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Naming outcomes of anterior temporal lobectomy in epilepsy patients: A systematic review of the literature
Epilepsy & Behavior 24 (2012) 194–198
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Review
Naming outcomes of anterior temporal lobectomy in epilepsy patients: A systematic review of the literature Victoria Lyn Ives-Deliperi a,⁎, James Thomas Butler b, c a b c
Department of Human Biology, University of Cape Town, South Africa Department of Neurology, University of Stellenbosch, South Africa Department of Neurology, University of Cape Town, South Africa
a r t i c l e
i n f o
Article history: Received 19 March 2012 Revised 2 April 2012 Accepted 3 April 2012 Available online 7 May 2012 Keywords: Naming Dysnomia Epilepsy Surgery ATL Neuropsychology Aphasia Cognition Anterior temporal lobe Language
a b s t r a c t Anterior temporal lobectomy (ATL) is the standard surgical treatment for medically intractable temporal lobe epilepsy (TLE). While seizure outcome is favorable, cognitive outcomes are a concern, particularly in respect of memory and naming. A systematic review of the literature on the naming outcomes of ATL is presented in this article. Searches were conducted on PubMed and PsycInfo, yielding a total of 93 articles, 21 of which met inclusion criteria. Declines in visual naming are common following ATL in the dominant hemisphere, and particularly, for naming living stimuli or famous faces. The Boston Naming Test (BNT) declines by a mean of 5.8 points, exceeding the Reliable Change Index (RCI). There are no reports of deficits in auditory naming following ATL, despite the fact that auditory naming has shown to be a more sensitive measure of dysnomia than the BNT in TLE patients. The absence of structural hippocampal pathology and late-onset epilepsy are the strongest predictors of naming decline. Recommendations are made for further study. © 2012 Elsevier Inc. All rights reserved.
1. Introduction The surgical treatment of medically intractable temporal lobe epilepsy (TLE) is highly effective in controlling seizures [1,2]. Anterior temporal lobectomy (ATL) is the standard surgical procedure for TLE; while seizure outcome has been shown to be favorable, post-operative declines in cognitive performance are frequently reported. Verbal memory and naming are the two cognitive modalities at the greatest risk of decline following ATL performed in the language-dominant hemisphere [3,4]. Post-operative naming declines are observed in between 25 and 60% of patients undergoing ATL [5]. There are no reports of naming decline following non-dominant hemisphere resection. A recent systematic review calculating pooled estimates of neuropsychological outcomes after temporal lobe resections reported a 44% risk of decline in verbal memory and 34% risk of decline in naming after left-sided surgery [4]. No significant declines in IQ were found following ATL in the dominant hemisphere, and improvements in verbal fluency and executive functioning were reported. In addition, quality of life has been shown to significantly improve in surgically-treated TLE patients compared to medically-treated patients [2]. ⁎ Corresponding author at: 209(b) Mediclinic Constantiaberg, Burnham Road, Plumstead, 7800, South Africa. Fax: + 27 21 7979960. E-mail address: [email protected] (V.L. Ives-Deliperi). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.04.115
While seizure control is of primary interest in the surgical treatment of TLE, preserving or improving cognitive outcome is equally important. For this reason, there has been a growing application of more selective surgical procedures expected to reduce postoperative cognitive impairment [6,3]. In the case of the standard ATL, 3–6 cm of anterior temporal neocortex is resected along with the amygdala and hippocampus, while in more selective procedures, like the selective amygdalohippocampectomy (SAH), the amygdala, hippocampus, and parahippocampal gyrus are resected and the neocortex is spared as far as possible [7]. There is a lack of evidence to show that more selective procedures produce favorable cognitive outcomes, and further research in this area is required. In order to support such research, it is important to review the neural substrates of naming, elucidate the nature of naming deficits following ATL, and identify the assessments that are most sensitive and specific to such declines. Naming is the earliest milestone in linguistic development. Much like the broader modality of language, naming relies on a number of distinct but interacting cognitive processes and mental representations that are subserved by a distributed network of brain regions [8,9]. Disruption to any of these regions can effect naming. In addition to this, research has shown that specific categories of naming rely on the functional integrity of discrete regions in the dominant hemisphere. Distinctions have been made between regions supporting
V.L. Ives-Deliperi, J.T. Butler / Epilepsy & Behavior 24 (2012) 194–198 Table 1 Inclusion and exclusion criteria for articles on naming outcomes following ATL. Inclusion criteria Original research article or literature review Anterior temporal lobectomy Adult temporal lobe epilepsy population Pre- and post-surgical testing of naming Exclusion criteria Pediatric epilepsy population
living stimuli/ people and animals versus non-living stimuli/objects [10,11], where the former rely on medial or posterior regions of dominant temporal lobe and the latter on regions situated more anteriorly. Likewise, differential substrates are involved in visual versus auditory naming tasks. As the label implies, visual naming, otherwise referred to as confrontation naming, involves the presentation of stimuli in the form of pictures or drawings; Auditory naming, also referred to as descriptive naming, involves generating the name from a verbal description of a stimuli. Functional neuroimaging and electrocortical stimulation have shown visual naming to be subserved by more posterior temporal lobe regions [12,13], and auditory naming to rely on regions situated more anteriorly in the temporal lobe [14,15]. To our knowledge, no research has been conducted on the different regions involved in visual versus auditory category-specific naming. The neural correlates of visual, auditory, and categoryspecific naming are important considerations when investigating dysnomia as an outcome of different surgical resections. The purpose of this review is to summarize what has been learned about naming deficits following ATL. This information is aimed to guide further research on the differential outcomes of surgical interventions in the treatment of TLE.
