the automatic orienting of attention is essential. A specific deficit in this particular area could reflect the persistence of a neglect behaviour contrasting with good performance on tests. These discrepancies are problematic, both for detecting difficulties that could have an impact on the patient’s daily life, and for assessment of the generalisation of effects in therapeutic trials. Several recent reviews have underlined that the absence of ecological measures of the efficacy of treatment is a frequent weakness of numerous therapeutic trials [5]. Several evaluation instruments have been proposed to assess the impact of unilateral neglect in daily life, and a few reviews have
http://dx.doi.org/10.1016/j.rehab.2015.12.005 1877-0657/ß 2016 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2015.12.005
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REHAB-949; No. of Pages 5 P. Azouvi / Annals of Physical and Rehabilitation Medicine xxx (2016) xxx–xxx
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been published recently on assessment of unilateral neglect [6–8], or more specifically on the use of virtual reality in the assessment of neglect, which we will nor discuss here because these tools are not yet in widespread use [9,10]. However, to our knowledge, no review has been devoted specifically to ecological evaluations. Yet, the issue is important, in particular for the evaluation of the efficacy of rehabilitation among patients with unilateral neglect. The aim of the present article is to present a critical review of these tools, with a particular focus on their psychometric qualities and on their limitations. 2. The Behavioural Inattention Test (BIT) The BIT [11,12], in addition to conventional tests, comprises a set of nine tests termed ‘‘behavioural’’, which simulate daily living activities, thus thought to draw closer to the real impact of the condition. The subject is asked to describe three large-sized photographs showing familiar scenes (a meal, a bathroom, and a large hospital ward), to dial a telephone number, to read a menu in four columns on an A3 format sheet, to read a newspaper article, to tell the time on a clock (digital and analogue) and to put a clock right, to point out coins among 18 items belonging to six categories, to copy an address and a sentence, to follow a route on a map, and to point out cards in an arrangement of 16 cards (Table 1). Each subtest is scored out of 9 (with a higher score corresponding to a better performance) giving a maximum score of 81. The validation study showed that the number of patients obtaining a pathological score was larger among those with lesions in the right than in the left hemisphere, except for the item entailing following a route on a map [12]. The most discriminant subtests between patients with unilateral neglect and those without (on the basis of the pencil-and-paper test battery) was the coin-sorting task. Test–retest reliability and inter-rater reliability were satisfactory. However, the behavioural battery was not more sensitive than the conventional tests, nor was it better correlated statistically with actual difficulties experienced, assessed using an occupational therapy checklist or an autonomy measure. It is thus difficult to conclude that these subtests possess better ecological relevance than the pencil-and-paper tests included in the battery. 3. Two semi-structured scales for the assessment of personal and extra-personal hemineglect Zoccolotti et al. [13,14] proposed an evaluation based on semistructured situations and simulations of daily living tasks using real objects. This evaluation comprises two scales, corresponding to ‘‘extra-personal hemineglect’’ (serving tea, dealing cards to four people sitting round a square table, describing three complex pictures, and describing a room) and to ‘‘personal hemineglect’’ (use of everyday objects: razor or make-up, comb, glasses). Each item is scored from 0 (normal) to 3 (severe). Inter-rater reliability
was good. A statistical analysis of the internal validity of the test showed a differentiation between extra-personal and personal items, confirmed by single-case studies evidencing double dissociations. The extra-personal scale was significantly correlated with the pencil-and-paper tests, but this was not so for the personal scale. Thus, the distinction between these two types of hemineglect appears as one of the original contributions of this scale. Beschin and Robertson [15] refined the scoring of the personal scale by counting the number of strokes of the comb (or a razor) on each side for 30 seconds (comb and razor test). Committeri et al. [16], using these semi-structured scales, showed that bodily and extra-bodily hemineglect resulted from lesions with different topology (extra-personal hemineglect was linked mainly to a network implicating the right frontal cortex and the upper temporal regions, while personal hemineglect was linked to the right lower parietal cortex). 