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Diagnostic validity of a neuropsychological test battery for Hispanic patients with epilepsy
Epilepsy & Behavior 16 (2009) 479–483
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Diagnostic validity of a neuropsychological test battery for Hispanic patients with epilepsy William B. Barr a,*, Heidi A. Bender a, Chris Morrison a, Daniel Cruz-Laureano b, Blanca Vazquez a, Ruben Kuzniecky a a b
NYU Langone Medical Center, Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY, USA Division of Neuropsychology, Department of Neurosurgery, Scott & White Memorial Hospital, Texas A&M Health Science Center, Temple, TX, USA
a r t i c l e
i n f o
Article history: Received 29 June 2009 Revised 26 August 2009 Accepted 26 August 2009 Available online 30 September 2009 Keywords: Memory Naming Processing speed Neuropsychology Temporal lobe epilepsy Spanish Cultural
a b s t r a c t The Neuropsychological Screening Battery for Hispanics (NeSBHIS) was developed to address the growing need for linguistically appropriate Spanish-language assessment measures. Despite the potential benefits to clinical practice, no prior study has assessed its diagnostic validity in populations with epilepsy. One hundred and fifteen patients with confirmed epilepsy were evaluated via the NeSBHIS; these data were standardized according to age- and education-based norms. Performance decrements were observed in more than 40% of participants on measures of processing speed and naming. Deficits in verbal and visual recall were also exhibited by 29 and 26% of the sample, respectively. No significant differences in test performance emerged between patients with VEEG evidence of left (N = 48) versus right (N = 24) temporal lobe epilepsy. Although the NeSBHIS is sensitive to the cognitive impairments commonly observed in populations with epilepsy, there are limitations to its ability to identify lateralized neuropsychological impairment in patients with temporal lobe epilepsy. Ó 2009 Elsevier Inc. All rights reserved.
1. Introduction Neuropsychology’s role in comprehensive epilepsy centers has evolved in recent decades because of changes in the characteristics and numbers of patients undergoing surgical intervention as a treatment for medically refractory seizures [1–3]. Test batteries used for neuropsychological assessment of surgical candidates typically include measures of global intellectual functioning, as well as tests of other more specific neuropsychological domains including language and memory [4]. Much is now known about the psychometric properties and diagnostic utility of neuropsychological tests administered to English-speaking individuals, particularly those evaluated in North America. However, very little information exists on neuropsychological testing of patients with epilepsy from other cultural and linguistic backgrounds. The paucity of culturally and linguistically appropriate neuropsychological test measures is of particular concern to the Hispanic immigrant community in the United States, as this population represents the most rapidly growing segment of the country’s population. There are indications that Hispanic immigrants are now presenting for treatment at U.S. epilepsy centers with increasing * Corresponding author. Address: NYU Comprehensive Epilepsy Center, 223 East 34th Street, New York, NY 10016, USA. Fax: +1 (646) 385 7167. E-mail address: [email protected] (W.B. Barr). 1525-5050/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2009.08.030
regularity. With this comes an increased need for linguistically and culturally relevant neuropsychological assessment tools, including those appropriate for presurgical contexts. Experience has shown that the solution to this problem is not to simply translate existing test materials into Spanish; test developers must ensure that the assessment materials are culturally and linguistically appropriate for the population in question [5,6]. One must also determine whether the normative data used to interpret the tests are drawn from a group that is ethnically and demographically similar to the clinical sample. The Neuropsychological Screening Battery for Hispanics (NeSBHIS) was developed by researchers at UCLA in the 1990s to address the fundamental lack of resources available to Spanish-speaking Hispanic individuals [7]. Modeled after a battery first used by the World Health Organization [8], the NeSBHIS was designed to assess multiple cognitive domains. One of the primary advantages of the battery is that it has been among the few to provide data on its psychometric characteristics in addition to test norms stratified by age, gender, and education using a moderately large (N = 300) Spanish-speaking sample [9]. Although the NeSBHIS represents a significant advancement in Spanish-language neuropsychological assessment, concerns exist regarding the generalizability of this instrument to a more medically heterogeneous sample [10]. Although preliminary investigation suggests adequate clinical utility in some patient groups, its
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construct validity and diagnostic utility in patients with epilepsy are unknown. The present study aims to examine the diagnostic validity of the NeSBHIS in identifying relevant cognitive impairments in Spanish-speaking Hispanic patients with epilepsy and in predicting seizure lateralization in surgical candidates. 2. Methods 2.1. Subjects Test data were acquired from a consecutive series of 136 Hispanic patients with epilepsy who had completed neuropsychological evaluations at the New York University Comprehensive Epilepsy Center between 2000 and 2006. All participants described themselves as ‘‘Hispanic”, emigrated from Spanish-speaking countries, and opted for Spanish-language assessment. A diagnosis of epilepsy was confirmed in each case through results of continuous video/EEG (VEEG) monitoring. Data from 21 patients were excluded from analysis because the VEEG results demonstrated no epileptiform abnormality (N = 10) or the presence of nonepileptic seizures with no accompanying EEG changes (N = 11). Demographic characteristics of the final study sample of 115 patients are provided in Table 1. VEEG findings indicated that the majority of the sample demonstrated electrophysiological evidence of partial epilepsy. Fifteen participants exhibited generalized VEEG findings. Results from imaging studies using magnetic resonance imaging (MRI) were available for 95 subjects. Nearly half (47%) had normal MRI scans or findings limited to the presence of mesial temporal sclerosis (MTS). Thirty percent of the patients showed evidence of lesions including benign tumors, vascular malformations, and cortical malformations. Additional analyses were conducted on a subgroup of 83 participants evaluated as surgical candidates who were found to have VEEG results demonstrating the presence of a temporal lobe seizure focus. A total of 48 subjects were determined to have seizures emanating from the left temporal lobe (LTL), and 24 had seizures Table 1 Sample characteristics for 115 Spanish-speaking patients undergoing neuropsychological testing.
