key: cord-0951877-rkjsffyv
authors: Carino, Marylin; Quill, Zoe; Gabbs, Melissa; Sellers, Elizabeth; Hamilton, Jill; Pinto, Teresa; Jetha, Mary; Ho, Josephine; Alecio, Onalee Garcia; Dart, Allison; Wicklow, Brandy
title: The impact of the COVID-19 pandemic on adolescents and young adults living with type 2 diabetes
date: 2022-01-31
journal: Can J Diabetes
DOI: 10.1016/j.jcjd.2022.01.002
sha: 5d632f0e8dc95c136c69260a9c65be0899926db3
doc_id: 951877
cord_uid: rkjsffyv

OBJECTIVES: The aim of this study was to assess the impacts of the COVID-19 pandemic on adolescents and young adults living with type 2 diabetes (T2D) involved in the national Improving Renal Complications in Adolescents with T2D through REsearch (iCARE) study. METHODS: The Environmental influences on Child Health Outcomes (ECHO) COVID-19 Questionnaire developed by the National Institutes of Health ECHO COVID-19 Task Force was administered to participants (n=85) from the iCARE study between June 2020 and October 2020. Children 12 years old (via parent report) and adolescents and young adults ≥13 years old (via self-report) participated. The questionnaire assessed the impact of the pandemic on health-care appointments, lifestyle, internet use, social connections and mental health. RESULTS: Participants were 17.0±3.1 (range, 12 to 27) years of age and predominantly female (61.3%). During the pandemic, 69.4% were able to attend their health-care appointments by telephone or virtual platforms, 31.7% ate more, 45.1% slept more and 29.3% spent less time on physical activities. There was an increase in internet use for both educational (42.0%) and noneducational purposes (54.9%). Participants felt less socially connected (64.6%). Participants also felt sometimes (59.2%), often (19.7%) and very often (6.7%) satisfied with their lives. DISCUSSION: Our study revealed that the COVID-19 pandemic has had various impacts on the daily lives of adolescents and young adults living with T2D. Future research should include longitudinal studies of the health burden of the COVID-19 pandemic on this population, with a more in-depth evaluation of mental health outcomes and clinical outcomes.

The coronavirus disease pandemic has had widespread impact, affecting virtually every country across the world. As of June 24, 2021, there have been 1,410,927 confirmed cases of COVID-19 in Canada, including 26,175 deaths (1). Infectious disease outbreaks have become one of the major threats in global public health, with significant physical and mental health impacts (2). Since March 2020, countries have implemented various regional and countrywide lockdowns to mitigate the risks of transmission. The effects of these containment measures have drastically modified daily societal routines.

In Canada, some of the main provincial measures taken to reduce community transmission have been mask wearing, handwashing, social distancing, closure of schools and businesses, and limitation of gathering sizes in both indoor and outdoor spaces (3). These public health measures have also included pivoting chronic disease care to virtual platforms (4).

Adults living with type 2 diabetes (T2D) are disproportionately affected by COVID-19; with disruption in diabetes management and care contributing to poorer metabolic control since the pandemic began (5) . Evidence suggests that those with poorer diabetes control are also more likely to experience COVID-19 infections, hospitalization, and death compared to the general population (6, 7) . The Centers for Disease Control and Prevention have included type 2 diabetes in the list of underlying medical conditions that increase the risk for severe illness caused by COVID-19 (8) .

In contrast, there is limited data available regarding the health outcomes of adolescents and young adults living with T2D with respect to COVID-19 infection and morbidity. Available pediatric data shows that children do not seem to develop severe clinical manifestations of COVID-19 (9) . However, the indirect effects of the pandemic, including public health restrictions have had a significant impact on children and adolescents overall, and those living with chronic disease (10) . Substantial changes to daily routines may cause disruption in sleep and wake cycles, meal consumption and timing and diabetes management, along with physical and social isolation causing high levels of psychological stress.

Provinces in Canada have implemented strict inter-provincial travel restrictions and mandatory isolation J o u r n a l P r e -p r o o f for returning travellers (11). This could disproportionately impact adolescents and young adults living with T2D who live in rural Northern communities with the need to travel for medical appointments to see specialists (12) . In the province of Manitoba, the Northern region includes all land in Manitoba above the 53 rd parallel (13) . Many schools have implemented alternate day schedules to ensure social distancing, while some in the Northern Manitoba have been closed since the pandemic began (14). Additionally, a significant proportion of youth with T2D live in poverty or socially disadvantaged households (15). The unintended consequences of these public health measures may be heightened anxiety and fear regarding chronic illnesses management, food insecurity, and decreased access to health care services. The aim of this research was to evaluate the direct impacts of COVID-19 infection and exposure on adolescents and young adults living with T2D; as well as the indirect impacts of the public health measures associated with the pandemic.