4. The Subjective Neglect Questionnaire [17] The above scales require the patient to be placed in a test situation, which is therefore artificial. Towle and Lincoln [17] proposed a 19-item questionnaire administered to patients and proxies, asking them to rate the presence of difficulties in certain situations of daily living (for instance, bumping into furniture or doorways, putting only one foot on the footrest of the wheelchair, having difficulty telling the time on a clock face). Initially, each item was scored on a five-point scale according to the frequency of the occurrence of the difficulty (ranging from at most once a month to at least once a day). This scoring system however proved difficult to use, and was replaced by a binary score (present or absent in the preceding month). Scores were significantly correlated to performances on the star cancellation test. These authors also demonstrated differences between patients’ and relatives’ ratings. Finally, the relatives (unlike the patients) signalled significantly more problems among patients with unilateral neglect, in particular for the items difficulty in maintaining the trajectory for the wheelchair, clumsiness, and difficulty telling the time. 5. The Baking Tray Task This test consists in distributing 16 cubes regularly across a board (as if they were buns on a baking tray to be put in the oven) [18]. The board measures 75 100 cm, and the cubes 3.5 cm. The scoring, using a grid, is based on the number of cubes in each half of the board. Double dissociations were observed between this test and classic pencil-and-paper tests, and the baking tray test appeared more sensitive than the conventional tests. The score was not significantly correlated with those of the pencil-and-paper tests. The authors tested a version with a smaller board (A4 format) on a few patients, and it appeared slightly less sensitive. The advantages of this test are its simplicity and speed of completion.
Table 1 Comparison of the main ecological scales assessing unilateral neglect. Scale
Scoring method
Neglect components
Inter-rater reliability
Assessment of anosognosia
BIT [11,12] Semi-structured scale for personal and extra-personal neglect [13,14] Subjective neglect questionnaire [17] Baking tray task [18] Wheelchair obstacle course [19,20] Standardised activities of daily living [21] CBS [22–25]
Standardised testing Observation in standardised conditions
P P and EP
+ +
No No
Questionnaire (self and proxy) Testing under standardised conditions Testing under semi-standardised conditions Standardised testing Observation in naturalistic conditions and self-questionnaire
P and EP EP EP P and EP P and EP and anosognosia
NT NT NT + +
Yes No No No Yes
BIT: Behavioural Inattention Test; CBS: Catherine Bergego Scale; P: personal neglect; EP: extra-personal neglect; +: good inter-rater reliability; NT: not tested.
Please cite this article in press as: Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2015.12.005
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However, any advantage over the other tools, and especially its ecological relevance, need to be ascertained. 6. Wheelchair obstacle course Several authors looked specifically at ‘‘driving’’ a wheelchair, often a source of difficulties for patients with unilateral neglect, as they tend to bump into objects located to their left [19,20]. The test consists in asking the patient to manoeuvre the wheelchair along a pre-determined itinerary, looking for target landmarks and/or avoiding obstacles. The scoring takes account of the presence of bumps, and where they occurred (front, lateral right or left). However, this type of evaluation is difficult to reproduce from one facility setting to another. 7. Standardised activities of daily living testing Eschenbeck et al. [21], along the lines of the BIT, proposed an assessment battery combining 6 classic pencil-and-paper tests and 8 daily living activities, also providing threshold scores. The aim was to achieve better standardisation of the situations assessed, and to take account of the different components of space, personal, peri-personal and extra-personal (while the BIT explores only the peri-personal space). The daily living activities used were: copying an address, dialling a phone number, telling the time, putting cream on the face, brushing hair, completing a form, assembling items on a tray, and sorting coins. For several of these tasks, the patient needed to detect an item essential to the task that was located to their left. Inter-rater reliability was good. The conventional tests were however more sensitive than the ecological tests. Dissociations were observed for 7 patients between the two assessments (6 presented neglect on the penand-paper battery but not on the ecological battery, and one presented the reverse). Severity of the neglect phenomenon on this battery was linked to the presence of right frontal-parietal network lesions. 8. The Catherine Bergego Scale (CBS) We have developed a functional scale for the evaluation of unilateral neglect, the Catherine Bergego Scale (CBS) [22–25] (Table 2). This scale aims to score neglect behaviours in standardised, semi-quantitative manner, using observation of the patient by a therapist in different daily living situations. The second objective of the CBS is to assess the patient’s awareness of his or her difficulties, by comparing observation data with interview data. The scale comprises 10 items relating to elementary activities, each scored from 0 (normal) to 3 (severe unilateral neglect). A global score is then
