Post-Stroke Aphasia Prognosis: a Review of Patient-Related and Stroke

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Journal of Evaluation in Clinical Practice ISSN 1365-2753

Post-stroke aphasia prognosis: a review of patient-related

and stroke-related factorsjep_1650 689..694 Emily Plowman PhD1 Brecken Hentz MS2 and Charles Ellis Jr PhD3

1Assistant Professor, Department of Communication Sciences and Disorders, College of Behavioral and Community Sciences, University of South Florida, Tampa, FL, USA 2Staff Therapist, Department of Speech Pathology and Audiology, Duke University Medical Center, Durham, NC, USA 3Associate Professor, Department of Health Sciences & Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, USA

Keywords Abstract aphasia, prognosis, recovery Rationale, aims and objectives Recovery of language function in individuals with post- Correspondence stroke aphasia is associated with a variety of patient and stroke-related indices. Amidst Dr Charles Ellis Jr a complex interaction of a multitude of variables, clinicians are faced with the arduous Medical University of South Carolina challenge of predicting aphasia recovery patterns and subsequently, long-term outcomes in Department of Health Sciences and these individuals. Unfortunately, predictive factors are highly variable making prognosis of Research aphasia recovery difficult. Therefore, the objective of this review was to assess the influence College of Health Professions of patient-related and stroke-related factors on language recovery in individuals with 77 President Street, MSC 700 post-stroke aphasia. Charleston, SC 29425 Methods We completed a literature review to assess and identify evidence-based patient USA and stroke-related variables shown to be influential in aphasia recovery. E-mail: [email protected] Results A range of patient-related (gender, handedness, age, education, socio-economic status and intelligence) and stroke-related indices (initial severity, lesion site and lesion Accepted for publication: 9 February 2011 size) were identified as potential influential factors to post-stroke aphasia recovery. Initial severity of aphasia emerged as the factor most predictive of long-term aphasia recovery. doi:10.1111/j.1365-2753.2011.01650.x Other influential factors of post-stroke language recovery included lesion site and size. Conclusions Stroke-related factors, including aphasia severity, lesion site and lesion size, appear most critical to post-stroke aphasia recovery. The findings presented in this review offer clinicians an evidenced-based framework to assist in prediction of post-stroke aphasia recovery patterns and subsequent long-term functional communication outcomes.

Introduction indicators for general post-stroke function [4–6]. A clear under- standing of the specific factors critical to the prediction of aphasia Each year approximately 795 000 people experience a stroke and recovery patterns, however, is yet to emerge. Even in the absence many are left with serious long-term disability [1]. Of those who of this much needed and critical prognostic information, clinicians experience a stroke, approximately 100 000 will acquire aphasia are constantly challenged to predict aphasia recovery. during the acute phase of recovery and an estimated one million A prognosis is a prediction of the course of a disease or condi- Americans are currently living with aphasia [2]. Aphasia is defined tion based upon experience, intuition and evidence-based informa- as ‘an acquired communication disorder caused by brain damage tion [7]. Determining a prognosis in aphasia requires consideration that impairs a person’s ability to understand, produce and use of a multitude of inter-related patient-specific and stroke-specific language’ (p. 2) [3]. Aphasia can result from a variety of neuro- variables believed to influence functional outcomes for individuals logical disorders; however, stroke is the predominate neurological with aphasia. Patient-related variables include: age, handedness, condition associated with aphasia and will therefore constitute the gender, educational level, intelligence, motivation, depression, focus of this review. family support, beliefs and attitude regarding health care, and There exists a comprehensive literature related to prognostic access to medical treatment. In contrast, stroke-related indices indicators for general stroke recovery. For example, the presence include: site of lesion, size of lesion, aphasia type and pattern of of prior stroke, old age, urinary and bowel incontinence, visuospa- recovery, and initial aphasia severity. Identifying the correct com- tial deficits and initial Functional Independence Measure (FIM) bination of factors critical to an accurate prognosis is a daunting scores below 60 have all been identified as negative prognostic task for the new and even experienced clinician. Clinicians are

