Hopkins Verbal Learning Test Revised: Norms for Elderly African Americans

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1 The Clinical Neuropsychologist /02/ $ , Vol. 16, No. 3, pp # Swets & Zeitlinger Hopkins Verbal Learning Test Revised: Norms for Elderly African Americans Melissa A. Friedman 1, John A. Schinka 1,2, James A. Mortimer 3, and Amy Borenstein Graves 4 1 James A. Haley VA Medical Center, Tampa, FL, USA, 2 Department of Psychiatry, University of South Florida, Tampa, FL, USA, 3 Institute on Aging, University of South Florida, Tampa, FL, USA, and 4 Department of Epidemiology and Biostatistics, University of South Florida, Tampa, FL, USA ABSTRACT The Hopkins Verbal Learning Test Revised (HVLT-R) is a memory test commonly used in neuropsychological evaluations, but for which there are currently no normative data for elderly African Americans. The current study examined the influence of demographic characteristics on HVLT-R performance measures in a community-dwelling sample of 237 African American older adults (60 84 years). Age, gender, and accounted for moderate amounts of variance in HVLT-R performance. Based on these results, normative tables for HVLT-R scores, stratified by age and with score adjustments for and gender, are provided. The size of the elderly population has been growing dramatically over the past several decades, with the proportion of persons over 65 years of age expected to increase from 13% of the total United States population in 1996 to 20% in Similar increases are expected across the most predominant ethnic subgroups, with the African American elderly population expected to increase from 8 to 14% (Smith, 1998) over the same time period. For this group, the shift in population statistics is especially critical, as approximately one in four elderly African Americans experiences cognitive impairment short of dementia (Unverzagt et al., 2001). The high prevalence of cognitive impairment in the context of a growing elderly population emphasizes the need for demographically appropriate norms for neuropsychological instruments. Such data will contribute to accurate detection of dementia among African Americans and help identify individuals who may be helped by treatment interventions. The Hopkins Verbal Learning Test (HVLT; Brandt, 1991) is a memory test commonly used in neuropsychological evaluations, for which there are currently no normative data on African Americans. This brief verbal learning and memory instrument is well suited for use with difficultto-test or relatively severely impaired patients. The HVLT consists of a 12-item word list presented in three consecutive trials. The word list is composed of three semantic categories with four words in each. A yes=no recognition task immediately follows the three successive learning trials. The recognition task consists of 24 words, 12 from the recall list, 6 distracters that are semantically related to the recall items, and 6 unrelated words. Six equivalent forms were created to reduce practice-related measurement error for patients who undergo serial testing. The HVLT has shown evidence of utility and convergent validity with similar measures such as the CVLT (Lacritz & Cullum, 1998a). In a sample of Address correspondence to: John A. Schinka, Ph.D., Psychology Service (116B), James A. Haley Veterans Hospital, Bruce B. Downs Blvd., Tampa, FL 33612, USA. jschinka@hsc.usf.edu Accepted for publication: August 14, 2002.

