Recovery of Visuospatial Neglect Subtypes and Relationship to Functional Outcome Six Months After Stroke

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Recovery of Visuospatial Neglect Subtypes and Relationship to Functional Outcome Six Months After Stroke

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Margaret J. Moore, BSc, Kathleen Vancleef, PhD, M. Jane Riddoch, PhD, ...

First Published July 16, 2021 Research Article 

https://doi.org/10.1177/15459683211032977

Article information

Abstract

Background/Objective. 

This study aims to investigate how complex visuospatial neglect behavioural phenotypes predict long-term outcomes, both in terms of neglect recovery and broader functional outcomes after 6 months post-stroke.  

Methods. 

This study presents a secondary cohort study of acute and 6-month follow-up data from 400 stroke survivors who completed the Oxford Cognitive Screen’s Cancellation Task. At follow-up, patients also completed the Stroke Impact Scale questionnaire. These data were analysed to identify whether any specific combination of neglect symptoms is more likely to result in long-lasting neglect or higher levels of functional impairment, therefore warranting more targeted rehabilitation. 

Results. 

Overall, 98/142 (69%) neglect cases recovered by follow-up, and there was no significant difference in the persistence of egocentric/allocentric (X² [1] = .66 and P = .418) or left/right neglect (X² [2] = .781 and P = .677). Egocentric neglect was found to follow a proportional recovery pattern with all patients demonstrating a similar level of improvement over time. Conversely, allocentric neglect followed a non-proportional recovery pattern with chronic neglect patients exhibiting a slower rate of improvement than those who recovered. A multiple regression analysis revealed that the initial severity of acute allocentric, but not egocentric, neglect impairment acted as a significant predictor of poor long-term functional outcomes (F [9,300] = 4.742, P < .001 and adjusted R² = .098).  

Conclusions. 

Our findings call for systematic neuropsychological assessment of both egocentric and allocentric neglect following stroke, as the occurrence and severity of these conditions may help predict recovery outcomes over and above stroke severity alone.

Keywords

visuospatial neglect, stroke, cognitive assessment, recovery, neuropsychology

Introduction

Visuospatial neglect is a common neuropsychological syndrome characterised by consistently lateralised perceptual deficits.^1,2 The neglect syndrome is represented by a highly heterogeneous group of symptoms and contains many subtypes.^3-5 Although visuospatial neglect is a common consequence of stroke, it is not yet clear whether different subtypes of neglect follow similar recovery trajectories or whether neglect subtypes are differentially associated with poor long-term functional outcomes.

The occurrence of post-stroke cognitive impairments has been strongly associated with reduced quality of life throughout recovery.^6-9 However, not all cognitive deficits appear to affect quality of life and functional recovery to the same extent. Previous research has demonstrated that patients who experience visuospatial neglect following stroke are significantly more likely to report higher levels of functional impairment and lower quality of life than patients without visuospatial neglect impairment.^6,7,10 This particularly robust effect has been documented across multiple different timepoints using a wide range of functional outcome measures. For example, Jehkonen et al.⁶ found that performance on the Behavioural Inattention Test was the single best predictor (compared to hemianopia, age and verbal memory) of poor functional outcome at 3-, 6- and 12-month follow-up appointments. Cherney et al.¹⁰ determined that higher neglect severity was predictive of lower Functional Independence Measure scores at admission, discharge and 3-month follow-up. Katz et al.⁷ found that acute neglect was associated with lower scores on various activities of daily living measurements as well as on standardised cognitive measures throughout the first 5 months following stroke. Similarly, Buxbaum et al.¹¹ concluded that the occurrence of neglect deficits predicted poor recovery outcome following stroke over and above general stroke severity metrics. These findings demonstrate that the occurrence of visuospatial neglect acts as a significant predictor of functional recovery outcome.

However, neglect is not a unitary syndrome. Following stroke, patients can exhibit visuospatial neglect within a self-centred (egocentric) and/or object-centred reference frame (allocentric neglect).^3,3,4,12-16 For example, a patient with egocentric neglect might fail to notice objects presented on their neglected side while a patient with allocentric neglect might fail to perceive features appearing on the neglected side of individual objects, regardless of where these objects are presented in space.¹⁷ While egocentric and allocentric neglect do frequently co-occur, these conditions have been demonstrated to represent doubly dissociated, independent cognitive impairments.^3,14,18,19 Importantly, additional subtypes of neglect have been documented. Patients can selectively exhibit neglect within peri-personal (near space) and extra-personal space.^20-23 Patients have also been found to exhibit spatial attentional biases in additional sensory modalities including auditory neglect^24-26 and motor neglect.^27-29 However, standardised neuropsychological tests which can reliably detect and differentiate between these additional neglect subtypes are not commonly employed in clinical environments.^30-32 For this reason, this analysis will focus on exploring the recovery trajectories of egocentric and allocentric neglect. The present study aims to investigate only differences between egocentric and allocentric neglect with the implication being that if these two subtypes recover differentially, additional research will be needed to investigate whether these differences are also present within other subtypes of neglect.

