Performance discrepancies on the California Verbal Learning Test Second Edition (CVLT-II) after traumatic brain injury

Archives of Clinical Neuropsychology 23 (2008) 113 118 Brief report Performance discrepancies on the California Verbal Learning Test Second Edition (CVLT-II) after traumatic brain injury Monica L. Jacobs, Jacobus Donders Mary Free Bed Rehabilitation Hospital, Grand Rapids, MI, USA Accepted 14 September 2007 Abstract One hundred fourteen patients with traumatic brain injury (TBI), selected from a 5-year series of consecutive rehabilitation referrals, completed the California Verbal Learning Test Second Edition (CVLT-II) within 1 year after injury. Various performance contrasts (i.e., proactive interference, retroactive interference, rapid forgetting, and retrieval problems) were evaluated. Initial analyses revealed higher rates of rapid forgetting in the TBI group as compared to the standardization sample. Follow-up analyses between those patients with and without unusual degrees of rapid forgetting did not reveal any significant differences between these groups on demographic or neurological variables (p > 0.10 for all variables). It is concluded that performance discrepancies on the CVLT-II should never be used in isolation to determine the presence or absence of acquired cerebral or memory impairment. However, regardless of the cause, such discrepancies may still be relevant for clinical treatment recommendations. 2007 National Academy of Neuropsychology. Published by Elsevier Ltd. All rights reserved. Keywords: Learning; Memory; Traumatic brain injury The California Verbal Learning Test Second Edition (CVLT-II; Delis, Kramer, Kaplan, & Ober, 2000) is an updated version of the original California Verbal Learning Test (CVLT; Delis, Kramer, Kaplan, & Ober, 1987) that can be used to evaluate learning and memory in persons between the ages of 16 89 years. Several studies have used the CVLT-II to examine changes in learning and memory associated with clinical conditions ranging from dementia to schizophrenia (Baldo, Delis, Kramer, & Shimamura, 2002; Brooks, Weaver, & Scialfa, 2006; Delis et al., 2005; Fiszdon et al., 2006; Smith, Tivarus, Campbell, Hillier, & Beversdorf, 2006). Studies examining the usefulness of the CVLT-II in the evaluation of persons with traumatic brain injury (TBI) are also starting to appear (Donders & Nienhuis, 2007; Jacobs & Donders, 2007). The purpose of this investigation was to evaluate the degree to which adult patients with TBI demonstrate unusual performance contrasts on the CVLT-II, and whether this is related to demographic or neurological variables. The CVLT-II offers the opportunity to consider six discrepancies between various variables, which are of potential clinical utility: one for proactive interference, one for retroactive interference, two for rapid forgetting, and two for retrieval problems (Delis et al., 2000). The detrimental effect of prior learning on subsequent new learning or proactive interference (PI), concerns the difference between the number of correct words recalled on the single trial of List B as This research was supported by a grant from the Campbell Foundation. Corresponding author at: Psychology Service, Mary Free Bed Rehabilitation Hospital, 235 Wealthy S.E., Grand Rapids, MI 49503, USA. E-mail address: jacobus.donders@maryfreebed.com (J. Donders). 0887-6177/$ see front matter 2007 National Academy of Neuropsychology. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.acn.2007.09.003

114 M.L. Jacobs, J. Donders / Archives of Clinical Neuropsychology 23 (2008) 113 118 compared with the first trial of List A (A1). The detrimental effect of new learning on subsequent recall of previously learned information or retroactive interference (RI), concerns the difference between total correct words recalled on the short delay free recall trial (SDFR) compared with total correct words recalled on the fifth trial of list A (A5). Two other discrepancies are suggested for consideration of the possibility of rapid forgetting. The first (RF 1 ) involves the savings on the long delay free recall trial (LDFR) of correct words that the examinee recalled on trial A5, and the second (RF 2 ) considers the savings on LDFR of correct words that the examinee recalled on SDFR. Poor performance on LDFR as compared to either A5 or SDFR may be the result of loss of access to the originally learned information during the delay interval. Finally, the last two discrepancies consider degrees of retrieval problems. Both of these involve consideration of recognition discriminability (REC-D), a variable of overall