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. 2011 Feb 19;34(1):59–66. doi: 10.1007/s11357-011-9215-7

Executive functions in elderly men

Mu-En Liu 1, Yun-Hsuan Chang 2,3,4, Yan-Chiou Ku 5, Sheng-Yu Lee 2,4,6, Chih-Chung Huang 4, Shiou-Lan Chen 2, Shih-Heng Chen 2, Chun-Hsien Chu 2, Wen-Chien Liu 7, Ru-Band Lu 2,3,4,8,9,
PMCID: PMC3260367  PMID: 21336568

Abstract

The executive function deficit is greater in depressed patients with cardiovascular disease than in depressed patients without cardiovascular disease. Late-life depression is said to have a vascular etiology and would worsen the executive function. A cross-sectional design was used for this study. The study was done in outpatient clinics of Kaohsiung Veterans General Hospital and National Cheng Kung University Hospital, Taiwan. Three hundred thirty-five older elderly men (>75 years old) were chosen as study participants, some military veterans and some not. The mini-mental state examination was used to exclude those suspected of dementia, the Mini-International Neuropsychiatric Interview to screen those undergoing a current major depressive episode, and the revised Geriatric Depression Scale Short Form to measure the severity of depression. Specialist physicians obtained past histories of medical illnesses through chart reviews, history taking, and health examinations. Elderly men with major depression comorbid with cardiovascular disease had worse executive functions. Executive function impairment is greater in elderly men diagnosed with major depression comorbid with cardiovascular disease than in those without cardiovascular disease.

Keywords: Elderly men, Cardiovascular comorbidity, Major depression, Executive function

Introduction

The aging society has become a common phenomenon worldwide. More than 10% of the total population in Taiwan has consisted of elderly persons (≥65 years old) since 2007. A significant growing number of the old-old population older elderly (>75 years old), 42.1% of older population (≥65 years old) were also noted (Ministry of the Interior Statistical Information Service et al. 2006). Military veterans account for one sixth of these elderly (Veterans Affairs Commission EY et al. 2004) and have unique characteristics. When the Chinese civil war ended in 1949, many of the nationalist armed forces relocated from mainland China to Taiwan. After resigning from the armed forces, many of these men remained in Taiwan and the majority never married (Weng 1999). Their languages, habits, and value systems were different from those of local people, which made it difficult for them to develop new social networks and get jobs in Taiwan (Lu 1998). In addition, because they have more medical disabilities, are more vulnerable to depression, and are more dependent on social support than are the younger elderly (60–74 years old) (Blelsky 1990), their symptomatic expressions are complex and contribute to their increased vulnerability in Taiwan. However, because current knowledge about and studies on the medical comorbidities and psychiatric illnesses of elderly patients are limited, it is a challenge for physicians to identify them early and precisely.

Depression is the leading cause of geriatric psychiatric problems and increases with age in the Han Chinese old elderly population in Taiwan (Chou and Chi 2005). Between 1% and 4% of the elderly have major depressive disorder (Blazer 2003), and its prevalence in the elderly older than 85 years is twice that in those 70 years old (Palsson et al. 2001). In Taiwan, the prevalence of depression in the elderly is 39.2% in psychiatric hospitals and 29.5% in the community (Lin et al. 2004). The high prevalence of major depression seems to be a significant risk factor of suicide in the very elderly (Conwell et al. 2002).

