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Epilepsy & Behavior 23 (2012) 142–145

Contents lists available at SciVerse ScienceDirect

Epilepsy & Behavior


journal homepage: www.elsevier.com/locate/yebeh

Predictive value of Spanish neuropsychological testing for laterality in patients


with epilepsy
Guido Lancman a, Gonzalo A. Vazquez-Casals a, Kenneth Perrine a, b, Enrique Feoli a, Lorna Myers a,⁎
a
Northeast Regional Epilepsy Group, New York, NY, USA
b
Department of Neurological Surgery, Weill–Cornell Medical College, New York, NY, USA

a r t i c l e i n f o a b s t r a c t

Article history: In presurgical treatment planning for patients with epilepsy, neuropsychological testing assists in lateraliza-
Received 19 July 2011 tion of the seizure focus. Previous research with English speakers has shown that patients with left
Revised 25 October 2011 hemisphere (LH) onsets versus right hemisphere (RH) onsets perform worse on naming and other verbal
Accepted 3 November 2011
skills tests, but similar findings with Hispanic patients are limited. Thirty-nine Spanish-speaking patients
Available online 22 December 2011
were administered a comprehensive battery of neuropsychological tests in Spanish. LH-onset patients
Keywords:
performed significantly worse than RH-onset patients on verbal comprehension (P = 0.006), visual matching
Hispanics (P = 0.047), the Ponton–Satz Boston Naming Test (P = 0.001), and the dominant hand trial of the Grooved
Spanish Pegboard Test (P = 0.012). A stepwise regression model to predict seizure laterality from these tests was
Neuropsychology significant (F = 12.10, P = 0.001), but only the Ponton–Satz Boston Naming Test was retained. This
Lateralization comprehensive battery of neuropsychological tests in Spanish proved useful in predicting lateralization in
Epilepsy patients with partial epilepsy.
Neuropsychological Screening Battery for © 2011 Elsevier Inc. All rights reserved.
Hispanics
Batería Woodcock Muñoz
Boston Naming Test

1. Introduction This is only the second study reporting on neuropsychological


assessment of Hispanic patients with epilepsy in the United States.
Neuropsychological testing of global intellectual functioning and Barr et al. used the Neuropsychological Screening Battery for
more specific neuropsychological functional areas (e.g. attention, Hispanics (NeSBHIS) [8] and reported that it might lack sensitivity in
language, memory, visuospatial, executive, psychomotor functions) the lateralization of deficits of patients with temporal lobe seizures
is typically used to assist in the lateralization of the seizure focus in [3]. However, this contradicts a large body of literature, in English and
candidates for epilepsy surgery [1,2]. Although there is a large body other languages, that shows significant deficits in naming ability of pa-
of literature supporting the diagnostic utility of batteries developed tients with left hemisphere epilepsy [9–13]. Furthermore, Barr et al. did
for use with and administered to English-speaking North Americans, not assess global intellectual functioning, apart from Raven's Standard
information about neuropsychological testing of patients with Progressive Matrices Test, which they found loaded most heavily on
epilepsy from Hispanic backgrounds is lacking [3]. the visuospatial factor. Our study reports the use of a more comprehen-
Hispanics account for 16% of the US population and are expected to sive neuropsychological testing battery, which includes the NeSBHIS
constitute 30% by 2050 [4]. As a result, the availability of assessment (with the exception that the Pin Test is replaced by the Grooved Peg-
instruments that are culturally and linguistically appropriate becomes board Test) and the Brief Intellectual Ability (BIA) of the Batería III Prue-
extremely relevant. In the past, the neuropsychological status of bas de Habilidad Cognitiva [14]. Results were analyzed to determine its
Spanish-speaking patients was assessed with informal translations lateralizing value in Spanish-speaking patients with partial epilepsy.
of existing testing materials into Spanish, the use of interpreters, and
reliance on English-based norms. However, it is now understood 2. Material and methods
that this is not adequate. Rather, it has been pointed out that devel-
opers of tests must ensure that their assessment materials are both 2.1. Subjects
culturally and linguistically relevant for the target population [5–7].
Sixty-nine consecutive patients with epilepsy who completed
⁎ Corresponding author at: Northeast Regional Epilepsy Group, 820 Second Avenue,
neuropsychological testing in Spanish at the Northeast Regional
Unit 6C, New York, NY 10017, USA. Fax: + 1 212 661 7496. Epilepsy Group's offices between 2005 and 2010 were originally in-
E-mail address: lmyers@epilepsygroup.com (L. Myers). cluded in this study. Patients originated from South and Central

