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Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uear20
Telephone Screening for Mild Cognitive Impairment in Hispanics Using the Alzheimer’s Questionnaire a
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Ricardo Salazar , Carlos E. Velez & Donald R. Royall
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Department of Psychiatry, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA b
Departments of Psychiatry, Medicine, Family and Community Medicine, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA c
South Texas Veterans Health Administration Geriatric Research Education and Clinical Care (GRECC), San Antonio, Texas, USA Published online: 13 Mar 2014.
To cite this article: Ricardo Salazar, Carlos E. Velez & Donald R. Royall (2014) Telephone Screening for Mild Cognitive Impairment in Hispanics Using the Alzheimer’s Questionnaire, Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process, 40:2, 129-139, DOI: 10.1080/0361073X.2014.882189 To link to this article: http://dx.doi.org/10.1080/0361073X.2014.882189
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Experimental Aging Research, 40: 129–139, 2014 Copyright © Taylor & Francis Group, LLC ISSN: 0361-073X print/1096-4657 online DOI: 10.1080/0361073X.2014.882189
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TELEPHONE SCREENING FOR MILD COGNITIVE IMPAIRMENT IN HISPANICS USING THE ALZHEIMER’S QUESTIONNAIRE Ricardo Salazar and Carlos E. Velez Department of Psychiatry, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
Donald R. Royall Departments of Psychiatry, Medicine, Family and Community Medicine, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA; and South Texas Veterans Health Administration Geriatric Research Education and Clinical Care (GRECC), San Antonio, Texas, USA Background/Study Context: There is a need for a simple and reliable screening test to detect individuals with mild cognitive impairment (MCI). The authors analyzed the relationship between performance of the Alzheimer’s Questionnaire (AQ), an informant-rated measure of dementia-related behaviors, relative to the Telephone Interview for Cognitive Status—modified (TICS-m), Memory Impairment Scale— telephone version (MIS-t), and the Telephone Executive Assessment (TEXAS) as predictors of MCI. Methods: Comparative cross-sectional design, with data collected from participants in the Texas Alzheimer’s Research and Care Consortium’s (TARCC) San Antonio site. One-hundred percent of our sample was Hispanic. The San Antonio subset of TARCC sample is highly enriched with Mexican Americans (MAs). Fifty-five percent of the interviews were Received 27 December 2012; accepted 19 March 2013. Some of these findings have been previously presented as a poster at the Annual Meeting of the American Medical Directors Association in Long-Term Care Medicine in San Antonio, Texas, March 8–11, 2012. Address correspondence to Ricardo Salazar, MD, Department of Psychiatry, The University of Texas Health Science Center at San Antonio, Division of Aging and Geriatrics, Room 718E, 7703 Floyd Curl Drive MC 7792, San Antonio, TX 78229, USA. E-mail: [email protected]
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R. Salazar et al. conducted in Spanish. Of the 184 persons enrolled, 124 were normal controls (NCs), and 60 participants had MCI. MCI status and Clinical Dementia Rating Scale Sum of Boxes (CDR-SOB) were determined through clinical consensus and performed blind to telephone assessments. Controlling for age, gender, education, and language of interview, the association between telephone measures and CDR-SOB was evaluated by multivariate regression. Results: AQ scores were not affected by education, gender, and language of interview, but subject’s age did show a positive correlation with informant AQ ratings. The AQ predicted CDR-SOB independently of the cognitive measures, adding variance above and beyond demographics. The TICS-m and the TEXAS appear to have additive value in improving the detection of cognitively impaired patients. The MIS-t failed to contribute significantly to CDR-SOB, independent of the other measures. Conclusion: The AQ may have utility as a culture-fair telephone screening for MCI. The AQ was able to modestly distinguish MCI from NCs. The TEXAS adds variance to a model of dementia severity independent of the AQ, suggesting that the latter may weakly assess that cognitive domain (executive control function). On the other hand, the AQ attenuates the MIS-t effect. This suggests a prominent AQ bias in favor of detecting memory impairment. Additional studies are required to determine if the AQ can distinguish between amnestic and dysexecutive MCI subtypes, or between MCI and Alzheimer’s disease in Hispanics.