performance on the recognition trial that takes into account both correct and incorrect responses. The first (RP 1 ) considers the difference between REC-D and LDFR, and the second (RP 2 ) contrasts REC-D with the discriminability index for LDFR (LDFR-D), a variable that considers not only the number of words correctly recalled but also intrusive errors on that trial. Better scores on REC-D, as compared with LDFR or LDFR-D, may indicate that the examinee had difficulty with the independent retrieval of information but that the material was not lost (see Delis et al., 2000 for a more detailed description of all six performance contrasts). Performance contrasts on the CVLT-II have received only limited attention in the literature, even though they may be potentially relevant for the diagnostic process or for treatment recommendations. Using the original CVLT, Vanderploeg, Crowell, and Curtiss (2001) found that, compared to a control group that was matched on age and initial performance on A5 and the sum of trials A1 A5 (thereby controlling for initial level of acquisition), patients with TBI only showed a statistically significant difference in the rate of decline in performance between A5 and SDFR, which the authors interpreted as evidence for a consolidation deficit. In order to avoid confusion when comparing studies, it should be noted that Vanderploeg and colleagues described the contrast between SDFR and A5 as an index of rate of forgetting, whereas it would be classified as retroactive interference according to the terminology in the current CVLT-II manual. Furthermore, it is not clear to which their findings would generalize because their TBI sample was overwhelmingly male (82%) and fairly well-educated (58% with at least partial college education). The performance contrast that has received the greatest degree of scrutiny is that of PI. Some studies have found that increased susceptibility to PI is linked to frontal dysfunction (Gershberg & Shimamura, 1995; McDonald, Bauer, Grande, Gilmore, & Roper, 2001; Smith, Leonard, Crane, & Milner, 1995). Yet, research with the children s version of the CVLT-II has found that although children with TBI had higher rates of PI compared to the standardization sample, frontal lesions were distinctly not associated with an increase in susceptibility to PI (Donders & Minnema, 2004). Furthermore, in the adult literature, some studies have failed to find clearly elevated levels of PI on the CVLT-II in patients with focal frontal lesions as compared to control participants (Baldo et al., 2002). Thus, the degree to which any of the six performance contrasts are truly unique in clinical patients like those with TBI, who often have difficulties with novel learning and memory (Hanks, Ricker, & Millis, 2004; Vakil, 2005), is not clear at this time. The base rates of the six performance discrepancies were not included in the CVLT-II manual. However, without knowledge of those base rates, clinicians may misinterpret apparent differences as indicative of acquired pathology. Donders (2006) examined base rates of these performance discrepancies in the CVLT-II standardization sample (n = 1087) and found that apparently large contrasts (e.g., 1S.D.) were actually fairly common. Using a criterion for unusual performance discrepancies as those occurring in less than approximately 10% of the standardization sample, potentially clinically significant values for the specific contrasts were defined (in z score units) as PI 1.5, RI 1, RF 1 1, RF 2 1, RP 1 1.5, and RP 2 1.5. It should be realized that occurrences of any of these six unusually large performance discrepancies were not mutually exclusive. In fact, about one third of the CVLT-II standardization sample had at least one of the six contrasts in the unusual range. In the current study, we examined whether or not patients with TBI demonstrate such unusually large performance contrasts on the CVLT-II to a statistically significant degree more than persons in the standardization sample. We also planned to investigate with those performance contrast for which such potentially meaningful differences were found, the degree to which they were related to demographic (e.g., education) and/or neurological variables (e.g., length of coma). Based on the extant literature (Donders & Minnema, 2004; Vanderploeg et al., 2001), it was hypothesized that there would be elevated rates of proactive and retroactive interference in patients with TBI, as compared to the standardization sample, but that there was no clear theoretical reason to anticipate unusual degrees of rapid forgetting or retrieval problems.

