Schoen, C. B & Holtzer, R. (2017)
Schoen, C. B & Holtzer, R. (2017)
Schoen, C. B & Holtzer, R. (2017)
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Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. Author manuscript; available in
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Abstract
Research suggests a reciprocal relationship between late-life anxiety and cognition, particularly
attention and executive functions. Whereas evidence supports a conceptual distinction between
cognitive and somatic dimensions of anxiety, their differential relationship with cognitive
outcomes has not been examined, particularly on tests of attention/executive functions that rely on
processing speed. Study goals were threefold: (a) to describe levels of overall, cognitive, and
somatic anxiety in a sample of older adults without dementia, (b) to determine if overall anxiety is
associated with performance on select measures of attention/executive functions that rely on
processing speed, and (c) to determine if a differential relationship exists between cognitive and
somatic anxiety and cognitive performance. Participants were 368 community-dwelling older
adults. Results showed that elevated levels of somatic, but not cognitive anxiety were associated
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with poorer performance across measures. Findings suggest that the nature of anxiety symptoms
may have important implications for cognitive performance in older adults.
Keywords
anxiety; attention; executive functions; processing speed; aging
adults who report anxiety symptoms but do not meet criteria for anxiety disorders are even
higher, ranging from 15% to 52.3% in community-dwelling samples (Bryant, 2010). Late-
life anxiety has been linked to subjective distress, reduced life satisfaction, and functional
impairment (Mendlowicz & Stein 2000). Furthermore, older individuals who present with
some anxiety symptoms have been found to be just as negatively affected in their quality of
life as those who meet diagnostic criteria for an anxiety disorder (De Beurs et al. 1999).
Correspondence: Roee Holtzer, Ph.D., Professor, Ferkauf Graduate School of Psychology, Department of Neurology - Albert Einstein
College of Medicine/Yeshiva University, 1225 Morris Park Avenue, Bronx, NY 10461, Phone: (718) 430 3962, Fax: (718) 430-3829,
roee.holtzer@einstein.yu.edu.
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Despite high prevalence rates, research on anxiety in older adults has grown at a much
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slower rate compared to research on anxiety in younger populations (Therrien & Hunsley,
2012). In fact, relatively little is known about the presentation and experience of anxiety
among the older adult population, particularly in individuals with milder, sub-clinical
symptoms. This knowledge gap extends to limitations in evidence-based assessment of
anxiety in aging (Dennis, Boddington, & Funnell, 2007). Although the assessment of
anxiety in older adults is notably challenging for a variety of reasons, self-report measures
continue to be the dominant method for gathering information about anxiety in both clinical
and research settings (Therrien & Hunsley, 2012).
important interactions between cognitive and physiological factors. That is, cognitive
appraisals and expectations play a role in the generation of emotional arousal, and arousal
feedback influences the ongoing process of appraisal and reappraisal (Lazarus & Folkman,
1984). Despite the apparent functional relatedness of cognitive and affective systems,
traditional models assert that they are distinctive aspects of the anxiety process, reflected in
individual differences in the experience and expression of anxiety reactions (Davidson &
Schwartz, 1976; Deffenbacher, 1980).
Several studies have built upon this theoretical framework to provide further evidence for the
cognitive-somatic distinction. The literature suggests that while cognitive and somatic
symptoms interact with one another, they may also be elicited by different classes of
antecedents. For example, threat of electric shock has been shown to have its primary
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In an original factor analysis of the Beck Anxiety Inventory (BAI), a widely used self-report
anxiety questionnaire, Beck and colleagues (1988) found that the BAI yielded two factors,
corresponding mainly to cognitive and somatic dimensions of anxiety. The authors broadly
defined cognitive anxiety as “negative expectations, worries, and concerns about oneself, the
situation at hand, and potential consequences” and somatic anxiety as “the perception of
one’s physiological arousal.” A similar two-factor structure was replicated in a number of
studies, with the somatic factor containing items such as “numbness,” “unsteadiness,” and
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“feeling hot” and the cognitive factor consisting of items such as “fear of the worst
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happening,” “terrified,” and “fear of losing control” (Hewitt & Norton, 1993; Kabacoff,
Segal, Hersen, & Van Hasselt, 1997). Researchers have also reported more complex factor
solutions depending on the sample examined and statistical approach used (Therrien &
Hunsley, 2012). Nonetheless, a robust body of evidence supports the conceptual distinction
between cognitive and somatic domains of anxiety, in younger and older populations alike
(Smith et al., 1990).
poorer prognosis for late-life clinical anxiety (Mohlman & Gorman, 2005). Thus, a better
understanding of this relationship may elucidate the pathophysiological mechanisms by
which age-related cognitive decline occurs and furthermore, may facilitate improved
treatment development for anxiety in older adults (Beaudreau & O’Hara, 2008).