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2. Method A focused literature search was conducted using PubMed and PsycInfo databases. Search terms included: epilepsy, surgery, naming, dysnomia, and language. The initial search yielded 93 articles of which 20 met inclusion criteria. Inclusion and exclusion criteria are outlined in Table 1. Articles were retrieved and read in full, and references were examined to identify additional studies. One additional study was identified for inclusion through this process. Articles that focused exclusively on pediatric populations were excluded, because of potential confounding effects of language development on naming outcome. Particular attention was paid to the sample sizes in these studies, the interval between surgery and post-operative testing, and the instruments used to assess naming the type of naming assessed. With these factors in mind, the primary interest was in the prevalence of reported post-operative dysnomia in patients undergoing dominant-hemisphere resections. Secondary interests were in the type of naming most vulnerable to decline following resection of the anterior temporal lobe and factors predicting naming decline. 3. Results Details of the 21 articles included in the review are presented in Table 2. The sample sizes of the studies ranged from 17 to 217 (mean = 58). A 1-year interval between surgery and post-operative cognitive testing is considered by some to be optimal [6], and four of the studies reviewed relied on this interval or longer [16–19], while in 12, post-operative testing was conducted between 6 and 10 months following surgery [6,20–30]. Post-operative testing was conducted at two and three-week intervals in two studies [31,32] and unspecified in the remaining three [33–35].
Table 2 Details of the studies included in the review. Date
First author
N
Tasks
Results
Predictor
2010 Hamberger Prospective 2010 Kovac Retrospective
45 (25 LH) 101 (50 LH)
ANT, VNT BNT
HS Atypical dominance
2009 Schwarz
Prospective
58 (24 LH)
BNT
Significant declines in VN following DH ATL, no declines in AN Significant declines in VN following DH ATL in patients with atypical language representation Significant decline in VN following DH ATL in patients with left TLE
2007 2007 2005 2005 2005
Prospective Retrospective Prospective Retrospective Retrospective
12 HS+ 12 HS− 23 (LH) 24 (LH) 80 (LH) 45(LH)
ANT, VNT Custom CS BNT Custom VN BNT
Significant declines in VN following DH ATL only in patients without HS Significant declines in VN following DH ATL Declines in VN greater than RCI in 54% of patients No decline and some improvement in naming following tailored resection Post-ATL decline equal to the RCI on BNT
2003 Glosser
Retrospective
2000 Bell 2000 Strauss 1999 Hermann
Retrospective Prospective RCT
63 + 10 controls 48 (26 LH) 79 (LH) 30
1999 Hermann
Retrospective
217
1998 Davies
Prospective
99 (LH)
Hamberger Yucus Davies Liejten Schwarz
Study type
Impaired semantic functions HS Age of seizure onset Age of seizure onset – Seizure onset post 14 yrs
1998 Seidenberg Prospective
88 (54 LH)
1996 Langfitt 1996 Tippett
59 37 (17 LH)
BNT + custom CS Impaired naming of famous people in all groups, most significant in left ATL patients BNT + custom CS 17 of 26 LH ATL patients demonstrated meaningful decline on BNT Age of word acquisition BNT Significant decline in naming following DH ATL, particularly for living things BNT + custom No significant differences between the groups in naming VN BNT Significant declines in VN following DH ATL regardless of surgical Age of seizure onset technique BNT + custom Significant declines in VN following DH ATL. HS VN Significantly worse preop scores for HS + VN-MAT Significant declines in VN following DH ATL in non-MTLE group, not in the MTLE group BNT Significant decline in VN following DH ATL in 25% of patients Custom VN Left ATL patients disproportionately impaired in naming non-living things
154 (85 LH) 95 (53 LH) 162 (85 LH) 45
BNT BNT VN-MAT BNT
1995 1995 1994 1990
Saykin Davies Hermann Stafinaik
Retrospective Crosssectional Prospective Prospective Prospective Prospective
Significant declines in language overall after DH resection No significant declines in LHD ATL group Mild decline in left group Significant decline in VN following ATL in 60% patients with no early risk
Age of seizure onset
BNT, Boston Naming Test; ANT, Auditory Naming Test; VNT, Visual Naming Test; VN-MAT Visual Naming Test from the Multilingual Aphasia Test; HS, hippocampal sclerosis; LH, left hemisphere.