Patients who eventually develop clinical Alzheimer’s disease (AD) pass through a transitional state that has been labeled as mild cognitive impairment (MCI) (Petersen et al., 1999). Unfortunately, many cognitive screening tests are insensitive to MCI (Kaufer et al., 2008). Moreover, MCI subtypes have been proposed based on differences in their psychometric profiles (Petersen et al., 2001; Petersen, 2004). The relationship of these subtypes to each other and to AD, as opposed to other dementing illnesses, remains unknown (Brandt et al., 2009). Other assessment issues complicate dementia screening (i.e., mobility, financial constraints). Telephone screening tools can be relatively cost-effective and clinically useful for dementia screening (Graff-Radford et al., 2006; Ferrucci et al., 1998; Van Uffelen, Chin A Paw, Klein, van Mechelen, & Hopman-Rock, 2007). On the other hand, few measures have been validated for use in Hispanic populations (Chin, Negash, & Hamilton, 2011). Some dementia rating systems, such as the Washington University Clinical Dementia Rating (CDR) (Hughes, Berg, Danziger, Coben, & Martin, 1982) and the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE) (Jorm, Scott, Cullen, & MacKinnon, 1991), incorporate information from a collateral source to assess change
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in a patient`s cognitive function and ability to conduct their accustomed daily activities. These systems do not require a baseline assessment for comparison and minimize issues such as practice effects and educational and sociocultural influences that confound interpretation of longitudinal assessments. However, both are lengthy, require interpretation by an experienced clinician, and can be costly. The Alzheimer’s Questionnaire (AQ) (Sabbagh et al., 2010) was developed to overcome these shortcomings. The AQ is a 21-item, informantbased dementia assessment designed for ease of use in a primary care setting. AQ items are divided into five domains, including Memory, Orientation, Functional Ability, Visuospatial Ability, and Language. Items are posed in a yes/no format, with the sum of “yes” items equaling the total AQ score (0–27). Six items known to be predictive of a clinical AD diagnosis (Malek-Ahmadi, Davis, Belden, Jacobson, & Sabbagh, 2012) are weighted more heavily in the total score by being worth two points rather than one. The AQ has been translated into Spanish for use in the Texas Alzheimer’s Research and Care Consortium (TARCC). The AQ can also be administered by telephone. The purpose of our study was to analyze the ability of the AQ to explain variance in dementia severity in relation to other telephone-administered cognitive assessments, i.e., the Telephone Interview of Cognitive Status—modified (TICS-m) (Brandt, Spencer, & Folstein, 1988; Knopman et al., 2010), the Memory Impairment Screen— telephone (MIS-t; a test of semantic memory) (Lipton et al., 2003), and the Telephone Executive Assessment Scale (TEXAS); a test of executive functions derived from five items of the Executive Interview (EXIT25) (Royall, Mahurin, & Gray, 1992), among Hispanic TARCC participants with MCI and controls. METHODS Study Population The University of Texas Health Science Center at San Antonio institutional review board approved this project. All individuals discussed the study with trained research staff and provided written informed consent. The current sample comprised 184 English- and Spanish-speaking Hispanic participants in a longitudinal and observational cohort study on Alzheimer’s disease, the Texas Alzheimer’s Research Consortium and Care (TARCC) study. Details on TARCC methods are available elsewhere (Waring et al., 2008). These data include only participants at The University of Texas Health Science Center at San Antonio site.
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Evaluations were conducted in either English or Spanish, on the basis of the participant’s opinion of which language would yield the best performance. Examiners available were balanced bilinguals for participants that choose Spanish as their preferred language.
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Consensus Diagnosis TARCC clinical diagnoses were adjudicated by consensus review. This followed an in-person clinical interview and neurological examination by a geriatric psychiatrist specializing in cognitive disorders and/or a geriatrician with expertise in dementias, and the administration of a battery of standardized neuropsychological tests by a psychometrician. After each clinical assessment, a group of two geriatric psychiatrists and a senior research associate with experience in normative testing reviewed the medical, functional, neurological, psychiatric, and neuropsychological data blinded to any of the telephone-based assessments data, including the AQ, reaching a consensus diagnosis based on the presence or absence of dementia using criteria from the Diagnostic and Statistical Manual of Mental Disorders (Fourth Edition, Text Revision; American Psychiatric Association, 2000), as well as diagnosis of MCI and normal controls using strict inclusion and exclusion criteria (Waring et al., 2008). Telephone Screening Interview The subject and/or his informant were asked whether the subject would like to complete the interview during the initial recruitment call. If the participant became fatigued during the actual interview, an additional phone call(s) to complete the interview was scheduled at a time convenient to the subject and/or informant to minimize poor effort bias. During the interview, cognitive function was assessed using the Telephone Interview for Cognitive Status—modified (TICS-m), the Telephone Memory Impairment Screen—telephone (MIS-t), and the TEXAS, the telephone version of the Executive Interview (EXIT25), a measure of executive function (Royall et al., 1992). Failing the screen was defined by any one or more of the following scores: TICS-m (scores below 28), MIS-t (scores below 4), and TEXAS (scores above 3). The MIS-t and the TICS-m was administered and scored in accordance with published procedures described elsewhere (Lipton et al., 2003; Brandt & Folstein, 2003). The TEXAS consists of five items of the original EXIT25 and includes the “Number-Letter Task,” “Word Fluency,” “Memory/Distraction Task,” “Serial Order Reversal Task,” and “Anomalous Sentence Repetition” items. The total score for the TEXAS
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instrument ranges from 0 to 10, with higher scores corresponding to greater impairment. The TEXAS Cronbach’s α = .74. Based on previous work (Sabbagh et al., 2010), AQ scores corresponding to three levels of cognitive function have been defined: ≤4: normal; 5–14: mildly impaired, suggestive of MCI; ≥15: demented. A recent pilot study indicated that the AQ is a brief, sensitive measure for detecting both MCI and AD (Sabbagh et al., 2010). More recently, the AQ has been validated for its diagnostic accuracy, with high sensitivity and specificity for detecting MCI, 89% and 91%, respectively, as well as AD, with 99% sensitivity and 96% specificity. Area under the curve (AUC) values also indicated high diagnostic accuracy for both MCI and AD, at 0.95 and 0.99, respectively. Internal consistency of AQ was also high (Cronbach’s α = .89) (Malek-Ahmadi et al., 2012). In addition to assessing mental function, information about a participant’s family history of problems with memory, Parkinson’s disease, heart attack, and stroke among parents and siblings was obtained. Other variables collected from participants included general health status, history of visual hallucinations, falls, and loss of consciousness during the previous year; cardiovascular risk factors; depressive symptoms; frailty status; ability to perform activities of daily living; and education level. Information about the socioeconomic status of the neighborhood in which participants live was obtained by linking census data to participants’ zip codes. Statistical Analysis We used CDR-SOB, a continuous measure of dementia severity (see Table 1), as a dependent variable in a set of nested multivariate regression models. Demographic covariates, age, gender, education in years, and language of interview, were entered first, followed by the AQ and cognitive performance measures. All analyses were conducted in STATISTICA version 10 for Windows (StatSoft, Tulsa, OK, USA; www.statsoft.com).
