S.-W. Peng1, C.-Y. Wang2, S.-Y. Lin3, Y.-L. Lee4,5, Y.-C. Lin3,7, Y.-J. Lin6,8, P.-N. Wang8,9,10
1. Department of Neurology, Keelung Hospital, Ministry of Health and Welfare, Keelung, Taiwan; 2. Department of internal medicine, Pingtung Veterans General Hospital, Pingtung, Taiwan; 3. Department of Neurology, Taipei Municipal Gan-Dau Hospital, Taipei, Taiwan; 4. Institute of Brain Science, National Yang Ming Chiao Tung University, Taipei, Taiwan; 5. Division of Neurology, Department of Medicine, Taipei City Hospital Renai Branch, Taipei, Taiwan; 6. Department of Neurology, National Yang Ming Chiao Tung University Hospital; 7. Institute of Neuroscience, School of Life Sciences, National Yang Ming Chiao Tung University, Taipei, Taiwan; 8. Department of Neurology, Faculty of Medicine, School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan; 9. Division of General Neurology, Department of Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan; 10. Brain Research Center, National Yang-Ming Chiao Tung University, Taipei, Taiwan
Corresponding Author: Pei-Ning Wang, Neurological Institute, Taipei Veterans General Hospital, No. 201, Sec. 2 Shih-Pai Rd, Taipei 112, Taiwan, Tel: +886-2-28757578, Fax: +886-2-28757386; Email: linda2860@gmail.com
J Prev Alz Dis 2023;
Published online April 19, 2023, http://dx.doi.org/10.14283/jpad.2023.47
Abstract
Background: Subjective cognitive decline is proposed to be associated with future mild cognitive impairment and dementia. A better understanding of the roles of self-reported and informant-reported subjective cognitive complaints can provide a more delicate picture in dementia recognition and early diagnosis.
Objectives: To evaluate the accuracy of self-reported and informant-reported subjective cognitive complaints and the relation of subjective cognitive complaints and neuropsychological function in cognitively unimpaired, mild cognitive impairment and populations with dementia.
Design: We conducted a cross-sectional survey and evaluate the relations between subjective cognitive complaint scores and cognitive function in the different diagnostic groups.
Setting: We recruited individuals diagnosed with cognitively unimpaired or mild cognitive impairment or dementia with Alzheimer’s clinical syndrome from a memory clinic in a tertiary medical center in Taiwan.
Participants: Participants, age greater than 50 years old, were enrolled in this study. Participants’ informants were also enrolled for the cognitive questionnaire assessment.
Measurements: Participants’ and informants’ subjective cognitive complaint scores were collected based on a 12-item questionnaire. Neuropsychological assessments of global cognitive function, memory, language, executive function, visuospatial function and calculation were performed. The relations between subjective cognitive complaint scores and cognitive function in the different diagnostic groups were assessed by linear regression model.
Results: There were 1536 individuals and 1028 informants enrolled in this study. Self-reported subjective cognitive complaint scores from early and late mild cognitive impairment and dementia with Alzheimer’s clinical syndrome participants showed no significant differences, but informants’ subjective cognitive complaint scores showed a significant increase. Informant-reported subjective cognitive complaint scores related to neuropsychological tests in population with dementia. Neither self-reported nor informant-reported subjective cognitive complaint scores related to neuropsychological tests in cognitively unimpaired and mild cognitive impairment populations.
Conclusions: Self-reported subjective cognitive complaints alone may not be sufficient to demonstrate clinical significance in different stages of cognitive impairment. Incorporating informant-reported subjective cognitive complaints, along with considering individual’s anxiety and depressive status, are crucial in assessing cognitive statuses in clinical practice.
Key words: Subjective cognitive decline, mild cognitive impairment, dementia.
Introduction
An individual’s subjective concern about cognitive changes is a core clinical criterion for mild cognitive impairment (MCI) and Alzheimer’s dementia (AD) (1). Subjective memory symptoms could occur as early as the late stage of preclinical AD, before the threshold of MCI or dementia is reached, and this finding has drawn attention in recent years for its potential benefit in prevention and predementia treatment (2).
