Telephone Interview for Cognitive Status Scores Associate with Cognitive Impairment and Alzheimer’s Disease Pathology at Death

Abstract

Background:

Early diagnosis of Alzheimer’s disease (AD) provides an opportunity for early intervention. Cognitive testing has proven to be a reliable way to identify individuals who may be at risk of AD. The Telephone Assessment for Cognitive Screening (TICS) is proficient in screening for cognitive impairment. However, its ability to identify those at risk of developing AD pathology is unknown.

Objective:

We aim to investigate associations between TICS scores, collected over a period of 13 years, and the cognitive status of participants at death. We also examine relationships between TICS scores and neuropathological indices of AD (CERAD score, Thal phase, and Braak stage).

Methods:

Between 2004 and 2017, participants from The University of Manchester Longitudinal Study of Cognition in Normal Healthy Old Age underwent cognitive assessment using TICS. Scores from four time points were available for analysis. Cognitive impairment and AD pathology at death was evaluated in 101 participants.

Results:

TICS scores at time points 2, 3, and 4 were significantly lower in those cognitively impaired at death compared to those considered cognitively normal. There were significant negative correlations between TICS scores and CERAD score and Braak stage at time points 2 and 4. No correlations between Thal phase and TICS were found.

Conclusion:

Findings indicate that TICS could be used not only to screen for cognitive impairment, but also to identify individuals at risk of developing AD pathology, many years before any overt symptoms occur. Once identified, ‘at risk’ individuals could be targeted for early interventions which could attenuate the progression of the disease.

Keywords

Cognitive dysfunction dementia neuropathology neuropsychological test

INTRODUCTION

As advances in public health and medicine lead to increased life expectancy, the propensity for age-related disease rises. Alzheimer’s disease (AD) is the most common neurodegenerative disease in the elderly and increasing age is one of the most important risk factors in those aged 65 and over with the incidence of AD doubling every five years [1].

Although no cure is available for patients with AD, early diagnosis is paramount as it enables early intervention. Pathological events linked with AD are thought to occur many years before the clinical symptoms [2], thus treatment may be more effective in the preclinical stage of disease.

Neuropsychological testing has shown that associations can be found between dementia and scores obtained from a variety of cognitive tests with testing periods predating dementia by 10 to 18 years [3 –6]. Likewise, previous studies have shown that scores from neuropsychological tests conducted up to 20 years before death can associate with AD pathology [7 –10]. Early identification of patients at risk of developing AD will increase the efficacy of pharmacological interventions targeting amyloid-β (Aβ) and tau.

However, neuropsychological testing can be lengthy and laborious and may require specialist personnel to conduct the test. The Mini-Mental State Examination (MMSE) is a common cognitive testing tool, and a shortened version can easily be performed in general practice and produces reliable results [11]. It has been previously suggested that scores from the MMSE can predict AD between 7 years before the onset of signs and symptoms [12] and 9 years before a formal diagnosis [13]. Similarly, scores on MMSE can correlate with cortical neurofibrillary tangle density [14, 15] and Braak stage [16].

Attendance in person to participate in cognitive testing may not always be possible. During the recent SARS-CoV-2 (COVID19) pandemic, face-to-face general practice consultations declined, and it is thought that the delivery of general practice in the future is more likely to involve telemedicine [17, 18]. As such, going forward, cognitive tests such as MMSE may not be as suitable for dementia screening.

The Telephone Interview for Cognitive Status (TICS) was developed in 1988 [19] to provide a cognitive screening tool that did not need face-to-face interaction between patient and clinician. The fact that the test could be conducted remotely also allowed large-scale studies of cognitive impairment to occur. There is a strong correlation between TICS and MMSE and several studies have demonstrated that TICS has high test-retest reliability [19 –21]. A modified version of TICS (TICSm) has been shown to be more predictive of memory abilities than MMSE [22] and is useful in the detection of amnestic mild cognitive impairment (MCI) [23]. However, others have urged caution in using TICSm alone to identify subjects with MCI or dementia [24].

Overall, TICS and TICSm are considered important tools that are best used as screening instruments to rule in or exclude cognitive impairment. Although some cognitive domains cannot be assessed over the telephone (e.g., spatial cognition) examination of most others, such as orientation and verbal memory, is feasible [25]. The ability of TICS scores to differentiate between those with and without the pathology associated with AD is, to date, unknown.