In addition, most of the depressed elderly are comorbid with physical illness, cognitive impairment, disability, or social isolation (Alexopoulos et al. 2002). In addition, some medical illnesses, such as cardiovascular comorbidities, are associated with depression (Eastwood et al. 1989). There is imaging evidence to support that specific cardiovascular lesions are related to late-onset depression (Krishnan 1991). Depression in the elderly is also more likely to increase the risk of type II diabetes mellitus (DM) and hypertension (Brown et al. 2004). The deficits in executive functioning measured by the Wisconsin Card Sorting Task (WCST) may be the result of damage to the frontal–subcortical circuits of the brain (Campbell et al. 2001), a series of discrete pathways supporting executive cognitive functions (Mega and Cummings 1994). This region is particularly vulnerable to ischemic injury because of its relatively long, small diameter, penetrating branches deriving from the anterior and middle cerebral arteries (Campbell et al. 2001). Moreover, dysregulation between the prefrontal cortex and the limbic system has been implicated in the pathogenesis of major depressive disorder (Davidson et al. 2002) and might be associated with decreased cognitive functioning (Elderkin-Thompson et al. 2009). In summary, both depression and cardiovascular disease may both be associated with frontal lobe dysfunction and an increased risk for the development of cognitive impairment (Elderkin-Thompson et al. 2009; Gianaros et al. 2006; Hoshi et al. 2010). Moreover, the management and prognosis of underlying medical illnesses can be affected by major depression. Therefore, the association between depression and cardiovascular diseases have been reported and suggested for clinicians, who are urged to take it into account while the aging becomes important gradually.

The elderly usually have executive function disabilities in planning, initiating, shifting, working memory, and so on (Lockwood et al. 2002). Moreover, chronic illness, such as cardiovascular diseases, hypertension, heart disease, and DM were reported to be associated with executive dysfunction (Lowe et al. 1994; Schillerstrom et al. 2005). Both depression and cardiovascular diseases are risk factors for cognitive impairment (Austin et al. 2001; Barnes et al. 2006), but the various neuropsychological mechanisms underlying late-life depression can lead to different patterns of cognitive impairment (Crocco et al. 2010). Based on these findings, physicians may be able to find occult depression or cardiovascular disease by carefully evaluating the patient’s cognitive functions. However, whether these symptoms are caused just by underlying cardiovascular diseases or are related to depression is unclear. In this study, we tried to clarify to what extent the executive function would be impaired in older elderly men with major depression with or without the comorbidity of cardiovascular disease. In addition, investigated and discuss whether the depression or cardiovascular disease or both are crucial in executive dysfunction.

Methods

Participants and procedures

This study was approved by the institutional review board of National Cheng Kung University Hospital. Participants were recruited from newly admitted residents of the Taiwan National Veterans’ Care Homes in Tainan and Kaohsiung. They had voluntarily applied for residency in these home care centers because they were living alone, in poor health, lacking family and social support, or physically handicapped. The majority were ambulatory, physically capable, and able to provide for their own daily needs with no assistance from others. Only a few were physically disabled and required a wheelchair, cane or other ambulatory equipment, or needed other assistance.

Three hundred thirty-five residents, who had completed health examinations between 2004 and 2008 at clinics affiliated with the Veterans’ Care Home, volunteered for this study. The study procedures were fully explained, and written informed consent was obtained from all.

The inclusion criteria were: (1) 75 years old or older, (2) male gender, (3) able to speak Mandarin or Taiwanese, and (4) capable of verbal communication. For the group with late-life depression (LLD), those with a diagnosis of current major depressive disorder were recruited. For the group with cardiovascular disease (CVD), medical measures were completed by a physician based on the interviews and medical chart review. Those with hypertension, diabetes, coronary heart disease, cigarette smoking, atrial fibrillation, and left ventricular hypertrophy were classified as patients with CVD. Patients in the LLD + CVD group were diagnosed as having a current depressive disorder and cardiovascular disease. The exclusion criteria were factors that might interfere with the presentation of depressive symptoms: (1) a history of dementia or suspected dementia, (2) a current diagnosis of psychiatric disorders other than current major depressive disorder, (3) currently using antipsychotics or mood stabilizers, or (4) current substance abuse.

All participants were interviewed by an attending psychiatrist for an initial evaluation, and then by psychiatrists and psychologists using the mini-mental state examination (MMSE), the Geriatric Depression Scale (GDS), and the Mini-International Neuropsychiatric Interview (MINI). All the patients with major depression in their depressive symptom-free stage were given an antidepressant and a small dose of benzodiazepines. To increase inter-rater reliability, all the interviewers were intensively trained on how to use the interview instruments, and all the interviewers were closely supervised by two of the authors (RBL and YKY). All demographic data, medical charts, and histories of medical illnesses were reviewed, and then the results of the participants’ health examinations were analyzed. All participants were divided into four groups: healthy controls (HC), patients with CVD, patients with late-life major depression (LLD), and patients with major depression comorbid with cardiovascular diseases (LLD + CVD).

