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Article

Information Recognition and Recall in Older Adults Bearing Vascular Risk Factors with or without Diagnosis of Mild Cognitive Impairment

by
Glykeria Tsentidou
1,2,3,*,
Despina Moraitou
1,2,3,
Elvira Masoura
1,
Panayiota Metallidou
1,
Efstathios Papadopoulos
4,
Vasileios Papaliagkas
5 and
Magda Tsolaki
2,3,5
1
Laboratory of Psychology, Department of Experimental and Cognitive Psychology, School of Psychology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
2
Greek Association of Alzheimer’s Disease and Related Disorders (GAADRD), 54248 Thessaloniki, Greece
3
Laboratory of Neurodegenerative Diseases, Center for Interdisciplinary Research and Innovation (CIRI), AUTh, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
4
Laboratory of Evaluation of Human Biological Performance, Department of Physical Education and Sports Science, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
5
Department of Biomedical Sciences, School of Health Sciences, International Hellenic University, 57001 Thessaloniki, Greece
*
Author to whom correspondence should be addressed.
J. Dement. Alzheimer's Dis. 2024, 1(1), 72-86; https://doi.org/10.3390/jdad1010005
Submission received: 1 August 2024 / Revised: 3 September 2024 / Accepted: 16 September 2024 / Published: 23 September 2024
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Abstract

:
Episodic memory is affected early and is a basic indication of neurodegeneration especially for Alzheimer’s disease. The aim of this study was to examine whether adults with vascular risk factors are differentiated in their episodic memory performance from individuals with mild cognitive impairment (MCI). The episodic memory of adults diagnosed with MCI, adults with vascular risk factors (VRF; blood pressure, diabetes mellitus, or hypercholesterolemia), and healthy controls was assessed using the Doors and People test. Statistical processing included mediation analyses which were performed separately for the VRF and healthy control groups, and the MCI and healthy control groups. ANOVA was used for the MCI and VRF groups which were matched in age and education. ANOVA showed that the MCI adults had significantly lower performance than the VRF adults in verbal recall only, F (1, 83) = 9.541, p = 0.003, and ηp2 = 0.10. A direct effect of diagnosis on verbal recall was found via mediation analysis as concerns individuals with MCI and healthy controls, b = 0.506, SE = 0.128, p < 0.001, and 95%CI: 0.221–0.771, in favor of the healthy controls. Concerning the VRF and healthy groups, a tendency of diagnosis to directly affect verbal recall was shown (α = 0.005) in favor of the healthy controls, b = 0.388, SE = 0.150, p = 0.010, and 95%CI: 0.043–0.720. In conclusion, it is supported that patients with MCI present deficit performance in verbal recall; in addition, the diagnostic category affects all the groups’ performance on the same condition. These results indicated that the verbal recall aspect of episodic memory can be a sensitive indicator that can differentiate healthy adults from adults with mild cognitive impairment and vascular risk factors, as well as the two pathological groups from each other.