a
Age
37.0 (12.4)a
Sex Male Female
41 74
Years of education
11.9 (4.0)a
Handedness Right Left
100 15
Land of origin Puerto Rico Central America South America Dominican Republic Other Caribbean
52 30 9 12 2
Age at epilepsy onset
15.9 (13.0)a
VEEG results Temporal Frontal Other focal Generalized
83 8 9 15
MRI findings (N = 95) Normal Mesial temporal sclerosis only Atrophy Lesion Other
29 16 18 30 2
Mean (SD).
localized to the right (RTL). The remaining 11 subjects demonstrated bilateral EEG findings or results that were inconclusive based on the surface recordings. The demographic and MRI characteristics of the subjects with temporal lobe seizures were similar to those seen in the larger sample. No significant differences in demographic or seizure variables were observed between LTL and RTL subjects. Wada test results were available for half of the sample, with the majority (86%) demonstrating language localization in the left cerebral hemisphere. 2.2. Procedures The present study was performed according to the policies of the institutional review board of New York University School of Medicine. Participants were tested individually in one or two sessions totaling approximately 90 minutes. All tests were administered and scored by bilingual examiners who had completed advanced graduate-school training in neuropsychological assessment. The NeSBHIS was designed as a battery of 10 subtests chosen to evaluate the domains of mental control (i.e., attention and concentration), language, memory, visuospatial functions, and psychomotor speed (see Pontón et al. [7,10] for a more comprehensive review). Most measures of this battery were adapted from subtests used internationally by the World Health Organization [8,11]. The majority of subtests constituting the NeSBHIS are already used extensively in some form by North American neuropsychologists working in comprehensive epilepsy centers. The NeSBHIS was administered for this study in conjunction with other neuropsychological tests. The battery is described as follows: 1. Raven Standard Progressive Matrices (RSPM) [12]: This test was used to assess the ability to perceive relationships and to reason by analogy, independent of language and education. This measure is considered one of the most widely administered measures of nonverbal reasoning and intelligence. 2. Digit Span Subtest—Escala de Inteligencia Wechsler para Adultos (EIWA) [13]: The Digit Span subtest from the EIWA was administered as a measure of attention and working memory. This subtest is identical in content to the Wechsler Adult Intelligence Scale— Revised (WAIS-R) [14] but involves different scoring parameters. 3. Digit Symbol Subtest—EIWA: This test was included as a measure of attention and processing speed. Unlike its English-language counterpart, the EIWA Digit Symbol task has six target symbols and the total number of possible responses is 110 (as compared with 93 on the WAIS-R/Wechsler Adult Intelligence Scale III) [14]. 4. Color Trails Test, Forms 1 and 2 (CTT) [15]: The CTT was administered as a measure of sustained tracking and set shifting. Both forms consist of colored circles numbered 1–25; odd numbers are pink and even numbers are yellow. On Trails 1, examinees were instructed to connect the circles in sequential order as quickly as possible. On Trails 2, examinees were asked to connect the circles in sequential order (while maintaining numerical sequence) and simultaneously alternate colors. 5. Pontón–Satz Boston Naming Test (P–S BNT) [16]: The P–S BNT is the 30-item Spanish-language equivalent of the 60-item English-language Boston Naming Test (BNT) [17] and was used as a measure of confrontation naming abilities. Culturally loaded items (e.g., ‘‘pretzel” and ‘‘beaver”) are also excluded from this measure to ensure cultural relevance and appropriateness for Spanish-speaking populations. 6. Controlled Oral Word Association Test (FAS) [18]: COWAT is a popular measure of verbal fluency that has been adapted for both English- and Spanish-speaking individuals. On this task, participants are given 1 minute to generate as many words as possible beginning with a target letter (in this case, ‘F’, ‘A’, and ‘S’).
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7. Block Design Subtest—EIWA: This subtest was given to all participants as a visuoconstruction task. Although similar in structure to the subtest from the WAIS-R, the EIWA Block Design has slightly different content and awards fewer time-dependent bonus points. 8. Rey–Osterrieth Complex Figure Test (ROCFT) [19]: The ROCFT copy condition was administered as a measure of visuospatial construction. Participants were asked to copy a complex geometric figure with numerous embedded details. The Taylor scoring system was used to evaluate the accuracy of the designs produced [20]. Figure recall was evaluated with this test after a half-hour delay. 9. WHO–UCLA Auditory Verbal Learning Test (WHO–UCLA AVLT) [11]: This is a version of an auditory list-learning paradigm that was developed for ease of translation into various languages. Participants are presented a serially presented list of 15 Spanish words and are asked to repeat as many as they can remember immediately following each presentation. Scores from the fifth and final learning trial (Trial V) and 20-minute delayed recall trial (LDFR) were all evaluated for this study.