Cross-sectional investigations generally support the hypothesis that the presence and severity
of anxiety are both associated with poorer cognitive performance in older adults (Beaudreau
& O’Hara, 2008). Older adults reporting elevated state, trait, or clinical anxiety symptoms
have been shown to demonstrate poorer global cognitive function on screening assessments
(Schutz, Moser, Bishop, & Ellingrod, 2005) as well as poorer performance on challenging
neuropsychological tests (Hogan, 2003). However, the specific cognitive domains most
affected by late-life anxiety are still not well delineated in the literature (Beaudreau &
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O’Hara, 2008). Findings from previous studies examining the impact of late-life anxiety
symptoms on objective memory performance are mixed, as some authors have demonstrated
a significant inverse linear relationship between anxiety levels and memory performance
(Mantella et al., 2007; Stillman, Rowe, Arndt, & Moser, 2012), while others have reported
no significant associations or inverted U-shape relationships (Bierman, Comjis, Rijmen,
Jonker, & Beekman, 2008). Notably, a robust body of evidence supports the notion that
elevated anxiety levels are associated with increased subjective memory complaints among
older adults Kliegel, Zimprich, & Eschen, 2005; Pearman, Hertzog, & Gerstorf, 2014).
These findings are consistent with previous work showing links between self-reported
cognitive complaints and models of health anxiety, such as dementia worry, suggesting that
older adults with increased concern about developing dementia may be more likely to
demonstrate subjective, but not objective decline, leading to potential misdiagnosis,
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unnecessary treatment, and/or increased anxiety levels (Kinzer & Suhr, 2016).
While it is evident that the association between late-life anxiety and memory functioning is
complex, the relationship between anxiety and executive functioning in older adults is
similarly unclear. Interestingly, recent work by Yochim and colleagues (2013) suggests that
the association between late-life anxiety and memory may in fact be mediated by poor
executive abilities. Additional studies have provided support for the notion that the presence
of late-life anxiety is associated with decreased performance on measures of executive
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functions. Specifically, in a study of 102 healthy older adults aged 60 and older, higher BAI
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scores were associated with poorer performance on measures of inhibitory control (Stroop
Test) and processing speed/shifting attention (Symbol Digit Modality Test; SDMT), but not
verbal fluency (Controlled Oral Word Association Test; COWAT) (Beaudreau & O’Hara,
2009). Another study of community-dwelling older adults showed that anxiety levels
explained some of the variance on Trail Making Test B time, but not Stroop performance
(Booth, Schinka, Brown, Mortimer, & Borenstein, 2006). Finally, Hogan (2003) reported
that higher anxiety was associated with poorer divided attention on word-comparison and
pursuit-rotor tasks in older, but not younger adults. Taken together, these studies highlight
the variability among neuropsychological tests selected and correspondingly, the specific
facets of executive functioning potentially impacted by sub-clinical symptoms of late-life
anxiety. Based on the existing literature, further investigation is required to identify the
specific mechanisms underlying the relationship of anxiety with reduced performance on
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(Deptula, Singh, & Pomara, 1993). However, the individual contribution of somatic anxiety
symptoms to this theoretical framework is unclear. Specifically, it is possible that a specific
subset of anxiety symptoms (e.g., somatic or cognitive) may compromise performance on
measures that assess speed of processing. Processing speed is a key determinant in many
measures of executive functions and its effect on performance differences on such measures
has been well documented (Salthouse, 1996). Given previous research linking late-life
anxiety to reduced performance on various measures of executive functions (Beaudreau &
O’Hara, 2009), further investigation is needed to clarify the role of anxiety, and specific
types of anxiety symptoms, on measures of executive functions that rely more heavily on
processing speed.