2 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 357 healthy older adults, Lacritz and Cullum (1998a) found a correlation of 0.74 between the total number of words learned across trials for both tests. In the initial research (Brandt, 1991), parallel forms of the HVLT were found to be equivalent for total learning and discrimination. Rasmusson, Xeno, Frederick, and Brandt (1995) found that over a period of 9 months HVLT performance was stable for each alternate form. Limitations of the original HVLT were its lack of delayed recall or delayed recognition trials. Benedict, Schretlen, Goninger, and Brandt (1998) revised the HVLT (HVLT-R) to address these limitations by adding a min delay between the learning trials and the delayed free recall and recognition trials. The authors argue that the HVLT-R still maintains its brevity and utility with difficult populations, while providing a more comprehensive assessment of memory. The six parallel forms have been shown to be equivalent for the learning trials, as well as free recall, percent retained, and recognition of true positives (Benedict et al., 1998; Benedict & Zgaljardic, 1998). The HVLT-R has been found to have adequate convergent validity with the CVLT across learning and recognition trials in demented patients (Lacritz & Cullum, 1998b). Although the HVLT-R has promising psychometric characteristics, to date there have been no norms published for use with elderly African Americans. Use of norms based on Caucasian individuals is associated with the risk of misdiagnosing African Americans as impaired in the absence of cognitive decline. This risk of misclassification was demonstrated in a study of several standardized measures used as screens for dementia (Fillenbaum, Heyman, Williams, Prosnitz, & Burchett, 1990). Overall, the measures, including the Mini-Mental Status Exam (Folstein, Folstein, & McHugh, 1975), produced a much greater rate of false positive dementia identifications among African Americans than Caucasians. Lower, older age, and socioeconomic factors have been associated with lower MMSE scores (Brayne & Calloway, 1990; Crum, Anthony, Bassett, & Folstein, 1993) and may partly account for the differential false positive identification rates. In their study of nondemented, elderly individuals, Manly et al. (1998) demonstrated lower neuropsychological performance in African Americans compared with Caucasians. Statistically significant differences were seen on measures of verbal abstract reasoning, category fluency, visuospatial skill, and figure memory, although the mean differences between groups were sometimes so small as to be of questionable clinical significance. The differences remained statistically significant after matching groups on years of, and could not be accounted for by occupational attainment or by cerebrovascular risk factors. In contrast to these findings, Fillenbaum, Heyman, Huber, Gunguli, and Unverzagt (2001) found that when sex, age, and were controlled, race was not a statistically significant predictor of any score on a well-known neuropsychological battery (CERAD). Additionally, these authors pointed out that normative performance of any particular group may need to take into account factors whose influence on performance may be less obvious. For instance, while years of is often a control variable in research studies, geographic location of such is rarely controlled. Elderly African Americans educated in segregated schools in the South may have received a very different quality of than their Northern counterparts with an equal number of years of. Studies of individuals diagnosed with Alzheimer s disease have yielded varying results based on race. In one study, African Americans with Alzheimer s disease obtained lower scores than Caucasians with Alzheimer s disease on measures of visual naming, construction, and MMSE scores, and the differences remained after controlling for the effects of age,, dementia severity, and disease duration (Welsh et al., 1995). In another study of individuals with Alzheimer s disease, however, no significant differences were found between African Americans and Caucasian Americans on measures of naming, picture vocabulary, verbal abstraction, verbal list learning, and pragmatic language use, after controlling for MMSE score and (Ripich, Carpenter, & Ziol, 1997). The implications of using inappropriate norms in the elderly African American population are