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calculated, ranging from 0 to 30. We chose to arbitrarily distinguish three levels of severity for CBS scores: from 1–10, mild neglect, 11–20 moderate neglect, and 21–30 severe neglect. Inter-rater agreement was good [24]. On a group of 50 patients, we noted that internal consistency, (assessed from the correlation of each of the 10 items with the global score) was good, and that the global CBS score was significantly higher in the group of patients presenting unilateral neglect on paper-and-pencil tests [22]. The global score was significantly correlated with functional independence [22]. The three most sensitive items were awareness of the left hemi-body, dressing, and moving around (collisions) [22]. The internal structure of the scale was assessed on a group of 83 patients with a right hemisphere stroke [23]. Both principal component analysis (PCA) and the Rasch model showed that the 10 items in the scale corresponded to a single underlying factor. Differing results were reported by Goedert et al. [26]. These authors studied 51 patients with unilateral neglect following right hemisphere stroke, on average 22.3 days after the stroke. They used PCA, which showed two underlying factors in the CBS: one perceptive-attentional factor (named CBS-PA) and one motorexploratory factor (CBS-ME). Only this second factor was predictive of dependence for daily living activities as assessed by the Barthel index. The perceptive-attentional factor was correlated with the clinical tests (on the BIT) but was not predictive of functional dependence. In all the above-mentioned studies, the CBS appeared more sensitive than any of the paper-and-pencil tests considered alone, and dissociations were observed between the two types of evaluation. Another advantage of the CBS is that it takes account of different aspects of unilateral neglect: bodily, peri-personal, and extra-personal, which is not the case for most of the other assessment tools. Further to this, we were also able to study unilateral neglect in daily life following left hemisphere lesion [25]. Surprisingly, a large number of patients (77.3%) obtained a score above 0 on at least one item. Nevertheless, right-sided neglect was not very severe, since only 5.4% of the patients reached a score above 10 (versus 36% for left neglect following right hemisphere stroke). Right neglect mainly involved the personal space. An anosognosia score can be calculated from the difference between the examiner and the patient ratings. This anosognosia score was strongly significantly correlated to the severity of the unilateral neglect [23]. However, dissociations were observed, with certain patients presenting moderate unilateral neglect having anosognosia scores that were close to 0 [25]. Vocat et al. [27] studied anosognosia using the CBS in patients with right hemisphere lesions, and showed that disagreements between examiner and patient were very marked in the acute phase, but decreased at a more
Table 2 Catherine Bergego Scale – (English translation for information only, not validated in English).
1. 2. 3. 4. 5. 6. 7. 8. 9. 10.
Fails to groom or shave the left part of his/her face When dressing fails to adjust the left side correctly (sleeve, slipper. . ..) Leaves food on the left side of his/her plate Forgets to wipe the left side of his/her mouth after eating Exhibits difficulty in looking towards the left Ignores the left part of his/her body (e.g. does not put his/her upper limb on the armrest, or his/her left foot on the wheelchair footrest, or forgets to use his/her left arm when he/she needs to) Does not notice or pay attention to noise or people addressing him/her from the left Collides with people or objects on the left side, such as doors or furniture (when walking or in a wheelchair) Has difficulty in finding his/her way towards the left when moving about in familiar places or in the rehabilitation unit Has difficulty finding his/her personal belongings in the room or bathroom when they are on the left side Total score (/30)
0
1
2
3
& & & & & &
& & & & & &
& & & & & &
& & & & & &
& &
& &
& &
& &
&
&
&
&
&
&
&
&
0: non neglect; 1: mild neglect; 2: moderate neglect; 3: severe neglect.