1. Introduction

The ability to encode and retrieve experiences is called episodic memory [1,2]. It enables people to recall and re-experience episodes associated with past spatial and temporal contexts [3]. Episodic memory is supported basically by the neural circuits of the medial temporal lobe, including the hippocampus, interacting with a large number of cortical and subcortical neural structures [2]. However, the studies of the past decade have explored frontal systems that mediate episodic memory, serving the functions of encoding and retrieval, and even indicating age-related health differences (white matter hyperintensities) [4]. It is suggested [5] that episodic memory performance could probably distinguish between normal aging and a progression towards dementia up to 6 years prior to dementia onset. Based on such findings, subsequent studies have attempted to shed light on episodic memory in mild cognitive impairment [6], namely the pathological entity referring to older adults with mild cognitive deficits but no dementia [7], and even in the earlier stages of cognitive decline, subjective cognitive impairment [8]. It is well known that a percentage of MCI adults eventually progress to Alzheimer’s disease dementia (ADD), whereas a smaller percentage progresses to vascular dementia [9]. Researchers [10] suggest that vascular risk factors, such as diabetes mellitus, hypercholesterolemia, hypertension, obesity, and cigarette smoking history, usually lead to vascular pathology and are related to episodic memory decline. Moreover, it is generally stated that vascular health is a commonly known predictor of cognitive variability in aging [11]. In combination with the above, it is considered that vascular risk factors are associated with aging and are linked to a decrease in cognitive domains and memory capacities [10,12,13]. Based on all the above, the present study deals with episodic memory performance in adults with vascular pathology compared to MCI adults’ performance and to healthy controls.
Reviewing the literature on episodic memory, the great work that has been carried out in recent years is evident. Several reasons contribute to this; firstly, episodic memory is affected by various brain disorders such as frontal lesions, cerebrovascular accidents, traumatic brain injuries, and dementia [10,14,15,16]. It also impacts extensive brain areas [17], significantly affecting everyday functioning in patients [18]. More specifically, several previous studies have examined how episodic memory has been affected by aging—deficits are manifested over 60 years [19]. It has also recently been explained that it is mediated by medial temporal fibers which seem to be involved in neural signals across the lifespan of older adults [20]. The atrophy of the medial temporal lobe is a hallmark of the most common neurodegenerative diseases [21,22] related to dementia with primary deficits in episodic memory, which is typically affected early in the neuropathological changes associated with Alzheimer’s disease [10]. Gray matter atrophy, cortical thinning, and reduction in the hippocampal volume are also associated with memory impairment in the AD spectrum [23]. There is a discussion on the importance and the correlation of AD biomarkers and age in episodic memory decline that hippocampal atrophy is the main predictive factor for memory decline in older adults, while Aβ in cerebrospinal fluid reaches the same outcome in slightly younger old adults [24]. Concerning MCI and the correlation with impaired episodic memory, fMRI studies have revealed that important effects on brain activity occur in the medial temporal lobe, the frontal and prefrontal cortex, the posterior cingulate cortex, and the inferior parietal cortex; these are the brain areas that mediate episodic memory [25,26].
Additionally, low episodic memory performance has been linked to vascular changes [27]. A recent study [28] concluded that the medial temporal lobe is affected by elevated blood pressure and hypertension, resulting in AD pathogenesis. On the other hand, blood pressure is also related to the development of vascular cognitive impairment, cognitive changes, and memory complaints, not due to dementia [29] but rather due to subcortical ischemic vascular disease. In particular, additional vascular risk factors affecting episodic memory changes are diabetes mellitus, hypercholesterolemia, obesity, and cigarette smoking [10]. The authors claim that while a lot of research has been conducted on how vascular factors affect episodic memory, there is no clear evidence of these changes in adults with subjective memory impairment [10].
The controversy over episodic memory impairment and subjective memory complaints has also been shown by imaging studies. Some cases [30,31] supported the case of hippocampal atrophy, while others rejected it [32]. In a study conducted in 2021, the researchers [17] attempted to explain these differences in the research data and have so far supported the case of two functional networks linked to memory performance: the default mode network [33,34] and the bilateral frontoparietal control network [35]. Based on previous findings [36,37], the authors suggested that the correlations of episodic memory performance with neural correlations in patients with neurodegenerative disease are more “robust”. It has been argued that the connection between structure and memory capacity was more crucial in the parietal and occipital lobes compared to the medial temporal lobe and frontal lobes [38,39].
Moreover, differences in episodic memory performance may occur because some studies use a composite score of episodic memory ability [40,41], while others focus on specific aspects such as verbal delayed recall, visual recognition, and discrimination [42]. A prior study [43] showed that recognition memory is typically found to be better preserved than recall in healthy aging. More recent studies with imaging findings have also confirmed the differentiation of the dimensions of episodic memory in neural brain areas [44,45,46]. Regarding this view, it seems that the prefrontal cortex has functional connections with the lateral and medial portions of the posterior parietal lobe. The medial temporal regions create a support network for recognition memory tasks [47]. On the other hand, they supported that the occipito-temporal areas, temporal areas, and the insular cortex assist in the visual and linguistic processing of words [46].
Considering the contrast between the previous research findings, the present study aimed to assess information recognition and recall in three different diagnostic groups of older adults: two pathological (MCI and VRF) groups and one group of healthy adults. The study attempted to shed light on the modification in the recall and recognition of visual and verbal memory. According to the study design, two hypotheses were examined: (a) adults with VRF diagnosed with MCI would perform worse compared to the other groups, at least in some conditions, such as the “recall” conditions; (b) regarding the group of adults with vascular risk factors (VRFs) without MCI, the hypothesis was that their performance would be higher than that of individuals with MCI and would be lower from that of healthy controls, at least in the ”recall” conditions.