The present study used eligible participants from The University of Manchester Longitudinal Study of Cognition in Normal Healthy Old Age (UMLCHA) [26] to investigate associations between the scores of two versions of TICS (TICSm and TICS-27 – as detailed in the Materials and Methods section), collected over a period of 13 years, and the cognitive status of eligible participants at death. In addition, we examined associations between TICS test scores and three neuropathological indices of AD (CERAD score, Thal phase, and Braak stage) in the same group of eligible individuals.

MATERIALS AND METHODS

Participants and study design

In 1983, UMLCHA recruited 6,542 cognitively healthy individuals (aged between 42 and 92 years) via local advertisements in newspapers, radio, and television. Study participants were approached in 2003 for consent to brain donation and 312 individuals agreed to donate their brain after death. To date, 138 donations have occurred. Detailed information on the clinical and neuropathological profile of this sub-cohort has been previously described [27, 28].

Between 2004 and 2017, participants underwent assessments of cognition using a modified Telephone Assessment for Cognition (TICSm) and the TICS-27 assessment. Scores from four time points (TPs) are available for analysis. Both tests were administered at the same assessment visit. The TICSm assessment is a 13-item telephone administered assessment with a maximum total score of 39 [29, 30]. The items included test orientation (day of week, date, season, age and telephone number), immediate memory (10 word list) and delayed memory (10 word list repeated after delay), attention/calculation (subtracting serial sevens from 100; counting backwards from 20), comprehension/semantic/recent memory (answering what is used to cut paper, what is the name of the prickly plant in the desert, who is the current monarch, who is the current prime minister, what is the opposite of East), language/reception (stating the phrase ‘Methodist episcopal’). A cut off threshold for cognitive impairment in the survey is below 21. Using the same interview data, we also computed an alternative (TICS-27) score which has a maximum total score of 27 [31]. This score contains 10 word immediate and delayed recall, a serial sevens subtraction test and counting backwards from 20. Using TICS-27, individuals can be classified as probable dementia (score 0–6), probably cognitive impairment non-dementia (CIND) (score 7–11), and cognitively normal (score 12–27). In the present study, both TICSm and TICS-27 scores were used in the analyses. Participants without any TICS scores were excluded from the study.

Cognitive status at death was ascertained using clinical notes obtained from donor’s general practitioner, cause of death as recorded on the death certificate and conversations at time of death between the Brain Bank Coordinator (PT) and the family of the deceased.

The study was approved by Manchester Brain Bank Management Committee (REC reference 19/NE/0242). Under conditions agreed with the Research Ethics Committee, The Manchester Brain Bank can supply tissue or data to researchers, without requirement for researchers to apply individually to the REC for approval.

Pathological examination

Neuropathological assessment was performed by two experienced neuropathologists (DM and FR) who used consensus criteria to establish the presence and staging of common neurodegenerative diseases.

Brains were dissected and sampled following standard procedures. Samples included: superior frontal gyrus, anterior cingulate, temporal (including superior and middle temporal gyrus), inferior parietal lobule, primary visual cortex, hippocampus, amygdala, corpus striatum, thalamus, midbrain, brainstem, and cerebellum. The specimens were then processed and embedded into paraffin blocks and 6-μm sections were cut from the blocks. The sections were stained as previously described [10 , 28] to assess pathological features including Aβ, tau, TAR DNA-binding protein 43 (TDP-43), and phosphorylated α-synuclein.

For the purpose of this study, cases with alpha-synucleinopathy or non-AD tauopathy were excluded when they represented the primary neuropathological finding. We also excluded AD cases where there was severe secondary or concomitant pathology (other than cerebral amyloid angiopathy or small vessel disease) such as features of co-existent progressive supranuclear palsy or alpha-synucleinopathy. We included cases of Aging-related Tau Astrogliopathy, Primary Ageing-Related Tauopathy, and Limbic-predominant Age-related TDP-43 Encephalopathy owing to the fact that they are common aging-related pathologies. Of the 138 UMLCHA participants who had donated their brain, 101 were eligible. An overview of the pathology of eligible participants is available (Supplementary Table 1).