RESULTS Table 2 presents the descriptive statistics. The average age of the sample was 67.6 years, 55% of the participants were women, and the average number of years of formal education was 13.6. The total sample self-identified themselves as Mexican Chicano/Mexican Americans, with English being language of interview in 45%. The mean scores for the telephone screens, i.e., TICS-m, MIS-t, TEXAS, and AQ, were respectively 35.74 (range: 20–46), 7.26 (range: 1–8), 1.65 (range: 0–7), and 2.45
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Sum of Boxes staging categories
CDR Sum of Boxes range
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0 0.5–4.0 0.5–2.5 3.0–4.0 4.5–9.0 9.5–15.5 16.0–18.0
Staging category Normal Questionable cognitive impairment Questionable impairment Very mild dementia Mild dementia Moderate dementia Severe dementia
Note. Copyright O’Bryant, S. E., Waring, S. C., Cullum, C. M., Hall, J., Lacritz, L., Massman, P. J., Lupo, P. J., Reisch, J. S., & Doody, R. (2008). Archives of Neurology, 65, 1091–1095. A Texas Alzheimer’s Research Consortium (TARC) study.
Table 2.
Descriptive statistics (N = 184), mean (SD)
Age Women (%) Education Language English (%) TICS-m MIS-t TEXAS AQ CDR-SOB
67.65 (7.17) 55% 13.6 (2.7) 45% 35.74 (5.2) 7.26 (1.24) 1.65 (1.47) 2.45 (3.95) 2.31 (1.13)
Note. TICS-m = Telephone Interview for Cognitive Status—modified; MIS-t = Memory Impairment Screen—telephone; TEXAS = Telephone Executive Assessment; AQ = Alzheimer’s Questionnaire; CDR-SOB = Clinical Dementia Rating Sum of Boxes.
(range: 0–24). The mean for the CDR-SOB was 2.31. Ranges not depicted in the table. Table 3 presents group mean differences on formal psychometrics. All cross-group comparisons are significant at p < .002 by Tukey’s honest significant difference test. The statistical associations between demographic variables and AQ scores are reported in Table 4. AQ scores were not significantly associated with education, gender, or language (participants were balanced bilinguals (English and Spanish). Only subject age had a significant positive association with the informant-rated AQ (R2 = .06). Table 5 presents the multiple regression analyses for prediction of “cognitive impairment severity” using CDR-SOB as the dependent variable.
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Table 3. Neuropsychological test performance difference between normal controls (NC) and mild cognitive impairment (MCI)∗
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Normal controls (n = 125)
Mild cognitive impairment (n = 57)
Variable
Mean
SD
Mean
SD
Trails B CLOX1 CLOX2 WMS3-LMI WMS3-LMII Boston Naming Animal Fluency WM3-VRI WM3-VRII Animal Fluency FAS Fluency F A S TICS-m MIS-t TEXAS
99.21 12.86 14.04 34.93 21.60 23.61 15.80 73.06 49.75 15.80
90.23 1.41 0.97 8.76 7.05 4.08 3.25 15.17 20.49 3.25
182.30 11.24 13.41 29.18 16.42 20.71 14.07 64.89 34.56 14.07
203.44 2.85 1.24 8.90 6.96 5.51 3.80 15.93 19.20 3.80
12.27 10.65 12.78 37.28 7.50 1.31
3.87 4.03 3.67 4.47 0.86 1.30
9.58 8.25 9.47 32.81 6.95 2.21
0.51 3.48 3.73 5.19 1.50 1.42
∗ All significant at p < .002 by Tukey’s honest significant difference test. Trails B = Trail Making Test part B; CLOX = an executive clock drawing task, part 1 and part 2; WMS3 = Wechsler Memory Scale, version 3; LMI = Learning Memory part I; LMII = Learning Memory part II; VRI = Visual Reproduction part I; VRII = Visual Reproduction part II; FAS = Verbal fluency test for letters F, A, and S.; TICS-m =Telephone Interview for Cognitive Status—modified; MIS-t = Memory Impairment Screen—telephone; TEXAS = Telephone Executive Assessment.