2. Materials and Method

2.1. Participants

We recruited a total of 109 adults from “Alzheimer Hellas” memory centers in Thessaloniki, Greece, from the outpatient clinics of the General Hospital of Katerini, Greece, and a representative sample of healthy adult volunteers from the wider community of Pieria (N: 24 males, 85 females). Their age ranged from 50 to 85 years (M = 66.09, S.D. = 9.02). The sample did not include adults with mood and/or anxiety disorders, neurological disorders of any type, dementia of any type, cancer patients diagnosed in the last five years, adults after stroke, myocardial infarction, and cardiac instabilities. All the participants were screened for depressive symptomatology using the Geriatric Depression Scale-15 [48,49], and persons with scores >6 were excluded from the study. To assess the ability of simple and complex sentence comprehension, we used the subscale “auditory perception” from the Boston Diagnosing Aphasia Examination [50]. To assess general cognitive ability, the MoCA was selected [51,52,53].
In detail, the first group consisted of 44 adults (9 men and 35 women, Mean Age = 70.2, and S.D. = 7) diagnosed using the Petersen criteria [54] with MCI during the last two years; 15 of them were diagnosed by a special neurologist at the General Hospital of Katerini and the other 29 were diagnosed by a specialized group of neurologists and neuropsychologists at the “Alzheimer Hellas” center in Thessaloniki. To meet the strict criteria of the study, all the MCI adults were re-assessed for their general cognitive ability and specific cognitive functions using extensive neuropsychological assessment to exclude comorbidities. It is emphasized that all the patients reported complaints of memory difficulties. According to the evaluations of physicians and the neuropsychological examination, the vast majority (over 80%) of the MCI participants were of the amnestic type with multiple domains. More importantly, it is underlined that 35 MCI adults had at least one diagnosed vascular risk factor (hypertension, hyperlipidemia, or diabetes mellitus) and were under medication. However, we did not have information about VRF for nine participants with MCI. Regarding the educational level, 11 participants had a low level of education (0–9 years), 17 had a medium level (10–12 years), and 16 were highly educated (13 years and over). It is important to note that education was measured based on the exact number of years of schooling.
The second group consisted of older adults from outpatient clinics at the General Hospital of Katerini, without a diagnosis related to cognitive decline, who were under medical supervision and medication due to vascular risk pathology (n = 41, 9 men and 32 women, Mean Age = 68.6, and S.D. = 7). Their hematology test taken the previous year reported at least one of three common vascular risk factors (hypertension, hyperlipidemia, or diabetes mellitus). Exclusion criteria comprised the diagnosis of MCI or dementia of any type and all the reference criteria described above, which were observed for all the groups. Their general cognitive status, as measured by the MoCA [53], ranged from 25 to 30 (M = 26.7, and S.D. = 1.4). Their educational level varied; 19 participants had a low educational level, 9 had a medium one, and 13 were highly educated.
According to the aim of the study, the control group consisted of healthy community-dwelling adult volunteers with excellent physical and mental health, who were asked not to receive any medication and whose hematological check-ups in the last six months did not show any VRF. Moreover, it is noted that the participants did not report memory complaints; this was examined using one question regarding whether the participants felt their memory to be worse than five years ago, to which they could reply “yes” or “no”. Τo meet this requirement, the third group consisted of younger adults (middle-aged, M = 54.25, and S.D. = 3.0). From the adults in this group, only 2 participants had a low educational level, 12 had a medium educational level, and 10 were highly educated. Their MoCA score ranged from 26 to 30 (M = 27.7, S.D. = 1.3).
Based on the criteria for admitting groups, as presented above, and aiming to instigate the assumption of whether the three groups differ from each other in terms of their demographic characteristics, ANOVAs were performed, as regards age and education. Hence, the three groups differ significantly in age, F (2, 108) = 52,403, p < 0.001, and in years of schooling, F (2, 108) = 4150, p = 0.018. No difference arose in the gender of the participants, χ2 (2, 1) = 0.187 p = 0.911, although it should be noted that the female gender was overrepresented in all the groups.
Reviewing the differences in the groups, it turned out that the healthy controls were younger compared to the MCI participants, I–J = −15.955, p < 0.001, and to the VRF adults, I–J = −14.360, p < 0.001, respectively. The control group tended to have a slight differentiation in education compared only to the adults with VRF, I–J = 2.829, p = 0.019. The MCI and VRF groups did not differ in age and education. The demographics of the three groups are shown in Table 1.

