On March 11, 2020, COVID-19 was declared by the World Health Organization as a global pandemic.1 The virus causes severe morbidity and mortality among older adults and especially in people with hypertension, obesity, and diabetes.2 Thus, many countries initiated a lockdown to minimize the virus spread. On March 21, 2020, the Israel government imposed a 5-week country-wide lockdown, which placed severe restrictions on public and private sectors and closure of nonessential work places, gyms, entertainment centers, and restaurants.3 This new and unprecedented state imposed significant changes on the day-to-day lives of the older adult population, and especially on individuals with chronic illness such as type 2 diabetes (T2D), who were at particularly high risk of morbidity and mortality due to the COVID-19 infection. In addition to macrovascular and microvascular complications, T2D is associated with an increased risk of anxiety, depression,4,5 increased brain atrophy, and poor motor function in older adults. Emotional complications of T2D are further exacerbated by social distancing, isolation, and disruption of the daily routine4,5; therefore, we explored the impact of the lockdown on our Israel Diabetes and Cognitive Decline (IDCD) population.
We leveraged the IDCD study to investigate in 429 participants the associations of cognitive and motor functions and total gray matter volume (GMV)—all associated with T2D6—measured before the COVID-19 outbreak, on emotional distress, during the first lockdown. We hypothesized that less emotional distress during lockdown is associated with better motor function, better cognition, and a greater volume of gray matter.
METHODS
Design
The IDCD is a community-based longitudinal cohort study of chronic conditions of aging with T2D and their impact on brain and cognition.6 It is a collaboration between the Icahn School of Medicine, New York, the Sheba Medical Center, Israel, and Maccabi Healthcare Services, Israel. Participants are all from Maccabi, providing detailed information on medications, diagnoses, and laboratory results since 1998. The IDCD methods and eligibility criteria are detailed elsewhere6 and include older adults (age 65+), T2D diagnosis, fluency in Hebrew, no dementia at baseline, and availability of an informant. We administered a telephone “COVID-19 lockdown questionnaire” during the first lockdown period in Israel. The Institutional Review Boards of the 3 institutions approved the study, and verbal consent was obtained from all subjects.
Active IDCD participants during the COVID-19 period (N=477) were approached by phone for the questionnaires of whom 429 agreed to answer. GMV data were available for 221 participants with magnetic resonance imaging (MRI). All participants reported not having contracted COVID-19.
The COVID-19 Lockdown Questionnaire
Two single-item measures were used to assess the degree of anxiety and depression:7 “Over the last 2 weeks, how much have you been bothered by feeling anxious or nervous?” and “Over the last 2 weeks, how much have you been bothered by feeling sad, down, or uninterested in life?”. Responses were on a 9-point scale (0- “not at all,” 9 “severely”).7 We also asked about general well-being (“How are you feeling in general?”, 1 “much worse than usual,” 5 “much better than usual”), optimism toward the future (“Are you optimistic toward the future?”, “yes”—“no”), and respective questions comparing to before the COVID-19 outbreak (eg, “Your anxiety level now, in comparison to the period before the coronavirus outbreak is:”, 1 “worse,” 2 “same,” 3 “better”). Please see Supplemental Tables 1 to 3, Supplemental Digital Content 1, https://links.lww.com/WAD/A426.
As part of the ongoing IDCD study assessments, participants undergo physical examinations, motor function assessment, and cognitive evaluations. A random subsample is invited to undergo brain MRI.
Motor function was assessed by 2 performance-based measures: (1) hand-grip strength was measured by an hydraulic Sammons Preston Jamar plus dynamometer, which measures isometric grip force ranging from 0 to 90 kg, and (2) 3-m gait speed, where participants are instructed to walk 3 m at their usual walking pace once prompted. The number of seconds to walk this distance was recorded. These 2 motor functions are strongly related to physical function.8–10
Cognitive Function
Thirteen cognitive tests were assessed and 4 cognitive domains based on factor analysis were produced:6 (1) episodic memory: immediate and delayed recall, and recognition from the Consortium to Establish a Registry for Alzheimer’s Disease neuropsychological battery11; (2) language/semantic categorization: similarities, letter fluency, and animal fluency; (3) attention/working memory: shape cancellation and digit span (forward and backward) from the Wechsler Memory Scale-Revised; and (4) executive functions: trail making test (A and B), the Consortium to Establish a Registry for Alzheimer’s Disease-constructional praxis, and digit symbol from the Wechsler Adult Intelligence Scale-Revised.
Raw scores of each cognitive test were converted to z scores using participants’ means and SDs. A composite measure of global cognitive function was created by averaging all the z scores.
Gray Matter Volume
MRI scans were performed in the diagnostic imaging department at Sheba Medical Center with a 3T scanner (GE, Signa HDxt, v16VO2). Total GMV was derived from high resolution T1-weighted MRI as detailed elsewhere.12
Statistical Analysis
Partial Spearman correlations were performed to examine the association between emotional distress measures and (1) motor function, (2) cognitive function, and (3) GMV, adjusting for sociodemographic variables (age, sex, and education), and T2D-related characteristics [hemoglobin A1C (HbA1c) and duration of T2D], and total intracranial volume for the GMV analyses.