Since Beck and colleagues (1988) proposed a two-factor structure in their original factorial
analysis of the BAI, several researchers have discussed the importance of the conceptual
distinction between cognitive and somatic domains of anxiety (Burton, 1988; Smith et al.,
1990). It remains unknown, however, whether a differential relationship exists between these
two domains of anxiety and cognitive performance and, in particular, on attention and
executive tasks that rely on processing speed. The current study was designed to address the
gap in knowledge concerning the relationship between distinct dimensions of anxiety and
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cognitive performance in aging. Specifically, the aims of the present study were threefold:
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(a) to descriptively examine symptoms of overall, cognitive, and somatic anxiety in a sample
of community-residing older adults without dementia, (b) to determine if overall anxiety is
associated with performance on select measures of attention and executive functions that
rely on processing speed, and (c) to determine if a differential relationship exists between
cognitive and somatic anxiety and these select measures. Ultimately, the present study
provides an opportunity for improved understanding of the neuropsychological correlates of
sub-clinical anxiety symptoms among a rapidly growing population of healthy aging,
community-dwelling older adults. Moreover, it offers valuable insight into the relative
impact of cognitive versus somatic anxiety symptoms on cognition, which could have
important implications for clinical and neuropsychological practice.
Method
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inability to ambulate independently, positive screen for possible dementia, significant loss of
vision and/or hearing, current or history of neurological or psychiatric disorders, recent or
anticipated medical procedures that may affect mobility, and receiving hemodialysis. After
completing the telephone interview, eligible individuals were scheduled for two in-person
visits at the research center lasting approximately three hours per visit. During the visits,
participants received comprehensive neuropsychological, cognitive, psychological, and
mobility assessments as well as a structured neurological examination. Participants’ current
medications were recorded by the study physician. Participants are followed longitudinally
at yearly intervals. Written informed consents were obtained on site according to study
protocols and were approved by the institutional review board. Study protocols have been
described in detail in previous work (Holtzer, Wang, & Verghese, 2014).
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were summed to provide a score ranging from 0 to 63, with higher scores indicative of
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higher levels of anxiety. Although the BAI was developed and normed with psychiatric adult
outpatients, the scale was found to have adequate psychometric properties with
heterogeneous samples of older adults (Morin et al., 1999).
Trail Making Test (TMT)—The TMT (Reitan, 1958) consists of two parts, each including
25 circles on a single sheet of paper. In the present study, both parts A and B were
administered. In part A (TMT A), circles contain numbers from 1 through 25 and
participants are asked to connect the circles in ascending numerical order as rapidly and
accurately as possible. Part B (TMT B) contains 13 circles numbered 1 through 13 and 12
circles lettered A through L. In this task, participants are asked to connect the circles in
sequential order alternating between numbers and letters (i.e. 1, A, 2, B, 3, C, etc.). Scores
were based on seconds to completion and attempts were discontinued after 5 minutes (300
seconds). The TMT has high reliability (Yochim, Mueller, & Segal, 2013) and has been used
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extensively as a measure of attention and executive functions in both normal and clinical
samples of older adults (Kowalczyk, McDonald, Cranney, & McMahon, 2001; Oosterman et
al., 2010).
Digit Symbol Substitution Test (DSST)—The DSST (a subtest of the Wechsler Adult
Intelligence Scale – Revised) (Wechsler, 1981) includes a key with nine numerical digits
matched with corresponding symbols. After completing practice items, participants are
given 120 seconds to match numerical digits with corresponding symbols. Scores are
calculated as total number of correctly matched symbols. The DSST has high test-retest
reliability and has been shown to be a valid measure of executive functions including
working memory, perceptual organization, visuomotor coordination, shifting attention, and
processing speed (Rosano, Newman, Katz, Hirsch, & Kuller, 2008).
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Covariates
Structured clinical interviews were used to identify self-reported medical conditions.
Dichotomous rating (presence or absence) of diabetes, chronic heart failure, arthritis,
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somatic symptomatology due to medical illness or depression, rather than anxiety itself.