Please cite this article in press as: Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2015.12.005
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chronic stage. They also showed that anosognosia of neglect, as assessed by the CBS, was not significantly correlated with anosognosia of hemiplegia, whatever the stage. Chen et al. [28,29] proposed a new scoring method for the CBS based on detailed instructions for observation and scoring (the Kessler Foundation Neglect Assessment Process). Using this scoring method, they found results comparable to ours for the one-dimensional structure of the scale and the significant correlations with measures of functional independence. Qiang et al. [30] noted a significant correlation between the CBS score and a standardised wheelchair driving test, and with the Functional Independence Measure (FIM). Luukkainen-Markkula et al. [31] compared the CBS and the BIT among 17 patients exhibiting neglect. Discrepancies were observed in certain patients between mild neglect in paper-and-pencil tests and severe ratings on the CBS. Only the line-bisection test in the BIT was significantly correlated with the CBS. Oh-Park et al. [32] recently showed that the CBS score in the early phase (less than two months after a stroke) was significantly predictive of mobility 6 months poststroke, in the same manner as with the BIT. Thus the proportion of patients unable to move around outside the home independently was 0%, 27.3% and 72.7% for patients respectively presenting mild, moderate or severe unilateral neglect on the CBS (total scores on the CBS: 1–10, 11–20, and 21–30). The CBS has been used in several studies on rehabilitation as an assessment criterion for efficacy and transfer of rehabilitation gains to everyday life. The scale has been used in several trials using prism adaptation [33–40], motor cueing [34,41], eye patching in association with constraint-induced therapy [42], virtual reality [43], upper limb training with a rehabilitation robot [44] or transcranial magnetic stimulation [45,46]. Several of these studies have shown that the CBS was sensitive to change and could therefore be used as a measure of the generalization of the effects of treatment to daily life. 9. Conclusion The behavioural assessment of unilateral neglect is a useful complement to classic pencil-and-paper tests. It can sometimes enable the detection of difficulties that might otherwise have gone unnoticed. The choice of the assessment instrument to use depends on the moment, the setting, and the time available. When the patient is still in a rehabilitation facility, the CBS is probably the best-suited measure. The CBS can also be used as a questionnaire for the patient’ relatives, but with adequate caution because its validity has not been established in this application. Disclosure of interest The author declares that he has no competing interest. Acknowledgements We would like to thank members of the GEREN group who contributed to some of the studies mentioned in this article, as well as the occupational and speech therapy teams in RaymondPoincare´ hospital (Garches) and La Salpeˆtrie`re hospital (Paris) who took part in the collection of data for the CBS. This article is dedicated to the memory of Catherine Bergego (1949–1994) who provided inspiration for a large part of this work. References [1] Heilman KM, Watson RT, Valenstein E. Neglect and related disorders. In: Heilman KM, Valenstein E, editors. Clinical neuropsychology. New York: Oxford University Press; 1993. p. 279–336.
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The ecological assessment of unilateral neglect Philippe Azouvi a,*,b a
AP–HP, hoˆpital Raymond-Poincare´, service de me´decine physique et de re´adaptation, 92380 Garches, France EA 4047 HANDIReSP, universite´ Versailles – Saint-Quentin, UFR des sciences de la sante´ – Simone-Veil, 2, avenue de la Source-de-la-Bie`vre, 78180 Montigny-Le-Bretonneux, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 May 2015 Accepted 23 December 2015
Conventional paper-and-pencil tests of unilateral neglect are of limited ecological validity. To address this issue, a number of assessment procedures have been proposed to provide clinicians and researchers with more ecologically valid assessments of unilateral neglect, which may be useful to plan rehabilitation and to measure the generalization of the effects of rehabilitation to daily life. We present here an overview of the different assessment measures available in the literature. The most widely used scales are the Behavioural Inattention Test (BIT), the semi-structured scales for assessment of personal and extra-personal neglect, the Subjective Neglect Questionnaire, the Baking Tray Task, the wheelchair obstacle course, the ADL-based neglect battery, and the Catherine Bergego Scale (CBS). The CBS is probably, to date, the most widely used behavioural assessment instrument for unilateral neglect. It has been found to be reliable, valid, and sensitive to change during rehabilitation. It also enables the assessment of awareness of the consequences of unilateral neglect in daily life skills. ß 2016 Elsevier Masson SAS. All rights reserved.
