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ORIGINAL ARTICLE
Table 1: Baseline Characteristics for Patients in the VEM and Mann-Whitney U tests were used to test for within-group
SC Groups differences on each of the rehabilitation practice and outcome
Characteristics VEM (n⫽38) SC (n⫽33) variables: time to first out-of-bed episode (mobilization), min-
utes of therapy per day, and length of hospital stay. Z tests were
Age (y) 74.6⫾14.6 74.9⫾9.8
used to test interactions between neglect status and group on
Sex (M) 22 (58) 16 (48)
each of these variables (analogous to Altman and Bland19).
Previous stroke 11 (29) 7 (21)
Logistic regression analyses were used to determine whether
Diabetes 11 (29) 4 (12)
neglect was an important prognostic factor for discharge des-
Stroke type*
tination and for functional outcome (mRS) at 12 months.
TACI 10 (26) 6 (18)
PACI 13 (34) 10 (30) RESULTS
POCI 7 (18) 5 (15)
LACI 5 (13) 6 (18) Baseline Characteristics
ICH 3 (8) 6 (18)
NIHSS 9.5 (5–18) 8 (4–12)
Baseline characteristics for the 71 stroke patients are pre-
Mild 15 (39) 15 (45)
sented in table 1. None of the differences between groups were
Moderate 13 (34) 11 (33)
statistically significant.
Severe 10 (26) 7 (21)
Neglect
Neglect 20 (53) 19 (58)
Of the 71 patients, 70 were assigned a score for unilateral
NOTE. Values are mean ⫾ SD, n (%), or median (IQR). neglect on the NIHSS item (missing data for 1 subject), and 42
Abbreviations: ICH, intracerebral hemorrhage; IQR, interquartile were assessed using the Star Cancellation Test. Twenty-nine
range; LACI, lacunar infarct; M, male; PACI, partial anterior circula-
tion infarct; POCI, posterior circulation infarct; TACI, total anterior
patients were unable to complete the Star Cancellation Test
circulation infarct. because of stroke severity, low level of cognition, aphasia, or
*Oxfordshire classifications. the need for repeated stimulation to maintain arousal. All 17
patients who had a severe stroke (NIHSS total score ⬎16) were
not testable on Star Cancellation. Of the testable patients, 31
of space. For the purposes of the current study, patients were (44%) of 70 had neglect on the NIHSS item, and 17 (41%) of
identified as having neglect if they were scored as either 1 or 2 42 had neglect on Star Cancellation. Despite the similar prev-
on this inattention item. The second method used to identify alence of neglect as indicated by the 2 measures, there was
patients with neglect was the Star Cancellation Test, a valid considerable disagreement (table 2).
and sensitive test18 that requires the patient to cross out all the Eight patients identified as having neglect on Star Cancella-
small stars in an array of larger stars and other items. A trained tion were “missed” on the inattention item of the NIHSS, and
assessor administered this test. A score of less than 51 out of 54 3 patients who were rated as having neglect on the NIHSS item
was taken to indicate neglect on the Star Cancellation Test.11 performed within normal range on Star Cancellation. Level of
Patients were classified as having neglect if they had a positive agreement between the NIHSS item and Star Cancellation was
result on either test (ie, scoring 1 or 2 on NIHSS inattention .42 for all 3 correlation coefficients, which is considered to be
item or scoring ⬍51 on Star Cancellation, or both). on the border between “fair” and “moderate” agreement.20
Using our classification (a positive result on either test indi-
Outcome Measures cates neglect), 55% (39/71) of patients had neglect at baseline.
Patients with neglect were equally distributed between the
Patient characteristics collected at baseline included sex, VEM group (20/38, 53%) and the SC group (19/33, 58%). In
age, stroke severity (NIHSS total score), and previous stroke keeping with previous findings, neglect was more common
history. There were 3 primary outcome measures in the current after right hemisphere (24/35, 69%) than left hemisphere (15/
study: time to first mobilization (measured in hours), amount of 36, 42%) stroke, as established through cerebral imaging (com-
therapy (measured in minutes per day), and length of acute puted tomography or magnetic resonance imaging) in all cases.
hospital stay (measured in days). Secondary outcome measures
were discharge destination from the acute hospital and 12- Time to First Mobilization
month death and disability (measured using the mRS).
Number of hours to first mobilization was compared be-
Blinding tween groups in patients with and without neglect (fig 2). Three
Patients consented to undergo randomization to 1 of 2 reha-
bilitation styles (A or B) and were blind to group allocation.
Blinding was possible because the rehabilitation styles differed Table 2: Agreement Between Measures of Neglect
only in their timing (the intervention group received mobiliza-
NIHSS Item
tion sooner and more often) and not in their content. Although
trial therapists and nursing staff could not be blinded to inter- Variables Neglect No Neglect Missing
vention group, the importance of maintaining blinding of pa- Star Cancellation Test
tients and assessors was stressed to them. Intervention sessions Neglect 9 8 0
were not documented in the medical record and were con- No neglect 3 21 1
ducted behind closed curtains where possible. Unable 19 10 0
Stroke severity (unable)
Statistical Analyses
Mild 0 3
All analyses were performed using SPSS version 14.0.a The Moderate 5 4
level of agreement between the 2 methods of identifying ne- Severe 14 3
glect (NIHSS item and Star Cancellation) was analyzed using
kappa, intraclass, and concordance correlation coefficients. NOTE. Values are number of patients.