Table 4. Multivariate associations between demographic predictors and Alzheimer’s Questionnaire scores∗ (N = 184) Variable Intercept Age Gender Education Language ∗ Regression
β
SE β
p value
0.11 −0.58 −0.18 2.40
0.04 0.58 0.11 3.91
.47 .007 .33 .11 .54
summary for dependent variable AQ: R2 = .06.
Model 1 uses demographic variables as predictors. Older age was positively associated with CDR-SOB. Education, gender, and language of interview did not add any variance to the model.
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Table 5. Summary of regression models comparing telephone screens and demographics with CDR-SOB as dependent variable (N = 184) Model 1∗ β
SE β
p value
0.02 −0.29 −0.03 −0.55
0.01 0.17 0.03 1.13
.000000 .03 .09 .30 .62
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Variable Intercept Age Gender Education Language AQ TICS-m MIS-t TEXAS
Model 2†
Model 3‡
β
SE β
p value
0.01 −0.23 −0.02 −0.77 0.09
0.01 0.16 0.03 1.07 0.02
.000013 .18 .15 .58 .47 .0000
β
SE β
p value
0.01 −0.20 −0.00 −0.91 0.08 0.04 −0.08 0.15
0.01 0.16 0.03 1.07 0.02 0.02 0.07 0.07
.000000 .38 .22 .86 .40 .0002 .03 .26 .03
∗ Regression
summary for dependent variable CDR-SOB: R2 = .5. summary for dependent variable CDR-SOB: R2 = .14. ‡ Regression summary for dependent variable CDR-SOB: R2 = .18. TICS-m = Telephone Interview for Cognitive Status—modified; MIS-t = Memory Impairment Screen—telephone; TEXAS = Telephone Executive Assessment; AQ = Alzheimer’s Questionnaire; CDR-SOB = Clinical Dementia Rating Sum of Boxes. † Regression
In Model 2, the AQ explained 9% of the variance in CDR-SOB above and beyond the demographics. In Model 3, when adding the rest of the telephone screens, the TICS-m and the TEXAS together explained an additional 4% of the variance in CDR-SOB scores. DISCUSSION A number of telephone-based cognitive measures have been developed. In general, they have been effective in distinguishing between individuals with dementia and cognitively healthy controls (Smith, Tremont, & Ott, 2009). However, they are less useful in distinguishing between MCI and controls (Knopman et al., 2010). The AQ has recently been shown to be effective in detecting amnestic MCI subtype from those with normal cognition (Malek-Ahmadi, Davis, et al., 2012). In this study, we confirm the usefulness of the AQ as a telephone-based screening tool for MCI, and demonstrate its potential utility as a culturefair measure in Hispanic patients. We have shown that the administration of the AQ to an informant and by telephone is associated with CDR-SOB, independently of other telephone screening measures. In Hispanics, the AQ is not affected by the subject’s gender, years of education, or the language used in the interview (English or Spanish).
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The AQ displaces the MIS-t from our model but not the TEXAS (see Table 5). This suggests that the AQ may have a bias in favor of the detection of amnestic MCI cases, consistent with Malek-Ahmadi, Davis, et al.’s (2012) findings. However, it also suggests that the AQ might underdiagnose “dysexecutive” MCI cases. Moreover, memory performance is less strongly related to instrumental activities of daily living (IADLs) than is executive function (Royall, Palmer, Chiodo, & Polk, 2005). Because the IADL-impaired fraction of MCI cases have a higher dementia conversion risk (Chang et al., 2011), the AQ may be limited in its ability to detect MCI cases at increased risk to near-term conversion. On the other hand, amnestic MCI cases are more likely to convert specifically to AD (Morris, 2012). The AQ’s memory bias might make it more sensitive and specific to preclinical AD. In conclusion, the AQ appears to provide a culture-fair instrument for the telephone-based diagnosis of MCI among Hispanics. It explains variance in dementia severity above and beyond of that provided by other telephone-administered assessments, and may help detect amnestic MCI cases more at risk of conversion to clinical AD. Limitations of our study include that we did not explicitly distinguish between amnestic and nonamnestic MCI subtypes. However, even patients defined as “pure” amnestic MCI on screening tests are likely to have executive impairments, when a comprehensive neuropsychological examination of executive cognition is performed (Brandt et al., 2009). Thus, the distinction may be prone to measurement bias. Strengths of our study include the independence of the clinical assessment used as a standard by which to judge the validity of the telephone-based instruments, and the potential availability of longitudinal follow-up data to confirm diagnostic accuracy.
