November/December 2018

Touch Your Toes! A Brief Measure of Executive Function in Older Adults
By Eric S. Cerino; Karen Hooker, PhD; Robert S. Stawski, PhD; and Megan McClelland, PhD
Today's Geriatric Medicine
Vol. 11 No. 6 P. 24

With approximately 5.7 million Americans facing the individual, social, and financial burdens of the dementia stage of Alzheimer's disease, brief and valid cognitive assessments are essential for practitioners treating older patients with subjective and objective cognitive concerns.1

In a 2014 AARP survey of individuals 34 to 75 years of age, 93% of the 1,200 respondents thought maintaining or improving cognitive health was very or extremely important.2 Furthermore, a recent report from the Healthy Brain Initiative found 1 in 9 adults 45 years of age and older report increased confusion or memory loss, with one-half of these individuals identifying disruptions in everyday tasks such as cooking, cleaning, and medication adherence.3

While memory functioning is a common concern for individuals as they grow older, the higher-level cognitive processes known as executive function (EF) abilities (eg, attention, inhibitory control, working memory) are some of the cognitive domains most likely to show age-related declines.4-6

Adults with subjective cognitive decline report disruptions in maintaining concentration or switching attentional focus among multiple stimuli (ie, attention) and inhibiting one's attention to irrelevant details (ie, inhibitory control)—two components of EF necessary for many everyday tasks. Cooking, for example, requires keen focus on the necessary steps of a recipe, many of which contain multiple tasks to be done at once that require the inhibition of irrelevant ingredients or distractions.

Current measurement of EF in older adults tends to be computer based in a laboratory setting and thus lacks generalizability to real-world scenarios such as cooking.7 This article describes a brief measure of EF, the Head-Toes-Knees-Shoulders Task (HTKS),8 which is low cost, easy to administer, and involves motoric engagement and social interaction in ways that existing EF measures do not. It's a gamelike behavioral measure administered between participant and examiner originally designed to assess aspects of attention, inhibitory control, and working memory in children.9,10

The HTKS has recently been adapted for use with community-dwelling older adults and has strong potential to be used by practitioners interested in assessing patients' current EF levels; the authors have been published on this subject.11

Test Details
The HTKS comprises 30 test items divided equally across three sections with a maximum of four behavioral rules involving touching the head and toes. Each section begins with the participants being asked to touch heads or toes, followed by an opposite command. Part 1 includes two behavioral rules, and Parts 2 and 3 increase difficulty by adding two additional rules and by switching the rules.

In the validation study, all participants advanced to the third section and completed the 30 test items.11 The examiner scores the participants' responses based on how well they can follow the directions and do the opposite to a given command. Scores range from 0 to 60, with higher scores indicating higher EF levels.

In addition to the total score, a modification for older adults included measuring how long (in seconds) each participant takes to complete the HTKS. Therefore, a second outcome measure (ie, completion time) is generated using a digital stopwatch (available on most smartphones) beginning at the start of the HTKS task instructions and ending on the final behavioral response to the task. Faster completion times indicate better EF, as shorter completion times show more efficient cognitive processing.

The HTKS is currently available for research to those who submit an online request at http://health.oregonstate.edu/labs/kreadiness/resources. Clinical use will be possible in the future when norms are developed. Online training, which is required for researchers who intend to use the HTKS, can be obtained upon completion of the online request form.

The Validation Study
The purpose of the recent validation study was to determine whether the HTKS could be adapted to older adult populations.11 A sample of 150 adults 60 years of age and older were recruited for a one-hour assessment in a research office at Oregon State University. Because this work was the first adaptation of the HTKS to older adults, the sample was limited to individuals with cognitive capacity to consent to research. To collect a representative sample of community-dwelling older adults, however, there was no structured screening excluding individuals with chronic medical conditions.

Participants were predominately female (72%), Caucasian (95%), self-identifying as Not Hispanic or Latino/Latina (96%), married (62%), well-educated (81% had at least a Bachelor's degree), and relatively healthy; self-reported mental and physical health was slightly better and more homogenous than in the general US population. Of the 150 participants in the study, 31 reported subjective memory loss in the past year.