1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.yebeh.2011.11.012
G. Lancman et al. / Epilepsy & Behavior 23 (2012) 142–145 143

America, Iberia, and the Caribbean countries and spoke Spanish as second 15-word distracting list, and finally 20–25 minutes later. The
their primary language. Lateralized partial epilepsy was confirmed target words of the test are different from those used in the Rey
with prolonged inpatient video/EEG monitoring, based on ILAE Auditory–Verbal Learning Test (RAVLT) [21] and thus do not
criteria. Nonepileptic seizures were excluded by recording all typical represent a direct translation. A delayed recognition trial consisting
episodes/seizures described by the patient or relatives that failed to of 30 words, among them the 15 target words, is also given.
reveal any evidence of ictal epileptiform activity. Severe psychiatric 2.2.1.1.7. Color Trails Test, Forms 1 and 2. The Color Trails Test,
illness, dementia, and probable developmental delay were ruled out Forms 1 and 2 (CTT) [22], is a measure of sustained visual attention
by record review and testing results. Thirty-nine patients met all or tracking and set shifting. Both forms present the subject with
inclusion criteria and were considered for our final analysis. colored circles numbered 1–25; odd numbers are pink and even
numbers are yellow. On CTT1 participants are asked to connect the
2.2. Procedures circles in a sequential order as fast as possible. On CTT2 examinees
are instructed to connect the circles in sequential order while also
In 2005, the Spanish neuropsychology division of the Northeast alternating the colors.
Regional Epilepsy Group (G.A.V., L.M.) established this battery as 2.2.1.1.8. Rey–Osterrieth Complex Figure Test. The Rey–Osterrieth
standard for all Spanish-speaking patients. It should be noted that in Complex Figure Test (ROCFT) [23] copy is a measure of visuospatial
some instances, specific characteristics of the case (e.g., fatigue, construction and the delayed recall condition is a measure of visual
resistance to testing) did not permit for all tests to be administered. memory.
Participants were tested individually in one session totaling approxi- 2.2.1.1.9. Grooved Pegboard Test. The Grooved Pegboard Test (GPT)
mately 3 to 3.5 hours. All patients were tested in outpatient offices in [24] test was added as a replacement for the out-of-print Pin Test in
a distraction-free environment by psychologists licensed by the State the NeSBHIS. The GPT is a manipulative dexterity test that requires
of New York who had completed a 2-year postdoctoral fellowship in complex visual–motor coordination. Participants taking this test are
neuropsychology and who had been in full-time practice in neuropsy- asked to place key-shaped pegs into a board that has 25 multidirec-
chology for 5 or more years. Both neuropsychologists administering tional key-holes, arranged in five rows with five holes each, as fast
the batteries are native and fluent Spanish speakers. No graduate as possible. The first trial is completed with the dominant hand, and
students or trainees administered or interpreted tests. The following the second trial with the nondominant hand.
measures were used.
2.2.2. Batería III Pruebas de Habilidad Cognitiva
2.2.1. Neuropsychological Screening Battery for Hispanics The complete Batería III Pruebas de Habilidad Cognitiva [14] is
The Neuropsychological Screening Battery for Hispanics (NeSBHIS) made up of 20 subtests that are either translations or adaptations of
was developed by Ponton et al. in 1996 to address the lack of appropri- the parallel tests in the Woodcock–Johnson III [25]. The Batería III is
ate measures for the neuropsychological assessment of Hispanics in the only measure of broad cognitive abilities in existence in the
the United States [8]. It provides psychometric standardization on United States that has been standardized and normed on a represen-
tests of memory (visual and verbal), language, mental control, reason- tative adult Spanish-speaking population. The normative sample
ing, visuospatial skills, and psychomotor speed, stratified by age, gen- included 8818 randomly selected individuals from geographically
der, and education on a sample composed of 300 Spanish-speaking diverse areas within a stratified sampling design (socioeconomic,
subjects. specific community, and individual variables).
The Habilidad Intelectual Breve (Brief Intellectual Ability, BIA) of
2.2.1.1. Subtests the Batería III provides a brief measure of intelligence that consists
2.2.1.1.1. Pontón–Satz Boston Naming Test. The Pontón-Satz Boston of three tests: Comprensión Verbal (Verbal Comprehension), For-
Naming Test (P-S BNT) [15] is a 30-item Spanish version of the longer mación de Conceptos (Concept Formation), and Pareo Visual (Visual
60-item English-language Boston Naming Test [16]. Cultural appropri- Matching). The BIA was included to improve the range of our neu-
ateness and relevance for Spanish-speaking populations were secured ropsychological battery and because previous Spanish studies had
by removing items with high cultural loadings in North American cul- not obtained specific measures of intellectual functioning. Although
ture (e.g., “pretzel,” “beaver”). this is the first time this measure was used in an epilepsy popula-
2.2.1.1.2. Controlled Oral Word Association Test. The Controlled Oral tion, it has been thoroughly validated in the US Spanish-speaking
Word Association Test (COWAT) [17] is a measure of verbal fluency in population and has the potential to contribute to our understand-
which participants are given 1 minute to generate as many words as ing of cognitive function in Spanish-speaking patients with
possible beginning with a specific target letter (‘F’, ‘A’, and ‘S’ are epilepsy.
used).
2.2.1.1.3. Digit Span Subtest. The Digit Span Subtest (Escala de 2.2.2.1. Subtests
Inteligencia Wechsler para Adultos [EIWA]) [18] measures auditory 2.2.2.1.1. Verbal Comprehension. This measure is made up of four
attention and working memory, but uses different scoring criteria subtests: picture vocabulary, synonyms, antonyms, and verbal
than the English version. analogies.
2.2.1.1.4. Block Design Subtest. Although structurally similar to the 2.2.2.1.2. Concept Formation. This subtest measures nonverbal
corresponding subtest from the older Wechsler Adult Intelligence inductive reasoning by requiring the respondent to determine a rule
Scale—Revised [19], the content of the Block Design Subtest of the that distinguishes two sets of figures. On each test item the examinee
EIWA is somewhat different and fewer time-dependent bonus points is asked to verbalize the difference (i.e., color, shape, size, or number)
are awarded. between two sets of figures.
2.2.1.1.5. Digit Symbol Subtest. In contrast to the English version, 2.2.2.1.3. Visual Matching. This subtest assesses perceptual and
the EIWA Digit Symbol subtest has six target symbols and 110 visuomotor speed and involves circling identical pairs of numbers in
possible total responses with a time limit of 90 seconds. rows of six digits during a 3-minute period.
2.2.1.1.6. WHO/UCLA Auditory–Verbal Learning Test. In the WHO/
UCLA Auditory–Verbal Learning Test (WHO/UCLA AVLT) [20], exam- 2.3. Data analysis
inees are presented with a list of 15 Spanish words in a serial fashion
and then asked to repeat as many as they are able to remember im- Descriptive statistics (means and SD for continuous data, frequen-
mediately after each of five learning presentations, then after a cies for nominal data) were calculated on the demographic variables.
144 G. Lancman et al. / Epilepsy & Behavior 23 (2012) 142–145