3 358 MELISSA A. FRIEDMAN ET AL. substantial. Use of Caucasian norms confers the risk of misdiagnosing African Americans as demented. Additionally, for African Americans who have been appropriately diagnosed with dementia, inadequate norms would cause individuals with mild to moderate advancement to be classified as severely impaired. Such individuals may be systematically excluded from new drug investigations, which tend to recruit individuals with mild to moderate impairment. Similarly, individuals misclassified as having severe impairment may not be considered for treatment with existing drugs, because of the belief that their disease is too advanced for them to benefit from the drug (Shadlen, Larson, Gibbons, McCormick, & Teri, 1999). The purpose of the present study was to evaluate the effects of age, and gender in a representative sample of African American older adults, and based on the results of these analyses, to provide normative data for this minority group of community-dwelling elderly. METHOD Participants Data for the present study were obtained from the Hillsborough Elder African American Life Study (HEALS). HEALS is a representative, populationbased, cross-sectional study of 255 African American individuals, aged 60 84, living in Tampa, Florida. Information was obtained by structured interviews with participants addressing demographic variables, personal and family medical history, smoking and alcohol consumption, depression, anxiety, social support, work history, physical and mental exercise, and risk factors for dementia. Participants also received a battery of cognitive ability measures that included the HVLT-R. More complete information on HEALS participant selection and data collection procedures is provided in Schinka, Belanger, Mortimer, and Graves (in press). Procedures Form 1 of the HVLT-R was administered in the standard fashion as part of a larger battery of tests. The following indices were scored: Trial 1, Trial 2, Trial 3, Learning, Sum of Trials 1 to 3, Delayed Recall, Delayed Cued Recall, Percent Retained, Recognition True Positives, Recognition False Positives, and Discrimination Index. The Delayed Cued Recall score is a new score not previously reported. Following delayed free recall subjects were given memory cues and asked, one subcategory at a time, to recall all words on the list that were from the subcategories: (1) places to live, (2) four-legged animals, and (3) precious stones. The Learning measure is calculated as the higher of Trial 2 or Trial 3 recall, minus Trial 1 recall. The Percent Retained score is the Delayed Recall score divided by the better of Trail 2 or Trial 3 recall, multiplied by 100. The Discrimination Index is calculated as the Recognition True Positives minus False Positives. RESULTS Exploratory data analyses were conducted to examine distributions of scores for the HVLT-R and to identify cases with missing or inconsistent demographic data. Of the 255 participants, two individuals were eliminated due to missing demographic data. Cases were also excluded if they reported a history of any of the following: endarterectomy, transient ischemic attacks, cerebrovascular accidents, Parkinson s disease, or traumatic head injury with loss of consciousness and retrograde amnesia. A total of 15 cases were dropped for meeting one or more of these criteria. One participant was excluded due to refusal to complete Trial 3 of the HVLT-R. Participant data were not screened for history of psychiatric disorder. The final data set available for analysis consisted of 237 individuals, 108 men and 129 women. There was a distinct bimodal distribution of age, and participants were divided into two age groups consistent with the bimodal distribution. Age Group 1 consisted of 111 individuals, years of age, and Age Group 2 consisted of 126 individuals years of age. These two groups were found to differ significantly on HVLT-R measures (p <.01 for each comparison) with effect sizes exceeding.40. For descriptive purposes, patients were also grouped by al attainment, with groups defined by whether they completed fewer than 12 years of (n ¼ 173), 12 years of (n ¼ 42), or more than 12 years of (n ¼ 22). Table 1 provides descriptive statistics on the ages of individuals by age, gender and categories. We used multiple linear regression to examine the effects of gender, age, and on

4 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 359 Table 1. Mean Age and Education by Age, Gender, and Education Categories. Age Group Gender Years of Mean Age (SD) Mean N Education Education (SD) Males < (2.93) 9.73 (0.80) (2.82) ( ) 11 > (1.60) (1.51) 6 Total (2.77) (2.29) 54 Females < (3.61) 9.37 (1.22) (1.93) ( ) 16 > (3.16) (1.79) 11 Total (3.33) (2.48) 57 Total < (3.23) 9.57 (1.02) (2.53) ( ) 27 > (2.77) (1.78) 17 Total (3.08) (2.38) Male < (2.12) 7.25 (2.22) (2.63) ( ) 4 > (.) ( ) 1 Total (2.24) 7.78 (2.84) 54 Female < (2.71) 8.25 (1.87) (3.04) ( ) 11 > (3.10) (1.92) 4 Total (2.81) 9.22 (2.67) 72 Total < (2.45) 7.77 (2.09) (2.89) ( ) 15 > (4.39) (2.00) 5 Total (2.58) 8.60 (2.82) 126 HVLT-R scores, separately by age group. All of the HVLT-R measures were examined separately: Trials 1, Trial 2, and Trail 3, Sum of Trials 1 to 3, Learning, Delayed Free Recall, Delayed Cued Recall, Percent Retained, True Positives, False Positives, and Discrimination Index. We ran two sets of linear regression analyses for each age group. The first set of analyses examined whether age, gender, and, entered simultaneously into a regression model, were predictive of any of the HVLT-R measures. The second set of analyses examined whether the interaction of gender and was predictive of any HVLT-R measures. These regression analyses revealed that gender and, but not age, accounted for a statistically significant (p <.01) proportion of the variance in performance across multiple HVLT-R measures. Given these results, we produced gender and corrections for normative distributions for each of the two age groups on the HVLT-R measures. Means and standard deviations for each measure by and gender category are provided for each age group in Appendix A. For norming purposes, data from all three categories and both gender categories were combined to obtain frequency distributions of scores and standardized levels of performance, for each HVLT-R measure, for each age group (Tables 2 and 3). To account for the influence of and gender on HVLT-R scores within each age group, Table 4 provides gender and adjustments, for each age category. The adjustments were calculated by stratifying participants by group and gender within each age category. The mean of each stratified subgroup was then subtracted from the mean of all individuals in that age category, for each measure. The