Upon providing informed consent, participants were given a paper-and-pencil questionnaire that collected information on demographics, subjective memory loss (via a single item from the Cognitive Module of the Behavioral Risk Factor Surveillance System),3 and self-reported health (via the 12-item short-form health survey).12 The research protocol continued with HTKS administration and the question, "Would you be interested in playing a game similar to the task you just completed in other studies?" to explore whether participants may be receptive to engaging in gamelike tasks such as the HTKS in future research. This was followed by the National Institutes of Health (NIH) Toolbox for the Assessment of Neurological and Behavioral Function Cognition Battery (NIHTB-CB).13

The validation study showed that the HTKS reliably measured components of EF that have been identified in studies using the "gold standard" measures from the NIH Toolbox.11 In this relatively healthy older adult sample, many participants' total scores were close to perfect (M=57.03, SD=4.42; 83% of the sample obtained scores between 56 to 60).

However, the HTKS completion time showed more variability in scores (M=4 min, 43 s, SD=29.92 s, Range=3 min, 56 s–6 min, 53 s) and could potentially be used in combination with the total score to assess EF.

Results
The HTKS demonstrated adequate internal consistency in the validation study's sample of community-dwelling older adults (=0.84). Faster HTKS completion time was significantly associated with higher scores on a measure of attentional set shifting, the Dimensional Change Card Sort (DCCS) test (r=-0.21, p<0.01), and the Flanker task, a measure of inhibitory control and attention (r=-0.20, p<0.05), but not the List Sort working memory test (r=-0.10, p>0.05).

Regression analyses showed higher DCCS scores (b=-0.75, SE=0.25, p<0.01) and higher Flanker scores (b=-0.67, SE=0.27, p<0.05) significantly related to faster HTKS completion time after adjusting for the influences of age, processing speed, and subjective health ratings and explained 18% of the variance and 16% of the variance in HTKS completion time, respectively. Higher HTKS total score was associated with higher scores on the DCCS (r=0.17, p<0.05) but not the Flanker (r=0.07, p>0.05) or List Sort (r=-0.01, p>0.05).

After adjusting for age, processing speed, and subjective health ratings, higher DCCS scores related to higher HTKS total score (b=0.09, SE=0.04, p<0.05) and explained 9% of the variance in HTKS total score. Associations among HTKS and NIHTB-CB measures were strongest for completion time (not total score) as the measure of HTKS performance. Furthermore, regression models explained more variance in HTKS completion time (16% to 18%) than HTKS total score (9%). The validation study revealed the HTKS was a reliable measure and associated with "gold standard" measures of attentional set shifting and inhibitory control.

Study Limitations
Including only cognitively intact individuals in the study was deliberate in the first adaptation of the HTKS in older adults. However, work examining HTKS performance among individuals with mild cognitive impairment or early dementia has yet to be conducted. Furthermore, a more representative sample of older adults with a wide range of cognitive, mental, and physical health conditions would be ideal for understanding the generalizability of the HTKS as a measure of EF in older adults.

Implications for Practitioners
The brief, low-cost HTKS has the potential to be a viable tool for practitioners interested in measuring current levels of EF while incorporating motoric engagement in ways that existing EF measures do not. Average time to complete the HTKS was less than five minutes in the validation study.11 In comparison, administration of the four NIHTB-CB measures took roughly 20 to 25 minutes when accounting for each task's preparation and directions.

Well-known EF measures typically necessitate computer-based equipment that adds preparation time and resource allocation to purchase the necessary equipment. For example, the NIHTB-CB offers iPad administration of its measures for a yearly subscription cost of $499.99. The HTKS expands the cognitive assessment toolkit by offering an alternative, brief measure to assess EF without the need for computer-based equipment.

The HTKS may also have potential for practitioners interested in incorporating the task into routine check-ups as a practical complement to existing measures in the field. A cognitive task that facilitates face-to-face interaction and motoric engagement may promote a more positive atmosphere and overall experience in a medical setting where some patients may feel particularly nervous. In fact, 93% of the participants in the validation study reported interest in future studies that incorporate gamelike tasks such as the HTKS, suggesting older adults may be receptive to engaging in the HTKS protocol.11

Administering measures that are engaging is an important consideration for adherence in the context of medical evaluation.14 Importantly, HTKS administration may not be valid for individuals who understand the directions of the task but are unable to make the appropriate discernable motion due to physical limitations—for example, stroke survivors.