This research involves a sub-group of adolescents and young adults living with T2D that were recruited from an ongoing longitudinal cohort study, the Improving Renal Complications in Adolescents with type 2 diabetes through REsearch (iCARE) cohort study (ClinicialsTrial.gov identifier: NCT02818192) (16) . The iCARE study is a prospective observational cohort study designed to identify the bio-psycho-social risk factors for early onset albuminuria and the progression of chronic kidney disease in adolescents living with T2D. The sub-study protocol was approved by the biomedical research board at the University of Manitoba (HS13255-B2011:024). In accordance with the Declaration of Helsinki and prior to enrollment, every parent or guardian gave verbal informed consent via telephone, and every youth gave verbal informed assent via telephone.

J o u r n a l P r e -p r o o f Active participants (n=250) were approached by telephone to participate in this sub-study which involved the administration of a one-time questionnaire. Participants who agreed to take part in the substudy were 12-27 years old at the time of survey collection.

The Environmental influences on Child Health Outcomes (ECHO) COVID-19 Questionnaire developed by the National Institutes of Health ECHO COVID-19 Task Force was used to collect data on the impacts of the COVID-19 pandemic on adolescents and young adults participating in the iCARE Cohort Study (17). The questionnaire was administered over the telephone by trained research associates from June 4, 2020 to October 31, 2020. Telephone contact was attempted three times for each potential participant. Children over age 12 years (n=83) completed the survey facilitated by a research associate via self-report, and children 12 years and younger (n=2) had their parents or guardian complete the survey as their proxy via parent-report. A full copy of the questionnaire can be found in the online supplemental material (Appendix A).

To compare the clinical characteristics, the demographics of participating individuals were obtained at the last follow-up visit in the pre-COVID-19 period and compared to the assessments made during the COVID-19 period. For this research, the 'pre-COVID-19 period' was defined as the time period before March 11, 2020, the day the World Health Organization declared COVID-19 as a Public Health Emergency of International Concern (18) . The 'COVID-19 period' was defined as the time period from June 4, 2020 to October 31, 2020, the start and end date of survey collection, respectively. The variables collected in the pre-COVID-19 period included age, sex, duration of diabetes, self-reported ethnicity, type of residence (urban vs rural), hemoglobin A1c (A1C), urine albumin-to-creatinine ratio (ACR), the average daytime reading of 24-hour ambulatory blood pressure monitoring (ABPM) (19) , family characteristics (number of household occupants, number of rooms in the house, water supply J o u r n a l P r e -p r o o f source, and annual family income), and food security as measured by the Canadian Community Health Survey (20). During the COVID-19 period, the variables collected included A1C, urine ACR, a one-time clinical blood pressure reading, and the duration from last follow-up visit. The duration of diabetes was calculated from the date of diagnosis noted in medical records to the date of survey completion.

Continuous variables are reported as mean and standard deviation (SD); and median and interquartile range (IQR) for non-normally distributed data. Descriptive analysis was performed using R version 6.2 (R Core Team, Vienna, Austria). A paired t-test was conducted to compare the A1C and ACR values of the survey respondents from the pre-COVID-19 period and the COVID-19 period.

The first section of the ECHO COVID-19 questionnaire assessed participants' direct experience with COVID-19 infection in regards to possible exposure, symptoms, testing method, and test results. The responses were reported using Yes or No, and multiple checkbox options.

The second section of the questionnaire evaluated the indirect impacts of the COVID-19 pandemic related to public health restrictions. The questions were grouped according to their impact on healthcare appointments, school, internet usage, food security, lifestyle, social connections, mental health, and stress and anxiety levels. The responses were reported using a Yes or No option, a multiple checkbox option, or a Likert Scale ranging from 'much less' (score 1) to 'no change/same amount' (score 3) to 'much more' (score 5). 'More healthy coping strategies' were defined as: doing activities like puzzles or J o u r n a l P r e -p r o o f reading books; engaging in more family activities; meditation or mindfulness practices; talking to mental healthcare providers (ie. psychologist, therapists, or counsellors); and doing volunteer work. 'Less healthy coping strategies' were defined as: eating more often, including snacking; using marijuana; vaping marijuana or other substances; using tobacco; and drinking alcohol.