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Statistical Analysis
Characteristics of the study sample, including levels of overall, cognitive, and somatic
anxiety as well as performance on measures of attention/executive functions that rely on
processing speed were tabulated. Three separate linear regressions were conducted to
examine the relationship between overall anxiety (as measured by Total BAI Score) and
performance on the three neuropsychological tests. Total BAI Score was used as the
predictor variable and raw scores on each cognitive measure (specified above) served as the
outcome variables. The predictors and covariates were entered simultaneously.
Items of the BAI were categorized into two domains: cognitive and somatic, according to the
original two-factor structure proposed by Beck and colleagues (1988). The “cognitive”
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domain included 8 items and the “somatic” domain included 13 items. BAI item scores were
summed for both domains and used as predictor variables to examine associations with
performance on the three neuropsychological tests. Three linear regression analyses were
performed to examine the relations of somatic and cognitive BAI scores and covariates,
entered simultaneously, with each neuropsychological outcome measure. Data were
inspected descriptively and graphically and model assumptions were formally tested. Fully
adjusted models controlled for gender, age, education, depression, and disease comorbidity.
Statistical analyses were performed using International Business Machines (IBM) Statistical
Package for the Social Sciences (SPSS) version 20 (IBM, Somers, NY).
Results
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Participants in this study were recruited from CCMA between 6/27/11 and 7/15/14. During
this period, 407 individuals completed phone interviews, were deemed eligible for
participation, and attended at least one in-person visit at our research center. Of these 407
individuals, 27 individuals did not attend their second in-person visit, during which the BAI
is administered. Reasons for not returning for in-person visits include but are not limited to
change in health status, lack of interest, time conflicts, and change in residence. A total of
380 participants completed both day 1 and day 2 protocols and this sample was frozen in
order to preserve the integrity of the data. These participants were not demented, as
determined by established diagnostic clinical case conference procedures as previously
described (Holtzer et al., 2008). At the time of the data freeze, 8 participants were excluded
due to incomplete or invalid TMT B or DSST protocols and an additional 4 were excluded
due to incomplete BAI data. Thus, 368 participants were analyzed for the current study, with
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a mean age (76.42 years; ±6.71), education (14.54 years; ±2.99), and gender distribution
(%female = 56.8) that is broadly representative of the demographic characteristics of
individuals in this age group who reside in the study catchment area. The sample was also
not different from the larger CCMA cohort in terms of key demographic characteristics. The
mean disease comorbidity summary score (1.21 ± 0.98) was indicative of relatively good
health and the mean Repeatable Battery for the Assessment of Neuropsychological Status
standardized total score (91.27 ± 15.24) was in the Average range of cognitive function.
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Scaled scores for each of the three selected outcome measures also fell within the Average
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range (TMT A = 10; TMT B = 9; DSST = 11). Of note, raw scores were used in all linear
regression analyses. The mean Beck Anxiety Inventory Total Score (4.95 ± 5.72) was in the
Minimal range of anxiety severity (Beck & Steer, 1993). Mean total somatic and cognitive
anxiety scores were 2.85 ± 3.71 and 2.10 ± 2.87, respectively. Baseline cohort characteristics
are presented in Table 1.
The linear regression analyses revealed that the relationship between overall levels of
anxiety (Total BAI Score) and processing speed was not significant (Table 2).
Table 3 summarizes the results of three separate linear regression analyses examining the
relationship of cognitive and somatic domains of anxiety with measures of attention/
executive functions that rely on processing speed. As expected, correlation between somatic
and cognitive domains were moderately significant (Pearson Correlation = .507; p<0.001),
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but did not pose a threat to model stability. Somatic anxiety was related to performance on
all three neuropsychological tests. Elevated levels of somatic symptoms were associated
with greater time to completion on TMT A (β = .148, p < .05) and TMT B (β = .19, p < .
01). Additionally, somatic symptoms were associated with lower number of correct
responses on DSST (β = −.138, p < .05). Table 3 also reveals a significant inverse
relationship between cognitive anxiety and time to completion on TMT B (β = −.158, p < .
05). However, the association between cognitive anxiety and the remaining two tests were
not significant.