The clinical significance of subjective cognitive decline (SCD) varied widely in previous studies, which is partially due to the different strategies of assessments, including the terms used in the questions, questionnaire items and clinical setting, and the variability in cultural expectations among different countries and languages. Due to the absence of common standards regarding subjective cognitive decline, Jessen et al. (3) proposed a framework for preclinical AD research in 2014. Accordingly, SCD was defined as self-experienced persistent cognitive decline without objective cognitive impairment. To raise the sensitivity, nonmemory complaints were included, with the concept of self-perception of cognitive performance as the main theme, independent of cognitive testing.
Self-reported SCD has been shown to be related to future risk of MCI and AD dementia, especially in individuals who report concern about memory decline. SCD with memory concerns at baseline predicted the conversion to dementia during one and a half, and three-year follow-ups, and showed more significance than in participants with SCD without concerns (4). Cognitively normal subjects with memory concerns alone even carry the same risk of developing AD as individuals with early MCI (5).
However, informant-reported SCD has been suggested to have a better correlation with cognitive function tests and the prediction of future dementia than self-reported SCD (6, 7). The significance of informants’ SCD through dementia disease stages might be different. In the AD population, self-provided SCD was significantly lower than informant-provided SCD. In the MCI group, no obvious differences were detected between self-provided SCD and informant-provided SCD (7). In a cognitively normal population with memory complaints, however, self-provided SCD was significantly higher than informant-provided SCD (7). Thus, both self- and informant-reported SCD questionnaires were recommended to be obtained by the Subjective Cognitive Decline Initiative (SCD-I) working group (8).
The correlation between self-reported subjective cognitive complaint (SCC) scores and cognitive function, nevertheless, is controversial in cognitively unimpaired and MCI populations. In individuals with MCI, a correlation between cognitive complaints and baseline cognitive function was found (9). A weak correlation between self-reported SCC scores and cognitive function was also found in the cognitively normal population (10-12). However, others debated that self-reported memory complaints showed a stronger association with stress and anxiety but weaker correlations with neuropsychological tests (7).
The design of this study is based on SCD research recommendations proposed by the SCD-I working group. We included multiple cognitive domains in SCD assessments to evaluate the correlations with neuropsychological tests. Both self- and informant-reported data were collected for analysis. The aim of this study was to assess the relationship between SCC scores and cognitive function in patients without dementia and compare self- and informant-provided SCCs in different dementia stages.
Methods
Participants
We enrolled participants from a memory clinic in a tertiary medical center in Taiwan from January 1, 2015, to December 31, 2018 and assessed them with clinical review and cognitive tests. The main inclusion criterion was age greater than 50 years old, who had either memory concern or no memory concern but were willing to take questionnaire and cognitive assessments due to personal interests. The exclusion criteria were history of major brain trauma, brain tumor, stroke, epilepsy, alcoholism, major psychiatric illness, medication or other systemic diseases that affect cognitive function. Participants’ informants were also enrolled for the cognitive questionnaire assessment, and had accompanied the participants to the clinic visits. The informants were mostly close relatives of the participants, who lived with the participant or had frequent visits, without medical professional backgrounds. This study was approved by the Local Ethics Committee of Human Research in Taipei Veterans General Hospital in Taiwan.
Assessment
Subjective cognitive decline questionnaire
Participants were interviewed in the hospital by neurologists. Subjective cognitive complaints were assessed by 12 questions using the Mandarin self-assessment questionnaire, proposed by Cheng CH et al (13-15). The English translated version is shown (Supplementary Table S1). The self-assessment questionnaire was dichotomously based (yes or no) and designed for multidomain cognitive assessment. Participants were asked to compare their current cognitive function to their status two years earlier. Participants scored 1 point if they answered “yes” and 0 points if they answered “no”. The score of questions 1 to 12 was added as the total SCC score. Participants’ informants were also asked to complete the questionnaire.