© 2011 Blackwell Publishing Ltd, Journal of Evaluation in Clinical Practice 18 (2012) 689–694 689 Aphasia prognosis E. Plowman et al. now faced with new challenges due to the widespread distribution post-stroke aphasia in men. Kertesz and Sheppard [12] reported a of misleading information available to the public on the internet 1.6:1.0 ratio (male : female) in 204 patients with aphasia, while that must be carefully considered when discussing and providing Basso et al. [13] observed a similar male to female ratio of 1.5:1.0 prognostic information to caregivers and family members. In this in 192 patients with aphasia. review we will examine a range of variables previously docu- Consequently, evidence regarding gender and prevalence of spe- mented and that are believed to influence aphasia outcomes post cific aphasia type is also mixed. For example, De Renzi and stroke. Unfortunately, studies designed to examine aphasia prog- colleagues [14] reported a higher prevalence of males with non- nosis have either examined the natural history of aphasia or fluent aphasia, and Hier et al. [10] documented that Wernicke’s primarily examined one aphasia outcome prognostic variable inde- global and anomic aphasias were more common in women while pendently [8]. Consequently, few previous reports have attempted Broca’s aphasia was somewhat more prevalent in men. Con- to consolidate the evidence to present a clear picture for clinicians. versely, other studies have not reported any association between Therefore, it was our goal to systematically organize available gender and type of aphasia. Specifically, Engelter and colleagues evidence so as to provide clinicians the foundation for a more [11] observed no gender differences on measures of auditory com- accurate and evidenced-based prognostic approach to aphasia prehension, expressive language and ratings of everyday commu- recovery in post-stroke individuals. nication function, and Godefroy et al. [15] concluded that sex did not significantly influence aphasia type in 295 individuals. Research design and methods In addition, evidence has shown that gender does not appear to be related to aphasia recovery [16–18]. In summary, evidence is For this review, we considered all studies that recruited patients largely equivocal and gender does not appear to significantly with a diagnosis of aphasia following stroke and reported stan- impact incidence of aphasia, aphasia type or recovery patterns in dardized measures designed to predict aphasia outcomes. We used post-stroke individuals. the Cochrane Collaboration Group search strategy as outlined in the Cochrane Handbook for Systematic Reviews of Interventions Handedness [9]. We searched: Medline (from 1966–2007), CINAHL (from 1982–2007), PsycINFO (1966–2007), REHABDATA (1966– As early as the 19th century, Paul Broca proposed that the left 2007) and the Cochrane Library. The following (MESH) terms hemisphere was dominant for language functions in right-handed were used in our search: ‘stroke, aphasia, prognosis and terms individuals. Interestingly, in 1958, Surbirana noted that prognosis associated with the prediction of aphasia outcomes including: age; for aphasia recovery following stroke is better for those who are handedness; gender; educational level; intelligence; site of lesion; left-handed compared with right-handed individuals. A more size of lesion; aphasia type and pattern of recovery; and initial recent study of handedness and language dominance among aphasia severity’. We also considered all other variables that healthy adults, however, reported that left-handedness is not nec- are known to influence general stroke outcomes such as: motiva- essarily a consequence of right-hemisphere language dominance, tion; depression; family support; beliefs and attitude regarding but rather left-handedness increases the likelihood of right- health care; and access to medical treatment. From these terms, hemisphere dominance [19]. Consequently, it appears that left- we attempted to identify other terms associated with aphasia handed and ambidextrous individuals are more likely to have a prognosis. bi-hemispheric representation of language and therefore the poten- We identified studies that reported ‘aphasia outcomes’ even if tial for greater recovery from aphasia [20]. While it appears that the study’s primary purpose was not designed to identify aphasia ambidextrous and left-handed individuals may have a greater prognosis. We completed hand searches of reference lists and a neural capacity for recovery, handedness when studied as an inde- search of Google Scholar. We also searched for reviews of aphasia pendent factor has not been shown to influence aphasia recovery prognosis and websites that reported variables associated with [21,22]. aphasia prognosis. Given the heterogeneity of studies, we decided a priori not to use meta-analysis to pool the results of studies. Age Instead, the presentation of results provides a qualitative assessment of the studies. Early studies of influential prognostic indicators of acute stroke ranked age as a primary variable [23,24]. Consequently, older Results individuals are more likely to have aphasia than younger ones [11]. Engelter and colleagues [11] studied 269 individuals following their first ischemic stroke, and reported the mean age of aphasic Patient-related factors patients to be five years higher than their non-aphasic counterparts (80 vs. 75 years). In addition, Smith noted that aphasia severity Gender increased with advancing age [25]. Further, studies of age and According to the National Institute of Neurological and Commu- aphasia type demonstrate that individuals with fluent aphasia tend nication Disorders and Stroke (NINCDS) Stroke Data Bank, the to be older than individuals with non-fluent aphasia. [21,26] incidence of aphasia post stroke is slightly higher among women De Renzi and colleagues [14] reported that individuals with compared with men in the USA [10]. Similarly, in an international Broca’s aphasia were significantly younger than individuals with study of 269 stroke patients, a higher incidence of aphasia was Wernicke’s aphasia, and similarly, Kertesz and Sheppard [12] observed among women in 80 individuals with aphasia [11]. In documented that individuals with Broca’s aphasia were younger contrast, other investigators have reported a higher incidence of than individuals with other aphasia types.