3. Results Raw scores from the NeSBHIS were converted into z-scores using norms from an expanded sample of 297 healthy native Spanish-speaking control subjects [9]. The norms were stratified by age and education. Analysis based on country of origin revealed no differences among groups from Caribbean, Central American, or South American countries on tests from this battery. A graphic profile of mean z-scores from the entire sample of 115 subjects is presented in Fig. 1. Norms for Trial V performance on the WHO–UCLA AVLT were not available. All of the computed mean z-scores were below a level of zero, indicating that the level of performance observed in this sample of patients with various forms of epilepsy is generally lower than what is seen in healthy control subjects. The highest mean scores were obtained on measures of intellectual functioning, attention, and verbal fluency. The lowest scores were obtained on measures of mental tracking, naming, and memory. Test scores from individual subjects were considered to be in the ‘‘impaired” range if the z-score value exceeded a level of –2, which by definition represents a level of performance that is 2 SD below the mean of the normative group or the equivalent of scoring below the 2nd percentile. The percentage of subjects with epilepsy exhibiting ‘‘impaired” test scores for each measure is provided in Table 2. The results indicated that more than 40% of subjects from this sample exhibited impaired scores on measures of
Fig. 1. Profile of z-transformed test scores of 115 Spanish-speaking patients with a VEEG-verified diagnosis of epilepsy.
Table 2 Percentage of patients (N = 115) with neuropsychological test scores in the ‘‘impaired” range, as defined by scores lower than 2 SD below the normative mean. Test
‘‘Impaired” (%)
Raven Progressive Matrices EIWA Digit Span EIWA Digit Symbol Color Trails Test 1 Color Trails Test 2 Verbal Fluency (FAS) Boston Naming Test (Ponton–Satz) EIWA Block Design Rey Figure Copy Rey Figure Recall WHO–AVLT Learning Trial V WHO–AVLT Long Delay Recall
12.3 15.0 13.8 40.0 31.2 9.0 41.4 16.7 23.8 26.2 46.3 29.2
mental tracking and confrontation naming. Deficits in verbal and visual recall were observed in 29% and 26% of the subjects, respectively. Mean test scores from the LTL and RTL groups are listed in Table 3. Group differences were assessed with a series of independent ttests. All analyses were two-tailed with a criterion for statistical significance (a) set at 0.05. Results of the t-tests indicated that there were no group differences. v2 comparisons were made between the rates of ‘‘impaired” test scores observed in the LTL and RTL groups. Rates of impairment from measures of intelligence, attention, language, and visuospatial performance did not differ between the two groups. Analyses of memory scores indicated that 36% of the LTL group exhibited impairment on the delayed recall trial of the WHO–UCLA AVLT, as compared with only 17% of the RTL group. However, the difference between these rates was at only a ‘‘trend” level of significance (v2 = 2.901, P = 0.089). The rates of impairment in nonverbal memory, as measured with the ROCFT, were equal (LTL rate = 28%, RTL rate = 28%; v2 = 0.003, NS). The significance and pattern of results did not change when analyses were limited to subjects with left hemisphere language dominance verified through the Wada test. 4. Discussion Results of this study indicate that the NeSBHIS holds promise as a brief and clinically relevant battery of neuropsychological tests that can be administered to Spanish-speaking patients in their native language. Findings from this study indicate that the test battery is sensitive to identifying impairments in cognitive functioning seen commonly in patients with epilepsy, although there may be some limitations in its sensitivity in identifying deficits in patients with lateralized temporal lobe seizures. Analyses from our sample of 115 patients indicated that the lowest levels of performance were observed on measures of processing speed, naming, and memory. The pattern of findings using this test battery is similar to what has been reported in previous studies of cognitive functioning in patients with epilepsy conducted in multiple countries and languages [4,21–24]. However, in contrast to most other investigations, this study found that impairments in naming and processing speed occur more frequently than deficits in memory. Decreased scores on tests of naming and processing speed were identified in more than 40% of our sample, whereas only 30% of the subjects exhibited low scores on memory testing. The latter proportion is much lower than the 66% rate of memory impairment reported in a recent study of Spanish-speaking patients from Argentina evaluated with a different battery of tests [25]. It is possible that these findings result from the inclusion of a more heterogeneous sample of patients than what has been previously reported throughout the literature.
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Table 3 Descriptive statistics on raw scores (mean/SD) and t-test results for comparisons of neuropsychological test scores in patients with VEEG findings of focal left or right temporal lobe epilepsy.
a
Test
LTL group (N = 48)
RTL group (N = 24)
t-Statistica
Raven Progressive Matrices EIWA Digit Span EIWA Digit Symbol Color Trails Test 1 Color Trails Test 2 Verbal Fluency (FAS) Boston Naming Test (Ponton–Satz) EIWA Block Design Rey Figure Copy Rey Figure Recall WHO–AVLT Trial Five Recall WHO–AVLT Long Delay Recall
32.6 (14.1) 8.7 (2.4) 43.3 (17.5) 70.0 (28.9) 135.8 (58.4) 22.7 (10.6) 18.9 (5.4) 27.1 (10.7) 25.9 (9.0) 8.6 (7.3) 10.3 (3.0) 7.9 (3.5)
27.4 (13.3) 8.9 (3.3) 42.7 (21.2) 68.0 (41.6) 141.5 (78.5) 25.4 (10.1) 18.1 (4.5) 26.0 (9.5) 24.1 (7.5) 10.9 (7.0) 9.7 (2.7) 8.4 (2.8)
1.42 0.29 0.11 0.21 0.30 1.07 0.60 0.38 0.79 1.03 0.43 0.60
All values nonsignificant.