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The findings of 14 of the 21 studies reviewed relied on results from the Boston Naming Test (BNT) [6,16,19–24,26,27,29,31,32,34], two relied on results of the Visual Naming Test from the Multilingual Aphasia Test battery [30,33], and the remaining two studies relied on the results of customized visual naming tests [25,28], using line drawing from Snodgrass and Vanderwart [36]. Two of the studies in the review used both the Visual Naming Test (VNT) and Auditory Naming Test (ANT) [17,18], and one used a single category-specific naming assessment [35]. Of the 14 studies administering the BNT, one added a category-specific naming task [31], and two ran additional analyses to assess the differential effects of ATL on the naming of living versus non-living items on the BNT (14 living:46 non-living) [20,34]. Significant declines in visual confrontation naming following ATL were reported in all but two studies reviewed [16,23], and deficits in the naming of living versus non-living stimuli/famous faces were reported in five studies that measured category-specific naming [20,28,34,35,37]. No significant changes in auditory naming were reported. Of the 14 studies in which results of the BNT were reported, significant declines on the measure post-ATL were noted in all but two [6,16]. In four of the 12 studies, reliable change indices (RCIs) were calculated and naming declines exceeded the RCI in all cases [20,21,23,27]. Significant declines following surgery were also reported in all of the studies relying on customized visual naming assessments. Significant declines in visual naming were reported in both studies using the VNT [17,18]. These results are depicted in Fig. 1. Raw scores were used (where available) to calculate the average decline on the BNT in patients who underwent dominanthemisphere ATL across the studies reviewed, in the interest of assessing whether overall change scores on the test exceeded the reported RCI of ≥5 [38,39]. There was an average decline of 5.8 points on the BNT for the pooled sample of patients (N = 495) across nine studies that reported raw scores. Of the 20 articles in this review reporting significant declines in visual naming following ATL, 11 assessed predictors of post-operative dysnomia. In six studies, late onset epilepsy was cited as a significant predictor of post-operative naming decline [20,21,27,29,30,35], and three studies have shown the absence of hippocampal sclerosis to be a significant predictor of dysnomia [6,17,18,22]. Davies [22] and Hermann [6] included both age of epilepsy onset and the absence of hippocampal sclerosis in their analyses and found a stronger correlation between naming declines and the absence of hippocampal sclerosis.
4. Discussion Dysnomia is frequently reported in patients with TLE, and naming declines are observed in a high percentage of patients undergoing ATL. In this review of the literature, significant declines in naming following ATL in the dominant hemisphere were reported in 19 of the 21 articles reviewed. All of the reported declines were in visual confrontation naming. To date, there is no evidence of significant postoperative declines in auditory naming, even though auditory naming has been shown to be auditory naming assessment has been shown in TLE patients and is considered a closer analog to word-finding difficulties in daily life [23,40,41]. However, auditory naming was only assessed in two of the 22 articles reviewed, and in one of these studies, 24% of patients exhibited declines on the ANT [17]. In terms of category-specific naming declines, there is evidence that the naming of living stimuli/famous faces is particularly vulnerable to decline following ATL. Paradoxically, ATL appears to carry a greater risk to visual naming than to auditory naming, despite the evidence from cortical stimulation and fMRI indicating that auditory naming systems are located in the region resected, while visual naming systems are typically spared [17]. Some authors have reasoned that improvements in executive functioning following ATL, which are well described, may explain the preservation of auditory naming, since this type of naming relies more heavily on executive functioning [40]. Additionally, results of cortical stimulation have shown that auditory naming sites are more posteriorly distributed in patients with HS [17] and therefore spared in ATL. Stratifying samples based on the presence or absence of HS may therefore reveal significant declines in auditory naming in surgical patients without HS. Further research in this area is necessary. Deficits in the naming of living stimuli/famous faces appear to be particularly vulnerable to anterior temporal lobe resection, as reported in several studies reviewed [20,28,34,37]. These findings are consistent with what has been learned about the neural substrates of category-specific naming: The functional integrity of the posterior region of the dominant TL has been shown to be associated with the naming of objects or non-living stimuli, and integrity of the anterior region has been shown to be associated with the naming of living objects/famous faces [42,43]. Dysnomia, in the category of living stimuli, has been reported in ATL patients in a recent study that did not meet the inclusion criteria of this review, because a pre- and post-surgical design was not employed, but nevertheless demonstrated significant deficits in naming famous faces and animals in patients with dominant anterior temporal lobe seizure onset/resection [44]. The authors note
Fig. 1. Naming outcomes of ATL with the number of studies that reported significant post-operative declines in naming — highlighted in red. BNT, Boston Naming Test; VNT, Visual Naming Test; ANT, Auditory Naming Test; CS, category-specific naming tests.