While age does appear to influence both the incidence and type tion between intelligence level and initial aphasia severity but not of post-stroke aphasia, the impact of age on aphasia recovery is with recovery of language function following stroke. In an early unclear. Younger patients have been reported to demonstrate a review of prognostic indicators of aphasia recovery, Ferro et al. higher recovery rate than older patients [27]; however, conflicting concluded that intelligence did not appear to influence aphasia reports have deemed age to be a poor prognostic indicator of recovery [20]. Thus, there is some data to suggest that intelligence aphasia recovery [16,17,22,28]. Thus, even though age has been may impact initial aphasia severity; however, it appears that this identified as an important prognostic indicator for general stroke variable does not influence aphasia recovery patterns post stroke. recovery, no consistent data have emerged regarding age and expressive or receptive language recovery patterns post stroke. In Stroke-related factors sum, incidence of aphasia is higher in older stroke patients, and of these patients a higher likelihood of fluent forms is seen in Initial stroke and aphasia severity older adults and non-fluent forms in younger adults with no clear relationship between age and the ability for language recovery in Recent studies indicate that initial stroke severity is associated post-stroke aphasia. with initial aphasia severity, which in turn, is associated with poorer outcomes [27,28,38]. For example, Laska et al. documented that individuals with milder aphasia tended to have a Education, socio-economic status and intelligence higher degree of aphasia recovery [27]. Similar findings were Carl Wernicke (1874) proposed that aphasia in highly educated reported by Pedersen and colleagues, who studied 270 aphasia individuals would differ from those with less education; however, patients post-stroke using the Western Aphasia Battery Aphasia a clear relationship between educational level and aphasia recov- Quotient (WAB AQ) [28]. These authors observed that language ery has yet to emerge [25]. This is likely due to the existence of a outcomes could be predicted by initial stroke and aphasia severity plethora of confounds, such as literacy levels, general intelligence, but not by other factors such as age, gender or aphasia type. At existence of learning disabilities, socio-economic status (SES) and 1-year post-neurological insult, aphasic symptoms still remained cultural influences, that make this area particularly challenging to for 61% of these individuals; however, the majority demonstrated study. Indeed, the existence of these confounds requires adjust- a reduction in the severity of language deficits with some degree of ments and careful planning of experimental designs in order to functional improvement [28]. While a strong relationship existed draw any valid conclusions regarding the impact of education on between initial aphasia severity and language outcomes, the rela- aphasia. tionship was most predictive of long-term language outcomes Educational achievement is frequently linked to SES, a variable during the 2- to 4-week post-stroke period, suggesting an optimal involving the complex interaction of a wide range of associated prognostic time window. Thus, clinicians are encouraged to con- factors including: income, insurance status, access to health care sider initial stroke, and subsequently initial aphasia severity, as and health-related beliefs that are associated with stroke-related predictive factors when determining aphasia prognosis. outcomes [11,29–33]. Thus, one might hypothesize that SES rep- resents a related variable critical to aphasia prognosis. Two studies Site and size of lesion have examined the relationship between SES and education with aphasia. Connor and colleagues examined 39 individuals with A wealth of literature supports the notion that lesion size and aphasia at both 4 and 103 months post onset to determine the location constitute important clinical predictors of aphasia type. degree to which educational achievement and SES influenced For example, certain semantic deficits are correlated with damage initial aphasia severity and recovery [34]. These authors noted that to the left posterior temporal and inferior parietal region [39]. both educational achievement and SES did not impact aphasia Similarly, large lesions to the third frontal gyrus involving Broca’s recovery rate; however, initial aphasia severity was worse in those area and the lower part of the precentral gyrus, in conjunction with with less education then in those with a higher level of education. lesions in the opercular and insular regions, are associated with In contrast to this later finding, Lazar and colleagues reported no more severe naming difficulties and overall expressive language relationship between education level, initial aphasia severity or deficits in individuals with Broca’s aphasia [40]. Likewise, lesions recovery [35]. While data regarding the influence of educational localized to the left superior temporal gyrus are common in levels on aphasia outcomes remain limited, data to date suggest patients with significant and persisting global aphasia and gener- no consistent relationship between education level and aphasia ally associated with poor language recovery [41]. severity or recovery. Lesion location and size have also been documented to influ- Closely associated with educational achievement level, higher ence aphasia recovery patterns in post-stroke individuals. Mazzoni pre-morbid intelligence has been examined as a potential posi- and colleagues documented different recovery patterns based on tive prognostic factor for individuals with aphasia. Kertesz and lesion size in 45 patients with aphasia [42]. Specifically, patients McCabe measured non-verbal intelligence in 111 individuals with with small lesions exhibited significant improvement in auditory aphasia and 52 control patients taken from the same hospital with comprehension, verbal expression and written expression; patients a range of medical diagnoses [36]. The authors observed that while with medium sized lesions improved in both auditory compre- non-verbal intelligence was impaired in the former, overall there hension and verbal expression; while patients with large lesions were no significant differences between the two groups. In a improved in only auditory comprehension. Goldenberg and Spratt similar study, David and Skilbeck investigated the impact of examined lesion size specific to Wernicke’s area in 18 individuals intelligence on aphasia severity and recovery of language function with aphasia over an 8-week recovery period [43]. Size of lesion post-stroke in 148 patients [37]. These authors reported a correla- negatively influenced overall recovery, with larger lesions to the