Statistical analysis

Differences between those cognitively impaired at death and those cognitively normal at death when comparing sex and severity of AD pathology were analyzed with the Chi-squared test, while differences for age at death and years of education were analyzed with the T-test.

Differences in TICS scores between the cognitive status groups were analyzed using the Mann-Whitney U Test.

Spearman correlations were used to assess whether any of the measures of AD pathology (CERAD score, Thal phase, and Braak stage) correlated with TICS scores. Analyses were not corrected for multiple comparisons.

In all cases, a p value of < 0.05 was considered significant.

RESULTS

Demographics

Information pertaining to the demographics of the 101 eligible participants are shown in Table 1. No significant differences in sex, age at death, or level of education were found between those considered cognitively normal at death when compared with those cognitively impaired at death. However, as expected, individuals who were cognitively impaired at death were more likely to be pathologically classified as CERAD score B–C (χ² = 30.6; p < 0.001), Thal phase 4–5 (χ² = 8.3; p = 0.004), and Braak stage III–VI (χ² = 26.1; p < 0.001).

Table 1

Descriptive characteristics, stratified by cognitive status at death, for eligible individuals from UMLCHA.

	CI at death
	No	Yes
N	71	30
Female	52 (73.2%)	22 (73.3%)
CI at death	n/a	n/a
Age at death (Mean±SD)	88.69±6.07	90.30±4.82
Education in ISCED y (Mean±SD)^a	15.56±3.54	16.21±3.51
CERAD score B–C	19 (26.8%)	26 (86.7%)
Thal phase 4–5	7 (9.9%)	10 (33.3%)
Braak stage III–VI	16 (22.5%)	23 (76.7%)

Bold indicates significant difference between inclusive cognitive/pathology groups. (CI, cognitive impairment). ^aOne participant missing education data.

Mean age at each TICS assessment point and mean number of years between assessment and death can be found in Table 2. Each assessment period was separated by approximately two years. Age at baseline TICS testing was 80.5±5.7 years which was 8.4±3.7 years before death.

Table 2

Mean (±SD) values for age at TICS testing and years between TICS testing and death for eligible participants

	Assessment period 1	Assessment period 2	Assessment period 3	Assessment period 4
N	101	90	75	51
Age at testing (Mean±SD)	80.5±5.7	82.5±5.5	84.0±5.4	86.3±5.4
Years between test and death (Mean±SD)	8.4±3.7	6.9±3.2	5.3±2.8	3.4±2.5

Associations between TICS scores and cognitive impairment at death

Of the 101 eligible participants, 30 were considered cognitively impaired at death whereas 71 were considered cognitively normal.

At baseline TICS assessment (TP1), there was no difference in TICSm or TICS-27 test score between the cognitive groups (TICSm: U = 1003.5, p = 0.646; TICS-27: U = 1000.0, p = 0.627). However, at all subsequent TPs, scores were significantly lower in those cognitively impaired at death when compared with those cognitively normal at death (Fig. 1).

Fig. 1

Boxplots comparing TICSm (A) scores and TICS-27 (B) scores between those cognitively impaired at death (grey) and those cognitively normal at death (white). The boxes represent the interquartile (IQ) range which contains the middle 50% of the records. The whiskers represent the highest and lowest values which are no greater than 1.5 times the IQ range. The line across the boxes indicates the median. Differences between cognitive groups were analyzed using the Mann-Whitney U Test.

Associations between TICS scores and AD pathology

Breakdown of AD pathology measures, stratified by TICS TP can be found in Table 3.

Table 3

Breakdown of AD pathology measure, stratified by TICS assessment period

	Assessment period 1	Assessment period 2	Assessment period 3	Assessment period 4
N	101	90	75	51
CERAD score
0	28	25	21	14
A	28	27	25	18
B	37	33	25	18
C	8	5	4	1
Thal phase
0	28	25	21	13
1	16	15	15	9
2	11	11	11	9
3	29	26	20	14
4	9	7	4	4
5	8	6	4	2
Braak stage
0	12	10	10	5
I	20	19	16	14
II	30	29	24	15
III	21	17	14	10
IV	9	7	4	3
V	3	2	2	1
VI	6	6	5	3

CERAD score

CERAD score negatively correlated with TICSm score and TICS-27 score at TP2 (TICSm: r_s = –0.281, p = 0.007; TICS-27: r_s = –0.259, p = 0.014) and TP4 (TICSm: r_s = –0.276, p = 0.050; TICS-27: r_s = –0.303, p = 0.031), but not at TP1 (TICSm: r_s = –0.069, p = 0.490; TICS-27: r_s = –0.068, p = 0.501) or TP3 (TICSm: r_s = –0.070, p = 0.553; TICS-27: r_s = –0.060, p = 0.610) (Fig. 2).