RESULTS
Participants averaged 77.05 years of age during the lockdown; the majority of the participants were male (57.8%). At the IDCD baseline, participants had 13.77 years of education, 6.73 HbA1c, suggesting relatively good glycemic control, and a duration of T2D of almost a decade (Table 1).
TABLE 1 -
Demographic and Main Questionnaire Data
| Variable |
Mean |
SD |
| Age |
77.05 |
4.42 |
| Years of education |
13.77 |
3.46 |
| 3-m walk (s) |
4.09 |
1.97 |
| Grip strength (kg) |
29.57 |
9.84 |
| Overall cognition (composite z score) |
−0.13 |
0.89 |
| Gray matter volume |
516.59 |
50.27 |
| Mean HbA1C (%) |
6.73 |
0.70 |
| Duration of T2D |
9.46 |
4.37 |
| Sadness level (range: 0-9) |
1.98 |
2.53 |
| Sadness compared with before COVID-19 outbreak (range: 1-3) |
2.28 |
0.50 |
| Anxiety level (range: 0-9) |
1.36 |
2.19 |
| Anxiety compared with before COVID-19 outbreak (range: 1-3) |
2.15 |
0.43 |
| General feeling (range: 1-5) |
2.82 |
0.51 |
HbA1C indicates hemoglobin A1C; T2D, type 2 diabetes.
Figure 1 presents the associations of cognitive and motor functions, and of GMV with lockdown-related emotional distress variables. Lower grip strength before lockdown was associated with higher sadness (r=−0.160, P<0.001) and anxiety (r=−0.115, P=0.021) scores, and with less optimism (r=0.113, P=0.026) but not with general well-being, nor with self-perceived change in anxiety and depression since the COVID-19 outbreak. Slower gait speed was associated with higher sadness scores (r=0.127, P=0.009). Lower GMV was related to both greater anxiety during the lockdown (r=−0.251, P=0.001) and greater anxiety in comparison to before the COVID-19 outbreak (r=−0.246, P=0.001), and with lower optimism (r=0.178, P=0.020). Global cognition was not associated with any emotional distress measure. When additionally adjusting for gray matter, all associations remained significant except for grip strength with anxiety and gait speed with sadness (Supplemental figure 1, Supplemental Digital Content 1, https://links.lww.com/WAD/A426).
;)
FIGURE 1: Heatmap of relationships of self-rated emotional distress with motor function, cognitive function, and gray matter volume, according to Spearman correlations adjusting for age, sex, education, hemoglobin A1C and duration of type 2 diabetes, and for TICV for the gray matter volume analysis. A higher positive correlation value is denoted by red and higher negative correlation is denoted by blue color. TICV indicates total intracranial volume.
DISCUSSION
This study was designed to assess the emotional burden of the COVID-19 lockdown imposed on older adults with T2D who were at high risk for COVID-19 infection and at high risk for depression, anxiety, and cognitive impairment.13 Our results suggest that poorer motor function before lockdown, but not cognitive function, is associated with different parameters of emotional distress. Specifically, we found that weaker grip strength, a strong predictor for poorer physical and mental health, morbidity, and mortality,8,14 was associated with more self-reported anxiety and depression, less optimism, and with a worse general feeling after entering home confinement. These data are consistent with current studies among the elderly that report a decline of their well-being during lockdowns.14–16 Slower gait speed was also associated with increased sadness, which is consistent with the evidence from other groups, irrespective of the COVID-19 pandemic.17 Physical conditioning, a main driver of good motor function, is also a well-established protective factor for chronic emotional distress.14,18 There is evidence for beneficial effects of physical conditioning on depression and anxiety in acute periods of stress.19,20 Further investigation of the role of physical conditioning to reduce emotional distress in older adults with underlying conditions during acute stressful periods is warranted.
Higher GMVs have been associated with greater optimism and more positive emotions and feelings in older adults.21 Accordingly, in this study, we found an association between higher GMV and greater optimism, as well as lower anxiety during the lockdown, suggesting that higher GMV may represent at least in part the underlying neurobiology of good emotional health and well-being22 that supports older adults with T2D in the limiting conditions of home confinement. This is consistent with the loss of statistical significance for the association of grip strength with anxiety and of gait speed with sadness found in this study.
Surprisingly, cognitive function was not associated with any of the emotional distress measures. Home confinement and loneliness have been associated with cognitive decline.23 However, in line with our results, a study that examined prelockdown and postlockdown cognitive status in the context of COVID-19, reported that although older adults demonstrated a significant increase in anxiety and depression, they did not show significant cognitive decline in the Montreal Cognitive Assessment.24 This study is cross-sectional, and ongoing IDCD study follow-ups may shed light on the associations of lockdown-related emotional distress and cognitive decline in the future. This is particularly relevant in light of the new COVID-19 mutations, and the resulting longer-term self and/or government imposed restrictions due to the pandemic.