2.2. Procedure

The participants from Katerini (MCI, VRF adults, and healthy controls) were examined at the Day Care Center for Dementia Disease Patients at the General Hospital of Katerini, while the participants from Thessaloniki were examined at the two “Alzheimer Hellas” Centers. In addition, it is underlined that the same author completed the process of allocating the participants in each group based on medical examinations and diagnoses, medication, comprehensive medical history, and neuropsychological tests, as mentioned before. The assessments were completed in two sessions; in the initial meeting, all the adults were evaluated using the selected tools for screening, as described above. Moreover, a comprehensive medical history of their health status was obtained. In the second session, the participants were assessed for their memory. They were also assessed for working memory capacity and prospective memory. However, this is not taken into consideration for the purposes of the present study. Short breaks were included between the different tests.

2.3. Instruments

Doors and People Test

The Doors and People test was designed to distinguish between visual and verbal memory, as well as between recall and recognition. The terms “visual” and “verbal” refer to the encoding rather than the modality of presentation, and the distinctions between recall and recognition refer to the retrieval, and arise from observations among patients, who perform worse on recall than recognition [55]. It includes four subtests assessing recall and recognition for both verbal and visual information, which are thought to be comparable in terms of difficulty.
In the first condition called the Verbal Recall—People subtest, the aim is for the examinee to memorize and remember the names and occupations of 4 people following the display of photographs. The instructions for the examinee are as follows: “I will ask you to find out the names of 4 people: a doctor, a merchant, a postman and a swimmer. I will show you 4 photos of these people which indicate their name and occupation. I would like you to remember the name of each person”. After the photographs of the four characters are presented and the requested information is read aloud, the examinee is asked to recall the associated name by answering the question “What is the name of the doctor?”. The procedure can be repeated a maximum of 3 times until the examinee correctly recalls all the requested names. One point is given for the correct forename, one point for the correct last name, and one point for each correct pairing, with a maximum total score of 36 for this condition. Delayed recall of the names was assessed after the administration of the visual recognition subtest. The examinee is asked to recall the names of the characters as indicated at the beginning, following the question “e.g., Could you remember the doctor’s name?”. It is mentioned that for the purposes of the present study, only delayed verbal recall was assessed, scoring from 0 to 12, according to the procedure described above. The aim was to measure the effects of potential interference in the recall process and not of simple coding [56].
Visual recognition—Doors subtest includes 27 photos of colored doors (three of them are given as examples to practice; the rest are divided by 12 into two graded difficulty conditions). In addition to the 24 target doors, there are 81 distractor doors. The process is as follows: the examinee is shown 12 target doors for 3 s each, and then, they are asked to identify each target door, among three others—distractors. In the first 12 doors (condition A), the distractor doors are very different from the target one (a garage door, a stable door, and a church door). In the second condition, they are the same type of target doors with only minor changes. One point is awarded for each correct response with a maximum total score of 24.
Visual Recall—Shapes subtest—The instructions are “You will be presented with four simple line drawings. You have to observe each one for 5 s and then remember it by heart”. The procedure is repeated a maximum of 3 times until all four shapes are recalled correctly. The maximum score for each shape is 3; one point for the features at the shape edges, one point for the centerpiece, and one for the total correct shape. Scores for the three trials are combined as for the verbal recall subtest. Delayed visual recall of the shapes is requested a few minutes later. It is noted that for the purposes of the present study, only the delayed visual recall (scoring: 0–12) condition was taken into account [56].
Verbal Recognition—Participants are presented with 27 forenames and surnames (three of which are given as examples to practice and the rest are divided by 12, into male and female names). Each name is displayed for 3” and participants are asked to read them aloud. The 12 target names are read, and lists are presented with the target name along with three distractor surnames. The purpose of the trial is to recognize the correct surname, as presented at the initial stage. One point is awarded for each correct response, giving a total score of 24.
Summarizing, the tool provides four variables: verbal recall (delayed), Verbal Recognition, visual recall (delayed), and visual recognition. The strength of this test is that no floor or ceiling requirements are reported [1], while the authors consider it “ecologically” meaningful, as also supported by the Greek version [56]. The Doors and People test is sensitive to the effects of various neurological impairments and has the advantage to evaluate several types of memory [1]. It is reported that the test is a reliable measure of memory with high internal reliability, Cronbach’s alpha = 0.80, and it is both a good research tool and a reliable clinical test assessment [56].

2.4. Ethics Statement

For the purposes of the study, the participants provided written informed consent at the time of their first visit, agreeing to their volunteer participation and their withdrawal at any time, without providing a reason and without cost. The present study is part of the cross-sectional study of the first author’s (Glykeria Tsentidou) doctoral dissertation. The protocol of the study was approved by the Scientific and Bioethics Committee of the Greek Association of Alzheimer’s Disease and Related Disorders (Scientific Committee Approved Meeting Number: 25/21-06-2016) and followed the principles outlined in the Helsinki Declaration of 1975, as revised in 2008. Moreover, the study was approved by the Hellenic Data Protection Authority, License number: 1971.