It is also possible that the tests developed for Spanish speakers used in this study have a different level of sensitivity than analogous measures used in English and other languages. This study failed to find any marked difference in neuropsychological test performance on group comparisons made in a smaller sample of 82 patients with EEG evidence of partial seizures localized to the left or right temporal lobes. A larger proportion of patients with LTL epilepsy (36%) than those with RTL epilepsy (17%) were found to be impaired on an auditory verbal learning paradigm, although the difference in these proportions was not statistically significant. Rates of impairment in nonverbal memory in these groups using the ROCFT were identical (28%). The pattern of these results is similar to what has been reported in other presurgical samples, where ‘‘material-specific” impairments in verbal memory in patients with LTL epilepsy are identified more readily than nonverbal memory deficits in patients with RTL epilepsy [26,27]. Furthermore, our study failed to demonstrate specific deficits in naming which have frequently been reported in patients with LTL epilepsy [26,28]. Future investigations are necessary to determine the utility of using the NesBHIS for purposes of identifying patterns of neuropsychological impairment to aid with presurgical localization and whether the addition of additional tests such as paragraph recall and/or design learning measures would enhance the sensitivity of the test battery in this context. The NesBHIS was developed in an effort to move in the direction of providing a more linguistically and culturally effective method for conducting neuropsychological assessment in samples of Spanish-speaking individuals [7]. Results from this study indicate that the battery provides an effective method for identifying cognitive impairment in patients with epilepsy, although a number of methodological factors still need to be addressed. One factor is that some of the tests used in the NesBHIS battery, including subtests from the EIWA and the verbal fluency measure (FAS), are less than optimal for contemporary use with Spanish-speaking patients. Additionally, it is also clear that the demographic characteristics of the NeSBHIS’s predominantly Mexican reference group may not be reflective of this study’s Hispanic population, residing primarily in the New York metropolitan region. Methodological limitations stemming from the use of insensitive tests and a suboptimal normative sample are likely to have affected the results of this study. As the Hispanic population residing in North America is such a heterogeneous group, extending the use of the NesBHIS to epilepsy centers in other metropolitan regions will be enhanced by obtaining local norms from healthy control subjects that come from cultural backgrounds similar to those of the Spanish-speaking patients in that geographic region or catchment area. Higher levels of diagnostic validity will likely follow the use of more appropriately matched normative groups combined with more sensitive
neuropsychological tests designed specifically for Spanish-speaking samples. Ethical approval 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. Conflict of interest statement None of the authors has any conflict of interest to disclose. Acknowledgments Work described in this article was supported, in part, by NIH Grants (1F32HS016819) and by Finding a Cure for Epilepsy and Seizures (FACES). References [1] Alexopoulos A, Lachhwani DK, Gupta A, et al. Resective surgery to treat refractory status epilepticus in children with focal epileptogenesis. Neurology 2005;64:567–70. [2] Bauman JA, Schuknecht B, Russo GL, et al. Multistage epilepsy surgery: safety, efficacy, and utility of a novel approach in pediatric extratemporal epilepsy. Neurosurgery 2005;56:318–34. [3] Myers L, Barr WB, Vazquez B, Devinsky O. An effective neuropsychological screening battery for Hispanic epilepsy patients. Clin Neuropsychol 2003;17:92. [4] Jones-Gotman M. Localization of lesions by neuropsychological testing. Epilepsia 1991;32(Suppl. 5):S41–52. [5] Artiola i Fortuny L, Mullaney HA. Neuropsychology with Spanish speakers: language use and proficiency issues for test development. J Clin Exp Neuropsychol 1997;19:615–22. [6] Puente AE, Ardila A. Neuropsychological assessment of Hispanics. In: FletcherJanzen TLE, Strickland Reynolds CR, editors. Handbook of cross-cultural neuropsychology. New York: Kluwer Academic/Plenum; 2000. p. 87–104. [7] Pontón MO, Satz P, Herrera L, et al. Normative data stratified by age and education for the Neuropsychological Screening Battery for Hispanics (NeSBHIS): initial report. J Int Neuropsychol Soc 1996;2:96–104. [8] Maj M, Satz P, Janssen R, et al. WHO Neuropsychiatric AIDS Study, crosssectional phase II: neuropsychological and neurological findings. Arch Gen Psychiatry 1994;51:51–61. [9] Ponton M, Corona-LoMonaco ME. Cross cultural issues in neuropsychology: assessment of the Hispanic patient. In: Uzzell BP, Ponton M, Ardila A, editors. International handbook of cross-cultural neuropsychology. Mahwah, NJ: Lawrence Erlbaum Press; 2007. p. 265–82. [10] Pontón MO, Gonzalez JJ, Hernandez I, Herrera L, Higareda I. Factor analysis of the Neuropsychological Screening Battery for Hispanics (NeSBHIS). Appl Neuropsychol 2000;7:32–9. [11] Maj M, D’Elia L, Satz P, et al. Evaluation of two new neuropsychological tests designed to minimize cultural bias in the assessment of HIV-1 seropositive persons: a WHO study. Arch Clin Neuropsychol 1993;8:123–35. [12] Raven J, Raven JC, Court JH. Manual for the Raven’s progressive matrices and vocabulary scale. Oxford: Oxford Psychologists Press; 1993.