V.L. Ives-Deliperi, J.T. Butler / Epilepsy & Behavior 24 (2012) 194–198
that naming and recognition deficits were infrequently detected by the BNT, which samples only a limited range of stimuli, and suggest that category-specific naming deficits may therefore have been undetected. Deficits in naming famous faces following resection of the anterior temporal lobe are consistent with the growing body of literature on proper name anomia, which is described as a selective anomia for famous people and places and is associated with anterior temporal lobe pathology [11,44,45,46]. Several studies have assessed predictors of naming decline in TLE patients undergoing ATL. The most commonly cited predictors are late onset of epilepsy and the absence of structural hippocampal pathology. These predictors are probably related to interhemispheric and intrahemispheric reorganization of language and the role of the hippocampus in higher-order visual processing [22,39,47]. The correlation between late onset of seizures and the risk of post-operative dysnomia is a robust finding [6,20,27,29,30,32,35]. Although earlier onset of epilepsy is associated with an increased proportion of anterior naming sites [48], presumably increasing the risk of dysnomia following ATL, it has been suggested that these patients undergo reorganization of the language-semantic-based knowledge system, rendering some of the anterior temporal lobe nominal language sites redundant in nominal speech [6]. More recent findings have shown that early onset of epilepsy and the associated functional disturbances interrupt normal development and result in more diffuse language organization [27]. Bell and colleagues [20] have added to this literature, demonstrating that when naming declines following ATL, it is lateracquired words that are most vulnerable to loss, presumably due to the temporal gradient of encoded memories. Age of acquisition of words has also been shown to predict the nature of naming decline in aphasic patients and patients with semantic dementia [49]. The hippocampus in the dominant hemisphere is considered to play a significant role in the neural network involved in visual confrontation naming [17,39,47,50]. The presence of hippocampal sclerosis in patients with TLE appears to offer some protection against post-operative dysnomia, due to the potential redistribution of visual naming sites in response to early hippocampal and associated pathology. It is important to consider cognitive gains and losses that follow ATL against those that may have occurred as a natural course of TLE. Progressive cognitive decline in patients with TLE has been reported previously, most notably for memory impairment [51–54]. Seizure frequency and left hippocampal atrophy have been associated with such declines. One study reported a correlation between cognitive decline and duration of epilepsy (duration ranging from 9 to 56 years), with each year of epilepsy related to an increase in the impairment index of 0.5% [54]. While these studies have been informative, many rely on small samples and cross-sectional designs. Those patients with the longest duration of epilepsy are likely to have the most severe forms of temporal lobe epilepsy, and therefore, the most severe hippocampal atrophy and the most severely impaired cognitive performance. Hence, cross-sectional studies that find an association between age and cognitive performance, suggesting progressive cognitive decline, may be confounded by the severity of the condition. Not all authors have found worsening of cognitive performance over time. In one study, cognitive deficits associated with MTLE in childhood remained stable across the adult lifespan, at least until 60 years of age, despite the intractable nature of the seizures [55]. Although none of these studies measured progressive declines in naming per se, it may be reasonable to assume, should naming progressively decline at all over time, that such a decline would be protracted, as is the case with IQ and memory decline, and thus would not confound the results of surgical outcomes. Based on the summary of the literature on naming outcomes following ATL presented in this review, visual confrontation naming is highly vulnerable to decline after ATL. The BNT has been the most frequently used formal assessment of visual naming and, perhaps because of this, the test that has reliably detected post-operative
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dysnomia. Since ATL has been shown to carry a risk to the naming of living versus non-living stimuli, and particularly the naming of famous faces, including category-specific assessments may provide a more sensitive measure of interval change than the BNT. This may enhance current understanding of the systems involved in the components of naming. Further research is also recommended to determine the effects of anterior temporal lobe resection on auditory naming, particularly in patients without HS. Previous research has found non-significant declines in auditory naming following ATL. This may relate to the observation that auditory naming sites, in patients with HS, are more posteriorly distributed and that HS is common in patients with TLE. The confounding role of executive performance in auditory naming and the differential neural substrates of visual versus auditory category-specific naming of particular interest. In recent years, it has also been shown that more selective surgical procedures and tailored surgeries may present modestly less risk to naming [6,56]. This needs to be confirmed in more robust studies applying randomizedcontrolled designs, and taking into account what has been learned from the literature on the nature of dysnomia following ATL.