Unpaired Student's t tests were performed on the neuropsy- 3.2. Neuropsychological testing
chological variables between the left and right hemisphere laterality
groups. Logistic regression was performed to predict seizure laterality Subjects with left hemisphere onsets had significantly lower
from the variables significant from the individual t tests. Sensitivity, scores than those with right hemisphere onsets on Visual Pairing
specificity, and positive and negative predictive values were (t = 2.07, P = 0.047) and Verbal Comprehension (t = 2.92, P = 0.006)
calculated for the variables significant from the logistic regression. from the Batería III, the P-S BNT (t = 3.48, P = 0.001) from the
P b 0.05 was considered significant. NeSBHIS, and the dominant hand trials of the Grooved Pegboard
Test (t = −2.68, P = 0.034). Results of all tests are detailed in Table 1.
Logistic regression analysis to predict laterality from the neuro-
3. Results psychological variables was performed using the variables found
significant in the individual t tests. A stepwise regression model was
3.1. Descriptive significant (F = 12.10, P = 0.001) but retained only the P-S BNT.
In predicting left hemisphere onset, the P-S BNT had a sensitivity
Thirty-nine Hispanic participants with epilepsy constituted the of 0.80 (95% CI: 0.56–0.93), specificity of 0.67 (95% CI: 0.24–0.94),
study sample after meeting inclusion criteria. There were 15 (39.5%) positive predictive value of 0.89 (95% CI: 0.64–0.98), and negative
males, the mean age was 41.7 ± 14.1 years, and the mean level of predictive value of 0.50 (95% CI: 0.17–0.83).
education was 9.4 ± 3.6 years. Seventeen participants were from
South America, 11 from Central America, 10 from the Caribbean,,
and 1 from Iberia. There were 37 right-handers (92.3%) and 2 (7.7%) 4. Discussion
left-handers; both left-handed patients had Wada-confirmed left
hemisphere dominance for language. Mean age at seizure onset was Results from the present study show that patients with a left
22.6 ± 19.4 years. Seizure onsets were exclusively temporal in 28 hemisphere focus performed significantly worse in measures of
(71.8%) subjects. Ten subjects had frontal onset and one had occipital verbal comprehension, naming ability, dominant hand dexterity,
onset. Seizure onsets identified by video/EEG were left-sided in 25 and visual scanning/visuomotor speed. The first two of these findings
subjects (64.1%) and right-sided in 14 (35.9%). are within expectation, as similar results have been reported previ-
Ten patients with right-sided onset were on antiepileptic drug ously in the literature for English speakers. For example, Loring
(AED) polytherapy, 3 were on AED monotherapy, and 1 was on no et al. found that patients with left temporal lobe epilepsy did
AED medication. The distribution included 9 on levetiracetam, 4 on significantly worse than those with right temporal lobe epilepsy in
phenytoin, 3 on carbamazepine, 3 on lamotrigine, 3 on topiramate, measures of confrontation naming (i.e., BNT, Multilevel Aphasia
2 on oxcarbazepine, 2 on zonisamide, 1 on lacosamide, and 1 on Examination Visual Naming) [9], and Busch et al. found that low
lorazepam. BNT scores, together with high FSIQ values and late age at seizure
Among the patients with left-sided onsets, 15 were on AED onset, were the best predictors of left temporal surgery [10]. This
polytherapy, 8 were on AED monotherapy, and 2 were on no AED finding also appears to hold cross-culturally. Schwarz and Pauli
medication. The distribution included 10 on levetiracetam, 8 on reported naming decline among German-speaking patients with left
oxcarbazepine, 5 on carbamazepine, 4 on topiramate, 4 on valproic temporal lobe epilepsy [11], Alessio et al. found significantly worse
acid, 3 on clonazepam, 3 on lamotrigine, 3 on phenobarbital, 3 on performance on different memory and language measures including
phenytoin, 2 on lacosamide, 2 on pregabalin, 1 on primidone, and 1 the BNT in their Brazilian subjects with left hippocampal atrophy
on zonisamide. [12], and Raspall et al. reported that their Spanish patients with left
Mean number of AEDs was 2.00 (SD 1.04) for patients with right- temporal lobe epilepsy had significantly lower scores than patients
sided onsets and 1.96 (SD 1.14) for those with left-sided onsets. This with right temporal lobe epilepsy on the BNT [13]. Barr et al., the
difference was determined not to be significant with Student's t test only similar study on Hispanics in the United States, failed to demon-
(P = 0.91). strate lateralization based on the P-S BNT or any other measure [3].