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Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uear20
Telephone Screening for Mild Cognitive Impairment in Hispanics Using the Alzheimer’s Questionnaire a
a
Ricardo Salazar , Carlos E. Velez & Donald R. Royall
bc
a
Department of Psychiatry, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA b
Departments of Psychiatry, Medicine, Family and Community Medicine, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA c
South Texas Veterans Health Administration Geriatric Research Education and Clinical Care (GRECC), San Antonio, Texas, USA Published online: 13 Mar 2014.
To cite this article: Ricardo Salazar, Carlos E. Velez & Donald R. Royall (2014) Telephone Screening for Mild Cognitive Impairment in Hispanics Using the Alzheimer’s Questionnaire, Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process, 40:2, 129-139, DOI: 10.1080/0361073X.2014.882189 To link to this article: http://dx.doi.org/10.1080/0361073X.2014.882189
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Experimental Aging Research, 40: 129–139, 2014 Copyright © Taylor & Francis Group, LLC ISSN: 0361-073X print/1096-4657 online DOI: 10.1080/0361073X.2014.882189
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TELEPHONE SCREENING FOR MILD COGNITIVE IMPAIRMENT IN HISPANICS USING THE ALZHEIMER’S QUESTIONNAIRE Ricardo Salazar and Carlos E. Velez Department of Psychiatry, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
Donald R. Royall Departments of Psychiatry, Medicine, Family and Community Medicine, The University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA; and South Texas Veterans Health Administration Geriatric Research Education and Clinical Care (GRECC), San Antonio, Texas, USA Background/Study Context: There is a need for a simple and reliable screening test to detect individuals with mild cognitive impairment (MCI). The authors analyzed the relationship between performance of the Alzheimer’s Questionnaire (AQ), an informant-rated measure of dementia-related behaviors, relative to the Telephone Interview for Cognitive Status—modified (TICS-m), Memory Impairment Scale— telephone version (MIS-t), and the Telephone Executive Assessment (TEXAS) as predictors of MCI. Methods: Comparative cross-sectional design, with data collected from participants in the Texas Alzheimer’s Research and Care Consortium’s (TARCC) San Antonio site. One-hundred percent of our sample was Hispanic. The San Antonio subset of TARCC sample is highly enriched with Mexican Americans (MAs). Fifty-five percent of the interviews were Received 27 December 2012; accepted 19 March 2013. Some of these findings have been previously presented as a poster at the Annual Meeting of the American Medical Directors Association in Long-Term Care Medicine in San Antonio, Texas, March 8–11, 2012. Address correspondence to Ricardo Salazar, MD, Department of Psychiatry, The University of Texas Health Science Center at San Antonio, Division of Aging and Geriatrics, Room 718E, 7703 Floyd Curl Drive MC 7792, San Antonio, TX 78229, USA. E-mail: [email protected]
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R. Salazar et al. conducted in Spanish. Of the 184 persons enrolled, 124 were normal controls (NCs), and 60 participants had MCI. MCI status and Clinical Dementia Rating Scale Sum of Boxes (CDR-SOB) were determined through clinical consensus and performed blind to telephone assessments. Controlling for age, gender, education, and language of interview, the association between telephone measures and CDR-SOB was evaluated by multivariate regression. Results: AQ scores were not affected by education, gender, and language of interview, but subject’s age did show a positive correlation with informant AQ ratings. The AQ predicted CDR-SOB independently of the cognitive measures, adding variance above and beyond demographics. The TICS-m and the TEXAS appear to have additive value in improving the detection of cognitively impaired patients. The MIS-t failed to contribute significantly to CDR-SOB, independent of the other measures. Conclusion: The AQ may have utility as a culture-fair telephone screening for MCI. The AQ was able to modestly distinguish MCI from NCs. The TEXAS adds variance to a model of dementia severity independent of the AQ, suggesting that the latter may weakly assess that cognitive domain (executive control function). On the other hand, the AQ attenuates the MIS-t effect. This suggests a prominent AQ bias in favor of detecting memory impairment. Additional studies are required to determine if the AQ can distinguish between amnestic and dysexecutive MCI subtypes, or between MCI and Alzheimer’s disease in Hispanics.