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Review
Naming outcomes of anterior temporal lobectomy in epilepsy patients: A systematic review of the literature Victoria Lyn Ives-Deliperi a,⁎, James Thomas Butler b, c a b c
Department of Human Biology, University of Cape Town, South Africa Department of Neurology, University of Stellenbosch, South Africa Department of Neurology, University of Cape Town, South Africa
a r t i c l e
i n f o
Article history: Received 19 March 2012 Revised 2 April 2012 Accepted 3 April 2012 Available online 7 May 2012 Keywords: Naming Dysnomia Epilepsy Surgery ATL Neuropsychology Aphasia Cognition Anterior temporal lobe Language
a b s t r a c t Anterior temporal lobectomy (ATL) is the standard surgical treatment for medically intractable temporal lobe epilepsy (TLE). While seizure outcome is favorable, cognitive outcomes are a concern, particularly in respect of memory and naming. A systematic review of the literature on the naming outcomes of ATL is presented in this article. Searches were conducted on PubMed and PsycInfo, yielding a total of 93 articles, 21 of which met inclusion criteria. Declines in visual naming are common following ATL in the dominant hemisphere, and particularly, for naming living stimuli or famous faces. The Boston Naming Test (BNT) declines by a mean of 5.8 points, exceeding the Reliable Change Index (RCI). There are no reports of deficits in auditory naming following ATL, despite the fact that auditory naming has shown to be a more sensitive measure of dysnomia than the BNT in TLE patients. The absence of structural hippocampal pathology and late-onset epilepsy are the strongest predictors of naming decline. Recommendations are made for further study. © 2012 Elsevier Inc. All rights reserved.
1. Introduction The surgical treatment of medically intractable temporal lobe epilepsy (TLE) is highly effective in controlling seizures [1,2]. Anterior temporal lobectomy (ATL) is the standard surgical procedure for TLE; while seizure outcome has been shown to be favorable, post-operative declines in cognitive performance are frequently reported. Verbal memory and naming are the two cognitive modalities at the greatest risk of decline following ATL performed in the language-dominant hemisphere [3,4]. Post-operative naming declines are observed in between 25 and 60% of patients undergoing ATL [5]. There are no reports of naming decline following non-dominant hemisphere resection. A recent systematic review calculating pooled estimates of neuropsychological outcomes after temporal lobe resections reported a 44% risk of decline in verbal memory and 34% risk of decline in naming after left-sided surgery [4]. No significant declines in IQ were found following ATL in the dominant hemisphere, and improvements in verbal fluency and executive functioning were reported. In addition, quality of life has been shown to significantly improve in surgically-treated TLE patients compared to medically-treated patients [2]. ⁎ Corresponding author at: 209(b) Mediclinic Constantiaberg, Burnham Road, Plumstead, 7800, South Africa. Fax: + 27 21 7979960. E-mail address: [email protected] (V.L. Ives-Deliperi). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.04.115
While seizure control is of primary interest in the surgical treatment of TLE, preserving or improving cognitive outcome is equally important. For this reason, there has been a growing application of more selective surgical procedures expected to reduce postoperative cognitive impairment [6,3]. In the case of the standard ATL, 3–6 cm of anterior temporal neocortex is resected along with the amygdala and hippocampus, while in more selective procedures, like the selective amygdalohippocampectomy (SAH), the amygdala, hippocampus, and parahippocampal gyrus are resected and the neocortex is spared as far as possible [7]. There is a lack of evidence to show that more selective procedures produce favorable cognitive outcomes, and further research in this area is required. In order to support such research, it is important to review the neural substrates of naming, elucidate the nature of naming deficits following ATL, and identify the assessments that are most sensitive and specific to such declines. Naming is the earliest milestone in linguistic development. Much like the broader modality of language, naming relies on a number of distinct but interacting cognitive processes and mental representations that are subserved by a distributed network of brain regions [8,9]. Disruption to any of these regions can effect naming. In addition to this, research has shown that specific categories of naming rely on the functional integrity of discrete regions in the dominant hemisphere. Distinctions have been made between regions supporting
V.L. Ives-Deliperi, J.T. Butler / Epilepsy & Behavior 24 (2012) 194–198 Table 1 Inclusion and exclusion criteria for articles on naming outcomes following ATL. Inclusion criteria Original research article or literature review Anterior temporal lobectomy Adult temporal lobe epilepsy population Pre- and post-surgical testing of naming Exclusion criteria Pediatric epilepsy population
living stimuli/ people and animals versus non-living stimuli/objects [10,11], where the former rely on medial or posterior regions of dominant temporal lobe and the latter on regions situated more anteriorly. Likewise, differential substrates are involved in visual versus auditory naming tasks. As the label implies, visual naming, otherwise referred to as confrontation naming, involves the presentation of stimuli in the form of pictures or drawings; Auditory naming, also referred to as descriptive naming, involves generating the name from a verbal description of a stimuli. Functional neuroimaging and electrocortical stimulation have shown visual naming to be subserved by more posterior temporal lobe regions [12,13], and auditory naming to rely on regions situated more anteriorly in the temporal lobe [14,15]. To our knowledge, no research has been conducted on the different regions involved in visual versus auditory category-specific naming. The neural correlates of visual, auditory, and categoryspecific naming are important considerations when investigating dysnomia as an outcome of different surgical resections. The purpose of this review is to summarize what has been learned about naming deficits following ATL. This information is aimed to guide further research on the differential outcomes of surgical interventions in the treatment of TLE.