Discussion
The present study was designed to examine the manifestation of anxiety symptoms in a
cohort of community-dwelling older adults without dementia and to evaluate the relationship
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between overall, somatic, and cognitive anxiety with performance on three select tests of
attention and executive functions that rely on processing speed. Our results indicated that
overall anxiety, as measured by Total BAI Score, was unrelated to the cognitive outcomes in
this study. However, separating overall anxiety into distinct domains revealed that higher
somatic but not cognitive anxiety was related to worse performance on all three
neuropsychological measures.
The few studies examining the association between late-life anxiety and cognition have
consistently found an inverse relationship between anxiety and performance on select
neuropsychological tests of executive functions (Booth et al., 2006; Hogan, 2003; Yochim et
al., 2013). In this literature, however, the variability among measures of anxiety and
cognitive functions is a limitation. Beaudreau and O’Hara (2009) examined a sample of
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community-dwelling older adults without dementia and found that anxiety, as assessed by
the BAI, was associated with worse performance on cognitive tests measuring processing
speed, shifting attention, and inhibition. The present study serves to further elucidate and
extend these previous findings by examining specific domains of anxiety in addition to
overall anxiety levels.
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Despite frequent references to the conceptual distinction between cognitive and somatic
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anxiety in the literature, the present study is the first to examine the differential relationship
of these two domains of anxiety with performance on neuropsychological tests. In fully
adjusted models, elevated somatic but not cognitive anxiety was associated with poorer
performance on the three tests reported herein. In the context of the processing speed theory
of cognitive aging (Salthouse, 1996; Finkel, Reynolds, McArdle, & Pederson, 2007), these
results suggest that somatic anxiety may have a greater capacity for interference with
processing speed compared to cognitive anxiety, particularly among older adults with
milder, sub-clinical symptoms. Specifically, the potential for somatic symptoms (e.g.,
autonomic hyperactivity, motor tension) to tax the attentional system may be substantial,
thus diminishing the availability of cognitive resources required for time-sensitive cognitive
tasks. Alternatively, the presence of somatic symptoms may lead to impairments in
functional status that cause significant concern. This concern may serve as powerful task-
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In contrast to previous findings, our results revealed that overall anxiety was unrelated to
performance on select tests of executive functions that involve processing speed. One reason
for this discrepancy, aside for variability among cognitive measures, may lie in the
covariates selected for analyses, which were unclear in Beaudreau and O’Hara’s (2009)
study. However, without adjustments, a trend was observed for an inverse relationship
between Total BAI Score and DSST (β = −.253, p = .051).
The results revealed that cognitive anxiety was unrelated to performance on TMT A and
DSST. However, lower cognitive anxiety was associated with slower completion time on
TMT B, suggesting that higher levels of cognitive anxiety may be related to improved
performance on a complex task requiring processing speed, visuomotor sequencing, and
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switching attention. Because significant associations were not found between cognitive
anxiety and the other two neuropsychological tests, this may be a spurious finding that
should be cautiously interpreted. Nonetheless, it is important to consider that the relationship
between anxiety and cognitive performance may be complex due to interactions between
anxiety and test difficulty (Hogan, 2003) and that subthreshold anxiety symptoms may in
fact facilitate cognitive performance (Beaudreau & O’Hara, 2008). Furthermore, the
differential association between somatic and cognitive anxiety with tests of attention and
executive functions that rely on processing speed may obscure this relationship when
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and somatic domains individually, the present study provides further insight into the
potentially facilitative effect of cognitive anxiety on test performance. One possible
explanation for this result is that cognitive anxiety, often associated with evaluative anxiety
(i.e. worry, fear of outcome), may activate some facilitative response system when presented
with a more complex task such as TMT B.
Several limitations to the present study should be considered. Although the BAI was found
to have adequate psychometric properties with samples of healthy aging older adults (Morin
et al., 1999), issues inherent in the standardized assessment of late-life anxiety must be
acknowledged. Previous studies have discussed the potential for confusion between anxiety
symptoms and medical illnesses, comorbid psychological disorders, and aspects of normal
aging (Kogan, Edelstein, & McKee, 2000). Despite controlling for disease comorbidity in
statistical analyses, it is possible that physical ailments unrelated to anxiety may still have
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served to obscure the origin of symptoms endorsed on the BAI. Also, the extent to which
older adults underreport psychological symptoms is unknown and may potentially differ
generationally or by gender (Fuentes & Cox, 2002). Moreover, the present study examined a
sample of older adults that was relatively cognitively and psychiatrically healthy, which
limited the generalizability of our findings to populations with more severe levels of anxiety,
depression, and/or cognitive function. Hence, replicating and extending the findings reported
herein to more diverse samples in terms of psychological and neurological functions would
be important. Additionally, it is well documented that individuals of Anglo-European
background are more likely to recognize anxiety as cognitively derived, while Hispanic and
Asian populations tend to experience anxiety somatically (Rao, Poland, & Lin, 2012).