2.5. Statistical Analysis

Because the MCI and VRF groups were matched in age and education, ANOVAs were performed to find the differences in the two diagnostic groups in memory performance in the different subtypes. As regards the differences in these two groups (MCI and VRF) in age and in education (only VRF) from the healthy controls, mediation analyses were conducted. Mediation analysis declares how a prognostic variable is related to an outcome variable, indicating that the relationship between the two variables is affected by a third variable called a mediator [56,57]. Direct and indirect effects emerge from mediation analysis. Direct effect is defined as the relation between the predictor variable and the outcome variable. Indirect effect is considered the effect of the predictor on the outcome through the mediator [57,58].
Mediation analysis in the Structural Equation Modeling context (path models including mediators) was used in this study (JASP 16) [59] to examine whether the diagnostic group (the predictor) directly or/and indirectly affects performance in memory in its aspects. As regards the formulation of the mediation models, the theory of the “vascular hypothesis of cognitive aging” [11,60] claims that age is only a descriptive index associated with cognitive decline due to the fact that vascular pathology and neurodegenerative conditions increase as one becomes older. Hence, there is no age as a numeric index that causes cognitive decline. It is the biological pathology behind age which increases as one grows older. The same pathologies (vascular or/and neurodegenerative) could set limits on the compensatory function of cognitive reserve in cognitive decline. Thus, the role of education as an important dimension of cognitive reserve could be limited by these pathologies. Based on this theoretical background, we considered “diagnosis” as the predictor variable in our mediation models, since it refers to the underlying pathology (vascular risk factors, VRFs and mild cognitive impairment, or none). In the same vein, age and education were considered as potential mediators, since they are factors that could be affected by the underlying pathology and simultaneously, they are typically associated with cognitive performance. Memory scores were set as the outcome variables.
The bootstrapping procedure was used to examine the significance of the indirect effect. Indirect effects were computed for each of the 1000 bootstrapped samples [61]. For the ANOVA and for correlation analysis conducted at the initial stage to examine prerequisites for mediation analysis, IBM SPSS Statistics (Version 24.0., IBM Corp, Armonk, NY, USA, 2016) was used [62].

3. Results

The mean of performance for each diagnostic group in all the subtests used in the current study is presented in Figure 1. It is obvious that verbal recall is the subtest that could differentiate the three groups.
As regards the MCI and VRF groups which were matched in age and education, the application of ANOVA, with diagnosis as the independent variable and verbal recall as the dependent variable, showed a significant difference in the delayed verbal recall performance, in favor of the VRF adults, F (1, 83) = 9.541, p = 0.003, and ηp2 = 0.10. These groups did not differ in the other subtests’ performance.

3.1. Prerequisites for Mediation Analysis—Correlations

Pearson correlations were computed to examine the relationships between age and education and the outcome variables (performance in the 4 subtests), while Spearman’s rank-order correlations were computed to investigate the relationships between diagnosis (predictor) and the other variables (potential mediators and outcomes).
The following tables show the respective correlations separately for (a) the VRF and healthy control groups, and (b) the MCI and healthy control groups.
As shown in Table 2, all the prerequisites for the mediation analysis are met for the VRF and healthy control groups, except for the case of visual recognition which does not correlate to diagnosis. At this point, it must be noted that the VRF and healthy controls were found to significantly differ in age and education.
As shown in Table 3, all the prerequisites for the mediation analysis are met for the MCI and healthy control groups, except for the case of visual recognition which does not correlate to diagnosis. It must be noted that the MCI and healthy controls were found to significantly differ in age only.