We futher summed the subgroup SCC scores up based on the cognitive domain each question represented. Questions 1 to 4 were grouped as the memory domain; questions 5 and 6 as the language domain; and questions 9 to 12 as the executive function domain. Questions 7 and 8 represented the calculation and visuospatial function domains, respectively.
Neuropsychological assessments
Neuropsychological assessments were conducted by trained psychologists and research assistants. The full battery is displayed below, and we categorized each test into six cognitive domains:
1. Global function: Mini-Mental State Examination (MMSE) (16); clock drawing test (17)
2. Memory: Chinese version of the verbal learning test (CVLT), total score (18); complex figure test – Taylor figure (CFT), delayed recalled score (19); Chinese version of the delay story recall test (20)
3. Executive function: forward and backward digit span (21); modified trail-making A & B (22)
4. Visuospatial function: clock copy test (17); CFT-copy (19)
5. Language: Boston Naming Test (BNT), total (23); cookie theft picture task (24); semantic fluency test (25)
6. Calculation: a 3 digits and 2 digits multiplication test, followed by 2 digits and 1 digit addition and subtraction tests, with total score of 5.
For further analysis, we compute z score for each test within the domains, by standardizing against the CU participants. Domain composite scores were computed by averaging z scores within each domain.
Clinical diagnosis
Participants were diagnosed as cognitively unimpaired (CU), early MCI, late MCI or dementia with Alzheimer’s clinical syndrome (ACS), with diagnoses based on clinical interviews, neurologic examinations, neuropsychological test batteries, laboratory findings, and neuroimaging evaluations.
The diagnosis of dementia with ACS is based on the criteria of the National Institute on Aging and the Alzheimer’s Association for probable AD dementia (26). The diagnosis of early and late MCI is based on the Alzheimer’s Disease Neuroimaging Initiative (ADNI) cohorts (27), with impaired episodic memory function documented by the Chinese version of the Wechsler Memory Scale – Logical memory subscale (WMS-LM) (Delayed Paragraph Recall). The cutoff of early MCI is 1-1.5 SD of norm data; the cutoff of late MCI is 1.5 SD below norm data.
Group definitions
We grouped normal participants into “cognitively unimpaired (CU) with SCD-concern” and “CU with SCD-no concern” based on participants’ responses to the additional question: “Generally, are you worry about that your daily life has been affected or even disturbed due to memory decline or the conditions mentioned above”. Participants who answered “yes” were grouped into “CU with SCD-concern”; participants who answered “no” were grouped into “CU with SCD-no concern”. Participants with other diagnoses were also grouped into “with SCD-concern” or “with SCD- no concern” groups based on the same question.
Anxiety and depression
Validated measurements of anxiety and depression were performed using the 15-item Geriatric Depression Scale (GDS15) (28) and an anxiety/depression rating score, which ranges from no anxiety/depression (score of 0) to very severe anxiety/depression (score of 5).
Statistical analysis
A reliability analysis for internal consistency of the SCC scores of the participants and the SCC scores of the informants was performed via measuring Cronbach’s alpha coefficient. A reliability coefficient of 0.70 to 0.95 is considered acceptable (29).
One-way ANOVA was used to compare the neuropsychological test scores, age and education years between different groups. Post hoc analysis was performed using Fisher’s least significant difference (LSD) test. The chi-square test was used to compare categorical variables, including gender, family history, and individual SCC questions.
For the comparison of participants’ and informants’ SCC scores, we analyzed only the data for which both scores were available. We conducted independent sample t-tests and one-way ANOVA to compare the discrepancy scores between participants’ and informants’ SCC scores, and mean SCC scores across different diagnostic groups, respectively.
As for determining the association of SCC scores and neuropsychological tests, linear regression models were performed, controlling age, gender, education, family history and anxiety/depression scores. The independent sample t-test was used to compare the SCC scores between CU and early MCI group; and the SCC scores and neuropsychological test scores in different groups based on “with concern” and “with no concern”. A p value of less than 0.05 was considered to indicate statistical significance; all tests were two-tailed. All statistical analyses were carried out using the statistical software SPSS (Statistical Package for the Social Science) 24 for Windows.