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2. Method A focused literature search was conducted using PubMed and PsycInfo databases. Search terms included: epilepsy, surgery, naming, dysnomia, and language. The initial search yielded 93 articles of which 20 met inclusion criteria. Inclusion and exclusion criteria are outlined in Table 1. Articles were retrieved and read in full, and references were examined to identify additional studies. One additional study was identified for inclusion through this process. Articles that focused exclusively on pediatric populations were excluded, because of potential confounding effects of language development on naming outcome. Particular attention was paid to the sample sizes in these studies, the interval between surgery and post-operative testing, and the instruments used to assess naming the type of naming assessed. With these factors in mind, the primary interest was in the prevalence of reported post-operative dysnomia in patients undergoing dominant-hemisphere resections. Secondary interests were in the type of naming most vulnerable to decline following resection of the anterior temporal lobe and factors predicting naming decline. 3. Results Details of the 21 articles included in the review are presented in Table 2. The sample sizes of the studies ranged from 17 to 217 (mean = 58). A 1-year interval between surgery and post-operative cognitive testing is considered by some to be optimal [6], and four of the studies reviewed relied on this interval or longer [16–19], while in 12, post-operative testing was conducted between 6 and 10 months following surgery [6,20–30]. Post-operative testing was conducted at two and three-week intervals in two studies [31,32] and unspecified in the remaining three [33–35].
Table 2 Details of the studies included in the review. Date
First author
N
Tasks
Results
Predictor
2010 Hamberger Prospective 2010 Kovac Retrospective
45 (25 LH) 101 (50 LH)
ANT, VNT BNT
HS Atypical dominance
2009 Schwarz
Prospective
58 (24 LH)
BNT
Significant declines in VN following DH ATL, no declines in AN Significant declines in VN following DH ATL in patients with atypical language representation Significant decline in VN following DH ATL in patients with left TLE
2007 2007 2005 2005 2005
Prospective Retrospective Prospective Retrospective Retrospective
12 HS+ 12 HS− 23 (LH) 24 (LH) 80 (LH) 45(LH)
ANT, VNT Custom CS BNT Custom VN BNT
Significant declines in VN following DH ATL only in patients without HS Significant declines in VN following DH ATL Declines in VN greater than RCI in 54% of patients No decline and some improvement in naming following tailored resection Post-ATL decline equal to the RCI on BNT
2003 Glosser
Retrospective
2000 Bell 2000 Strauss 1999 Hermann
Retrospective Prospective RCT
63 + 10 controls 48 (26 LH) 79 (LH) 30
1999 Hermann
Retrospective
217
1998 Davies
Prospective
99 (LH)
Hamberger Yucus Davies Liejten Schwarz
Study type
Impaired semantic functions HS Age of seizure onset Age of seizure onset – Seizure onset post 14 yrs
1998 Seidenberg Prospective
88 (54 LH)
1996 Langfitt 1996 Tippett
59 37 (17 LH)
BNT + custom CS Impaired naming of famous people in all groups, most significant in left ATL patients BNT + custom CS 17 of 26 LH ATL patients demonstrated meaningful decline on BNT Age of word acquisition BNT Significant decline in naming following DH ATL, particularly for living things BNT + custom No significant differences between the groups in naming VN BNT Significant declines in VN following DH ATL regardless of surgical Age of seizure onset technique BNT + custom Significant declines in VN following DH ATL. HS VN Significantly worse preop scores for HS + VN-MAT Significant declines in VN following DH ATL in non-MTLE group, not in the MTLE group BNT Significant decline in VN following DH ATL in 25% of patients Custom VN Left ATL patients disproportionately impaired in naming non-living things
154 (85 LH) 95 (53 LH) 162 (85 LH) 45
BNT BNT VN-MAT BNT
1995 1995 1994 1990
Saykin Davies Hermann Stafinaik
Retrospective Crosssectional Prospective Prospective Prospective Prospective
Significant declines in language overall after DH resection No significant declines in LHD ATL group Mild decline in left group Significant decline in VN following ATL in 60% patients with no early risk
Age of seizure onset
BNT, Boston Naming Test; ANT, Auditory Naming Test; VNT, Visual Naming Test; VN-MAT Visual Naming Test from the Multilingual Aphasia Test; HS, hippocampal sclerosis; LH, left hemisphere.