M.L. Jacobs, J. Donders / Archives of Clinical Neuropsychology 23 (2008) 113 118 115 Table 1 Demographic and injury characteristics of 114 patients with traumatic brain injury Variable n % Gender Male 63 55.26 Female 51 44.74 Ethnicity Caucasian 101 88.60 African American 9 7.90 Other 4 3.51 Injury circumstances Motor vehicle accident 82 71.93 Falls or recreation 20 17.54 Other 12 10.52 Neuroimaging a Diffuse lesion 18 15.79 Anterior focal lesion 40 35.09 Posterior focal lesion 18 15.79 Left focal lesion 35 30.70 Right focal lesion 27 23.68 Adult characteristic M S.D. Age (years) 38.24 17.93 Education (years) 12.90 2.43 Time since injury (days) 128.91 82.49 Length of coma (days) 1.30 2.95 a Categories are not mutually exclusive. 1. Method Following institutional review board approval, 114 participants were selected from a 5-year consecutive series of referrals to a Midwestern rehabilitation center, on the basis of the following criteria: (1) diagnosis of TBI through an external force to the head with associated alteration of consciousness, (2) age between 16 and 79 years at the time of psychometric assessment, (3) evaluation with the CVLT-II within 1 year after injury, (4) absence of a premorbid history of special education, substance abuse, or neurological or psychiatric illness, (5) performance in the valid range (i.e., score of at least 15/16) on the CVLT-II Forced Choice Recognition trial, a measure of effort and motivation (Moore & Donders, 2004), and (6) not currently involved in disputed financial compensation-seeking. Only initial evaluations were used in this study. During the course of this investigation, the CVLT-II was routinely included in neuropsychological assessments of patients with TBI at the facility where this research was completed, except under circumstances that would have invalidated the test results (e.g., not fluent in English). Characteristics of the final sample are presented in Table 1. Diffuse lesions on CT or MRI scan involved widespread involvement such as edema or axonal shearing. Focal lesions included discrete, localized abnormalities such as contusion or hematoma. Length of coma was defined as the number of days until the patient responded to verbal commands. Based on a combination of the worst score on the Glasgow Coma Scale (GCS) within the first 24 h and the results from acute care neuroimaging, severity of injury of 61 patients could be classified as mild (GCS 13 15 and negative CT/MRI scan; 54% of the sample), 11 as complicated mild (GCS 13 15 and positive CT/MRI scan; 10%), 13 as moderate (GCS 9 12; 11%), and 29 as severe (GCS 3 8; 25%). Forty-seven patients (41% of the sample) had been evaluated within 3 months after injury, 41 within 3 6 months (36%), 16 within 6 9 months (14%), and 10 within 9 12 months (9%). The majority (88%) of these participants had also been included in a previous study of the criterion validity of the CVLT-II (Jacobs & Donders, 2007) but performance discrepancies had not been addressed in that investigation. The CVLT-II was administered according to standardized procedures to the patients as part of a comprehensive neuropsychological evaluation. Almost all of them had been assessed as outpatients, when they were medically stable and could recall meaningful information from day to day. Patients 18 years and older provided informed consent, and