Results
Baseline characteristics
1536 participants and 1028 informants were enrolled in this study. The median age of the sample was 74.2 years (standard deviation 10.13), and 853 (55.5%) of them were female. A total of 394 (25.6%) participants presented with a family history of dementia. The mean years of education was 11.2 (standard deviation 4.6). Of 374 (24.3%) participants who were diagnosed as cognitively unimpaired (CU), 89 answered “yes” to the additional question and thus were assigned to the “CU with SCD-concern” group. The five groups differed significantly in terms of age, gender, and education year (Table 1).
Table 1. Demographic data and neuropsychological performances in the study population
CU: cognitively unimpaired; SCD: subjective cognitive decline; MCI: mild cognitive impairment; ACS: Alzheimer’s clinical syndrome; CVLT: Chinese version Verbal Learning Test; CFT: Complex Figure Test-Taylor figure; BNT: Boston Naming Test; † p<0.05 between CU without SCD and CU with SCD; ‡ p<0.05 between CU with SCD and early MCI; * p<0.05 between early MCI and late MCI; # p<0.05 between late MCI and dementia with ACS; Data is provided as mean (SD) in neuropsychological tests.
Neuropsychological tests
Of all 15 neuropsychological tests obtained, the “CU with SCD-concern” and the “CU with SCD-no concern” group performed equally well, without a significant difference. Generally, the early MCI group performed better than the late MCI group, whereas the dementia with Alzheimer’s clinical syndrome group performed the worst among all groups (Table 1, 2).
Table 2. Cognitive performances of the study population, demonstrated in z scores
CU: cognitively unimpaired; SCD: subjective cognitive decline; MCI: mild cognitive impairment; ACS: Alzheimer’s clinical syndrome; CVLT: Chinese version Verbal Learning Test; CFT: Complex Figure Test-Taylor figure; BNT: Boston Naming Test; Data is provided as z score (SD).
Comparison of participants’ and informants’ subjective cognitive complaint (SCC) scores
Reliability analysis of the participants’ SCC scores and informants’ SCC scores was performed. The analysis for the total of 12 questions showed very good Cronbach’s alpha scores: 0.81 for the participants’ SCC scores and 0.845 for the informants’ SCC scores.
A total of 1028 participants’ and informants’ SCC was included for SCC scores analysis. The total SCC scores (0-12) of the participants and informants are displayed in Figure 1. The mean total SCC score of participants and informants were 3.36 (standard deviation: 2.91), and 5.59 (standard deviation: 3.47), respectively.
Of the participants’ SCC scores, the “CU with SCD-concern” group showed the highest total score, rated as 4.4 among all groups. However, the total SCC scores in participants reached a plateau after entering the MCI stage, and the early MCI, late MCI and dementia with ACS groups showed no significant difference between each other. However, the trend of total SCC scores of informants showed an increase from CU toward dementia with ACS. (Fig. 1). The total SCC scores reported by both participants and informants were able to distinguish the CU group from the early MCI group, with informants’ reports demonstrating higher significance (p values of 0.022 and <0.001, respectively).
Figure 1. Comparison of total subjective cognitive complaint scores of participants and informants in the study groups
CU: cognitively unimpaired; SCD: subjective cognitive decline; MCI: mild cognitive impairment; ACS: Alzheimer’s clinical syndrome; Data provided as mean (SD); † p<0.05 between CU without SCD and CU with SCD within participants or informants; ‡ p<0.05 between CU with SCD and early MCI within participants or informants; * p<0.05 between early MCI and late MCI within participants or informants; # p<0.05 between late MCI and dementia with ACS within participants or informantsRelation between SCC scores and neuropsychological tests
Significant discrepancy was observed in the mean SCC scores of participants and informants across different diagnostic groups. The p-values were 0.008 in the cognitively unimpaired group and <0.001 in the MCI and dementia with ACS groups. The mean differences in SCC scores between participants and informants (participants’ total SCC scores minus informants’ total SCC scores) were 0.67 (SD: 2.9), -1.21 (3.7), and -4.3 (4.0) in the three respective groups (Supplementary table S2).