Keywords: Unilateral neglect Stroke Assessment Ecological validity
1. Introduction Unilateral neglect is defined as the ‘‘failure to report, respond, or orient to novel or meaningful stimuli presented to the side opposite a brain lesion, when this failure cannot be attributed to either sensory or motor defects’’ [1]. This complex disorder of spatial cognition can have an impact on numerous daily living activities. Patients affected behave as if they were oblivious of half of the space around them, or even of their own body. In the most severe cases, the patient presents permanent deviation of the head and gaze towards the right, and ignores any solicitations from the side opposite to the brain lesion. During meals, the patient may upset plates located to their left, or fail to eat the food on the left side of their plate. They omit the left-hand page in a book, or they miss details situated on the left of drawings or photographs. Paterson and Zangwill [2] also noted that one of their patients could not get his left leg into his trousers, and sometimes even tried to put both legs in the same trouser leg. Unilateral neglect can also appear in other elementary activities, such as writing, drawing or games. A tendency for the patients to systematically turn right when they should be turning left, leading sometimes to erratic circular movements, was noted in the early observations [3], as
* Correspondence. E-mail address: [email protected].
well as the occurrence of collisions with objects located to the left. Neglect can also affect the use of the body, with some patients losing motor spontaneity in their left hand, despite normal strength (motor neglect) [4]. Numerous clinical tests, whether pencil-and-paper or computerised, have been proposed to assess unilateral neglect, but they sometime lack sensitivity. A large body of research has shown the possibility of discrepancies between performance on classic clinical tests and patient functioning in everyday life, in particular among patients in the chronic phase. These discrepancies could be due to a retest effect, or to the differing nature of mechanisms involved in clinical tests and in daily life. Indeed, the administration of a test, like rehabilitation programmes, could rely essentially on mechanisms requiring the voluntary orienting of attention. In contrast, in daily life, the automatic orienting of attention is essential. A specific deficit in this particular area could reflect the persistence of a neglect behaviour contrasting with good performance on tests. These discrepancies are problematic, both for detecting difficulties that could have an impact on the patient’s daily life, and for assessment of the generalisation of effects in therapeutic trials. Several recent reviews have underlined that the absence of ecological measures of the efficacy of treatment is a frequent weakness of numerous therapeutic trials [5]. Several evaluation instruments have been proposed to assess the impact of unilateral neglect in daily life, and a few reviews have
http://dx.doi.org/10.1016/j.rehab.2015.12.005 1877-0657/ß 2016 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2015.12.005
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been published recently on assessment of unilateral neglect [6–8], or more specifically on the use of virtual reality in the assessment of neglect, which we will nor discuss here because these tools are not yet in widespread use [9,10]. However, to our knowledge, no review has been devoted specifically to ecological evaluations. Yet, the issue is important, in particular for the evaluation of the efficacy of rehabilitation among patients with unilateral neglect. The aim of the present article is to present a critical review of these tools, with a particular focus on their psychometric qualities and on their limitations. 2. The Behavioural Inattention Test (BIT) The BIT [11,12], in addition to conventional tests, comprises a set of nine tests termed ‘‘behavioural’’, which simulate daily living activities, thus thought to draw closer to the real impact of the condition. The subject is asked to describe three large-sized photographs showing familiar scenes (a meal, a bathroom, and a large hospital ward), to dial a telephone number, to read a menu in four columns on an A3 format sheet, to read a newspaper article, to tell the time on a clock (digital and analogue) and to put a clock right, to point out coins among 18 items belonging to six categories, to copy an address and a sentence, to follow a route on a map, and to point out cards in an arrangement of 16 cards (Table 1). Each subtest is scored out of 9 (with a higher score corresponding to a better performance) giving a maximum score of 81. The validation study showed that the number of patients obtaining a pathological score was larger among those with lesions in the right than in the left hemisphere, except for the item entailing following a route on a map [12]. The most discriminant subtests between patients with unilateral neglect and those without (on the basis of the pencil-and-paper test battery) was the coin-sorting task. Test–retest reliability and inter-rater reliability were satisfactory. However, the behavioural battery was not more sensitive than the conventional tests, nor was it better correlated statistically with actual difficulties experienced, assessed using an occupational therapy checklist or an autonomy measure. It is thus difficult to conclude that these subtests possess better ecological relevance than the pencil-and-paper tests included in the battery. 