W.B. Barr et al. / Epilepsy & Behavior 16 (2009) 479–483 [13] Wechsler D, Green RF, Martinez JN. Manual para la Escala de Inteligencia Wechsler Para Adultos (EIWA). Cleveland, OH: Psychological Corp.; 1968. [14] Wechsler D. Wechsler adult intelligence scale—Revised manual. New York: Psychological Corp.; 1981. [15] D’Elia F, Satz P, Uchiyama C. Color trails: adult form manual. Odessa, FL: Psychological Assessment Resources; 1994. [16] Pontón MO, Satz P, Herrera L, et al. Modified Spanish version of the Boston Naming Test. Clin Neuropsychol 1992;3:334. [17] Kaplan EF, Goodglass H, Weintraub S. The Boston Naming Test. Philadelphia: Lea & Febiger; 1983. [18] Benton AL, Hamsher K. Multilingual Aphasia Examination. Iowa City: Univ. of Iowa Press; 1976. [19] Osterrieth PA. Le test de copie d’une figure complexe [The complex figure copy test]. Arch Psychol 1944;30:206–356. [20] Taylor EM. Psychological appraisal of children with cerebral deficits. Cambridge, MA: Harvard Univ. Press; 1959. [21] Loring DW. Neuropsychological evaluation in epilepsy surgery. Epilepsia 1997;38(Suppl. 4):S18–23.
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[22] Lippé S, Lassonde M. Neuropsychological profile of intractable partial epilepsies. Rev Neurol (Paris) 2004;160:S144–53. [23] Campos-Castelló J, Campos-Soler S. Neuropsychology and epilepsy. Rev Neurol 2004;39:166–77. [24] Elger CE, Helmstaedter C, Kurthen M. Chronic epilepsy and cognition. Lancet Neurol 2004;3:663–72. [25] Oddo S, Solis P, Consalvo D, et al. Mesial temporal lobe epilepsy and hippocampal sclerosis: cognitive function assessment in Hispanic patients. Epilepsy Behav 2003;4:717–22. [26] Loring DW, Strauss E, Hermann BP, et al. Differential neuropsychological test sensitivity to left temporal lobe epilepsy. J Int Neuropsychol Soc 2008;14: 394–400. [27] Barr WB, Chelune GJ, Hermann BP, et al. The use of figural reproduction tests as measures of nonverbal memory in epilepsy surgery candidates. J Int Neuropsychol Soc 1997;3:435–43. [28] Busch RM, Frazier TW, Haggerty KA, Kubu CS. Utility of the Boston Naming Test in predicting ultimate side of surgery in patients with medically intractable temporal lobe epilepsy. Epilepsia 2005;46:1773–9.
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Diagnostic validity of a neuropsychological test battery for Hispanic patients with epilepsy William B. Barr a,*, Heidi A. Bender a, Chris Morrison a, Daniel Cruz-Laureano b, Blanca Vazquez a, Ruben Kuzniecky a a b
NYU Langone Medical Center, Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY, USA Division of Neuropsychology, Department of Neurosurgery, Scott & White Memorial Hospital, Texas A&M Health Science Center, Temple, TX, USA
a r t i c l e
i n f o
Article history: Received 29 June 2009 Revised 26 August 2009 Accepted 26 August 2009 Available online 30 September 2009 Keywords: Memory Naming Processing speed Neuropsychology Temporal lobe epilepsy Spanish Cultural
a b s t r a c t The Neuropsychological Screening Battery for Hispanics (NeSBHIS) was developed to address the growing need for linguistically appropriate Spanish-language assessment measures. Despite the potential benefits to clinical practice, no prior study has assessed its diagnostic validity in populations with epilepsy. One hundred and fifteen patients with confirmed epilepsy were evaluated via the NeSBHIS; these data were standardized according to age- and education-based norms. Performance decrements were observed in more than 40% of participants on measures of processing speed and naming. Deficits in verbal and visual recall were also exhibited by 29 and 26% of the sample, respectively. No significant differences in test performance emerged between patients with VEEG evidence of left (N = 48) versus right (N = 24) temporal lobe epilepsy. Although the NeSBHIS is sensitive to the cognitive impairments commonly observed in populations with epilepsy, there are limitations to its ability to identify lateralized neuropsychological impairment in patients with temporal lobe epilepsy. Ó 2009 Elsevier Inc. All rights reserved.