The participant characteristics are provided in Table 1 , which also shows the clinical characteristics of the cohort in the pre-COVID-19 period and during the COVID-19 period. Of the 250 participants contacted, 3 declined participation, 162 could not be reached, and 85 agreed to participate in the survey (35.6%). In the pre-COVID-19 period, the clinical characteristics of survey respondents (n=85) were collected at their last follow-up visit prior to March 11, 2020 at less than 3 months (n=27), 3 to 6 months (n=10), 6 to 9 months (n=8), 9 to 12 months (n=11), and more than 12 months (n=29). Survey 12.4 ± 10.3 months, respectively. Additionally, there were no significant differences in the A1C (p = 0.230) and ACR (p = 0.082) measures between the two periods. The blood pressure measurements were not compared since the measurements in the pre-COVID-19 period were taken using the average daytime loads of an ABPM device, while those in the COVID-19 period were taken using a one-time clinic blood pressure. During provincial-wide lockdowns, participants were, on average, isolating with six other J o u r n a l P r e -p r o o f people (three adults and three children) in a living space consisting of two or more bedrooms (92.3%), a kitchen (98.7%), a living room (100%), and the main source of water piped in (73.1%). The occupants-torooms ratio was 1.0.

The characteristics of survey nonrespondents (n=165) are also outlined in Table 1 . There were no differences in the demographics of those who participated compared to the overall iCARE cohort with respect to age, sex, duration of diabetes, ethnicity, and type of residence (urban vs rural).

All participants responded to all the questions in the survey. None of the participants tested positive for COVID-19. However, 1.2% had close contact with a case of COVID-19, 11.8% experienced symptoms suspicious of COVID-19, 4.7% were advised to self-isolate or quarantine, and 2.4% of participants went for testing and received negative results during the study period.

A summary of the indirect impacts of the COVID-19 pandemic are presented in Table 2 . During the pandemic, 69.4% of participants were able to attend their healthcare appointments with healthcare providers through telephone or virtual visits, while 30.6 % of participants were unable to attend their healthcare appointments due to concerns of contracting COVID-19 in healthcare facilities (8.2%), their appointments were cancelled and rescheduled (20.0%), or they were told to self-isolate by Public Health (2.4%). Prior to the COVID-19 pandemic, 12.9% of participants received free meals at school and subsequently experienced a worsening in food security because of school closures during the pandemic.

For a majority of participants, the impact to their lifestyle, varied: 48.8% ate the same amount, 45.1% slept more, 53.7% did the same amount of physical activity, and 61.0% spent less time outside. Almost pandemic on adults with T2D and type 1 diabetes (5, 21, 22) , and children and youth with type 1 diabetes (23) (24) (25) (26) , little is known on the impact of the pandemic on adolescents and young adults with T2D, the majority of whom reside in rural communities. Our findings provide additional insight to the current body of literature in pediatric patients with T2D in rural communities and the effects of the pandemic on their access to healthcare, education, internet usage, food security, lifestyle, social connections, mental health, and stress and anxiety levels.

Due to nationwide lockdowns and travel restrictions, it was found that adolescents and young adults with T2D, ate the same amount, slept more, did the same amount of physical activity, but spent less time outside. This is consistent with results of a Canadian national survey which reported that youth were more likely to sleep more (72.6%) and spend less time outside (41.6%) (27) . Participants were also unable to see their friends in person because of rules on social and physical distancing, but increased their social interactions virtually through video calls and text messages (28) . This has resulted in an increase use of the internet for engaging with their peers on social media platforms and mobile messaging applications.

Participants further reported engaging in more recreational screen-based activities such as playing video J o u r n a l P r e -p r o o f and computer games. There was also an increase in the use of the internet for educational purposes due to school closures and the subsequent migration to distance and online learning systems. Studies from Australia (29) and Bangladesh (30) reported similar outcomes of increased online media consumption in adolescents and young adults compared to before the pandemic. Australian adolescents aged 13 -19 years had increased social media and internet use (OR = 1.86), and Bangladeshi young adults, with a mean age of 23.7 years, engaged in more social media use (64.9%) and recreational online activities such as watching movies or television series (78.0%).