Future Directions and Conclusion
It's important to note that there haven't been predictive studies with older adults that specify a threshold score for distinguishing cognitive status to determine whether it may prospectively predict changes in cognitive functioning. These are critical next steps to ultimately identify brief, valid measures of cognitive functioning that may allow for widespread use among practitioners as well as wider screenings aimed toward early intervention when treatments are most viable.15

Although the HTKS is currently available for research use, it has strong potential to be used by practitioners interested in a brief, novel means of assessing EF that's low cost, easy to administer, and engaging for their older patients.

For more detailed information on the psychometric evaluation of the HTKS in community-dwelling older adults, see Cerino and colleagues.11 For access to the online request form and information on the required training to use the HTKS for research purposes only, visit http://health.oregonstate.edu/labs/kreadiness/resources.

— Eric S. Cerino; Karen Hooker, PhD; Robert S. Stawski, PhD; and Megan McClelland, PhD, are part of the School of Social and Behavioral Health Sciences at Oregon State University.

Author Note: Correspondence concerning this paper should be addressed to Eric Cerino, School of Social and Behavioral Health Sciences, College of Public Health and Human Sciences, Oregon State University, 401 Waldo Hall, Corvallis, OR 97331. E-mail: cerinoe@oregonstate.edu

References
1. Alzheimer's Association. 2018 Alzheimer's disease facts and figures. Alzheimers Dement. 2018;14(3):367-429.

2. Brain health important to 93% of Americans, but few know the 5 ways to help maintain or improve it. AARP website. https://press.aarp.org/2015-01-20-Brain-Health-Important-to-93-of-Americans-But-Few-Know-the-5-Ways-to-Help-Maintain-or-Improve-It. Published January 20, 2015.

3. Alzheimer's Association; Centers for Disease Control and Prevention. The Healthy Brain Initiative: the public health road map for state and national partnerships, 2018–2023. https://www.cdc.gov/aging/pdf/2013-healthy-brain-initiative.pdf

4. Fleischman DA, Yu L, Arfanakis K, et al. Faster cognitive decline in the years prior to MR imaging is associated with smaller hippocampal volumes in cognitively healthy older persons. Front Aging Neurosci. 2013;5(21):1-7.

5. Jurado MB, Rosselli M. The elusive nature of executive functions: a review of our current understanding. Neuropsychol Rev. 2007;17(3):213-233.

6. Zelazo PD, Craik FIM, Booth L. Executive function across the life span. Acta Psychol. 2004;115(2-3):167-183.

7. Müller U, Kerns K. The development of EF. In: Lerner R, Liben LS, Müller U, eds. Handbook of Child Psychology and Developmental Science. 7th ed. New York: Wiley; 2015:571-623.

8. McClelland MM, Cameron CE, Duncan R, et al. Predictors of early growth in academic achievement: the head-toes-knees-shoulders task. Front Psychol. 2014;5:1-14.

9. McClelland MM, Cameron CE, Connor CM, Farris CL, Jewkes AM, Morrison FJ. Links between behavioral regulation and preschoolers' literacy, vocabulary, and math skills. Dev Psychol. 2007;43(4):947-959.

10. Cameron Ponitz CE, McClelland MM, Matthews JS, Morrison FJ. A structured observation of behavioral self-regulation and its contribution to kindergarten outcomes. Dev Psychol. 2009;45(3):605-619.

11. Cerino ES, Hooker K, Stawski RS, McClelland M. A new brief measure of executive function: adapting the head-toes-knees-shoulders task to older adults [published online April 10, 2018]. Gerontologist. doi: 10.1093/geront/gny028.

12. Ware JE, Kosinski M, Keller SD. SF-12: How to Score the SF-12 Physical and Mental Health Summary Scales. 2nd ed. Boston, MA: The Health Institute, New England Medical Center; 1995.

13. Gershon RC, Wagster MV, Hendrie HC, Fox NA, Cook KF, Nowinski CJ. NIH Toolbox for assessment of neurological and behavioral function. Neurology. 2013;80(11 Suppl 3):S2-S6.

14. Cruz-Jentoft AJ, Franco A, Sommer P, et al. European silver paper on the future of health promotion and preventive actions, basic research, and clinical aspects of age-related disease. Eur J Ageing. 2009;6(1):51-57.

15. Prince M, Bryce R, Ferri C; Alzheimer's Disease International. World Alzheimer Report 2011: the benefits of early diagnosis and intervention. https://www.alz.co.uk/research/WorldAlzheimerReport2011.pdf. Published September 2011.