1. Introduction Neuropsychology’s role in comprehensive epilepsy centers has evolved in recent decades because of changes in the characteristics and numbers of patients undergoing surgical intervention as a treatment for medically refractory seizures [1–3]. Test batteries used for neuropsychological assessment of surgical candidates typically include measures of global intellectual functioning, as well as tests of other more specific neuropsychological domains including language and memory [4]. Much is now known about the psychometric properties and diagnostic utility of neuropsychological tests administered to English-speaking individuals, particularly those evaluated in North America. However, very little information exists on neuropsychological testing of patients with epilepsy from other cultural and linguistic backgrounds. The paucity of culturally and linguistically appropriate neuropsychological test measures is of particular concern to the Hispanic immigrant community in the United States, as this population represents the most rapidly growing segment of the country’s population. There are indications that Hispanic immigrants are now presenting for treatment at U.S. epilepsy centers with increasing * Corresponding author. Address: NYU Comprehensive Epilepsy Center, 223 East 34th Street, New York, NY 10016, USA. Fax: +1 (646) 385 7167. E-mail address: [email protected] (W.B. Barr). 1525-5050/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2009.08.030
regularity. With this comes an increased need for linguistically and culturally relevant neuropsychological assessment tools, including those appropriate for presurgical contexts. Experience has shown that the solution to this problem is not to simply translate existing test materials into Spanish; test developers must ensure that the assessment materials are culturally and linguistically appropriate for the population in question [5,6]. One must also determine whether the normative data used to interpret the tests are drawn from a group that is ethnically and demographically similar to the clinical sample. The Neuropsychological Screening Battery for Hispanics (NeSBHIS) was developed by researchers at UCLA in the 1990s to address the fundamental lack of resources available to Spanish-speaking Hispanic individuals [7]. Modeled after a battery first used by the World Health Organization [8], the NeSBHIS was designed to assess multiple cognitive domains. One of the primary advantages of the battery is that it has been among the few to provide data on its psychometric characteristics in addition to test norms stratified by age, gender, and education using a moderately large (N = 300) Spanish-speaking sample [9]. Although the NeSBHIS represents a significant advancement in Spanish-language neuropsychological assessment, concerns exist regarding the generalizability of this instrument to a more medically heterogeneous sample [10]. Although preliminary investigation suggests adequate clinical utility in some patient groups, its
480
W.B. Barr et al. / Epilepsy & Behavior 16 (2009) 479–483
construct validity and diagnostic utility in patients with epilepsy are unknown. The present study aims to examine the diagnostic validity of the NeSBHIS in identifying relevant cognitive impairments in Spanish-speaking Hispanic patients with epilepsy and in predicting seizure lateralization in surgical candidates. 2. Methods 2.1. Subjects Test data were acquired from a consecutive series of 136 Hispanic patients with epilepsy who had completed neuropsychological evaluations at the New York University Comprehensive Epilepsy Center between 2000 and 2006. All participants described themselves as ‘‘Hispanic”, emigrated from Spanish-speaking countries, and opted for Spanish-language assessment. A diagnosis of epilepsy was confirmed in each case through results of continuous video/EEG (VEEG) monitoring. Data from 21 patients were excluded from analysis because the VEEG results demonstrated no epileptiform abnormality (N = 10) or the presence of nonepileptic seizures with no accompanying EEG changes (N = 11). Demographic characteristics of the final study sample of 115 patients are provided in Table 1. VEEG findings indicated that the majority of the sample demonstrated electrophysiological evidence of partial epilepsy. Fifteen participants exhibited generalized VEEG findings. Results from imaging studies using magnetic resonance imaging (MRI) were available for 95 subjects. Nearly half (47%) had normal MRI scans or findings limited to the presence of mesial temporal sclerosis (MTS). Thirty percent of the patients showed evidence of lesions including benign tumors, vascular malformations, and cortical malformations. Additional analyses were conducted on a subgroup of 83 participants evaluated as surgical candidates who were found to have VEEG results demonstrating the presence of a temporal lobe seizure focus. A total of 48 subjects were determined to have seizures emanating from the left temporal lobe (LTL), and 24 had seizures Table 1 Sample characteristics for 115 Spanish-speaking patients undergoing neuropsychological testing.
a
Age
37.0 (12.4)a
Sex Male Female
41 74
Years of education
11.9 (4.0)a
Handedness Right Left
100 15
Land of origin Puerto Rico Central America South America Dominican Republic Other Caribbean
52 30 9 12 2
Age at epilepsy onset
15.9 (13.0)a
VEEG results Temporal Frontal Other focal Generalized
83 8 9 15
MRI findings (N = 95) Normal Mesial temporal sclerosis only Atrophy Lesion Other
29 16 18 30 2
Mean (SD).