5 360 MELISSA A. FRIEDMAN ET AL. resulting values can be used to adjust a given raw score for the effects of and gender, prior to obtaining the standardized level of performance associated with the score. In order to obtain gender- and - based percentile scores, first obtain the appropriate adjustment value from Table 4, based on the individual s age category,, and gender. After applying the adjustment value to the raw score, the adjusted score may be looked up in Table 2 or 3, depending on the individual s age category, in order to obtain the standardized level of performance associated with the adjusted score. Table 2. Normative Data for HVLT-R Performance for Individuals Years of Age. Cumulative Percentile Raw score Trial 1 Trial 2 Trial 3 Learning Sum (1 3) Delayed Recall Cued Recall True Positive False Discrimination % Retained Positive Percentile < <5 < < <2 <1 < < <2 <15 % Retained

6 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 361 Table 2. (continued). Cumulative Percentile Raw score Trial 1 Trial 2 Trial 3 Learning Sum (1 3) Delayed Recall Cued Recall True Positive False Discrimination % Retained Positive Percentile <3 Mean SD Range Related false positives only. In our sample, there was only one unrelated false positive response across groups. Also, reverse scored, for example, more False Positives is an indication of poor performance. Table 3. Normative Data for HVLT-R Performance for Individuals Years of Age. Cumulative Percentiles Raw score Trial 1 Trial 2 Trial 3 Learning Sum (1 3) Delayed Recall Cued Recall True Positive False Discrimination % Retained Positive Percentile < < < < < <1 20 <1 0 <2 2 < <1

7 362 MELISSA A. FRIEDMAN ET AL. Table 3. (continued). Cumulative Percentiles Raw score Trial 1 Trial 2 Trial 3 Learning Sum (1 3) Delayed Recall Cued Recall True Positive False Positive Discrimination % Retained Percentile % Retained <1 Mean SD Range Related false positives only. In our sample there was only one unrelated false positive response across groups. Also, reverse scored, for example, more False Positives is an indication of poor performance. Table 4. Education and Gender Adjustments to HVLT-R Raw Scores to Estimate Education and Gender-Based Level of Performance. HVLT-R Years of years old years old index Male Female Male Female Trial 1 < > Trial 2 < > Trial 3 < > Learning < >

8 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 363 Table 4. (continued). HVLT-R Years of years old years old index Male Female Male Female Sum of 1 3 < > Delayed Recall < > Cued Recall < > Percent Retained < > True Positives < > False Positives < > Discrimination Index < > Note. The values in the above table can be added to or subtracted from a raw score prior to looking up level of performance information in Tables 2 and 3. This would result in an - and gender-adjusted score. Correction provided applies only to the Related False Positive score. DISCUSSION Our analyses showed that age had a moderately large effect on HVLT-R performance, and we divided the sample into two age groups based on the characteristics of the HVLT-R score distributions. We also found that, and gender have significant, moderate-sized effects on HVLT-R performance. In contrast to Vanderploeg et al. (2001), who found that level of previously attained did not affect HVLT-R performance in a predominantly white community dwelling sample, did affect level of performance in this African American sample. Based on the results of these analyses, we provided - and gender-adjusted normative data for two age groups of elderly African Americans in the age range of 60 to 84. The availability of these normative data would hopefully benefit epidemiologic studies, public health initiatives, and recruitment of subjects for clinical drug trials for disorders affecting cognition, as well as facilitate the provision of timely and appropriate treatment for African Americans who suffer from disorders such as Alzheimer s disease. There are several limitations to the present study. First, the number of participants with greater than 12 years of was very small, which may affect the reliability, as well as the generalizability of the normative values for this group. Because this group s mean performance was much higher than both other groups on many measures, it could not be combined with the group of individuals with 12 years of. Second, only Form 1 of the HVLT-R

