East Asian Arch Psychiatry 2015;25:108-14

ORIGINAL ARTICLE

Dr Rakesh Balachandar, PhD, Department of Clinical Neurosciences , National Institute of Mental Health and Neurosciences, Bangalore, India.
Dr Ravikesh Tripathi, MPhil, PhD, Consultant Clinical Psychologist, Narayana Hrudayalaya, Bangalore, India.
Prof. Srikala Bharath, MD, FRCPsych, Department of Psychiatry, National Institute of Mental Health and Neurosciences, Bangalore, India.
Prof. Keshav Kumar, PhD Department of Clinical Psychology, National Institute of Mental Health and Neurosciences, Bangalore, India.

Address for correspondence:
Tel: (91-80) 2699 5271; Fax: (91-80) 2656 4830; Email: srikala.bharath@gmail.com

Submitted: 23 December 2014; Accepted: 3 March 2015 

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Introduction

Executive functions act at the highest level of cognition to enable optimal performance of the activities of daily living. Studies of ageing have demonstrated predominant age-related decline in executive functions compared with other cognitive domains.^1-4 Executive functions are presumably mediated by the frontal and temporal lobe neuronal system.^1,5 One of the important subcomponents of executive functions, planning, is also mediated via neuronal circuits involving the frontal lobe. Neuroimaging studies have reported predominant frontal lobe atrophy in healthy ageing.⁶ Planning is defined as a process of formulating a sequence of operations intended to achieve a final goal.⁷ It involves a 2-stage process: initially to formulate a logical strategy to determine the sequence of actions required to achieve the specific goal and later the ability to monitor and guide towards its successful completion.^3,8 The Tower of Hanoi (TOH), a neuropsychological tool, is often used to assess planning skills.^9,10

Planning along with working memory, verbal and visual organisation, judgement and reasoning are crucial for performing instrumental activities of daily living. They are tested during successful completion of a TOH task. Due to age-related cognitive decline, planning skills among the elderly fade compared with young adults and hence performance of tasks in the TOH also worsens with advancing age.¹⁰

The importance of planning skills is seen among patients with mild cognitive impairment (MCI) and Alzheimer’s disease (AD). Executive skills compensate for the memory impairment in amnestic MCI. Dysfunction in these cognitive domains has a higher prediction for the conversion of amnestic MCI to frank AD.¹¹ Further, patients with AD develop deficits in planning ability during the course of their illness.¹²

Previous studies among the elderly Indian population have documented a lack of cognitive tests that include planning skills.^13-15 As an important cognitive domain, planning needs to be assessed among the elderly population. We observed a need for a validated and reliable neuropsychological test to assess the planning skills of an elderly Indian population.

In the current study, we aimed to explore the utility of the TOH to assess planning skills in an elderly Indian population, including patients with early AD. We hypothesised that the classic TOH offered a means to assess planning skills in our elderly population. We also hypothesised that patients diagnosed with mild AD would perform less well on the TOH than matched cognitively healthy controls.

Methods

This study was conducted at the Geriatric Clinic & Services, National Institute of Mental Health and Neurosciences (NIMHANS), India after institutional ethics committee approval. After obtaining informed consent, all subjects underwent NIMHANS Neuropsychiatry Battery for Elderly¹⁵ testing along with TOH assessment.

A total of 215 cognitively normal elders (CNe) were recruited from the community (elderly forums) and elderly caregivers of patients visiting NIMHANS. They were aged between 55 and 80 years, and 60 of whom were females. All cognitively healthy volunteers gave informed consent and were screened for neuropsychiatric disorders using Instruments for Comprehensive Evaluation of the Elderly,¹⁶ and, subsequently, the Hindi Mental State Examination (HMSE).¹⁷ All elderly healthy volunteers were independent and autonomous in their activities of daily living. None reported any subjective memory complaints (relevant indicator of cognitive decline)¹⁸ or were taking any medication that could interfere with cognition. The CNe were divided into 2 groups (< 60 and ≥ 60 years). Subjects with a score of ≥ 24 in HMSE were included as CNe.¹⁹ Those with a score of < 24 were evaluated for causes of possible cognitive deficits and appropriately managed.

Another 24 patients with AD (4 of whom were females), with a mean age of 67.1 years, were recruited from the geriatric clinic, NIMHANS. These patients were clinically diagnosed according to the National Institute on Aging–Alzheimer’s Association criteria,²⁰ and with a Clinical Dementia Rating Scale score of < 1²¹ by a senior professor of psychiatry / neurology.