Based on subgroup SCC analysis, the memory domain scores increased from early MCI toward dementia with ACS. This trend was not seen in the subgroup SCC analysis regarding other cognitive domains (i.e., language, attention, executive function and visuospatial function) (Supplementary Table S3.). If we separated the nonmemory domain from the memory domain for SCC analysis, similarly, the nonmemory SCCs scores reached a plateau as the disease progressed and showed no significant differences between the early MCI, late MCI and dementia with ACS groups (Supplementary Figure S1). Total and subgroup SCC scores showed differences in all groups based on having or not having concern. Participants with concerns had higher SCC scores than those without concern (Supplementary Table S4).
Table 3. Linear regression of cognitive performance (via total z score) in different study groups
The results of the relation between participants’ and informants’ total SCC scores and neuropsychological tests showed that there was a significant relationship between the informants’ SCC scores and the participants’ neuropsychological tests in those with dementia, whereas no significant relationship was found in the CU and MCI populations. Specifically, in the CU population, the GDS scores were found to be significant, while neither the participants’ nor the informants’ SCC scores showed significance. (Table 2).
In SCC memory and nonmemory subdomains scores, neither participants’ nor informants’ SCC showed significance. (Supplement table 5)
In comparison of neuropsychological tests performance between “with SCD-concern” and “with SCD-no concern”, each diagnostic groups showed significance based on informants’ concern. Specifically, participants whose informants expressed concern about their cognitive performance decline exhibited poorer neuropsychological test performance (Supplement table 6) However, when comparing based on self-reported concern, we found no significant differences in any diagnostic group.
Discussion
Overall, our results showed that informant-reported SCC scores have a better relation with cognitive function tests than participant-reported SCC scores, especially in participants with dementia. Self-reported SCC scores show no relation to neuropsychological tests in CU, MCI and participants with dementia. In the CU population without dementia or MCI, depressive and anxiety statuses relate with cognitive performance.
Our study revealed that self-reported SCC scores could be affected by insight into the illness during disease progression. The self-reported SCC scores plateaued after early MCI stages, while the informant-reported SCC scores showed an increase from normal toward participants with dementia, with expanding discrepancy scores across the three diagnostic groups, consistent with previous studies (30, 31). Prior research showed that even in the early stage of the disease, clinical unawareness was noted (32), which then further progressed in the stage of AD (33). Although both participants’ and informants’ SCC scores were able to differentiate the early MCI group from the CU group in our study, informant-provided SCD showed greater discriminative ability, which is consistent with the findings of previous study (30).
Regarding the comparison of SCD with and without concerns, as expected, the SCC scores were significantly higher in CU participants with SCD-concern. A similar trend was also observed in the mild and late MCI groups and even in the dementia with ACS group, indicating that participants with concern had higher SCC scores, independent of disease stage. The results regarding CU participants are compatible with previous studies which showed that baseline SCC scores were higher in CU participants with concern than in those without concern (34, 35). However, SCD with concern is less discussed in terms of MCI and AD populations. Moreover, although the “with SCD-concern” group had higher SCC scores than the “with SCD-no concern” group in CU participants, there was no difference in cognitive performance between the two groups. This finding suggests that the higher SCC scores in the “with SCD-concern” group may be influenced by their higher levels of depression and anxiety.
The SCC scores from informant reports increased from CU participants to MCI and dementia groups in our study, which also emphasized the importance of incorporating informants’ information into SCD studies. The informant’s SCC result was similar to a previous study, which showed an increase along the spectrum from the cognitively normal population to AD patients (7). The differences between participant-provided SCCs and informant-provided SCCs expanded from early MCI toward AD. In the CU population without dementia, a slight degree of cognitive function changes could only be detected by the patients themselves, and only complicated neuropsychological tests could demonstrate cognitive function changes. However, throughout disease progression, informant-provided SCCs could better demonstrate participants’ cognitive function decline even in the early stage of the disease (i.e., MCI stage).