localized to the right (RTL). The remaining 11 subjects demonstrated bilateral EEG findings or results that were inconclusive based on the surface recordings. The demographic and MRI characteristics of the subjects with temporal lobe seizures were similar to those seen in the larger sample. No significant differences in demographic or seizure variables were observed between LTL and RTL subjects. Wada test results were available for half of the sample, with the majority (86%) demonstrating language localization in the left cerebral hemisphere. 2.2. Procedures The present study was performed according to the policies of the institutional review board of New York University School of Medicine. Participants were tested individually in one or two sessions totaling approximately 90 minutes. All tests were administered and scored by bilingual examiners who had completed advanced graduate-school training in neuropsychological assessment. The NeSBHIS was designed as a battery of 10 subtests chosen to evaluate the domains of mental control (i.e., attention and concentration), language, memory, visuospatial functions, and psychomotor speed (see Pontón et al. [7,10] for a more comprehensive review). Most measures of this battery were adapted from subtests used internationally by the World Health Organization [8,11]. The majority of subtests constituting the NeSBHIS are already used extensively in some form by North American neuropsychologists working in comprehensive epilepsy centers. The NeSBHIS was administered for this study in conjunction with other neuropsychological tests. The battery is described as follows: 1. Raven Standard Progressive Matrices (RSPM) [12]: This test was used to assess the ability to perceive relationships and to reason by analogy, independent of language and education. This measure is considered one of the most widely administered measures of nonverbal reasoning and intelligence. 2. Digit Span Subtest—Escala de Inteligencia Wechsler para Adultos (EIWA) [13]: The Digit Span subtest from the EIWA was administered as a measure of attention and working memory. This subtest is identical in content to the Wechsler Adult Intelligence Scale— Revised (WAIS-R) [14] but involves different scoring parameters. 3. Digit Symbol Subtest—EIWA: This test was included as a measure of attention and processing speed. Unlike its English-language counterpart, the EIWA Digit Symbol task has six target symbols and the total number of possible responses is 110 (as compared with 93 on the WAIS-R/Wechsler Adult Intelligence Scale III) [14]. 4. Color Trails Test, Forms 1 and 2 (CTT) [15]: The CTT was administered as a measure of sustained tracking and set shifting. Both forms consist of colored circles numbered 1–25; odd numbers are pink and even numbers are yellow. On Trails 1, examinees were instructed to connect the circles in sequential order as quickly as possible. On Trails 2, examinees were asked to connect the circles in sequential order (while maintaining numerical sequence) and simultaneously alternate colors. 5. Pontón–Satz Boston Naming Test (P–S BNT) [16]: The P–S BNT is the 30-item Spanish-language equivalent of the 60-item English-language Boston Naming Test (BNT) [17] and was used as a measure of confrontation naming abilities. Culturally loaded items (e.g., ‘‘pretzel” and ‘‘beaver”) are also excluded from this measure to ensure cultural relevance and appropriateness for Spanish-speaking populations. 6. Controlled Oral Word Association Test (FAS) [18]: COWAT is a popular measure of verbal fluency that has been adapted for both English- and Spanish-speaking individuals. On this task, participants are given 1 minute to generate as many words as possible beginning with a target letter (in this case, ‘F’, ‘A’, and ‘S’).
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7. Block Design Subtest—EIWA: This subtest was given to all participants as a visuoconstruction task. Although similar in structure to the subtest from the WAIS-R, the EIWA Block Design has slightly different content and awards fewer time-dependent bonus points. 8. Rey–Osterrieth Complex Figure Test (ROCFT) [19]: The ROCFT copy condition was administered as a measure of visuospatial construction. Participants were asked to copy a complex geometric figure with numerous embedded details. The Taylor scoring system was used to evaluate the accuracy of the designs produced [20]. Figure recall was evaluated with this test after a half-hour delay. 9. WHO–UCLA Auditory Verbal Learning Test (WHO–UCLA AVLT) [11]: This is a version of an auditory list-learning paradigm that was developed for ease of translation into various languages. Participants are presented a serially presented list of 15 Spanish words and are asked to repeat as many as they can remember immediately following each presentation. Scores from the fifth and final learning trial (Trial V) and 20-minute delayed recall trial (LDFR) were all evaluated for this study.
3. Results Raw scores from the NeSBHIS were converted into z-scores using norms from an expanded sample of 297 healthy native Spanish-speaking control subjects [9]. The norms were stratified by age and education. Analysis based on country of origin revealed no differences among groups from Caribbean, Central American, or South American countries on tests from this battery. A graphic profile of mean z-scores from the entire sample of 115 subjects is presented in Fig. 1. Norms for Trial V performance on the WHO–UCLA AVLT were not available. All of the computed mean z-scores were below a level of zero, indicating that the level of performance observed in this sample of patients with various forms of epilepsy is generally lower than what is seen in healthy control subjects. The highest mean scores were obtained on measures of intellectual functioning, attention, and verbal fluency. The lowest scores were obtained on measures of mental tracking, naming, and memory. Test scores from individual subjects were considered to be in the ‘‘impaired” range if the z-score value exceeded a level of –2, which by definition represents a level of performance that is 2 SD below the mean of the normative group or the equivalent of scoring below the 2nd percentile. The percentage of subjects with epilepsy exhibiting ‘‘impaired” test scores for each measure is provided in Table 2. The results indicated that more than 40% of subjects from this sample exhibited impaired scores on measures of
Fig. 1. Profile of z-transformed test scores of 115 Spanish-speaking patients with a VEEG-verified diagnosis of epilepsy.