116 M.L. Jacobs, J. Donders / Archives of Clinical Neuropsychology 23 (2008) 113 118 participants under the age of 18 assented with the consent of their parents. CVLT-II raw scores were converted to ageand gender-corrected z (M = 0, S.D. = 1) and T (M = 50, S.D. = 10) scores, using commercially available software (Delis & Fridlund, 2000). The following CVLT-II variables (in z scores) were included in this investigation: total words correctly recalled on A1, total words correctly recalled on A5, total words correctly recalled on SDFR of List A, total words correctly recalled on LDFR of List A, balance of correct and incorrect words on LDFR-D, and balance of correct and incorrect words on REC-D. Higher z scores reflect better performance on all of these variables. Performance discrepancies were then calculated by subtracting the respective scores from each other, according to the following formulas: Proactive interference index (PI) = B A1; retroactive interference index (RI) = SDFR A5; first rapid forgetting index (RF 1 ) = LDFR A5; second rapid forgetting index (RF 2 ) = LDFR SDFR; first retrieval problem index (RP 1 ) = REC-D LDFR; and second retrieval problem index (RP 2 ) = REC-D LDFR-D. On the basis of research with the standardization sample (Donders, 2006), each CVLT-II contrast was considered unusual if it met the following criteria: PI 1.5, RI 1, RF 1 1, RF 2 1, RP 1 1.5, and RP 2 1.5. Differences between the current clinical sample and the standardization sample in relative prevalences of such unusual performance contrasts were evaluated with a z test for proportions. 2. Results and discussion The average performances of the complete clinical sample on the seven CVLT-II variables of interest, along with the six performance contrasts, are presented in Table 2. Inspection of this table suggests that the patients with TBI performed, on average, about 1/3 to 3/4 of a S.D. below the normative mean on these CVLT-II variables, with the performance contrasts averaging less than 1/4 S.D. However, group means may obscure patterns of individual differences, and our interest was primarily in the proportions of participants with unusually large performance contrasts. In the complete sample, there were 10 patients (8.77%) who had PI effects 1.5; 14 patients (12.28%) who had RI effects 1; 24 patients (21.05%) who had RF 1 effects 1; 15 patients (13.16%) who had RF 2 effects 1; 5 patients (4.38%) who had RP 1 effects 1.5; and 3 patients (2.63%) who had RP 2 effects 1.5. Only for the RF 1 contrast was the difference with the respective prevalence in the CVLT-II standardization sample statistically significant (z = 2.22, p < 0.013; p > 0.10 for all other comparisons). Since only the first rapid forgetting index appeared to be more common in this group of patients with TBI than in the normative sample, we focused the subsequent analyses on comparisons of the group of patients with (n = 24) versus without (n = 90) unusually large RF 1 effects. Fig. 1 displays their respective CVLT-II performances. Inspection of this figure suggests that, despite comparable performance on A5, the group with the large RF 1 effect did more than a standard deviation worse than the other group on LDFR. Table 2 CVLT-II performance of 114 patients with traumatic brain injury Variable M S.D. List A1 a 0.74 1.11 List A5 a 0.48 1.16 List B a 0.53 0.83 SDFR a 0.43 1.11 LDFR a 0.54 1.17 LDFR-D a 0.39 1.16 REC-D a 0.43 1.19 PI (B A1) b 0.21 1.12 RI (SDFR A5) b 0.05 0.78 RF 1 (LDFR A5) b 0.06 0.83 RF 2 (LDFR SDFR) b 0.11 0.58 RP 1 (REC-D LDFR) b 0.11 0.76 RP 2 (REC-D LDFR-D) b 0.04 0.80 a z Score. b Difference between two component z scores.