3.2. Mediation Analyses

Ιn the subsequent analyses, diagnosis was defined as the predictor, each subtest’s performance was defined as the outcome variable, and age and education (in the 2nd mediation model only) were the mediators. Mediation analyses were performed separately for (a) the VRF and healthy control groups, and (b) the MCI and healthy control groups.
As concerns the comparison between VRF and healthy controls in verbal recall, the mediation analysis showed that the direct effect of diagnosis on performance is different from zero, b = 0.798, SE = 0.309, p = 0.010, and 95%CI: 0.147–1.489. At this point, it is important to clarify that 10 variables were measured; 4 for the first group comparison and 3 for each of the other two group comparisons (the visual recognition variable was not included in the mediation models); therefore, the significance level has been adjusted to p = 0.05/10 = 0.005 to avoid type 1 error. Hence, the direct effect of diagnosis on verbal recall, in favor of the healthy controls, can be seen as a trend. On the other hand, neither a significantly different from zero indirect effect via age was found, b = 0.309, SE = 0.289, p = 0.286, and 95%CI: −156–0.853, nor a significant indirect effect via education, b = 0.121, SE = 0.098, p = 0.218, and 95%CI: −0.023–0.346 (Figure 2).
Moreover, Verbal Recognition was not directly, b = −0.003, SE = 0.340, p = 0.992, 95%CI: −0.797–0.711, or indirectly, via age, b = 0.545, SE = 0.321, p = 0.089, 95%CI: −0.136–1.390, or education, b = 0.181, SE = 0.116, p = 0.118, 95%CI: 0.016–0.498, affected by diagnosis. In terms of visual recall, no significant results were found for the direct effect, b = −0.043, SE = 0.356, p = 0.904, 95%CI: −0.699–0.929; or for the indirect effects, for age and education, respectively: b = 0.484, SE = 0.335, p = 0.148, 95%CI: −0.402–1.181, b = 0.147, SE = 0.114, p = 0.197, 95%CI: −0.031–0.487.
As concerns the MCI and healthy control groups, the mediation analysis showed that the direct effect of diagnosis on verbal recall performance is significantly different from zero, b = 1.696, SE = 0.421, p < 0.001, 95%CI: 0.870–0.2522. Moreover, there was a slight tendency of age to mediate the effect of diagnosis on verbal recall, b = 0.671, SE = 0.338, p = 0.047, 95%CI: 0.008–1.334 (Figure 3).
Concerning the performance in Verbal Recognition and visual recall, no significant direct and indirect effects were found: b = 0.624, SE = 0.670, p = 0.352, 95%CI: −0.690–1.938, b = 0.748, SE = 0.533, p = 0.160, 95%CI: −0.297–1.793 for Verbal Recognition; b = 0.432, SE = 0.314, p = 0. 169, 95%CI: −0.183–1.047, b = 0.445, SE = 0.250, p = 0. 075, 95%CI: −0.045–0.935 for visual recall.