Fig. 2

Scatterplots with interpolation line showing change in TICS scores in relation to CERAD score. Panels A–D show TICSm scores and panels E–H show TIC-27 scores. The p value is shown where significant correlations were found.

Thal phase

Thal phase did not correlate with either TICSm score or TICS-27 score at any TP (Fig. 3).

Fig. 3

Scatterplots with interpolation line showing change in TICS scores in relation to Thal phase. Panels A D show TICSm scores and panels E–H show TIC-27 scores. No significant correlations were found.

Braak stage

Braak stage negatively correlated with TICSm score at TP2 (r_s = –0.286, p = 0.006) and TP4 (r_s = –0.272, p = 0.054) but not TP1 (r_s = –0.007, p = 0.944) or TP3 (r_s = –0.125, p = 0.284). Likewise, TICS-27 score also negatively correlated at TP2 (r_s = –0.255, p = 0.015) and TP4 (r_s = –0.296, p = 0.035), but not at TP1 (r_s = –0.030, p = 0.768) or TP3 (r_s = –0.116, p = 0.322) (Fig. 4).

Fig. 4

Scatterplots with interpolation line showing change in TICS scores in relation to Braak stage. Panels A–D show TICSm scores and panels E–H show TIC-27 scores. The p value is shown where significant correlations were found.

DISCUSSION

This study examined the associations between scores for TICS (obtained between 3.4±2.5 and 8.4±3.7 years before death), cognitive impairment at death and severity of AD pathology found at postmortem. We found associations between TICS scores and cognitive impairment at death at TP2, TP3, and TP4 (between 3.4±2.5 and 6.9±3.2 years before death). In addition, we observed associations between TICS scores and AD pathology (for CERAD and Braak stage) at TP2 (6.9±3.2 years before death) and TP4 (3.4±2.5 years before death). This suggests that TICS is not only valuable as a cognitive screening tool but may also be useful in identifying those who may be at risk of developing AD pathology.

TICS is well established as a cognitive screening tool and has high test-retest reliability [19 –21]. In the present study, we found that TICS scores at TP2, TP3, and TP4 were lower in those found to be cognitively impaired at end of life when compared with those cognitively intact. However, scores at TP1 could not differentiate between these cognitive groups. Disease duration of AD is thought to be between 5 and 12 years (from onset of overt AD symptoms to death) [32]. Although testing at TP1 was undertaken approximately eight years before death, and thus within the disease duration period, it is possible that TP1 occurred too far from death to pick up any subtle cognitive decline, as measured by TICS, in those who went on to develop AD.

Niche neuropsychological [7 –10] and more widespread clinical cognitive testing, such as MMSE [14 –16], correlate well with most AD pathology, even when testing is administered many years before death. However, it is known that Thal phase does not correlate well with antemortem cognition [27 , 34]. Unlike CERAD, Thal phase considers regional presence and severity of all Aβ pathology, including diffuse Aβ plaques. However, it is uncertain whether diffuse plaques are part of the aging process or whether they are an early stage in the development of neuritic Aβ plaques [35]. Importantly, diffuse plaques are less likely to be associated with cognitive decline in AD than cored, neuritic plaques [36]. Thus, the fact that Thal phase did not correlate with TICS scores at any of the testing TPs in the present study reflects the established literature.

Conversely, both CERAD and Braak stage correlated well with TICS scores at TP2. The proximity of this TP to death (6.9±3.2 years) may have allowed TICS scores to relay subtle changes in cognition which correspond to the pathological lesions in development. CERAD scores cored and neuritic plaques [37]. Braak stage measures neurofibrillary tangles/neuropil threads [38]. These scores are more likely to associate with cognition than Thal phase [7–10 , 16].