Previous research has suggested that patients with egocentric and allocentric neglect may exhibit differing levels of functional impairment. Bickerton et al.³ found that patients with allocentric neglect scored significantly lower (e.g. worse functional performance) on the Barthel Index activities of daily life measurement³³ compared to patients with egocentric neglect at a single, subacute timepoint. In this study, patients with both allocentric and egocentric neglect also reported significantly higher levels of depression on the Hospital Anxiety and Depression Scale than patients with either egocentric or allocentric neglect alone.³

Similarly, although neglect is most commonly thought of as a left-lateralised impairment occurring following unilateral right hemisphere damage, recent research has demonstrated that right-lateralised neglect impairments also frequently occur following stroke.^34-39 Patients with left and right neglect may exhibit differing levels of functional impairment. Ten Brink et al.⁴⁰ investigated the relationship between neglect lateralisation and performance on various cognitive and physical independence measures in a cohort of 335 acute stroke survivors. This study found that left-lateralised neglect impairment was more severe than right-lateralised neglect as assessed by both neuropsychological and observational measures. However, patients with right neglect exhibited lower scores on the Mini Mental State Examination^41,42 than patients without neglect (potentially through a co-occurring language deficit) and were more likely to exhibit impaired balance than patients with left neglect.⁴⁰ These findings suggest that the association between neglect and functional impairment may depend on the reference frame and lateralisation of neglect. However, these studies only employed data from a single timepoint acutely post-stroke.

Overall, previous studies which have tracked neglect recovery over time have found that the majority of neglect cases recover within the first 6 months following stroke.^36,39,43 Nijboer et al.⁴³ found that time post-stroke was a key and independent predictor of visuospatial neglect recovery, with 54% of patients recovering within the first 12 weeks and around 60% recovered within the first year. A subsequent study found that clinical characteristics including neglect severity, stroke severity, and severity of comorbid stoke deficits did not act as significant predictors of neglect recovery over the first 26 weeks following stroke.⁴⁴ These studies provide important insights into the recovery trajectory of neglect as a whole, but do not distinguish between egocentric and allocentric neglect deficits. Several previous studies have investigated how different neglect subtypes recover over time. Stone et al.,³⁹ in a group of 68 patients with neglect, found that neglect following right hemisphere damage (N = 34) was significantly slower to improve and less likely to fully recover than neglect following left hemisphere lesions (N = 34) over the first 6 months following stroke. Demeyere and Gillebert³⁶ found that of the 160 patients with follow-up data 81% of egocentric neglect (11 impaired at follow up vs 55 impaired at the stage) and 71% of allocentric neglect cases (10 chronic vs 39 acute) recovered within 6 months following stroke. Overall, a high proportion of visuospatial neglect cases were found to spontaneously recover within the first 6 months following stroke,^14,39 but this relationship may not be equivalently true for different neglect lateralisations and reference frames.

Previous research has suggested that some stroke-related deficits follow a proportional recovery rule in which the amount of improved function is proportional to the initial degree of function loss.^45,46 However, it is not yet clear whether egocentric and allocentric visuospatial neglect follow this proportional recovery pattern.^47,48 If neglect impairments follow a proportional recovery rule, neglect cases which are initially more severe should be less likely to fully recover than less severe cases.^45,46 Conversely, if neglect does not follow a proportional recovery pattern, the initial severity of neglect would not be expected to differentiate between patients who do and do not recover over time. Similarly, it is important to investigate differences in rates of improvement over time across different neglect subtypes. For example, it is possible that patients with milder deficits improve gradually over time while patients with severe impairments do not experience any improvement. Alternatively, it is possible that all patients with neglect exhibit the same rate of change in severity over time, regardless of the severity of their initial deficits. It is therefore critically important to better characterise recovery trajectories in different neglect subtypes in order to identify the specific patients who are least likely to fully recover.

Previous investigations into neglect recovery trajectories have not considered the interaction between neglect subtype and lateralisation when attempting to elucidate the predictive relationships between these acute factors and long-term recovery outcomes. Here, for the first time, we present data from a large and representative longitudinal sample of stroke survivors to attempt to disentangle how complex acute neglect behavioural phenotypes predict longer-term recovery outcomes, both in terms of long-lasting neglect symptoms as well as broader functional outcomes related to activities of daily life and participation 6 months after stroke. The present study aims to investigate which specific attributes of acute neglect impairment are related to a low likelihood of neglect recovery 6 months later and which are associated with worse functional outcomes. Importantly, this study does not aim to develop a quantitative prognostic model, but instead to investigate whether specific neglect subtypes are differentially associated with lasting impairment and functional outcomes. This, in turn, may help identify which specific patients are the most likely to benefit from targeted rehabilitation strategies.

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