9 364 MELISSA A. FRIEDMAN ET AL. was used. Although previous studies have demonstrated the equivalence of forms (Benedict et al., 1998; Benedict & Zgaljardic, 1998), it is not known whether and gender effects would be comparable across forms. Third, the version of the HVLT-R used in this study has a cued recall trial between the Delayed Free Recall and Delayed Recognition trials. The addition of this cued recall trial may influence performance on the recognition measure. Therefore, recognition trial data with this version of the HVLT-R may not be comparable with previously published recognition trial data. Finally, cultural and al factors affecting performance in this group of African Americans from Hillsborough County, Florida may not generalize to all African American individuals. Research findings (Fillenbaum, et al., 2001), as well as psychometric principles, point to the need to consider the limits of the generalizability of these findings to African American individuals of different geographic locales and origins. Nevertheless, it is well established that culturally appropriate norms represent an important component of interpretation of neuropsychological instruments (Ardila, 1995). In the absence of published norms on HVLT-R for African Americans, the current data contribute to the provision of appropriate norms for this minority group. ACKNOWLEDGEMENTS The Hillsborough Elder African American Life Study was conducted by a team of faculty at the University of South Florida, working with people from the community of Tampa, Florida. The study was funded by the National Alzheimer s Association. Preparation of this article was also supported in part by the Department of Veterans Affairs. REFERENCES Ardila, A. (1995). Directions of research in crosscultural neuropsychology. Journal of Clinical and Experimental Neuropsychology, 17, Benedict, R.H.B., Schretlen, D., Goninger, L., & Brandt, J. (1998). Hopkins Verbal Learning Test Revised: Normative data and analysis of inter-form and test-retest reliability. The Clinical Neuropsychologist, 12, Benedict, R.H.B., & Zgaljardic, D.J. (1998). Practice effects during repeated administrations of memory tests with and without alternate forms. Journal of Clinical and Experimental Neuropsychology, 20, Brandt, J. (1991). The Hopkins Verbal Learning Test: Development of a new memory test with six equivalent forms. The Clinical Neuropsychologist, 5, Brayne, C., & Calloway, P. (1990). The association of and socioeconomic status with the Mini- Mental State Examination and the clinical diagnosis of dementia in elderly people. Age & Aging, 19, Crum, R.M., Anthony, J.C., Bassett, S.S., & Folstein, M.F. (1993). Population-based norms for the Mini- Mental State Examination by age and al level. JAMA, 269, Fillenbaum, G.G., Heyman, A., Huber, M.S., Gunguli, M., & Unverzagt, F.W. (2001). Performance of elderly African American and White community residents on the CERAD neuropsychological battery. Journal of the International Neuropsychological Society, 7, Fillenbaum,G.,Heyman,A.,Williams,K.,Prosnitz,B.,& Burchett, B. (1990). Sensitivity and specificity of standardized screens of cognitive impairment and dementia among elderly black and white community residents. Journal of Clinical Epidemiology, 43, Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-Mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, Lacritz, L.H., & Cullum, C.M. (1998a). The Hopkins Verbal Learning Test and CVLT: A preliminary comparison. Archives of Clinical Neuropsychology, 13, Lacritz, L.H., & Cullum, C.M. (1998b, August). Utility of the Hopkins Verbal Learning Test Revised in Alzheimer s disease. Paper presented at the American Psychological Association conference, San Francisco, CA. Manly, J.J., Jacobs, D.M., Sano, M., Bell, K., Merchant, C.A., Small, S.A., & Stern, Y. (1998). Cognitive test performance among nondemented elderly African Americans and Whites. Neurology, 50, Murden, R.A., McRae, T.D., Kaner, S., & Bucknam, M.E. (1991). Mini-Mental state exam scores vary with in blacks and whites. Journal of the American Geriatrics Society, 39, Rasmusson, D., Xeno, B., Frederick, W., & Brandt, J. (1995). Stability of performance on the Hopkins Verbal Learning Test. Archives of Clinical Neuropsychology, 10,