Table 2 Percentage of patients (N = 115) with neuropsychological test scores in the ‘‘impaired” range, as defined by scores lower than 2 SD below the normative mean. Test
‘‘Impaired” (%)
Raven Progressive Matrices EIWA Digit Span EIWA Digit Symbol Color Trails Test 1 Color Trails Test 2 Verbal Fluency (FAS) Boston Naming Test (Ponton–Satz) EIWA Block Design Rey Figure Copy Rey Figure Recall WHO–AVLT Learning Trial V WHO–AVLT Long Delay Recall
12.3 15.0 13.8 40.0 31.2 9.0 41.4 16.7 23.8 26.2 46.3 29.2
mental tracking and confrontation naming. Deficits in verbal and visual recall were observed in 29% and 26% of the subjects, respectively. Mean test scores from the LTL and RTL groups are listed in Table 3. Group differences were assessed with a series of independent ttests. All analyses were two-tailed with a criterion for statistical significance (a) set at 0.05. Results of the t-tests indicated that there were no group differences. v2 comparisons were made between the rates of ‘‘impaired” test scores observed in the LTL and RTL groups. Rates of impairment from measures of intelligence, attention, language, and visuospatial performance did not differ between the two groups. Analyses of memory scores indicated that 36% of the LTL group exhibited impairment on the delayed recall trial of the WHO–UCLA AVLT, as compared with only 17% of the RTL group. However, the difference between these rates was at only a ‘‘trend” level of significance (v2 = 2.901, P = 0.089). The rates of impairment in nonverbal memory, as measured with the ROCFT, were equal (LTL rate = 28%, RTL rate = 28%; v2 = 0.003, NS). The significance and pattern of results did not change when analyses were limited to subjects with left hemisphere language dominance verified through the Wada test. 4. Discussion Results of this study indicate that the NeSBHIS holds promise as a brief and clinically relevant battery of neuropsychological tests that can be administered to Spanish-speaking patients in their native language. Findings from this study indicate that the test battery is sensitive to identifying impairments in cognitive functioning seen commonly in patients with epilepsy, although there may be some limitations in its sensitivity in identifying deficits in patients with lateralized temporal lobe seizures. Analyses from our sample of 115 patients indicated that the lowest levels of performance were observed on measures of processing speed, naming, and memory. The pattern of findings using this test battery is similar to what has been reported in previous studies of cognitive functioning in patients with epilepsy conducted in multiple countries and languages [4,21–24]. However, in contrast to most other investigations, this study found that impairments in naming and processing speed occur more frequently than deficits in memory. Decreased scores on tests of naming and processing speed were identified in more than 40% of our sample, whereas only 30% of the subjects exhibited low scores on memory testing. The latter proportion is much lower than the 66% rate of memory impairment reported in a recent study of Spanish-speaking patients from Argentina evaluated with a different battery of tests [25]. It is possible that these findings result from the inclusion of a more heterogeneous sample of patients than what has been previously reported throughout the literature.
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Table 3 Descriptive statistics on raw scores (mean/SD) and t-test results for comparisons of neuropsychological test scores in patients with VEEG findings of focal left or right temporal lobe epilepsy.
a
Test
LTL group (N = 48)
RTL group (N = 24)
t-Statistica
Raven Progressive Matrices EIWA Digit Span EIWA Digit Symbol Color Trails Test 1 Color Trails Test 2 Verbal Fluency (FAS) Boston Naming Test (Ponton–Satz) EIWA Block Design Rey Figure Copy Rey Figure Recall WHO–AVLT Trial Five Recall WHO–AVLT Long Delay Recall
32.6 (14.1) 8.7 (2.4) 43.3 (17.5) 70.0 (28.9) 135.8 (58.4) 22.7 (10.6) 18.9 (5.4) 27.1 (10.7) 25.9 (9.0) 8.6 (7.3) 10.3 (3.0) 7.9 (3.5)
27.4 (13.3) 8.9 (3.3) 42.7 (21.2) 68.0 (41.6) 141.5 (78.5) 25.4 (10.1) 18.1 (4.5) 26.0 (9.5) 24.1 (7.5) 10.9 (7.0) 9.7 (2.7) 8.4 (2.8)
1.42 0.29 0.11 0.21 0.30 1.07 0.60 0.38 0.79 1.03 0.43 0.60
All values nonsignificant.
It is also possible that the tests developed for Spanish speakers used in this study have a different level of sensitivity than analogous measures used in English and other languages. This study failed to find any marked difference in neuropsychological test performance on group comparisons made in a smaller sample of 82 patients with EEG evidence of partial seizures localized to the left or right temporal lobes. A larger proportion of patients with LTL epilepsy (36%) than those with RTL epilepsy (17%) were found to be impaired on an auditory verbal learning paradigm, although the difference in these proportions was not statistically significant. Rates of impairment in nonverbal memory in these groups using the ROCFT were identical (28%). The pattern of these results is similar to what has been reported in other presurgical samples, where ‘‘material-specific” impairments in verbal memory in patients with LTL epilepsy are identified more readily than nonverbal memory deficits in patients with RTL epilepsy [26,27]. Furthermore, our study failed to demonstrate specific deficits in naming which have frequently been reported in patients with LTL epilepsy [26,28]. Future investigations are necessary to determine the utility of using the NesBHIS for purposes of identifying patterns of neuropsychological impairment to aid with presurgical localization and whether the addition of additional tests such as paragraph recall and/or design learning measures would enhance the sensitivity of the test battery in this context. The NesBHIS was developed in an effort to move in the direction of providing a more linguistically and culturally effective method for conducting neuropsychological assessment in samples of Spanish-speaking individuals [7]. Results from this study indicate that the battery provides an effective method for identifying cognitive impairment in patients with epilepsy, although a number of methodological factors still need to be addressed. One factor is that some of the tests used in the NesBHIS battery, including subtests from the EIWA and the verbal fluency measure (FAS), are less than optimal for contemporary use with Spanish-speaking patients. Additionally, it is also clear that the demographic characteristics of the NeSBHIS’s predominantly Mexican reference group may not be reflective of this study’s Hispanic population, residing primarily in the New York metropolitan region. Methodological limitations stemming from the use of insensitive tests and a suboptimal normative sample are likely to have affected the results of this study. As the Hispanic population residing in North America is such a heterogeneous group, extending the use of the NesBHIS to epilepsy centers in other metropolitan regions will be enhanced by obtaining local norms from healthy control subjects that come from cultural backgrounds similar to those of the Spanish-speaking patients in that geographic region or catchment area. Higher levels of diagnostic validity will likely follow the use of more appropriately matched normative groups combined with more sensitive
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