© 2011 Blackwell Publishing Ltd 691 Aphasia prognosis E. Plowman et al. temporobasal area associated with lower improvement and less cerebral blood flow returns to the damaged brain is a dynamic and total recovery. Likewise, Knopman and colleagues noted that per- complex process occurring bilaterally and might therefore influ- sistent non-fluency was associated with large lesions located in the ence aphasia recovery because the right hemisphere appears to Rolandic cortical regions extending into underlying white matter have a definitive role in the early recovery of language function [44]. Finally, a recent study of 669 patients with aphasia by Maas [53–57]. For example, Karbe and colleagues reported that while and colleagues indicated that better outcomes were associated with the left superior temporal cortex was critical in determining long- clinically and radiographically smaller strokes as well as lower term prognosis in aphasia, the right hemisphere was important for prestrike disability [8]. speech processing when the left hemisphere areas were perma- Studies by Naeser and colleagues have generally concluded that nently damaged [56]. This has led to the hypothesis that long-term aphasia recovery is associated with both the specific location and aphasia recovery is linked to the right hemisphere’s slow and the size of lesion, rather than just the later [45–48]. Specifically, a gradual compensatory role in language function, particularly significant correlation was present between comprehension skills during the early post-stroke time period [53]. and the amount of temporal lobe involvement in Wernicke’s area, Finally, the continuous advent of more sophisticated neuroim- however not between comprehension abilities and total tempo- aging techniques has significantly advanced our current under- ro-parietal lesion size. Furthermore, patients with lesions that en- standing of the neural mechanisms by which aphasia recovers compassed more than half of Wernicke’s area generally had poor [58]. Recent neuroimaging studies have provided compelling evi- comprehension skills, even 1 year post stroke [46]. Finally, these dence to support the notion that the brain has the ability to engage authors reported that anterior–inferior temporal lobe lesions that in structural and functional plasticity that supports language recov- extended into the middle temporal gyrus were associated with the ery in individuals with aphasia [58]. For example, Schlaug et al., worst language recovery. A later study by this group did not iden- using diffusion tensor imaging, reported increases in the number tify a single neuroanatomical area where extent of lesion could and volume of fibres in the right arcuate fasiculus (AF), a large discriminate outcomes for spontaneous speech fluency; however, white matter tract with reciprocal connections between Broca’s Naeser et al. concluded that spontaneous speech fluency was sig- and Wernicke’s area, in six individuals with moderate to severe nificantly influenced by lesion size in two subcortical white matter expressive aphasia [59]. Schlaug et al. observed increases in areas when combined [48]. These two areas consisted of the most the number and volume of AF fibres that were accompanied medial and rostral portion of the subcallosal fasiculus and the by improvements in verbal expression following 75 sessions of periventricular white matter area near the body of the lateral ven- melodic intonation therapy [59]. Furthermore, a significant trend tricle and deep to the lower motor/sensory cortex area of the emerged between the relative improvement in conversational mouth. information units (elicited from a picture description task and Alexander and colleagues also noted that size of lesion in criti- during conversational speech) and the absolute