10 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 365 Ripich, D.N., Carpenter, B., & Ziol, E. (1997). Comparison of African American and White persons with Alzheimer s disease on language measures. Neurology, 48, Schinka, J.A., Belanger, H., Mortimer, J.A., & Graves, A.B. (in press). Effects of the use of alcohol and cigarettes on cognition in elderly, African American adults. Journal of the International Neuropsychology Society. Shadlen, M.F., Larson, E.B., Gibbons, L., McCormick, W.C., & Teri, L. (1999). Alzheimer s disease symptom severity in Blacks and Whites. Journal of the American Geriatrics Society, 47(4). Smith, D.I., in U. S. Department of Commerce, Bureau of the Census. (1998). Population profile of the Unites States: Current population reports, (Series P23-194). Washington, DC: U. S. Government Printing Office. Unverzagt, F.W., Gao, S., Baiyewu, O., Ogunniyi, A.O., Gueje, O., Perkins, A., Emsley, C.L., Dickens, J., Evans, R., Musick, B., Hall, K.S., Hui, S.L., & Hendrie, H.C. (2001). Prevalence of cognitive impairment. Data from the Indianapolis Study of Health and Aging. Neurology, 57, Vanderploeg, R.D., Schinka, J.A., Jones, T., Small, B.J., Graves, A.B., & Mortimer, J.A. (2001). Elderly norms for the Hopkins Verbal Learning Test Revised. The Clinical Neuropsychologist, 14, Vanderploeg, R.D., & Schinka, J.A. (1995). Predicting WAIS-R IQ premorbid ability: Combining subtest performance and demographic variable predictors. Archives of Clinical Neuropsychology, 10, Welsh, K.A., Fillenbaum, G., Wilkinson, W., Heyman, A., Mohs, R.C., Stern, Y., Harrell, L., Edland, S.D., & Beekly, D. (1995). Neuropsychological test performance in African American and White patients with Alzheimer s disease. Neurology, 45,

11 366 MELISSA A. FRIEDMAN ET AL. APPENDIX Table A1. Performance on HVLT-R Measures by Gender and Education Categories for Year-Old Individuals. Measure Gender Years of M SD N Trial 1 Male < < Total Female < > Total Total < > Total Trial 2 Male < > Total Female < > Total Total < > Total Trial 3 Male < > Total Female < > Total Total < > Total Learning Male < > Total

12 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 367 Table A1. (continued). Measure Gender Years of M SD N Female < > Total Total < > Total Sum (1 3) Male < > Total Female < > Total Total < > Total Delayed Recall Male < > Total Female < > Total Total < > Total Cued Recall Male < > Total Female < > Total Total < > Total

13 368 MELISSA A. FRIEDMAN ET AL. Table A1. (continued). Measure Gender Years of M SD N % Retained Male < > Total Female < > Total Total < > True Positive Male < > Total Female < > Total Total < > Total False Positive Male < > Total Female < > Total Total < > Total Discrimination Male < > Total Female < > Total

14 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 369 Table A1. (continued). Measure Gender Years of M SD N Total < > Total Related false positives only. In our sample, there was only one unrelated false positive response across groups. Also, reverse scored, for example, more False Positives is an indication of poor performance. Table A2. Performance on HVLT-R Measures by Gender and Education Categories for Year-Old Individuals. Measure Gender Years of M SD N edcation Trial 1 Male < > Total Female < > Total Total < > Total Trial 2 Male < > Total Female < > Total Total < > Total Trial 3 Male < > Total

15 370 MELISSA A. FRIEDMAN ET AL. Table A2. (continued). Measure Gender Years of M SD N Female < > Total Total < > Total Learning Male < > Total Female < > Total Total < > Total Sum 1 3 Male < > Total Female < > Total Total < > Total Delayed Recall Male < > Total Female < > Total Total < > Total

16 ELDERLY AFRICAN AMERICAN NORMS FOR THE HVLT-R 371 Table A2. (continued). Measure Gender Years of M SD N Cued Recall Male < > Total Female < > Total Total < > Total % Retained Male < > Total Female < > Total Total < > Total True Positive Male < > Total Female < > Total Total < > Total False Positive Male < > Total Female < > Total

17 372 MELISSA A. FRIEDMAN ET AL. Table A2. (continued). Measure Gender Years of M SD N Total < > Total Discrimination Male < > Total Female < > Total Total < > Total Related False Positives only. In our sample, there was only one unrelated false positive response across groups. Also, reverse scored, for example, more False Positives is an indication of poor performance.