Limitations of the study include the cross-sectional design, so causality cannot be concluded. We did not collect data on potential important confounders such as social and family support. The study has strengths including the large number of well-characterized older adults with T2D motor, cognitive and brain volume data, and directly measured (rather than self-reported) T2D and related characteristics.
ACKNOWLEDGMENTS
The authors thank the National Institutes of Aging for supporting the work.
REFERENCES
1. Cucinotta D, Vanelli M. WHO declares COVID-19 a pandemic. Acta Biomed. 2020;91:157.
2. Li X, Xu S, Yu M, et al. Risk factors for severity and mortality in adult COVID-19 inpatients in Wuhan. J Allergy Clin Immunol. 2020;146:110–118.
3. Ministry of Health (MOH) I. Israel Emergency Novel Coronavirus Emergency Regulations. 2020. Accessed February 10, 2021.
https://www.gov.il/he/Departments/policies/dec4911_2020.
4. De Groot M, Golden SH, Wagner J. Psychological conditions in adults with diabetes. Am Psychol. 2016;71:552.
5. Egede LE, Ellis C. Diabetes and depression: global perspectives. Diabetes Res Clin Pract. 2010;87:302–312.
6. Beeri MS, Ravona-Springer R, Moshier E, et al. The Israel Diabetes and Cognitive Decline (IDCD) study: design and baseline characteristics. Alzheimers Dement. 2014;10:769–778.
7. Young Q-R, Nguyen M, Roth S, et al. Single-item measures for depression and anxiety: validation of the Screening Tool for Psychological Distress in an inpatient cardiology setting. Eur J Cardiovasc Nurs. 2015;14:544–551.
8. Giampaoli S, Ferrucci L, Cecchi F, et al. Hand-grip strength predicts incident disability in non-disabled older men. Age Ageing. 1999;28:283–288.
9. Fried LP, Tangen CM, Walston J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56:M146–57.
10. Ganmore I, Elkayam I, Ravona-Springer R, et al. Deterioration in motor function over time in older adults with type 2 diabetes is associated with accelerated cognitive decline. Endocr Pract. 2020;26:1143–1152.
11. Welsh KA, Butters N, Mohs RC, et al. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part V. A normative study of the neuropsychological battery. Neurology. 1994;44:609–609.
12. Livny A, Ravona-Springer R, Heymann A, et al. Haptoglobin 1-1 genotype modulates the association of glycemic control with hippocampal volume in elderly individuals with type 2 diabetes. Diabetes. 2017;66:2927–2932.
13. Vindegaard N, Benros ME. COVID-19 pandemic and mental health consequences: systematic review of the current evidence. Brain Behav Immun. 2020;89:531–542.
14. Bohannon RW. Grip strength: an indispensable biomarker for older adults. Clin Interv Aging. 2019;14:1681.
15. González-Sanguino C, Ausín B, Castellanos MÁ, et al. Mental health consequences during the initial stage of the 2020 Coronavirus pandemic (COVID-19) in Spain. Brain Behav Immun. 2020;87:172–176.
16. De Pue S, Gillebert C, Dierckx E, et al. The impact of the COVID-19 pandemic on wellbeing and cognitive functioning of older adults. Sci Rep. 2021;11:1–11.
17. Kim H-j, Park I, joo Lee H, et al. The reliability and validity of gait speed with different walking pace and distances against general health, physical function, and chronic disease in aged adults. J Nutr Biochem. 2016;20:46.
18. Ku P-W, Fox KR, Chen L-J, et al. Physical activity and depressive symptoms in older adults: 11-year follow-up. Am J Prev Med. 2012;42:355–362.
19. Salmon P. Effects of physical exercise on anxiety, depression, and sensitivity to stress: a unifying theory. Clin Psychol Rev. 2001;21:33–61.
20. Taylor MK, Markham AE, Reis JP, et al. Physical fitness influences stress reactions to extreme military training. Mil Med. 2008;173:738–742.
21. Chowdhury R, Sharot T, Wolfe T, et al. Optimistic update bias increases in older age. Psychol Med. 2014;44:2003–2012.
22. Dolcos S, Hu Y, Iordan AD, et al. Optimism and the brain: trait optimism mediates the protective role of the orbitofrontal cortex gray matter volume against anxiety. Soc Cogn Affect Neurosci. 2016;11:263–271.
23. Borges-Machado F, Barros D, Ribeiro Ó, et al. The effects of COVID-19 home confinement in dementia care: physical and cognitive decline, severe neuropsychiatric symptoms and increased caregiving burden. Am J Alzheimers Dis Other Demen. 2020;35:1533317520976720.
24. Nogueira J, Gerardo B, Silva AR, et al. Effects of restraining measures due to COVID-19: Pre-and post-lockdown cognitive status and mental health. Curr Psychol. 2022;41:7383–7392.