By TP3, correlations between TICS scores and all measures of AD pathology dissipated. There are a number of reasons why this may have occurred. Loss of significance could simply be due to a decrease in available statistical power as participants died or dropped out from the study. Similarly, those with AD were more likely to have died (or dropped out) than their cognitively normal counterparts which may have ‘skewed’ the data. Another possible, but more speculative, explanation might be that at TP2, there was sufficient difference in AD pathology to allow TICS to differentiate between the stages whereas, at TP3, Aβ and tau pathology in the less affected participants may have increased to a level which affected their cognition enough to lead to a convergence in scores. If this is the case, it might be expected that at later time points, those with AD would experience a more severe decline in TICS scores as their condition, and pathology, progresses when compared with those who remain relatively stable both cognitively and pathologically. In fact, this is what is seen in the present study. By TP4, the correlation between TICS scores and CERAD score/Braak stage returns with those at later pathological stages scoring lower than those at early pathological stages. The authors have suggested this waxing and waning of pathology versus cognition in previous work examining cognitive differences between AD and primary age-related tauopathy [39].

The fact that TICSm and TICS-27 correlated with the same measures of AD pathology at the same time points suggests that the shorter TICS-27 test might be as sensitive as the longer TICSm test. Therefore, test times could be significantly reduced by using TICS-27 instead of TICSm. This reduction in testing time could only have a positive impact on patients and clinicians.

Longitudinal TICS assessments and the availability of postmortem brain examination make this a unique study. However, there are a few limitations. The number of cases at TP4 with severe AD pathology stages (CERAD C; Thal 4–5; Braak V–VI) are underrepresented. An overall reduction of cases at TP4 could be due to attrition affecting duration of follow up and, thus, reducing sample size over time. However, we believe that age at testing is a more likely candidate for the lack of cases with severe AD pathology at TP4. Those with more severe AD pathology loads are more likely to have died at an earlier age. In addition, those still alive in their 80s with severe AD pathology loads may well have a greater resilience to cognitive decline. It is possible that in a larger study, with a greater number of severe AD pathology individuals available, the effect seen here may be even more pronounced. The inclusion of eligible individuals with prominent vascular pathology (as measured by vascular cognitive impairment neuropathology guidelines (VCING) [40]) may have led to an underestimation of the contribution of cerebral vascular pathology to cognitive impairment. Future studies may wish to incorporate the staging of cerebrovascular pathology in dementia [41]. The late introduction of brain donation to the study meant many potential donors were lost. Design of future studies should incorporate brain donation from the beginning of the study to ensure the sample size is adequate. The recruitment method could also have been improved to avoid any self-selection and geographical influences.

Although modest, our findings indicate that TICS can be used, not only to screen for cognitive impairment, but also as a tool to identify individuals at risk of developing the pathology associated with AD, many years before any overt symptoms would bring them to the attention of healthcare professionals. Previously, we have shown that results from a simple test of visuospatial episodic memory (Memory Circle test) can identify individuals who are destined to develop AD pathology up to 20 years before death [10]. We suggest that a combination of TICS and Memory Circle tests could be used to more accurately indicate those individuals deemed at risk of developing AD pathology. Once identified, these ‘at risk’ individuals could be targeted for early interventions which could attenuate the progression of the disease.

It is important to stress that TICS is a cheap, effective test that can be conducted remotely. It allows assessment to take place with an individual in their own home where they feel most comfortable. TICS is also very easy to implement and is reliable, even over periods of multiple testing. The ability for TICS to not only screen for cognitive impairment but also for the pathology behind the impairment makes TICS suitable for evaluation of any study of AD drug efficacy.

Footnotes

ACKNOWLEDGMENTS

Longitudinal Cognitive studies were funded by Medical Research Council, Economic and Social Research Council, The Wellcome Trust [Grant reference number 003889], and Unilever PLC. The work of Manchester Brain Bank is supported by Alzheimer’s Research UK and Alzheimer’s Society through the Brains For Dementia Research (BDR) Programme. We would also like to thank Professor Neil Pendleton for his work on the UMLCHA cohort.

Authors’ disclosures available online ().

The supplementary material is available in the electronic version of this article: .

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