4. Discussion

The study examined memory through the four subtypes of it (verbal recall/Verbal Recognition, and visual recall/visual recognition), as assessed by the tool Doors and People, in two different diagnostic groups (a. adults with vascular risk pathology and b. adults with vascular risk factors and mild cognitive impairment) compared to a control group of healthy adults.
From the inspection of the mean performances (Figure 1), it seems that there are some differences in the performance of the three groups. Specifically, the MCI participants showed the worst performance in the verbal recall subtest, but they displayed almost the same performance in the others as that of the VRF group. The healthy controls, as expected, showed the highest scores in all the subtests.
According to the first hypothesis of the study, individuals diagnosed with MCI would perform worse compared to the other groups, at least in some aspects of memory and mainly in the “recall” aspects. Based on the mediation analysis, the hypothesis is partially confirmed, since only delayed verbal recall was able to differentiate the MCI adults from the other two groups. Several previous studies have shown that episodic memory is affected in MCI due to the common areas impacted [39] by preclinical characteristics predisposed to Alzheimer’s disease, such as hippocampal atrophy [63], β-amyloid deposits [64], and tau neurofibrillary tangles [65]. It could be argued that due to such brain lesions, individuals diagnosed with MCI show this “special” decline in delayed verbal recall which presupposes the successful handling of interference [55] and may be more demanding than simple coding (immediate recall) or recognition, at least for this type of pathology. Moreover, the association of MCI diagnosis with more advanced age can explain the mediating role that chronological age tends to play in the relationship between diagnosis and verbal recall performance when MCI and healthy adults are compared. Based on the new concept of Geroscience [59], age could reflect additional pathologies related to the aging process, which the MCI underlying pathology cannot capture.
Regarding the second hypothesis of the present study, it was assumed that adults with VRF would perform higher than individuals with VRF diagnosed with MCI, and would also perform lower than healthy controls, at least in specific aspects of memory and mainly in the “recall” aspects. Based on the mediation analysis, this hypothesis was also partially confirmed, since VRF outperformed MCI only in verbal recall, in which they showed a trend of lower performance compared to healthy controls. Several studies [66] have argued that vascular risk factors, notably diabetes mellitus, hypercholesterolemia, hypertension, being overweight/obese, and cigarette smoking history, are highly and negatively correlated with episodic memory performance. It has been shown that white matter abnormalities [67] and small vessel disease [68] develop in adults bearing vascular risk factors. Hence, any differences in performance between adults with VRF and healthy controls indicate the relative brain pathology of the VRF group as a result of their vascular pathology. At this point, it is underlined that the MCI participants also had vascular risk factors (diabetes mellitus, hypercholesterolemia, or hypertension). Therefore, in addition to the alterations that are based on AD pathology—hippocampal atrophy and β-amyloid deposits—MCI adults seem to be affected by lesions due to vascular pathology as well. Hence, their impairment could be due to both AD pathology and vascular pathology that can act additively. Moreover, vascular pathology may function as the substrate for the development of AD pathology [66,67].
Regarding the specific aspect of memory that was found to be affected by diagnosis, that is, verbal recall, it has been stated that it requires semantic organizational strategies to support the learning of the associations between names and occupations [69]. According to the same study [69], this seems to be performed by the frontal lobe and may not apply to visual recall. As regards specifically delayed verbal recall, it has been argued that reduced performance in verbal retrieval in MCI adults is attributed to their inefficient use of memory strategies [70]. Moreover, a PET study [71] indicated increased activation in the anterior cingulate in MCI individuals when they were asked to recall newly learned objects without semantic support, a fact that confirmed that such tasks pose additional demands on the patients. In the same vein, vascular risk factors are associated with worse executive function, verbal fluency, abstract reasoning, and attention [72].
In terms of the difference between recognition and recall, fMRI studies have shown that recognition has been linked to activation in multiple brain regions—(para)hippocampus and perirhinal cortex in the medial temporal lobe, parts of the prefrontal cortex, the thalamus, and the parietal cortex. In recall, on the other hand, the prefrontal cortex, precuneus, and visual cortex are activated via the hippocampus. [73,74,75,76,77,78,79,80]. It had already been explained, since 1998, [81] that recall is generally more difficult than recognition, indicating significant similarities between the two types of retrieval, such as the mediation of the frontal areas. The frontal areas, however, were ultimately differentiated into “far frontal” for recognition and more posterior frontal poles for recall.
Hence, from the findings of the present study, it turns out that the delayed verbal recall aspect of memory is a key element that should be assessed in vascular and neurodegenerative disorders, as it seems to be affected and decreased already from the early stages of the diseases’ progression. Verbal recall, as measured by the ‘Doors and People’ tool, may be revealed as a sensitive and reliable criterion for the differentiation of healthy adults, adults with vascular risk factors without MCI diagnosis, and adults with VRF and MCI diagnosis, as verbal recall performance can clearly reflect progress in the underlying brain pathologies.

Limitations

The study has limitations. In the present study, there were no imaging examinations of the participants; hence, neither silent brain infarctions can be excluded, nor can vascular lesions be confirmed. In addition, there were nine participants of the MCI group who did not give information about their VRF condition; while there is no detailed history of the evolution and course of patients with vascular pathology beyond one year. It is also noted that the first author, who is the only examiner, was not blinded to the clinical diagnosis of the three groups.

5. Conclusions

The study aimed to examine memory in two pathological groups (adults bearing VRF without and with MCI diagnosis) and healthy controls using the Doors and People tool. The results showed that the (delayed) verbal recall aspect of memory seems to be associated with two different types of brain pathology: Alzheimer’s disease and vascular pathology.
Therefore, verbal recall appears to be a strong candidate criterion for the diagnosis of adults with vascular pathology or/and neurodegenerative disorders, and worth further examining its usefulness as a clinical tool.

Author Contributions

G.T. designed the study under the supervision of D.M., examined all the participants, and participated in the statistical processing of the data and the writing of the manuscript. D.M. closely supervised all the phases of the study, which is a part of the cross-sectional study of the doctoral dissertation of G.T.; E.M. translated and standardized the Greek version of the Doors and People test which was selected for the purpose of the study. P.M. supported the writing of the study. E.P. treated the adults with vascular burden. V.P. provided guidance throughout the study and writing of this article. M.T. supported the study with general supervision, useful suggestions, and sample recruitment and diagnosis. All authors have read and agreed to the published version of the manuscript.

Funding

The study is funded by the State Scholarship Foundation of Greece co-funded by the EU: plan “Human resource development, Education and Lifelong Learning (2014–2020)”; and an action entitled “Scholarship Program for Postgraduate Studies”, with code OPS5003404.