However, the sample examined in the present study was predominantly Caucasian, making it
difficult to determine the impact of specific ethnic identity on the degree of reported somatic
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versus cognitive anxiety. Therefore, future studies should investigate the relationship
between these major domains of anxiety and cognitive performance in more culturally and
ethnically diverse populations of older adults.
the cross-sectional design of this study, causality cannot be inferred. Thus, future studies are
necessary to examine these associations longitudinally. Lastly, the relationship between
somatic anxiety and neuropsychological performance should be further evaluated in more
diverse samples of older adults, particularly in terms of anxiety severity and levels of
cognitive functioning.
Summary: The present study is the first to report on the association of specific domains of
anxiety with cognitive performance in a sample of older adults without dementia. Greater
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levels of somatic but not cognitive anxiety were related to poorer performance on select
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measures of attention and executive functions that require speed of processing and fine
motor skills. Taken together, these findings confirm previous reports that subthreshold
anxiety symptoms uniquely impact cognitive functioning, even after controlling for
depression, in a growing population of community-dwelling older adults. Moreover, they
suggest that the specific nature of anxiety symptoms may have important implications for
cognitive performance. Our results highlight the value of moving beyond the use of a
composite score and assessing major sub-domains of late-life anxiety in clinical practice, as
somatic and cognitive symptoms may differentially impact cognition. Whether in the context
of a clinical neuropsychological interview or by further analysis of a standardized BAI
score, clinicians may benefit from gathering information about their patient’s specific
anxiety symptomatology. Ultimately, this could help to elucidate the factors influencing test
performance, facilitate case conceptualization, and/or improve diagnostic clarity.
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Acknowledgments
This study was supported by the National Institutes of Health (NIH) under grant RO1AGO36921.
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Table 1
RBANS: Repeatable Battery for the Assessment of Neuropsychological Status; GDS: Geriatric Depression Scale; BAI: Beck Anxiety Inventory;
DSST: Digit Symbol Substitution Test (total number correct); TMT A: Trail Making Test Part A (time to completion in seconds); TMT B: Trail
Making Test Part B (time to completion in seconds).
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Table 2
Linear Regression Analysis of the Effect of Total Beck Anxiety Inventory Score on Attention/Executive Functions
TMT A: R = .324; R2 = .105; p = < .001 TMT B: R = .368; R2 = .135; p = < .001
Variables B 95% CI p B 95% CI p
Age .153 .208 to .967 .003 .192 .907 to 2.769 <.001
Schoen and Holtzer
Analyses controlled for age, sex, education, medical comorbidity, and depression. BAI: Beck Anxiety Inventory; GDS: Geriatric Depression Scale; TMT A: Trail Making Test Part A (time to completion in
seconds); TMT B: Trail Making Test Part B (time to completion in seconds); DSST: Digit Symbol Substitution Test (total number correct).
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Table 3
Linear Regression Analysis of the Effect of Cognitive and Somatic Anxiety on Attention/Executive Functions
TMT A: R = .344; R2 = .119; p = < .001 TMT B: R = .399; R2 = .159; p = < .001
Variables B 95% CI p B 95% CI p
Age .192 .210 to .965 .002 .192 .918 to 2.756 <.001
Schoen and Holtzer
Analyses controlled for age, sex, education, medical comorbidity, and depression. BAI: Beck Anxiety Inventory; GDS: Geriatric Depression Scale; TMT A: Trail Making Test Part A (time to completion in
seconds); TMT B: Trail Making Test Part B (time to completion in seconds); DSST: Digit Symbol Substitution Test (total number correct).
*
p < .05,
**
p < .01
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