The overall impact of the COVID-19 pandemic on the self-reported mental health for the adolescents and young adults in the study were varied. A majority of participants reported the pandemic as having a negative overall impact on their lives, with the remaining participants reporting no overall impact or a positive overall impact. However, more than half of the participants felt sometimes satisfied with their lives since the pandemic began. Almost 84% of participants had either no stress or mild stress since the start of the COVID-19 pandemic. Taken together, these findings highlight the unique, individualized and varied experiences of adolescents and young adults living with T2D during the pandemic. In our research, a large proportion of participants primarily utilized positive coping strategies such as reading books, doing activities like puzzles and crosswords, engaging in more family activities, practicing meditation or mindfulness methods, participating in volunteer work, and talking to healthcare providers more frequently including therapists, psychologists, and counselors to cope with the stress related to the COVID-19 pandemic. Youth and young adults in China and the United States reported the use of similar healthy coping strategies, including seeking social support and taking up old hobbies, respectively (31, 32) . Our results were in contrast with several studies that reported a deterioration of mental health in youth and adolescents in Canada, Australia, and India (28, 29, 33) . In Canadian children and adolescents aged 6-18 years, 67-70% of participants experienced a deterioration of mental health status in at least one mental health domain due to stress from social isolation (28) . In Australia, adolescents aged 13-19 years reported lower levels of happiness (OR = 0.38), lower levels of positive J o u r n a l P r e -p r o o f emotions (OR = 0.23), and slightly higher increases in psychological distress (OR = 1.48) upon the implementation of physical distancing measures (29) . In India, isolation was found to be associated with moderate to severe stress (37.4%), anxiety (30.9%), and depression (24.6%) in youth and young adults aged 15-30 years (33) .

None of the participants tested positive for COVID-19 infection and only a few experienced symptoms suspicious of COVID-19 and were advised to be tested and self-isolate, or quarantine. This may have been due to the implementation of strict emergency lockdown measures. Northern communities in Canada were one of the most well-protected regions in the early stages of the pandemic (36). For participants who were able to attend their healthcare appointments over the phone or virtually, there were minimal changes in glycemic control. However, adolescents and young adults living with T2D are dependent on physical activity and dietary choices to help manage glycemic control, and require support and resilience for managing day to day chronic disease management tasks (37) . Strict community lockdowns and limited access to nursing stations could have led to the disruption in self-management of diabetes care activities. These factors, coupled with being less physically active, sleeping more, and spending less time outside, may contribute to the disruption of diabetes management. A study in Japan reported increased A1C levels in adult patients living with T2D due to low levels of physical activity and increased food consumption due to pandemic stress (38) . A study in India of 1,510 persons living with type 1 and T2D with a mean age of 41.6 years reported that participants faced similar issues in the disruption of glycemic control during the COVID-19 pandemic, a majority experienced an increase in blood glucose levels (78.4%), a decrease in clinic visits due to fear of getting infected with COVID-19 (90.4%), decreased physical activity (69.1%), and increased food intake (46.9%) compared to before the pandemic (39).

Our study revealed that the COVID-19 pandemic has had various impacts on the daily lives of adolescents and young adults living with T2D. A majority of participants felt less socially connected and J o u r n a l P r e -p r o o f spent less time with their friends in person. However, they felt satisfied with their lives since the pandemic began, reporting positive strategies to cope with stress and anxiety.

One of the great strengths of the study is the description of a distinctive cohort of pediatric patients in Canada who reside mostly in rural First Nations communities with unique living circumstances. Given that the evidence on the impacts of the COVID-19 pandemic on adolescents and young adults living with T2D has been scarce in this area, this study provides novel insight into the challenges and experiences that this cohort currently faces. Second, we used the ECHO COVID-19

Questionnaire which is a standardized tool that is part of a repository of COVID-19 research tools developed by the ECHO COVID-19 Task Force in the United States, enhancing data harmonization and interoperability. There are several limitations in our study. First, it was limited by its cross-sectional design and self-reported mental health data. Second, the sample size was relatively small and lacked diversity compared to the broader pediatric T2D community. Participants who could not be reached had phone numbers that were not in service, or did not answer and return the calls. Third, the cohort was mainly from the province of Manitoba and may not be generalizable to other Canadian provinces nor to places outside of Canada. Although we do not know if our findings are generalizable, there are shared characteristics of youth and adolescents most at risk for the development of T2D including membership in an ethnic minority group, high rates of poverty, food insecurity, parental unemployment and low parental education (40) . Fourth, the survey was conducted during the first lockdown period and prior to the first COVID-19 epidemiological wave in Canada, where Manitoba was largely unaffected compared to other provinces in Canada (1). Fifth, the degree of public health restrictions varied between the provinces and between regional health districts within a province, which changed over the course of the pandemic. This A1C, hemoglobin A1C; ACR, albumin-to-creatinine ratio. Data is presented as mean ± SD, and median and IQR. All variables in Table 1 were collected in the pre-COVID-19 period, except for the COVID-19 period variables (A1C, ACR, and blood pressure), and the age and duration of diabetes for survey respondents which were calculated at the time of survey completion. 10 Loss of sense of smell or taste 11 Itchy/red eyes 12 None of the above  skip to Section A, Question 3.