Patients who eventually develop clinical Alzheimer’s disease (AD) pass through a transitional state that has been labeled as mild cognitive impairment (MCI) (Petersen et al., 1999). Unfortunately, many cognitive screening tests are insensitive to MCI (Kaufer et al., 2008). Moreover, MCI subtypes have been proposed based on differences in their psychometric profiles (Petersen et al., 2001; Petersen, 2004). The relationship of these subtypes to each other and to AD, as opposed to other dementing illnesses, remains unknown (Brandt et al., 2009). Other assessment issues complicate dementia screening (i.e., mobility, financial constraints). Telephone screening tools can be relatively cost-effective and clinically useful for dementia screening (Graff-Radford et al., 2006; Ferrucci et al., 1998; Van Uffelen, Chin A Paw, Klein, van Mechelen, & Hopman-Rock, 2007). On the other hand, few measures have been validated for use in Hispanic populations (Chin, Negash, & Hamilton, 2011). Some dementia rating systems, such as the Washington University Clinical Dementia Rating (CDR) (Hughes, Berg, Danziger, Coben, & Martin, 1982) and the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE) (Jorm, Scott, Cullen, & MacKinnon, 1991), incorporate information from a collateral source to assess change
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in a patient`s cognitive function and ability to conduct their accustomed daily activities. These systems do not require a baseline assessment for comparison and minimize issues such as practice effects and educational and sociocultural influences that confound interpretation of longitudinal assessments. However, both are lengthy, require interpretation by an experienced clinician, and can be costly. The Alzheimer’s Questionnaire (AQ) (Sabbagh et al., 2010) was developed to overcome these shortcomings. The AQ is a 21-item, informantbased dementia assessment designed for ease of use in a primary care setting. AQ items are divided into five domains, including Memory, Orientation, Functional Ability, Visuospatial Ability, and Language. Items are posed in a yes/no format, with the sum of “yes” items equaling the total AQ score (0–27). Six items known to be predictive of a clinical AD diagnosis (Malek-Ahmadi, Davis, Belden, Jacobson, & Sabbagh, 2012) are weighted more heavily in the total score by being worth two points rather than one. The AQ has been translated into Spanish for use in the Texas Alzheimer’s Research and Care Consortium (TARCC). The AQ can also be administered by telephone. The purpose of our study was to analyze the ability of the AQ to explain variance in dementia severity in relation to other telephone-administered cognitive assessments, i.e., the Telephone Interview of Cognitive Status—modified (TICS-m) (Brandt, Spencer, & Folstein, 1988; Knopman et al., 2010), the Memory Impairment Screen— telephone (MIS-t; a test of semantic memory) (Lipton et al., 2003), and the Telephone Executive Assessment Scale (TEXAS); a test of executive functions derived from five items of the Executive Interview (EXIT25) (Royall, Mahurin, & Gray, 1992), among Hispanic TARCC participants with MCI and controls. METHODS Study Population The University of Texas Health Science Center at San Antonio institutional review board approved this project. All individuals discussed the study with trained research staff and provided written informed consent. The current sample comprised 184 English- and Spanish-speaking Hispanic participants in a longitudinal and observational cohort study on Alzheimer’s disease, the Texas Alzheimer’s Research Consortium and Care (TARCC) study. Details on TARCC methods are available elsewhere (Waring et al., 2008). These data include only participants at The University of Texas Health Science Center at San Antonio site.
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Evaluations were conducted in either English or Spanish, on the basis of the participant’s opinion of which language would yield the best performance. Examiners available were balanced bilinguals for participants that choose Spanish as their preferred language.
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Consensus Diagnosis TARCC clinical diagnoses were adjudicated by consensus review. This followed an in-person clinical interview and neurological examination by a geriatric psychiatrist specializing in cognitive disorders and/or a geriatrician with expertise in dementias, and the administration of a battery of standardized neuropsychological tests by a psychometrician. After each clinical assessment, a group of two geriatric psychiatrists and a senior research associate with experience in normative testing reviewed the medical, functional, neurological, psychiatric, and neuropsychological data blinded to any of the telephone-based assessments data, including the AQ, reaching a consensus diagnosis based on the presence or absence of dementia using criteria from the Diagnostic and Statistical Manual of Mental Disorders (Fourth Edition, Text Revision; American Psychiatric Association, 2000), as well as diagnosis of MCI and normal controls using strict inclusion and exclusion criteria (Waring et al., 2008). Telephone Screening Interview The subject and/or his informant were asked whether the subject would like to complete the interview during the initial recruitment call. If the participant became fatigued during the actual interview, an additional phone call(s) to complete the interview was scheduled at a time convenient to the subject and/or informant to minimize poor effort bias. During the interview, cognitive function was assessed using the Telephone Interview for Cognitive Status—modified (TICS-m), the Telephone Memory Impairment Screen—telephone (MIS-t), and the TEXAS, the telephone version of the Executive Interview (EXIT25), a measure of executive function (Royall et al., 1992). Failing the screen was defined by any one or more of the following scores: TICS-m (scores below 28), MIS-t (scores below 4), and TEXAS (scores above 3). The MIS-t and the TICS-m was administered and scored in accordance with published procedures described elsewhere (Lipton et al., 2003; Brandt & Folstein, 2003). The TEXAS consists of five items of the original EXIT25 and includes the “Number-Letter Task,” “Word Fluency,” “Memory/Distraction Task,” “Serial Order Reversal Task,” and “Anomalous Sentence Repetition” items. The total score for the TEXAS
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instrument ranges from 0 to 10, with higher scores corresponding to greater impairment. The TEXAS Cronbach’s α = .74. Based on previous work (Sabbagh et al., 2010), AQ scores corresponding to three levels of cognitive function have been defined: ≤4: normal; 5–14: mildly impaired, suggestive of MCI; ≥15: demented. A recent pilot study indicated that the AQ is a brief, sensitive measure for detecting both MCI and AD (Sabbagh et al., 2010). More recently, the AQ has been validated for its diagnostic accuracy, with high sensitivity and specificity for detecting MCI, 89% and 91%, respectively, as well as AD, with 99% sensitivity and 96% specificity. Area under the curve (AUC) values also indicated high diagnostic accuracy for both MCI and AD, at 0.95 and 0.99, respectively. Internal consistency of AQ was also high (Cronbach’s α = .89) (Malek-Ahmadi et al., 2012). In addition to assessing mental function, information about a participant’s family history of problems with memory, Parkinson’s disease, heart attack, and stroke among parents and siblings was obtained. Other variables collected from participants included general health status, history of visual hallucinations, falls, and loss of consciousness during the previous year; cardiovascular risk factors; depressive symptoms; frailty status; ability to perform activities of daily living; and education level. Information about the socioeconomic status of the neighborhood in which participants live was obtained by linking census data to participants’ zip codes. Statistical Analysis We used CDR-SOB, a continuous measure of dementia severity (see Table 1), as a dependent variable in a set of nested multivariate regression models. Demographic covariates, age, gender, education in years, and language of interview, were entered first, followed by the AQ and cognitive performance measures. All analyses were conducted in STATISTICA version 10 for Windows (StatSoft, Tulsa, OK, USA; www.statsoft.com).