SC
No neglect 6 8
Neglect 2 17
VEM
No neglect 7 11
Neglect 5 15
“good outcome” (mRS 0 –2) and “poor outcome” (mRS ⬎2); 2 Bernhardt et al17). Furthermore, early and more frequent mo-
patients had missing data. Of the 38 patients identified with bilization may have contributed to a shorter length of stay. In
neglect, 33 (87%) had a poor outcome at 12 months. Of the 31 the VEM group, patients with and without neglect both had a
without neglect, only 14 (45%) had a poor outcome at 12 median length of stay of 6 days, whereas patients with neglect
months. Multivariate logistic regression was performed on in the SC group stayed in the hospital longer (median, 11d).
mRS outcome at 12 months. All variables included in the However, we also found that people with neglect were less
model were associated with poor mRS outcome: greater likely (regardless of group) to return home after their acute
stroke severity (⫽.34, SE⫽.12, P⫽.007), older age hospital episode of care.
(⫽.08, SE⫽.04, P⫽.030), and female sex (⫽1.72, It is well established that neglect after stroke has a strong
SE⫽.82, P⫽.035) were significantly related, while neglect negative impact on functional outcome,6,7 and our results are
neared significance (⫽–1.57, SE⫽.83, P⫽.060). consistent with this finding. Of the patients who had neglect in
the acute phase, 87% had a poor outcome at 12 months,
DISCUSSION whereas only 45% of the patients without neglect in the acute
This is the first study to describe the relationship between phase had a poor outcome. Even after accounting for other
neglect and rehabilitation practices in acute stroke, and it has relevant factors (age, sex, stroke severity), the impact of early
yielded 3 notable findings. First, agreement between the neglect on poor 12-month outcome neared significance.
NIHSS inattention item and the Star Cancellation Test was There were many strengths of this study, including a ran-
only fair to moderate (.42), illustrating the difficulty of assess- domized design, broad inclusion criteria, and a blinded out-
ing neglect early after stroke. Second, the introduction of a come assessment. Neglect was assessed very early after stroke
protocol promoting early and frequent mobilization was found and was measured using 2 different methods. Extensive data
to be feasible in stroke patients with neglect. Third, patients were collected on rehabilitation practices.
with neglect in the SC group had longer hospital stays than The small sample size was a limiting factor. Given the lack
those without neglect, but this was not the case in the inter- of statistical power, the interesting trends identified should be
vention group. seen as hypothesis-generating and need to be confirmed in a
Issues arising from the assessment of neglect are considered larger study.
first. Catchment with the NIHSS item was almost complete,
with missing data for 1 patient only. The Star Cancellation CONCLUSIONS
Test, however, could not be completed by 29 patients (includ- In terms of therapy and rehabilitation, we found no evidence
ing all 17 with severe stroke). Eight patients with neglect that neglect was a barrier to early and frequent mobilization of
identified on the Star Cancellation Test were “missed” on the stroke patients in the acute hospital setting. There was some
NIHSS. This is not altogether surprising; the Star Cancellation indication that patients with neglect who received this rehabil-
Test is one of the most sensitive tests of neglect,18 and mild itation intervention had a shorter hospital stay than those who
symptoms may have been missed by the examiner. Although received SC. Given that agreement between our 2 neglect
raters in this study had completed training and accreditation for assessments was only fair to moderate and the Star Cancella-
the NIHSS, the inattention item does rely on clinical judgment. tion completion rate was far from 100%, there remains scope to
Examiners with limited experience of neglect may be less identify a practical and valid measure (or combination of
likely to detect the clinical signs. This is a problem because measures) for neglect in acute stroke. Nevertheless, the assess-
mild neglect can still have a considerable impact on functional ments used here can be seen as useful screening tools that can
tasks, including gait. In clinical practice, to ensure mild neglect guide the introduction of interventions to remediate neglect
does not go undetected, one approach might be to routinely early in recovery.
administer a more sensitive test of neglect when a person A large, multicenter phase III trial to test the efficacy and
scores 0 (no abnormality) on the NIHSS inattention item. Three cost-effectiveness of VEM is currently underway. In AVERT
patients with neglect on the NIHSS item performed within phase III, we will continue to assess neglect using both the
normal limits on the Star Cancellation Test, and this finding NIHSS and Star Cancellation Test. In addition, a clock-draw-
may be related to the spatial constraints of the Star Cancellation ing task, part of the Montreal Cognitive Assessment cognitive
Test. Cancellation tests examine neglect only in peripersonal screening tool,22 has been included in the 3-month follow-up
(reaching) space, whereas the NIHSS item is based on general assessment. This should allow further study of neglect as a
observation and is not limited to one spatial domain. A further prognostic factor in the context of a larger rehabilitation trial
consideration is that the NIHSS inattention item involves bi- and permit us to determine whether neglect in the first days
lateral simultaneous stimulation testing, which is the classic persists at 3 months.
test for extinction. Since extinction can occur in the absence of
neglect,21 this may explain why some subjects would be as- References
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