Which of the following occurred as a result of your symptoms? (Mark all that apply) 01 I was kept overnight in a hospital because a healthcare provider thought I had COVID-19 02 I saw a healthcare provider in person, such as in a clinic, doctor's office, urgent care, or Emergency Room (ER)/Emergency Department (ED) 03 I spoke to a healthcare provider over the phone, by email, or online 04 I self-isolated or quarantined at home 05 None of the above 2.b. In the two weeks before you had symptoms, did you: (Mark all that apply) 01 Have contact with someone who tested positive for COVID-19 02 Have contact with someone who likely had COVID-19 (e.g., was not tested but had symptoms; was told by a healthcare provider that he/she likely had it) 03 Travel to a different state or country (please specify: ___________________) 04 None of the above 

Self-Report Primary Version iCARE Cohort Version 1 -May 2020

The Improving renal Complications in Adolescents with type 2 diabetes through REsearch (iCARE) cohort study 

Self-Report Primary Version iCARE Cohort Version 1 -May 2020

The Improving renal Complications in Adolescents with type 2 diabetes through REsearch (iCARE) cohort study 

Self-Report Primary Version iCARE Cohort Version 1 -May 2020

The Improving renal Complications in Adolescents with type 2 diabetes through REsearch (iCARE) cohort study 10 Loss of sense of smell or taste 11 Itchy/red eyes 12 None of the above  skip to Section A, Question 3.

Which of the following occurred as a result of the child's symptoms? (Mark all that apply) 01 The child was kept overnight in a hospital because a healthcare provider thought he/she had COVID-19 02 The child saw a healthcare provider in person, such as in a clinic, doctor's office, urgent care, or Emergency Room (ER)/Emergency Department (ED) 03 You/the child spoke to a healthcare provider over the phone, by email, or online 04 You/the child self-isolated or quarantined at home 05 None of the above 2.b. In the two weeks before the child had symptoms, did he/she: (Mark all that apply) 01 Have contact with someone who tested positive for COVID-19 02 Have contact with someone who likely had COVID-19 (e.g., was not tested but had symptoms; was told by a healthcare provider that he/she likely had it) 03 Travel to a different state or country (please specify: ___________________) 04 None of the above The Improving renal Complications in Adolescents with type 2 diabetes through REsearch (iCARE) cohort study 

COVID-19 daily epidemiology update

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COVID-19 in diabetic patients: Related risks and specifics of management

Comparative profile for COVID-19 cases from China and North America: Clinical symptoms, comorbidities and disease biomarkers

Associations of type 1 and type 2 diabetes with COVID-19-related mortality in England: a whole-population study

Certain Medical Conditions and Risk for Severe COVID-19 Illness

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Impact of COVID-19 and lockdown on mental health of children and adolescents: A narrative review with recommendations

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Type 2 diabetes in youth is a disease of poverty

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World Health Organization. WHO Timeline -COVID-19

Distribution of 24-h ambulatory blood pressure in children: Normalized reference values and role of body dimensions

Practical recommendations for the management of diabetes in patients with COVID-19

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Quarantine Due to the COVID-19 Pandemic From the Perspective of Pediatric Patients With Type 1 Diabetes: A Web-Based Survey. Front Pediatr

Caring for children and adolescents with type 1 diabetes mellitus: italian society for pediatric and adolescent diabetes (ISPED) Statements during COVID-19 pandemia

School and pre-school children with type 1 diabetes during Covid-19 quarantine: The synergic effect of parental care and technology

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Mostly worse, occasionally better: impact of COVID-19 pandemic on the mental health of Canadian children and adolescents

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Problematic internet use among young and adult population in Bangladesh: Correlates with lifestyle and online activities during the COVID-19 pandemic

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Needs and Coping Behaviors of Youth in the U.S. During COVID-19

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A cross sectional study reveals severe disruption in glycemic control in people with diabetes during and after lockdown in India

Youth-onset type 2 diabetes consensus report: Current status, challenges, and priorities

The authors thank all adolescents and young adults in the iCARE Cohort Study, their families and broader communities for their support of the iCARE study. The authors would also like to thank the NIH 

3. What type of internet access do you have at home? (Mark all that apply) 01 High-speed broadband internet ("WiFi") (e.g., DSL, cable, fiber optic) 02