M.L. Jacobs, J. Donders / Archives of Clinical Neuropsychology 23 (2008) 113 118 117 Fig. 1. Performance of patients with (RF 1 1; n = 24) and without (RF 1 > 1; n = 90) unusually large degrees of rapid forgetting on the California Verbal Learning Test Second Edition. There were no statistically significant differences between these two groups in terms of gender, ethnicity, age, education, time since injury, neuroimaging findings, or coma (p > 0.10 for all variables). Overall performance on the CVLT-II, as reflected in the composite T score, was also not statistically significant between the groups with (M = 48.08, S.D. = 7.35) and without (M = 46.37, S.D. = 11.84) unusually large RF 1 effects, (F(1, 112) = 0.46, p > 0.51), suggesting that the RF 1 findings could not be attributed to differences in acquisition of List A. CVLT-II indexes of learning style such as semantic clustering, slope, recall consistency, and intrusive errors, also did not reveal any statistically significant group differences (p > 0.10 for all variables). The fact that, contrary to our initial expectation, we did not find evidence for elevated prevalences of unusually large PI or RI effects suggests that when specific actuarial criteria are applied, patients with TBI show about the same distributions of performance contrasts as found in the standardization sample. The elevated proportion of unusually large RF 1 contrasts was an unexpected finding. The absence of any statistically significant differences between the groups with v without unusually large RF 1 effects raised the possibility that this may have been a chance finding, related to the fact that we made six independent comparisons with the standardization sample. In fact, when we applied a Stepdown Bonferroni procedure to balance the risk of Type I and Type II errors, the difference between the clinical and standardization samples in terms of relative prevalences of RF 1 effects 1 became a statistically non-significant trend (p > 0.062). Our findings differ somewhat from those of Vanderploeg et al. (2001) in that we did not find any performance discrepancies that were truly unique to TBI. This is likely due to the fact that we used more specific, empirically established criteria for the definition of the various contrasts (Donders, 2006). We conclude that the mere presence of a seemingly unusual performance discrepancy on the CVLT-II does not necessarily indicate that the discrepancy is due to acquired neurological dysfunction. At the same time, the presence of a sufficiently large performance discrepancy can still be potentially clinically useful in terms of rehabilitation recommendations. For instance, someone with a high degree of proactive (PI 1.5) or retroactive (RI 1) interference may be capable of learning new information, but might be advised to space different tasks sufficiently apart and to not switch rapidly between tasks. On the other hand, persons who exhibit rapid forgetting (RF 1 or RF 2 1) are unlikely to profit in the long run from multiple repetitions or cueing, but they may benefit from using compensatory strategies such a day planner or PDA. Alternatively, someone with a retrieval problem (RP 1 or RP 2 1.5) may have trouble with independent recall of information, but may be able to benefit from cues, such as multiple-choice exams as a substitute for open-ended tests. It should be noted that these interpretive guidelines are speculative at this time because we know of no large-scale empirical research establishing ecological proof that CVLT-II performance contrasts are reliably linked to such real-world phenomena. Furthermore, although various CVLT-II z scores have acceptable test retest reliability, they may still have a considerable degree of standard error (Woods, Delis, Scott, Kramer, & Holdnack, 2006). This only reinforces the need for caution with profile interpretation, with clear recognition of base rates and actuarial standards. Potential limitations of the present investigation should also be considered. The participants were recruited from a referred convenience sample at a rehabilitation hospital. This may have led to the inclusion of relatively more patients with serious neurological injuries than if they had been selected from consecutive emergency room admissions. At the same time, this also guaranteed a broad range of injury severity, which reduced the probability of unreliable findings due to restriction of range. The sample was also limited largely to Caucasian individuals from the Midwest; therefore,