3. Two semi-structured scales for the assessment of personal and extra-personal hemineglect Zoccolotti et al. [13,14] proposed an evaluation based on semistructured situations and simulations of daily living tasks using real objects. This evaluation comprises two scales, corresponding to ‘‘extra-personal hemineglect’’ (serving tea, dealing cards to four people sitting round a square table, describing three complex pictures, and describing a room) and to ‘‘personal hemineglect’’ (use of everyday objects: razor or make-up, comb, glasses). Each item is scored from 0 (normal) to 3 (severe). Inter-rater reliability
was good. A statistical analysis of the internal validity of the test showed a differentiation between extra-personal and personal items, confirmed by single-case studies evidencing double dissociations. The extra-personal scale was significantly correlated with the pencil-and-paper tests, but this was not so for the personal scale. Thus, the distinction between these two types of hemineglect appears as one of the original contributions of this scale. Beschin and Robertson [15] refined the scoring of the personal scale by counting the number of strokes of the comb (or a razor) on each side for 30 seconds (comb and razor test). Committeri et al. [16], using these semi-structured scales, showed that bodily and extra-bodily hemineglect resulted from lesions with different topology (extra-personal hemineglect was linked mainly to a network implicating the right frontal cortex and the upper temporal regions, while personal hemineglect was linked to the right lower parietal cortex). 4. The Subjective Neglect Questionnaire [17] The above scales require the patient to be placed in a test situation, which is therefore artificial. Towle and Lincoln [17] proposed a 19-item questionnaire administered to patients and proxies, asking them to rate the presence of difficulties in certain situations of daily living (for instance, bumping into furniture or doorways, putting only one foot on the footrest of the wheelchair, having difficulty telling the time on a clock face). Initially, each item was scored on a five-point scale according to the frequency of the occurrence of the difficulty (ranging from at most once a month to at least once a day). This scoring system however proved difficult to use, and was replaced by a binary score (present or absent in the preceding month). Scores were significantly correlated to performances on the star cancellation test. These authors also demonstrated differences between patients’ and relatives’ ratings. Finally, the relatives (unlike the patients) signalled significantly more problems among patients with unilateral neglect, in particular for the items difficulty in maintaining the trajectory for the wheelchair, clumsiness, and difficulty telling the time. 5. The Baking Tray Task This test consists in distributing 16 cubes regularly across a board (as if they were buns on a baking tray to be put in the oven) [18]. The board measures 75 100 cm, and the cubes 3.5 cm. The scoring, using a grid, is based on the number of cubes in each half of the board. Double dissociations were observed between this test and classic pencil-and-paper tests, and the baking tray test appeared more sensitive than the conventional tests. The score was not significantly correlated with those of the pencil-and-paper tests. The authors tested a version with a smaller board (A4 format) on a few patients, and it appeared slightly less sensitive. The advantages of this test are its simplicity and speed of completion.
Table 1 Comparison of the main ecological scales assessing unilateral neglect. Scale
Scoring method
Neglect components
Inter-rater reliability
Assessment of anosognosia
BIT [11,12] Semi-structured scale for personal and extra-personal neglect [13,14] Subjective neglect questionnaire [17] Baking tray task [18] Wheelchair obstacle course [19,20] Standardised activities of daily living [21] CBS [22–25]
Standardised testing Observation in standardised conditions
P P and EP
+ +
No No
Questionnaire (self and proxy) Testing under standardised conditions Testing under semi-standardised conditions Standardised testing Observation in naturalistic conditions and self-questionnaire
P and EP EP EP P and EP P and EP and anosognosia
NT NT NT + +
Yes No No No Yes
BIT: Behavioural Inattention Test; CBS: Catherine Bergego Scale; P: personal neglect; EP: extra-personal neglect; +: good inter-rater reliability; NT: not tested.