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The findings of 14 of the 21 studies reviewed relied on results from the Boston Naming Test (BNT) [6,16,19–24,26,27,29,31,32,34], two relied on results of the Visual Naming Test from the Multilingual Aphasia Test battery [30,33], and the remaining two studies relied on the results of customized visual naming tests [25,28], using line drawing from Snodgrass and Vanderwart [36]. Two of the studies in the review used both the Visual Naming Test (VNT) and Auditory Naming Test (ANT) [17,18], and one used a single category-specific naming assessment [35]. Of the 14 studies administering the BNT, one added a category-specific naming task [31], and two ran additional analyses to assess the differential effects of ATL on the naming of living versus non-living items on the BNT (14 living:46 non-living) [20,34]. Significant declines in visual confrontation naming following ATL were reported in all but two studies reviewed [16,23], and deficits in the naming of living versus non-living stimuli/famous faces were reported in five studies that measured category-specific naming [20,28,34,35,37]. No significant changes in auditory naming were reported. Of the 14 studies in which results of the BNT were reported, significant declines on the measure post-ATL were noted in all but two [6,16]. In four of the 12 studies, reliable change indices (RCIs) were calculated and naming declines exceeded the RCI in all cases [20,21,23,27]. Significant declines following surgery were also reported in all of the studies relying on customized visual naming assessments. Significant declines in visual naming were reported in both studies using the VNT [17,18]. These results are depicted in Fig. 1. Raw scores were used (where available) to calculate the average decline on the BNT in patients who underwent dominanthemisphere ATL across the studies reviewed, in the interest of assessing whether overall change scores on the test exceeded the reported RCI of ≥5 [38,39]. There was an average decline of 5.8 points on the BNT for the pooled sample of patients (N = 495) across nine studies that reported raw scores. Of the 20 articles in this review reporting significant declines in visual naming following ATL, 11 assessed predictors of post-operative dysnomia. In six studies, late onset epilepsy was cited as a significant predictor of post-operative naming decline [20,21,27,29,30,35], and three studies have shown the absence of hippocampal sclerosis to be a significant predictor of dysnomia [6,17,18,22]. Davies [22] and Hermann [6] included both age of epilepsy onset and the absence of hippocampal sclerosis in their analyses and found a stronger correlation between naming declines and the absence of hippocampal sclerosis.
4. Discussion Dysnomia is frequently reported in patients with TLE, and naming declines are observed in a high percentage of patients undergoing ATL. In this review of the literature, significant declines in naming following ATL in the dominant hemisphere were reported in 19 of the 21 articles reviewed. All of the reported declines were in visual confrontation naming. To date, there is no evidence of significant postoperative declines in auditory naming, even though auditory naming has been shown to be auditory naming assessment has been shown in TLE patients and is considered a closer analog to word-finding difficulties in daily life [23,40,41]. However, auditory naming was only assessed in two of the 22 articles reviewed, and in one of these studies, 24% of patients exhibited declines on the ANT [17]. In terms of category-specific naming declines, there is evidence that the naming of living stimuli/famous faces is particularly vulnerable to decline following ATL. Paradoxically, ATL appears to carry a greater risk to visual naming than to auditory naming, despite the evidence from cortical stimulation and fMRI indicating that auditory naming systems are located in the region resected, while visual naming systems are typically spared [17]. Some authors have reasoned that improvements in executive functioning following ATL, which are well described, may explain the preservation of auditory naming, since this type of naming relies more heavily on executive functioning [40]. Additionally, results of cortical stimulation have shown that auditory naming sites are more posteriorly distributed in patients with HS [17] and therefore spared in ATL. Stratifying samples based on the presence or absence of HS may therefore reveal significant declines in auditory naming in surgical patients without HS. Further research in this area is necessary. Deficits in the naming of living stimuli/famous faces appear to be particularly vulnerable to anterior temporal lobe resection, as reported in several studies reviewed [20,28,34,37]. These findings are consistent with what has been learned about the neural substrates of category-specific naming: The functional integrity of the posterior region of the dominant TL has been shown to be associated with the naming of objects or non-living stimuli, and integrity of the anterior region has been shown to be associated with the naming of living objects/famous faces [42,43]. Dysnomia, in the category of living stimuli, has been reported in ATL patients in a recent study that did not meet the inclusion criteria of this review, because a pre- and post-surgical design was not employed, but nevertheless demonstrated significant deficits in naming famous faces and animals in patients with dominant anterior temporal lobe seizure onset/resection [44]. The authors note
Fig. 1. Naming outcomes of ATL with the number of studies that reported significant post-operative declines in naming — highlighted in red. BNT, Boston Naming Test; VNT, Visual Naming Test; ANT, Auditory Naming Test; CS, category-specific naming tests.