118 M.L. Jacobs, J. Donders / Archives of Clinical Neuropsychology 23 (2008) 113 118 replication with a more ethnically and geographically diverse sample would be desirable. In this investigation, we made comparison to the CVLT-II standardization sample, and further studies may wish to explore comparison with a demographically matched control group with non-brain injures. With these reservations in mind, the findings from this investigation indicate that when combined with additional neuropsychological test data, patient history and behavioral observations, CVLT-II performance discrepancies may be clinically useful. However, the rates of these discrepancies in our TBI sample were generally not statistically different from those found in the standardization sample. Therefore, the presence of any seemingly large performance discrepancy on the CVLT-II should never be used in isolation to determine the presence or absence of acquired memory impairment or brain injury. References Baldo, J. V., Delis, D. C., Kramer, J. H., & Shimamura, A. P. (2002). Memory performance on the California Verbal Learning Test-II: Findings from patients with focal frontal lesions. Journal of the International Neuropsychological Society, 8, 539 546. Brooks, B. L., Weaver, L. E., & Scialfa, C. (2006). Does impaired executive functioning differentially impact verbal memory measures in older adults with suspected dementia? The Clinical Neuropsychologist, 20, 230 242. Delis, D. C., & Fridlund, A. J. (2000). CVLT-II comprehensive scoring program. San Antonio, TX: Psychological Corporation. Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (1987). California Verbal Learning Test. San Antonio, TX: Psychological Corporation. Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). California Verbal Learning Test (2nd ed.). San Antonio, TX: Psychological Corporation. Delis, D. C., Wetter, S. R., Jacobson, M. W., Peavy, G., Hamilton, J., Gongvatana, A., et al. (2005). Recall discriminability: Utility of a new CVLT-II measure in the differential diagnosis of dementia. Journal of the International Neuropsychological Society, 11, 708 715. Donders, J. (2006). Performance discrepancies on the California Verbal Learning Test Second Edition (CVLT-II) in the standardization sample. Psychological Assessment, 18, 458 463. Donders, J., & Minnema, M. T. (2004). Performance discrepancies on the California Verbal Learning Test Children s Version (CVLT C) in children with traumatic brain injury. Journal of the International Neuropsychological Society, 10, 482 488. Donders, J., & Nienhuis, J. B. (2007). Utility of California Verbal Learning Test Second Edition recall discriminability indices in the evaluation of traumatic brain injury. Journal of the International Neuropsychological Society., 13, 354 358. Fiszdon, J. M., McClough, J. F., Silverstein, S. M., Bell, M. D., Jaramillo, J. R., & Smith, T. E. (2006). Learning potential as a predictor of readiness for psychosocial rehabilitation in schizophrenia. Psychiatry Research, 30, 159 166. Gershberg, F. B., & Shimamura, A. P. (1995). Impaired use of organizational strategies in free recall following frontal lobe damage. Neuropsychologia, 33, 1305 1333. Hanks, R. A., Ricker, J. H., & Millis, S. R. (2004). Empirical evidence regarding the neuropsychological assessment of moderate and severe traumatic brain injury. In J. H. Ricker (Ed.), Differential diagnosis in adult neuropsychological assessment (pp. 218 242). New York: Springer. Jacobs, M. L., & Donders, J. (2007). Criterion validity of the California Verbal Learning Test Second Edition (CVLT-II) after traumatic brain injury. Archives of Clinical Neuropsychology, 22, 143 149. McDonald, C. R., Bauer, R. M., Grande, L., Gilmore, R., & Roper, S. (2001). The role of the frontal lobes in memory: Evidence from unilateral frontal resections for relief of intractable epilepsy. Archives of Clinical Neuropsychology, 16, 571 585. Moore, B. A., & Donders, J. (2004). Predictors of invalid neuropsychological test performance after traumatic brain injury. Brain Injury, 18, 975 984. Smith, M. L., Leonard, G., Crane, J., & Milner, B. (1995). The effects of frontal- or temporal-lobe lesions on susceptibility to interference in spatial memory. Neuropsychologia, 33, 275 285. Smith, R. M., Tivarus, M., Campbell, H. L., Hillier, A., & Beversdorf, D. Q. (2006). Apparent transient effects of recent ecstasy use on cognitive performance and extrapyramidal signs in human subjects. Cognitive and Behavioral Neurology, 19, 157 164. Vakil, E. (2005). The effect of moderate to severe traumatic brain injury (TBI) on different aspects of memory: A selective review. Journal of Clinical and Experimental Neuropsychology, 27, 977 1021. Vanderploeg, R. D., Crowell, T. A., & Curtiss, G. (2001). Verbal learning and memory deficits in traumatic brain injury: Encoding, consolidation, and retrieval. Journal of Clinical and Experimental Neuropsychology, 23, 185 195. Woods, S. P., Delis, D. C., Scott, J. C., Kramer, J. H., & Holdnack, J. A. (2006). The California Verbal Learning Test Second Edition: Test retest reliability, practice effects, and reliable change indices for the standard and alternate forms. Archives of Clinical Neuropsychology, 21, 413 420.