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However, any advantage over the other tools, and especially its ecological relevance, need to be ascertained. 6. Wheelchair obstacle course Several authors looked specifically at ‘‘driving’’ a wheelchair, often a source of difficulties for patients with unilateral neglect, as they tend to bump into objects located to their left [19,20]. The test consists in asking the patient to manoeuvre the wheelchair along a pre-determined itinerary, looking for target landmarks and/or avoiding obstacles. The scoring takes account of the presence of bumps, and where they occurred (front, lateral right or left). However, this type of evaluation is difficult to reproduce from one facility setting to another. 7. Standardised activities of daily living testing Eschenbeck et al. [21], along the lines of the BIT, proposed an assessment battery combining 6 classic pencil-and-paper tests and 8 daily living activities, also providing threshold scores. The aim was to achieve better standardisation of the situations assessed, and to take account of the different components of space, personal, peri-personal and extra-personal (while the BIT explores only the peri-personal space). The daily living activities used were: copying an address, dialling a phone number, telling the time, putting cream on the face, brushing hair, completing a form, assembling items on a tray, and sorting coins. For several of these tasks, the patient needed to detect an item essential to the task that was located to their left. Inter-rater reliability was good. The conventional tests were however more sensitive than the ecological tests. Dissociations were observed for 7 patients between the two assessments (6 presented neglect on the penand-paper battery but not on the ecological battery, and one presented the reverse). Severity of the neglect phenomenon on this battery was linked to the presence of right frontal-parietal network lesions. 8. The Catherine Bergego Scale (CBS) We have developed a functional scale for the evaluation of unilateral neglect, the Catherine Bergego Scale (CBS) [22–25] (Table 2). This scale aims to score neglect behaviours in standardised, semi-quantitative manner, using observation of the patient by a therapist in different daily living situations. The second objective of the CBS is to assess the patient’s awareness of his or her difficulties, by comparing observation data with interview data. The scale comprises 10 items relating to elementary activities, each scored from 0 (normal) to 3 (severe unilateral neglect). A global score is then
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calculated, ranging from 0 to 30. We chose to arbitrarily distinguish three levels of severity for CBS scores: from 1–10, mild neglect, 11–20 moderate neglect, and 21–30 severe neglect. Inter-rater agreement was good [24]. On a group of 50 patients, we noted that internal consistency, (assessed from the correlation of each of the 10 items with the global score) was good, and that the global CBS score was significantly higher in the group of patients presenting unilateral neglect on paper-and-pencil tests [22]. The global score was significantly correlated with functional independence [22]. The three most sensitive items were awareness of the left hemi-body, dressing, and moving around (collisions) [22]. The internal structure of the scale was assessed on a group of 83 patients with a right hemisphere stroke [23]. Both principal component analysis (PCA) and the Rasch model showed that the 10 items in the scale corresponded to a single underlying factor. Differing results were reported by Goedert et al. [26]. These authors studied 51 patients with unilateral neglect following right hemisphere stroke, on average 22.3 days after the stroke. They used PCA, which showed two underlying factors in the CBS: one perceptive-attentional factor (named CBS-PA) and one motorexploratory factor (CBS-ME). Only this second factor was predictive of dependence for daily living activities as assessed by the Barthel index. The perceptive-attentional factor was correlated with the clinical tests (on the BIT) but was not predictive of functional dependence. In all the above-mentioned studies, the CBS appeared more sensitive than any of the paper-and-pencil tests considered alone, and dissociations were observed between the two types of evaluation. Another advantage of the CBS is that it takes account of different aspects of unilateral neglect: bodily, peri-personal, and extra-personal, which is not the case for most of the other assessment tools. Further to this, we were also able to study unilateral neglect in daily life following left hemisphere lesion [25]. Surprisingly, a large number of patients (77.3%) obtained a score above 0 on at least one item. Nevertheless, right-sided neglect was not very severe, since only 5.4% of the patients reached a score above 10 (versus 36% for left neglect following right hemisphere stroke). Right neglect mainly involved the personal space. An anosognosia score can be calculated from the difference between the examiner and the patient ratings. This anosognosia score was strongly significantly correlated to the severity of the unilateral neglect [23]. However, dissociations were observed, with certain patients presenting moderate unilateral neglect having anosognosia scores that were close to 0 [25]. Vocat et al. [27] studied anosognosia using the CBS in patients with right hemisphere lesions, and showed that disagreements between examiner and patient were very marked in the acute phase, but decreased at a more
Table 2 Catherine Bergego Scale – (English translation for information only, not validated in English).