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that naming and recognition deficits were infrequently detected by the BNT, which samples only a limited range of stimuli, and suggest that category-specific naming deficits may therefore have been undetected. Deficits in naming famous faces following resection of the anterior temporal lobe are consistent with the growing body of literature on proper name anomia, which is described as a selective anomia for famous people and places and is associated with anterior temporal lobe pathology [11,44,45,46]. Several studies have assessed predictors of naming decline in TLE patients undergoing ATL. The most commonly cited predictors are late onset of epilepsy and the absence of structural hippocampal pathology. These predictors are probably related to interhemispheric and intrahemispheric reorganization of language and the role of the hippocampus in higher-order visual processing [22,39,47]. The correlation between late onset of seizures and the risk of post-operative dysnomia is a robust finding [6,20,27,29,30,32,35]. Although earlier onset of epilepsy is associated with an increased proportion of anterior naming sites [48], presumably increasing the risk of dysnomia following ATL, it has been suggested that these patients undergo reorganization of the language-semantic-based knowledge system, rendering some of the anterior temporal lobe nominal language sites redundant in nominal speech [6]. More recent findings have shown that early onset of epilepsy and the associated functional disturbances interrupt normal development and result in more diffuse language organization [27]. Bell and colleagues [20] have added to this literature, demonstrating that when naming declines following ATL, it is lateracquired words that are most vulnerable to loss, presumably due to the temporal gradient of encoded memories. Age of acquisition of words has also been shown to predict the nature of naming decline in aphasic patients and patients with semantic dementia [49]. The hippocampus in the dominant hemisphere is considered to play a significant role in the neural network involved in visual confrontation naming [17,39,47,50]. The presence of hippocampal sclerosis in patients with TLE appears to offer some protection against post-operative dysnomia, due to the potential redistribution of visual naming sites in response to early hippocampal and associated pathology. It is important to consider cognitive gains and losses that follow ATL against those that may have occurred as a natural course of TLE. Progressive cognitive decline in patients with TLE has been reported previously, most notably for memory impairment [51–54]. Seizure frequency and left hippocampal atrophy have been associated with such declines. One study reported a correlation between cognitive decline and duration of epilepsy (duration ranging from 9 to 56 years), with each year of epilepsy related to an increase in the impairment index of 0.5% [54]. While these studies have been informative, many rely on small samples and cross-sectional designs. Those patients with the longest duration of epilepsy are likely to have the most severe forms of temporal lobe epilepsy, and therefore, the most severe hippocampal atrophy and the most severely impaired cognitive performance. Hence, cross-sectional studies that find an association between age and cognitive performance, suggesting progressive cognitive decline, may be confounded by the severity of the condition. Not all authors have found worsening of cognitive performance over time. In one study, cognitive deficits associated with MTLE in childhood remained stable across the adult lifespan, at least until 60 years of age, despite the intractable nature of the seizures [55]. Although none of these studies measured progressive declines in naming per se, it may be reasonable to assume, should naming progressively decline at all over time, that such a decline would be protracted, as is the case with IQ and memory decline, and thus would not confound the results of surgical outcomes. Based on the summary of the literature on naming outcomes following ATL presented in this review, visual confrontation naming is highly vulnerable to decline after ATL. The BNT has been the most frequently used formal assessment of visual naming and, perhaps because of this, the test that has reliably detected post-operative
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dysnomia. Since ATL has been shown to carry a risk to the naming of living versus non-living stimuli, and particularly the naming of famous faces, including category-specific assessments may provide a more sensitive measure of interval change than the BNT. This may enhance current understanding of the systems involved in the components of naming. Further research is also recommended to determine the effects of anterior temporal lobe resection on auditory naming, particularly in patients without HS. Previous research has found non-significant declines in auditory naming following ATL. This may relate to the observation that auditory naming sites, in patients with HS, are more posteriorly distributed and that HS is common in patients with TLE. The confounding role of executive performance in auditory naming and the differential neural substrates of visual versus auditory category-specific naming of particular interest. In recent years, it has also been shown that more selective surgical procedures and tailored surgeries may present modestly less risk to naming [6,56]. This needs to be confirmed in more robust studies applying randomizedcontrolled designs, and taking into account what has been learned from the literature on the nature of dysnomia following ATL.
Ethical publication We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
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