Classic Tower of Hanoi Task

The TOH task involves the shifting of all disks (2-5 disks) from their primary position to a final position in a minimum number of moves without violating certain rules. These rules include: (a) a single disk should be moved at a time; (b) disks should be shifted only on the pegs; and (c) a larger disk may not be placed over a smaller disk.¹⁰

Studies that have explored planning skills of the elderly have used 3- and 4-disk tasks of the classic TOH.^3,9 In order to observe the feasibility of the test in the Indian elderly, we included 1-step, lower (2 disks) and higher (5 disks) tasks in our planning assessment. Hence we used the first 4 levels of the TOH task, starting from level 1 (2-disk task) to level 4 (5-disk task) with increasing levels of complexity. At each level the disks were placed in the primary position (extreme left peg), and shifted to the final position (extreme right peg) while complying with the rules. On completing the task, subjects moved to the next higher level. Performance measures were based on 3 main parameters: number of moves required, total time taken to complete the task, and number of rule violations during each task (mistakes).

Statistical Analyses

All statistical analyses were performed using R statistics. As the data (education and performance measure scores) followed a normal distribution (as assessed using Shapiro- Wilk test), 2-tailed independent t test was used for group comparisons. Univariate general linear model analysis was also used to detect age-related changes between the groups, adjusting for education as a covariate.

The randomly selected CNe were individually matched for age, gender, and education with that of mild AD patients to compare their TOH performance measures using independent t test. We also explored the sensitivity and specificity of the TOH in discriminating / differentiating patients with mild AD from CNe matched for age, gender, and education by performing receiver operating characteristic (ROC) curve analysis.

Results

Demographic details of subjects are shown in Table 1. Comparison of results between CNe subgroups, as well as that between patients with mild AD and matched CNe on TOH are presented in Tables 2 and 3, respectively. 

Performance of Cognitively Normal Elders

Cognitively normal elders aged from 55 to 80 years with a male predominance (73%). Those in the subgroup aged ≥ 60 years were significantly highly educated than those < 60 years (p = 0.04). In this sample of CNe a steep increase in the performance scores (time taken and total moves) was observed as task complexity increased. The number of CNe who could successfully complete the task also reduced as the complexity increased. An explorative independent t test between 2 CNe subgroups (< 60 and ≥ 60 years) did not reveal any statistical difference in their performance measures (Table 2). Univariate general linear model analysis revealed that education did not significantly affect the performance measures in the CNe group; further there was no significant difference in the performance measures between the 2 age-groups after controlling for education.

Performance of Patients with Mild Alzheimer’s Disease

Subjects with mild AD experienced severe difficulty in completing the TOH tasks. Only about 75% of patients with mild AD could complete the level 1 (2-disk) task.

In subsequent higher levels the number further dropped. Patients with mild AD exhibited a trend of reduced performance compared with CNe (Table 3). A significant difference (p < 0.05) was observed for performance measures of time taken for the 2-disk task and rule violations in 3-disk task. Explorative ROC curve analysis of performance measures revealed poor sensitivity and specificity in differentiating patients with mild AD from CNe (Fig).

Discussion

The present study aimed to observe the utility of the classic TOH to assess planning skills in an elderly Indian population. The TOH was administered to CNe and a sample of patients with mild AD. We also attempted to explore age-related cognitive decline by stratifying the sample of CNe into 2 groups based on their age (< 60 years and ≥ 60 years). A steep incline in the performance scores (total time taken, number of moves) was observed among CNe groups with increasing task complexity. We would like to stress that the number of additional steps taken by the elderly to solve tasks at each level also increased. This suggests that CNe experienced difficulties in planning, completing, and proceeding to subsequent higher levels of the task. The performance scores of our current study were inferior to the age-matched scores of another study.³ Interestingly, CNe of our study exhibited inferior performances in the classical TOH despite having more years of formal education in comparison with the above-mentioned study.³ We can confer that the normative data of classic TOH performance for Indian cognitively normal elderly subjects are different.