The relation between cognitive complaints and cognitive function in normal and MCI populations was inconsistent in previous studies, which may be attributed to multiple factors, including depressed mood (36, 37), overestimated self-reported SCCs in the normal population (6, 38), and loss of insight in the MCI population (39, 40). In populations without dementia, few studies have revealed a weak relation between self-reported cognitive complaints and cognitive functions (11, 12, 35). However, less evidence of a relation between self-reported SCCs and cognitive tests could be found in MCI patients (41, 42). In contrast, most studies demonstrated a good correlation between cognitive tests and informant-provided SCCs in MCI and populations with dementia (7, 10, 43). Our study did not find any relationship between self-reported cognitive complaints and cognitive performance in any of the study groups. In the CU population, there was a correlation between cognitive performance and depressive and anxiety statuses as evidenced by GDS scores. On the other hand, informants’ reports showed a significant correlation with cognitive performance in participants with dementia, which could be attributed to the loss of insight during the progression of the disease.
In our SCC multidomain analysis, only the memory domain SCC scores increased while the disease progressed. Memory complaints, rather than other cognitive domain complaints, were viewed as features of SCD-plus criteria, which increased the likelihood of underlying AD (3). van Harten et al. also proposed that the memory domain SCC score is the best single-domain-specific SCD measure to predict MCI when compared to other domains (44). The explanation from the previous study was that the memory-predominant phenotype is the most common among dementia. In our study, memory complaints seemed to be relatively “resistant” to loss of insight in dementia patients, highlighting the greater impact of memory complaints in these patients. Despite this, our study found no significant relationship between self-reported memory SCC scores and cognitive performance in all study groups. (Supplement table 5.) Rather, both informants’ memory and nonmemory SCC scores demonstrated a stronger correlation with cognitive performance. In the Mayo Clinic Study of Aging study, informant memory SCC did not outperform nonmemory SCC in predicting MCI risk. Instead, multidomain informant SCC showed better predictive value than memory SCC alone, highlighting the importance of considering different aspects of SCCs (44).
A strength of our study is the large sample size covering different cognitive stages, from middle to old age. The questionnaire that we designed is focused on recently presented SCC, which is another feature of SCD-plus that increases the likelihood of preclinical AD (3). We conducted a comprehensive investigation on multidomain SCC from both participants and informants, encompassing various aspects such as comparison between the two in different diagnostic groups, exploration of factors associated with differences, and examination of factors related to participants’ neuropsychological performances. Our study stands out from previous research in that it provides more extensive information on the relation between self-provided SCC and neuropsychological performances in MCI and AD groups, and also sheds light on SCD with concern, which has been less discussed in terms of MCI and AD populations in prior studies.
The main limitation of our study was that we only analyzed cross-sectional results. Further study is warranted to provide a detailed evaluation of longitudinal changes in cognitive performance. Furthermore, while we conducted paired comparisons between the SCC scores of participants and their informants, we had limited information available on the informants. Other limitations included that participants were from a memory clinic in a medical center, and we only sampled participants seeking medical help; thus, our results may not extend to community-based individuals directly. Moreover, ApoE genotype and biomarkers were not included in this study.
In summary, we demonstrated that self-reported SCCs alone may not be sufficient to demonstrate clinical significance in different stages of cognitive impairment. The self- and informant-provided SCC scores also revealed a “loss of insight effect” as the score differences increased during disease progression. Incorporating informant-reported SCCs, along with considering individual’s anxiety and depressive status, are crucial in assessing cognitive statuses in clinical practice and further longitudinal evaluations in this population.
Acknowledgments: We gratefully acknowledge the contribution of the study investigators, and the study participants and their informants. We would like to thank reviewers and the editor for their comments.
Funding: This work was financially supported by the Brain Research Center, National Yang-Ming University from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan, the National Science Council and the Ministry of Science and Technology, Taiwan (MOST 105-2325-B-182A-005-, MOST 108-2321-B-010-013-MY2, MOST 110-2321-B-010-007), Taipei Veterans General Hospital (V104C-059, V107C-090, V110C-093).
Conflicts of Interest: None are reported.
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