Measurements

We used the 30-item Chinese version of the MMSE (Guo et al. 1988) with a standardized norm to screen the participants. For those who had less than 2 years of education, the cutoff point score was 12/13; for those who had 3–9 years of education, the cutoff point score was 21/22; and for those who had more than 10 years of education, the cutoff point score was 23/24.

The Chinese version of the MINI was used to evaluate current major depressive episodes and other psychiatric diagnoses (Sheehan et al. 1998). The diagnostic criteria of the MINI are based on the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. The revised Chinese GDS was used to measure the severity of depression. The Chinese versions of the MINI and the GDS have been validated (Liao et al. 2000; Mui 1996).

Neuropsychological assessments

The WCST measures the ability to perform certain types of executive functions, including categorization, abstraction reasoning, maintain set, set switching, strategic planning, and modulate impulsive responding (Mohlman 2005). The test requires that certain cognitive functions be intact, for example, attention, working memory, and visual processing. Participants are required to try out different rules in order to find a correct method for sorting the cards. The test used cards that had to be sorted into piles in front of four stimulus cards. The participants were instructed to infer the matching principle from the feedback provided: “correct” or “incorrect,” depending on whether they guessed the rule correctly or not. The cards could be matched by number (1, 2, 3, or 4); color (yellow, green, blue, or red); or shape of the symbols (star, triangle, circle, or cross). The rule is applied for a run of trials and then changed without warning (Mei 1998). The inter-rater liability is 0.88–0.93, within-rater reliability is 0.91–0.96, and test–retest reliability is 0.57. Performance on the WCST was scored in terms of the total number of errors, perseverative errors, conceptual level response, number of categories completed (NCC), and trials to complete the first category (TCC) (Alexopoulos et al. 2005; Elderkin-Thompson et al. 2006; Elderkin-Thompson et al. 2004; Naismith et al. 2003, 2006; Nakano et al. 2008; Yuan et al. 2008).

Trail making test

The trail making test (TMT) (Lezak et al. 2004; Reitan 1958; Spreen and Strauss 1991) is a visuomotor task that consists of two parts; in part A, the participant was asked to draw lines to connect consecutively numbered circles on one worksheet, and then, in part B, to connect the same number of consecutively numbered and lettered circles by alternating between the two sets.

The instruction for both parts was to perform the test as correctly and as quickly as possible. The examiner has to point out errors made by the test as they occur so that the test can always complete the test without errors and the scoring can be based on time alone (Lezak et al. 2004). The time required to complete each task represents the relevant score. In contrast to part A, part B involves frequent switching between two mental sets. Because visual search and general motor speed are relevant for both parts of the test, calculating the difference in scores between parts A and B minimizes these interfering effects. The TMTB-A score is, therefore, well established as an instrument to assess executive functions with special emphasis on set shifting. While some researchers use the TMTB/A ratio for the same purpose (Arbuthnott and Frank 2000), a large-scale (n = 285) comparative assessment of the two scores yielded better discriminatory power of the TMTB-A score with respect to the detection of performance differences between young and elderly tests (Drane et al. 2002).

Results

Demographic data

All participants in the study were male. Their mean age was 81.23 ± 4.20, mean education level was 5.05 ± 4.65, and mean MMSE score was 24.43 ± 2.82. There were no significant differences in age between groups (F = 1.13, p = 0.34). Education levels (F = 5.34, p = 0.001) and MMSE scores (F = 2.92, p = 0.03) were significantly different, however. The post hoc showed that the CVD group had a significantly higher level of education (p = 0.001) and MMSE score (p = 0.045) than did the LLD + CVD group. The LLD and LLD + CVD groups had higher GDS scores than did the HC and CVD groups (p < 0.0005) (Table 1).

Table 1.