change in the cal language areas was highly predictive of aphasia severity and number of AF fibres. In this small sample, it appears that structural recovery patterns [49]. While shallow lesions of the frontal oper- brain plasticity may have facilitated functional improvement in culum resulted in transient disorders of language output with expressive language function following an intensive and salient normal articulation and repetition, lesions that extended into the rehabilitation program. deep white matter of the frontal isthmus and anterior periventricular white matter resulted in more severe and prolonged non-fluent verbal output. Alexander et al. concluded that a more severely Conclusions impaired expressive language profile resulted from disruption of A multitude of inter-related variables must be considered when the limbic-frontal projections and cingulated–striatal–frontal con- determining a prognosis for aphasia (see Table 1). While a prog- nections critical to expressive language output [49]. Similarly, nosis may only represent a clinician’s ‘best guess’, the current Kertesz et al. reported that poor recovery in comprehension abili- literature offers evidence, that when integrated, could offer clini- ties was associated with larger lesions involving the supramarginal cians a framework to facilitate a more accurate evidence-based gyrus, angular gyri and superior temporal area, while sparing of the superior temporal and middle temporal gyri was associated with good recovery of auditory comprehension in 22 individuals Table 1 Summary of patient and stroke-related aphasia prognostic with Wernicke’s aphasia [50]. Finally, Selness and colleagues variables examined 39 individuals with aphasia to determine the relationship Variable Prognostic Evidence between lesion localization, lesion volume and auditory comprehension outcomes [51]. In this study, poorer outcomes were Patient-related variables associated with lesions to the posterior superior temporal and Gender - infrasylvian supramarginal region and lesion volume was gener- Handedness - ally not associated with auditory comprehension abilities unless Age * extremely large or small. Education/socio-economic status - Metabolic factors, not typically measured by clinicians, have Intelligence * also been noted to influence short- and long-term aphasia progno- Stroke-related variables sis. Evidence suggests that cerebral metabolic rates of glucose Initial stroke and aphasia severity + in language regions, and cerebral blood flow adjacent to lesions Site/size of lesion + during the early post-stroke period, are critical to aphasia recovery. +, positive evidence; *, mixed/unclear evidence; -, no significant [52,53] Furthermore, the proposed mechanism by which adequate evidence.

692 © 2011 Blackwell Publishing Ltd E. Plowman et al. Aphasia prognosis assessment of a patient’s potential for recovery [7]. This paper and age on the incidence and type of aphasia. Cortex, 16 (4), 627– highlights evidence that can serve as a guide for such evidence- 630. based prognostic statements. Specifically, we report that while 15. Godefroy, O., Dubois, C., Debachy, B., Leclerc, M. & Kreisler, A. patient-related variables (age, gender, handedness, education and (2002) Vascular aphasias: main characteristics of patients hospitalized Stroke intelligence) do not appear to significantly influence aphasia prog- in acute stroke units. , 33 (3), 702–705. 16. Inatomi, Y., Yonehara, T., Omiya, S., Hashimoto, Y., Hirano, T. & nosis; stroke-related variables such as initial stroke and aphasia Uchino, M. (2008) Aphasia during the acute phase in ischemic stroke. impairment level, lesion size and lesion location, do influence Cerebrovascular Diseases, 25 (4), 316–323. recovery patterns. 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