1. 2. 3. 4. 5. 6. 7. 8. 9. 10.
Fails to groom or shave the left part of his/her face When dressing fails to adjust the left side correctly (sleeve, slipper. . ..) Leaves food on the left side of his/her plate Forgets to wipe the left side of his/her mouth after eating Exhibits difficulty in looking towards the left Ignores the left part of his/her body (e.g. does not put his/her upper limb on the armrest, or his/her left foot on the wheelchair footrest, or forgets to use his/her left arm when he/she needs to) Does not notice or pay attention to noise or people addressing him/her from the left Collides with people or objects on the left side, such as doors or furniture (when walking or in a wheelchair) Has difficulty in finding his/her way towards the left when moving about in familiar places or in the rehabilitation unit Has difficulty finding his/her personal belongings in the room or bathroom when they are on the left side Total score (/30)
0
1
2
3
& & & & & &
& & & & & &
& & & & & &
& & & & & &
& &
& &
& &
& &
&
&
&
&
&
&
&
&
0: non neglect; 1: mild neglect; 2: moderate neglect; 3: severe neglect.
Please cite this article in press as: Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2015.12.005
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chronic stage. They also showed that anosognosia of neglect, as assessed by the CBS, was not significantly correlated with anosognosia of hemiplegia, whatever the stage. Chen et al. [28,29] proposed a new scoring method for the CBS based on detailed instructions for observation and scoring (the Kessler Foundation Neglect Assessment Process). Using this scoring method, they found results comparable to ours for the one-dimensional structure of the scale and the significant correlations with measures of functional independence. Qiang et al. [30] noted a significant correlation between the CBS score and a standardised wheelchair driving test, and with the Functional Independence Measure (FIM). Luukkainen-Markkula et al. [31] compared the CBS and the BIT among 17 patients exhibiting neglect. Discrepancies were observed in certain patients between mild neglect in paper-and-pencil tests and severe ratings on the CBS. Only the line-bisection test in the BIT was significantly correlated with the CBS. Oh-Park et al. [32] recently showed that the CBS score in the early phase (less than two months after a stroke) was significantly predictive of mobility 6 months poststroke, in the same manner as with the BIT. Thus the proportion of patients unable to move around outside the home independently was 0%, 27.3% and 72.7% for patients respectively presenting mild, moderate or severe unilateral neglect on the CBS (total scores on the CBS: 1–10, 11–20, and 21–30). The CBS has been used in several studies on rehabilitation as an assessment criterion for efficacy and transfer of rehabilitation gains to everyday life. The scale has been used in several trials using prism adaptation [33–40], motor cueing [34,41], eye patching in association with constraint-induced therapy [42], virtual reality [43], upper limb training with a rehabilitation robot [44] or transcranial magnetic stimulation [45,46]. Several of these studies have shown that the CBS was sensitive to change and could therefore be used as a measure of the generalization of the effects of treatment to daily life. 9. Conclusion The behavioural assessment of unilateral neglect is a useful complement to classic pencil-and-paper tests. It can sometimes enable the detection of difficulties that might otherwise have gone unnoticed. The choice of the assessment instrument to use depends on the moment, the setting, and the time available. When the patient is still in a rehabilitation facility, the CBS is probably the best-suited measure. The CBS can also be used as a questionnaire for the patient’ relatives, but with adequate caution because its validity has not been established in this application. Disclosure of interest The author declares that he has no competing interest. Acknowledgements We would like to thank members of the GEREN group who contributed to some of the studies mentioned in this article, as well as the occupational and speech therapy teams in RaymondPoincare´ hospital (Garches) and La Salpeˆtrie`re hospital (Paris) who took part in the collection of data for the CBS. This article is dedicated to the memory of Catherine Bergego (1949–1994) who provided inspiration for a large part of this work. References [1] Heilman KM, Watson RT, Valenstein E. Neglect and related disorders. In: Heilman KM, Valenstein E, editors. Clinical neuropsychology. New York: Oxford University Press; 1993. p. 279–336.
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Please cite this article in press as: Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2015.12.005