Demographic data

Groups Statistics
HC (n = 45) CVD (n = 157) LLD (n = 43) LLD + CVD (n = 90) F (p value) Post hoc
Age (years) 81.41 ± 3.89 81.02 ± 4.22 80.53 ± 3.28 81.80 ± 4.67 1.13 (0.34)
Education (years) 5.23 ± 4.01 5.93 ± 5.14 4.79 ± 3.98 3.53 ± 3.98 5.34 (0.001) CVD > LLD + CVD (p = 0.001)
MMSE score 24.73 ± 3.03 24.78 ± 2.55 24.35 ± 2.57 23.72 ± 3.16 2.92 (0.03) CVD > LLD + CVD (p = 0.045)
GDS 2.25 ± 1.87 2.44 ± 1.31 7.47 ± 1.81 6.83 ± 2.60 121.43 (<0.0005) LLD, LLD + CVD > HC, CVD (p < 0.0005)

Data are means ± SD

SD standard deviation, CVD elderly men with cardiovascular disease, LLD elderly men with late-life depression, LLD + CVD elderly men with late-life depression comorbid with cardiovascular disease, GDS Geriatric Depression Scale

Neuropsychological data

A significant difference in educational level as well as in the MMSE score were found among the four groups, and an effect of education in WCST was reported (Boone et al. 1993). Multiple analysis of covariate analysis was used to analyze differences in WCST and TMT scores (education levels and MMSE scores were controlled as covariate variables). The WCST scores were significantly different between groups. The post hoc analysis showed that overall, the HC group had the highest WCST scores, and that the LLD + CVD group had the lowest WCST and TMT scores. However, no significant differences were found between the CVD and LLD groups or between the LLD and LLD + CVD groups (Table 2). There were no significant differences in the TMT-A and TMT-B (because of their poorly sustained attention, only 195 participants completed the TMT-B) scores between groups.

Table 2.

Comparison of executive functions among four groups of elderly men

HC (n = 45) CVD (n = 157) LLD (n = 43) LLD + CVD (n = 90) MANCOVA (F, p value) Post hoca
TNE 58.84 ± 25.62 69.11 ± 19.02 74.91 ± 14.14 78.47 ± 17.43 F = 10.43, p < 0.0005 HC > CVD > LLD + CVD, HC > LLD
PE 38.18 ± 22.81 41.25 ± 22.40 40.63 ± 19.84 49.64 ± 25.22 F = 2.78, p = 0.04 HC > LLD + CVD, CVD > LLD + CVD
CLR 47.80 ± 25.06 37.54 ± 21.34 31.65 ± 18.72 24.81 ± 20.31 F = 11.85, p < 0.0005 HC > CVD > LLD + CVD, HC > LLD
NCC 3.07 ± 1.96 1.86 ± 1.57 1.19 ± 1.16 0.73 ± 1.04 F = 26.17, p < 0.0005 HC > CVD > LLD, LLD + CVD
TCFC 41.82 ± 42.03 55.69 ± 46.32 76.69 ± 44.58 88.67 ± 48.27 F = 13.59, p < 0.0005 HC > LLD, HC > LLD + CVD
TMT-A 112.20 ± 83.87 124.59 ± 77.38 120.19 ± 36.63 140.40 ± 74.22 F = 1.07, p = 0.36
TMT-B 245.29 ± 140.02 268.98 ± 112.07 261.81 ± 63.72 303.97 ± 108.74 F = 1.81, p = 0.15

Data are means ± standard deviation (SD).

MANCOVA multiple analysis of covariate analysis, CVD elderly men with cardiovascular disease, LLD elderly men with late-life depression, LLD + CVD elderly men with late-life depression comorbid with cardiovascular disease, TNE total number of errors, PE perseverative errors, CLR conceptual level response, TCC trials to complete the first category

aThe direction shows the performance from better to worse.

Discussion

The association between depression and cognitive impairment agrees with previous studies (Austin et al. 1992; Merriam et al. 1999). Cardiovascular risk factors, such as hypertension and diabetes, are associated with poorer neuropsychological functioning as well as with increased rates of cognitive decline (Elias et al. 2004; Sims et al. 2008). In addition, the depressed elderly with executive dysfunction are more likely to have cardiovascular comorbidity (Rapp et al. 2005). However, whether the executive dysfunction is caused by depression or cardiovascular disease is unclear.