School-educated elderly subjects often become functionally illiterate due to underutilisation of their reading and writing skills, as these skills acquired during schooling may be redundant for their lifestyle or occupation. The inferior performance on classical TOH tasks of the Indian elderly in this study, though more educated (13.3 ± 4.9 years) than those in another study (6.3 ± 1.7 years),³ may be explained by functional illiteracy. Alternatively, variations in the performance of individuals with a low education level could be attributed to one or many other reasons such as task familiarity, performance anxiety, attitude towards the testing situation, and appropriateness of the test for a given population with a low level of education. It is therefore imperative to use ecologically valid and culturally appropriate tests to make definitive comments about the true cognitive status of a particular individual.

Previous studies have documented age-related decline in fluid intelligence such as planning ability.¹ Our attempt to explore the age-related cognitive decline by stratifying the elderly population into 2 groups (< 60 years and ≥ 60 years) could not demonstrate such changes. We propose the following observations possibly contributing to this finding. First, ageing studies that documented age-related changes have predominantly compared young adults and elderly subjects.³ The age difference between the 2 groups in our study population was very small: group 1 CNe (< 60 years) were aged between 55 and 59 years and group 2 CNe (≥ 60 years) comprised volunteers aged between 60 and 80 years. Age-related decline in fluid intelligence is likely a gradual process; hence narrow age differences in our study failed to demonstrate age-related decline in the planning process. Second, although our CNe were randomly recruited and stratified on the basis of age, the older group (≥ 60 years) were significantly (p = 0.04) more educated than the younger group (< 60 years).

Education, which is an important factor in cognitive reserve, may contribute to our current finding.^22-24 Fewer than 12 years of formal education indicates a pre-college level of education, whereas receiving education of ≥ 12 years indicates a college and postgraduate level. Because our CNe older group (≥ 60 years) received a mean education of > 12 years, the majority would have potentially been exposed to situations that exercised their cognitive functions including planning skills, and would thus have performed better than the less educated CNe (< 60 years). Univariate general linear model analysis, which was used to control the effects of education, did not reveal significant differences between the 2 age-groups.

Performance of Patients with Mild Alzheimer’s Disease

Patients with early AD experienced severe difficulty in solving TOH, as demonstrated by the proportion who could successfully complete the 2-disk task (level 1) of TOH. About 25% of AD patients could not complete this first level; this percentage further increased to 50%, 66.7% and 100% for the 3-disk, 4-disk, and 5-disk tasks, respectively.

Patients with mild AD performed worse than the matched CNe for all performance measures (Table 3). A significant statistical difference (p < 0.05) was observed in rule violations in the 3-disk task and time taken for the 2-disk task. An insignificant difference observed in other performance measures could be due to fewer patients successfully completing the levels when compared with matched CNe (Table 3), hence the statistical analysis could not detect significant differences. Despite the observed differences, ROC analysis of the classic TOH performance had poor discriminative ability to differentiate patients with mild AD and CNe (Fig). Patients with AD predominantly suffer from episodic memory deficit during the early stages of illness and later develop other cognitive domain deficits including executive functions.¹² In addition, studies that involve patients with early AD have demonstrated the importance of executive functions in overcoming episodic memory deficits and performing activities of daily living.^25,26 Thus we expected that explorative ROC would not discriminate patients with mild AD and healthy controls. Further work with a larger sample and inclusion of another study group with moderate AD would throw more light on this issue.

The following points should be emphasised in this study. For reasons of long testing hours and the steep increase in complexity of tests, our CNe experienced cognitive fatigue.²⁷ There is a need to develop planning tasks that start at an easy level and gradually increase in complexity. A task of this kind would accustom individuals to a testing situation and encourage them to perform better at subsequent higher levels. Further, we recommend that tasks be designed such that they can be completed in a short period of time.

Developing a tool that fulfils the above criteria has the advantage of obtaining a baseline planning performance. It is advantageous to record baseline planning deficits in patients with AD, especially to monitor disease progression or to evaluate the effects of intervention. A limitation of our study is the heterogeneity in education level between the 2 CNe groups. Our sample of CNe were all educated, contrary to our original intention to recruit predominantly illiterate elderly subjects.

Conclusion

Planning skills need to be assessed regularly in cognitively healthy elderly subjects, patients with MCI and those with AD. In this group of elderly we have demonstrated the need for a culturally appropriate neuropsychological tool to assess planning ability. Finally, there is a need to developing normative data for elderly Indian subjects after validating the planning tool.

Acknowledgements

We thank all participants for their complete cooperation.

Declaration

The authors declared no conflict of interest in this study.

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