RESULTS Table 2 presents the descriptive statistics. The average age of the sample was 67.6 years, 55% of the participants were women, and the average number of years of formal education was 13.6. The total sample self-identified themselves as Mexican Chicano/Mexican Americans, with English being language of interview in 45%. The mean scores for the telephone screens, i.e., TICS-m, MIS-t, TEXAS, and AQ, were respectively 35.74 (range: 20–46), 7.26 (range: 1–8), 1.65 (range: 0–7), and 2.45
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Sum of Boxes staging categories
CDR Sum of Boxes range
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0 0.5–4.0 0.5–2.5 3.0–4.0 4.5–9.0 9.5–15.5 16.0–18.0
Staging category Normal Questionable cognitive impairment Questionable impairment Very mild dementia Mild dementia Moderate dementia Severe dementia
Note. Copyright O’Bryant, S. E., Waring, S. C., Cullum, C. M., Hall, J., Lacritz, L., Massman, P. J., Lupo, P. J., Reisch, J. S., & Doody, R. (2008). Archives of Neurology, 65, 1091–1095. A Texas Alzheimer’s Research Consortium (TARC) study.
Table 2.
Descriptive statistics (N = 184), mean (SD)
Age Women (%) Education Language English (%) TICS-m MIS-t TEXAS AQ CDR-SOB
67.65 (7.17) 55% 13.6 (2.7) 45% 35.74 (5.2) 7.26 (1.24) 1.65 (1.47) 2.45 (3.95) 2.31 (1.13)
Note. TICS-m = Telephone Interview for Cognitive Status—modified; MIS-t = Memory Impairment Screen—telephone; TEXAS = Telephone Executive Assessment; AQ = Alzheimer’s Questionnaire; CDR-SOB = Clinical Dementia Rating Sum of Boxes.
(range: 0–24). The mean for the CDR-SOB was 2.31. Ranges not depicted in the table. Table 3 presents group mean differences on formal psychometrics. All cross-group comparisons are significant at p < .002 by Tukey’s honest significant difference test. The statistical associations between demographic variables and AQ scores are reported in Table 4. AQ scores were not significantly associated with education, gender, or language (participants were balanced bilinguals (English and Spanish). Only subject age had a significant positive association with the informant-rated AQ (R2 = .06). Table 5 presents the multiple regression analyses for prediction of “cognitive impairment severity” using CDR-SOB as the dependent variable.
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Table 3. Neuropsychological test performance difference between normal controls (NC) and mild cognitive impairment (MCI)∗
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Normal controls (n = 125)
Mild cognitive impairment (n = 57)
Variable
Mean
SD
Mean
SD
Trails B CLOX1 CLOX2 WMS3-LMI WMS3-LMII Boston Naming Animal Fluency WM3-VRI WM3-VRII Animal Fluency FAS Fluency F A S TICS-m MIS-t TEXAS
99.21 12.86 14.04 34.93 21.60 23.61 15.80 73.06 49.75 15.80
90.23 1.41 0.97 8.76 7.05 4.08 3.25 15.17 20.49 3.25
182.30 11.24 13.41 29.18 16.42 20.71 14.07 64.89 34.56 14.07
203.44 2.85 1.24 8.90 6.96 5.51 3.80 15.93 19.20 3.80
12.27 10.65 12.78 37.28 7.50 1.31
3.87 4.03 3.67 4.47 0.86 1.30
9.58 8.25 9.47 32.81 6.95 2.21
0.51 3.48 3.73 5.19 1.50 1.42
∗ All significant at p < .002 by Tukey’s honest significant difference test. Trails B = Trail Making Test part B; CLOX = an executive clock drawing task, part 1 and part 2; WMS3 = Wechsler Memory Scale, version 3; LMI = Learning Memory part I; LMII = Learning Memory part II; VRI = Visual Reproduction part I; VRII = Visual Reproduction part II; FAS = Verbal fluency test for letters F, A, and S.; TICS-m =Telephone Interview for Cognitive Status—modified; MIS-t = Memory Impairment Screen—telephone; TEXAS = Telephone Executive Assessment.