Table 1
Results of all neuropsychological tests, with unpaired Student's t tests used to compare left and right hemisphere onsets.

Test Mean (SD) Total N t statistic P value

Right-sided onset Left-sided onset

NeSBHIS
P-S BNT 19.31 (4.19) 14.48 (3.99) 38 3.48 0.001a
COWAT 21.80 (11.76) 17.53 (10.94) 29 0.98 0.338
Digit Span Subtest 7.70 (1.06) 7.17 (1.55) 34 0.99 0.329
Block Design Subtest 22.50 (10.20) 19.10 (12.00) 26 0.705 0.490
Digit Symbol Subtest 35.57 (11.36) 34.42 (14.54) 26 0.19 0.852
WHO/UCLA AVLT 5th trial 10.15 (2.67) 9.08 (2.59) 37 1.19 0.243
WHO/UCLA AVLT, short delay 7.62 (3.82) 5.88 (3.58) 37 1.38 0.176
WHO/UCLA AVLT, long delay 7.38 (4.41) 6.21 (3.18) 37 0.94 0.355
Color Trails Test 1 67.31 (36.20) 85.36 (42.80) 35 − 1.27 0.212
Color Trails Test 2 171.54 (85.38) 169.35 (84.17) 33 0.07 0.943
ROCFT 10.40 (5.48) 8.50 (4.08) 32 1.11 0.280
GPT, dominant handb 77.00 (16.87) 99.43 (29.58) 31 − 2.22 0.034a
GPT, nondominant handb 91.22 (22.48) 109.45 (31.06) 29 − 1.58 0.126
Bateria III
Verbal Comprehension 86.46 (9.59) 77.80 (8.18) 38 2.92 0.006a
Concept Formation 79.45 (12.00) 77.68 (9.37) 33 0.47 0.644
Visual Matching 80.55 (9.55) 70.24 (14.89) 32 2.07 0.047a
a
Significant.
b
The GPT is a replacement for the out-of-print Pin Test from the NeSBHIS.
G. Lancman et al. / Epilepsy & Behavior 23 (2012) 142–145 145

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