Institutional Review Board Statement

The study’s protocol was approved by the Scientific and Bioethics Committee of the Greek Association of Alzheimer’s Disease and Related Disorders (Scientific Committee Approved Meeting Number: 25/21-06-2016) and followed the principles outlined in the Helsinki Declaration of 1975, as revised in 2008. Moreover, the study has the approval of Hellenic Data Protection Authority, license number: 1971.

Informed Consent Statement

The participants gave written informed consent at the time of their visit.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

There are no conflicts of interest to declare.

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Figure 1. Mean scores for all the subtests of the Doors and People tool for the three diagnostic groups. (* p < 0.005).
Figure 1. Mean scores for all the subtests of the Doors and People tool for the three diagnostic groups. (* p < 0.005).
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Figure 2. Path model indicating the direct and indirect effects of diagnosis on memory subtests’ performance in the VRF and healthy control groups. * p = 0.01; the paths that indicate significant associations are marked with *.
Figure 2. Path model indicating the direct and indirect effects of diagnosis on memory subtests’ performance in the VRF and healthy control groups. * p = 0.01; the paths that indicate significant associations are marked with *.
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Figure 3. Path model indicating the direct and indirect effects of diagnosis (MCI and healthy controls) on memory subtests’ performance. * p < 0.001; the paths that indicate significant associations are marked with *.
Figure 3. Path model indicating the direct and indirect effects of diagnosis (MCI and healthy controls) on memory subtests’ performance. * p < 0.001; the paths that indicate significant associations are marked with *.
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Table 1. Mean Age, years of schooling, and gender representation for the three groups.
Table 1. Mean Age, years of schooling, and gender representation for the three groups.
GroupsMCI (n = 44)VRF (n = 41)Healthy Controls (n = 24)
Mean Age70.2 (S.D. = 7) **68.6 (S.D. = 7) **54.2 (S.D. = 3) **
Mean of Education Years11.4 (S.D. = 3)10.1 (S.D. = 4) *13 (S.D. = 3) *
Men/Women9/359/326/18
** p < 0.001. * p < 0.05.
Table 2. Correlations between diagnosis, outcome variables, and potential mediators for VRF adults and healthy controls.
Table 2. Correlations between diagnosis, outcome variables, and potential mediators for VRF adults and healthy controls.
Verbal RecallVerbal RecognitionVisual RecallVisual RecognitionAgeEducation
Diagnosis0.569 **0.349 **0.330 **0.227−0.792 **0.318 **
Education0.433 **0.482 **0.416 **0.355 *−0.628 **
Age−0.598 **−0.512 **−0.459 **−0.386 **
** p < 0.01. * p = 0.05.
Table 3. Correlations between diagnosis, outcome variables, and potential mediators for the MCI adults and healthy controls.
Table 3. Correlations between diagnosis, outcome variables, and potential mediators for the MCI adults and healthy controls.
Verbal RecallVerbal RecognitionVisual RecallVisual RecognitionAge
Diagnosis0.685 **0.361 **0.498 **0.237−0.798 **
Age−0.670 **−0.383 **−0.486 **−0.238
** p < 0.01.
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Tsentidou, G.; Moraitou, D.; Masoura, E.; Metallidou, P.; Papadopoulos, E.; Papaliagkas, V.; Tsolaki, M. Information Recognition and Recall in Older Adults Bearing Vascular Risk Factors with or without Diagnosis of Mild Cognitive Impairment. J. Dement. Alzheimer's Dis. 2024, 1, 72-86. https://doi.org/10.3390/jdad1010005

AMA Style

Tsentidou G, Moraitou D, Masoura E, Metallidou P, Papadopoulos E, Papaliagkas V, Tsolaki M. Information Recognition and Recall in Older Adults Bearing Vascular Risk Factors with or without Diagnosis of Mild Cognitive Impairment. Journal of Dementia and Alzheimer's Disease. 2024; 1(1):72-86. https://doi.org/10.3390/jdad1010005

Chicago/Turabian Style

Tsentidou, Glykeria, Despina Moraitou, Elvira Masoura, Panayiota Metallidou, Efstathios Papadopoulos, Vasileios Papaliagkas, and Magda Tsolaki. 2024. "Information Recognition and Recall in Older Adults Bearing Vascular Risk Factors with or without Diagnosis of Mild Cognitive Impairment" Journal of Dementia and Alzheimer's Disease 1, no. 1: 72-86. https://doi.org/10.3390/jdad1010005

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