Table 4. Multivariate associations between demographic predictors and Alzheimer’s Questionnaire scores∗ (N = 184) Variable Intercept Age Gender Education Language ∗ Regression
β
SE β
p value
0.11 −0.58 −0.18 2.40
0.04 0.58 0.11 3.91
.47 .007 .33 .11 .54
summary for dependent variable AQ: R2 = .06.
Model 1 uses demographic variables as predictors. Older age was positively associated with CDR-SOB. Education, gender, and language of interview did not add any variance to the model.
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Table 5. Summary of regression models comparing telephone screens and demographics with CDR-SOB as dependent variable (N = 184) Model 1∗ β
SE β
p value
0.02 −0.29 −0.03 −0.55
0.01 0.17 0.03 1.13
.000000 .03 .09 .30 .62
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Variable Intercept Age Gender Education Language AQ TICS-m MIS-t TEXAS
Model 2†
Model 3‡
β
SE β
p value
0.01 −0.23 −0.02 −0.77 0.09
0.01 0.16 0.03 1.07 0.02
.000013 .18 .15 .58 .47 .0000
β
SE β
p value
0.01 −0.20 −0.00 −0.91 0.08 0.04 −0.08 0.15
0.01 0.16 0.03 1.07 0.02 0.02 0.07 0.07
.000000 .38 .22 .86 .40 .0002 .03 .26 .03
∗ Regression
summary for dependent variable CDR-SOB: R2 = .5. summary for dependent variable CDR-SOB: R2 = .14. ‡ Regression summary for dependent variable CDR-SOB: R2 = .18. TICS-m = Telephone Interview for Cognitive Status—modified; MIS-t = Memory Impairment Screen—telephone; TEXAS = Telephone Executive Assessment; AQ = Alzheimer’s Questionnaire; CDR-SOB = Clinical Dementia Rating Sum of Boxes. † Regression
In Model 2, the AQ explained 9% of the variance in CDR-SOB above and beyond the demographics. In Model 3, when adding the rest of the telephone screens, the TICS-m and the TEXAS together explained an additional 4% of the variance in CDR-SOB scores. DISCUSSION A number of telephone-based cognitive measures have been developed. In general, they have been effective in distinguishing between individuals with dementia and cognitively healthy controls (Smith, Tremont, & Ott, 2009). However, they are less useful in distinguishing between MCI and controls (Knopman et al., 2010). The AQ has recently been shown to be effective in detecting amnestic MCI subtype from those with normal cognition (Malek-Ahmadi, Davis, et al., 2012). In this study, we confirm the usefulness of the AQ as a telephone-based screening tool for MCI, and demonstrate its potential utility as a culturefair measure in Hispanic patients. We have shown that the administration of the AQ to an informant and by telephone is associated with CDR-SOB, independently of other telephone screening measures. In Hispanics, the AQ is not affected by the subject’s gender, years of education, or the language used in the interview (English or Spanish).
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The AQ displaces the MIS-t from our model but not the TEXAS (see Table 5). This suggests that the AQ may have a bias in favor of the detection of amnestic MCI cases, consistent with Malek-Ahmadi, Davis, et al.’s (2012) findings. However, it also suggests that the AQ might underdiagnose “dysexecutive” MCI cases. Moreover, memory performance is less strongly related to instrumental activities of daily living (IADLs) than is executive function (Royall, Palmer, Chiodo, & Polk, 2005). Because the IADL-impaired fraction of MCI cases have a higher dementia conversion risk (Chang et al., 2011), the AQ may be limited in its ability to detect MCI cases at increased risk to near-term conversion. On the other hand, amnestic MCI cases are more likely to convert specifically to AD (Morris, 2012). The AQ’s memory bias might make it more sensitive and specific to preclinical AD. In conclusion, the AQ appears to provide a culture-fair instrument for the telephone-based diagnosis of MCI among Hispanics. It explains variance in dementia severity above and beyond of that provided by other telephone-administered assessments, and may help detect amnestic MCI cases more at risk of conversion to clinical AD. Limitations of our study include that we did not explicitly distinguish between amnestic and nonamnestic MCI subtypes. However, even patients defined as “pure” amnestic MCI on screening tests are likely to have executive impairments, when a comprehensive neuropsychological examination of executive cognition is performed (Brandt et al., 2009). Thus, the distinction may be prone to measurement bias. Strengths of our study include the independence of the clinical assessment used as a standard by which to judge the validity of the telephone-based instruments, and the potential availability of longitudinal follow-up data to confirm diagnostic accuracy.
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