We found that the LLD + CVD group had the worst performance among the four groups, which is consistent with previous reports (Elderkin-Thompson et al. 2009; Gianaros et al. 2006; Hoshi et al. 2010) that the depressed elderly with executive function deficits often have cardiovascular disease. However, a significant difference was found between the CVD and LLD groups, which implied the influence of late-life depression rather than cardiovascular comorbidity in the elderly. Although only the NCC Index was reported, for the other indices of the WCST, the CVD group performed significantly better than did the LLD + CVD group, but there was no difference between the LLD and LLD + CVD groups. It could be that depression and cardiovascular disease may have a similar pathogenesis, such as neuroendocrine, inflammatory process, autonomic dysregulation, platelet abnormalities, unhealthy behaviors, and certain vulnerability genes (Hoshi et al. 2010; Carney et al. 2002; McCaffery et al. 2006) all of which may lead to executive function deficits (Oxenkrug 2007) and to a cumulative effect of comorbidity on the degree of cognitive deficit (Sheline et al. 2006; Smith et al. 2007).

Nevertheless, although the four groups performed significantly differently on the WCST, there were no significant differences in the performance of TMT tasks, which indicated that there were no differences in attention between the four groups of elderly men in our study. Attention deficits are reported (Rapp et al. 2005) in the depressed elderly, but neither the severity of those deficits nor the comorbidity with cardiovascular disease were evaluated. In addition, while the TMT tasks assess attention and visuomotor processing speed, they also demand mental flexibility (Reitan 1958). The participants in our study were more than 75 years old, and some had cardiovascular disease, which may have influenced their task performance. In addition, although the participants wore glasses, most of them had bad corrected eyesight, which also may have influenced their performance in tasks that demand speed.

We found evidence that cardiovascular comorbidities worsened the executive function in the LLD groups; however, there was no significant difference in executive function performance between the CVD and LLD groups. It could be that both depression and cardiovascular disease are associated with frontal lobe dysfunction and the development of cognitive impairment (Elderkin-Thompson et al. 2009; Gianaros et al. 2006; Hoshi et al. 2010). In addition, the subtypes and the severity of cardiovascular disease could be other confounding factors, a possibility that needs confirmation. Moreover, the CVD group had more education than did the other three groups, which might be the reason for their slower decline in cognitive performance than the LLD + CVD, but this needs further investigation. The effect of education on WCST scores was reported to be non-significant (Shan 2008), but the authors did not take the illiterate elderly into account when calculating the norm. In addition, the education effect on the WCST for the illiterate elderly with depression or cardiovascular disease deserves further investigation. Moreover, only older men were studied in our study, which prevents its findings from being generalized to all elderly groups. Further, because in the present study only the WCST and TMT were used to measure executive function and inconsistent impairment were found for the both tests, we are unable to generalize our findings on executive impairment in the depressed elderly with comorbid cardiovascular disease.

Depression that occurs in late life is often considered to be an “organic model” of depression (Baldwin and Tomenson 1995) and a major health problem that causes executive function dysfunction. Psychiatrists often pay more attention to this type of depression because it frequently could be a secondary disorder associated with a treatable underlying medical illness. Identifying the risk factors of cardiovascular disease in those with depression and discriminating the dysfunctional executive function between depression and cardiovascular disease may provide evidence of an organic etiology for depression; such symptoms should prompt psychiatrists to conduct additional examinations to check for possible cardiovascular illnesses.

Acknowledgments

This work was supported in part by grant VGHKS99-101 from the Kaohsiung Veterans General Hospital, Taiwan (to YCK) and by the National Cheng Kung University Project for Promoting Academic Excellence and Developing World Class Research Centers (to RBL).

Disclosure The study was approved by the ethical committee of the National Cheng Kung University in accordance with the Declaration of Helsinki. Written informed consent was obtained from all participants before the experiment. For all authors, there is no actual or potential conflict of interest.

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