Impact of COVID-19 lockdown on blood glucose levels in pediatric patients with type 1 diabetes mellitus
Article information
Abstract
Purpose
The coronavirus disease 2019 (COVID-19) pandemic brought stringent social distancing measures, resulting in changes to daily routines such as increased time at home, remote learning, altered meal schedules, and reduced physical activity. Therefore, we aimed to investigate the impact of the COVID-19 lockdown on glycemic control among pediatric patients with type 1 diabetes.
Methods
This study retrospectively analyzed the medical records of 47 pediatric patients with type 1 diabetes who visited Ajou University Hospital before and after the lockdown. To analyze the effects of the lockdown on glycemic control, we examined the change in glycated hemoglobin (HbA1c) levels before and after the lockdown.
Results
Among 47 patients, 23 (49%) were female and the average age before the lockdown as of March 2020 was 11.65±3.03 years. The mean HbA1c levels were 8.22%±1.69% and 7.86%±1.57% before and after the lockdown, respectively, showing better glycemic control during the lockdown (P=0.001). The decrease in HbA1c was more significant in subjects with higher pre-lockdown HbA1c levels, older patients, and individuals not using continuous glucose monitoring or continuous subcutaneous insulin infusion. However, from a long-term perspective, HbA1c levels at 3 years and 1 year before and after the lockdown were not significantly different.
Conclusions
This study demonstrated the beneficial effect of intensive social distancing for COVID-19 on blood glucose control in pediatric patients with type 1 diabetes mellitus. Furthermore, changes due to the lockdown had a more pronounced effect on patients with existing poor glycemic control.
Highlights
· During the COVID-19 lockdown, glycemic control improved in pediatric type 1 diabetes patients, especially in older ones and those with poorer pre-lockdown control.
· These findings emphasize the positive impact of lifestyle changes on glucose regulation in struggling patients.
Introduction
In December 2019, a novel respiratory virus known as severe acute respiratory syndrome coronavirus type 2, causing coronavirus disease 2019 (COVID-19), emerged in Wuhan, China, and spread worldwide, leading to its declaration as a pandemic by the World Health Organization in 2020 [1]. To prevent the spread of COVID-19, many countries imposed movement restrictions and quarantines, greatly affecting the lifestyles of patients with chronic diseases such as type 1 diabetes mellitus (T1DM). In South Korea, a stringent social distancing policy was implemented in March 2020, encompassing restrictions on private gatherings, active promotion of remote work, transition of schools to online classes, and pre-screening tests before hospital visits [2,3].
Appropriate insulin administration, lifestyle modifications, emotional stress, and parental involvement are important factors in regulating blood glucose in pediatric patients with T1DM [4]. During the COVID-19 lockdown, significant changes occurred in the lifestyles of T1DM children, potentially affecting their blood glucose regulation. Based on previous studies, evidence indicated a deterioration in glycemic control among pediatric patients with T1DM during the COVID-19 lockdown period, attributed to reduced physical activity and difficulties in hospital visits [5,6]. However, contrasting findings indicated that prolonged stays at home facilitated effective collaboration with parents and enabled a structured lifestyle, improving blood glucose regulation [7-9].
This study aimed to assess the effects of the COVID-19 lockdown on blood glucose regulation in pediatric patients with T1DM in Korea.
Materials and methods
1. Study participants
A retrospective analysis was conducted on data from all patients <18 years of age diagnosed with T1DM and receiving follow-up care at the Pediatric Endocrinology Clinic at Ajou University Hospital in Suwon, South Korea. Due to the implementation of stringent social distancing measures in South Korea in March 2020, we selected patients with documented glycated hemoglobin (HbA1c) levels before and after March 2020 as our study participants. To assess the prolonged effects of the COVID-19 lockdown, we included only patients who had regularly visited the hospital since at least 2017. We excluded cases in which the medical records at the time of T1DM diagnosis were unclear or changed to a diagnosis of type 2 diabetes mellitus (T2DM) during treatment. In addition, patients with concurrent conditions that could affect serum glucose levels were excluded. This study was approved by the Institutional Review Board of Ajou University Hospital (approval No. AJOUIRB-DB-2024-057).
2. Variable measurements and definitions
Demographic characteristics, anthropometric measurements, and factors affecting glycemic control were obtained from medical records. Body mass index (BMI) was calculated as weight divided by height in meters squared (kg/m2), with BMI z-scores determined based on the 2017 Korean National Growth charts [10]. HbA1c levels were determined using a turbidimetric inhibition immunoassay at Ajou University Hospital.
The diagnosis of T1DM adhered to the 2023 American Diabetes Association criteria [11]. All participants underwent serum C-peptide, anti-insulin antibody, and anti-glutamic acid decarboxylase II antibody tests to confirm the type of diabetes. Diabetic ketoacidosis was defined as hyperglycemia (serum glucose >200 mg/dL) with venous blood pH <7.3, bicarbonate level <15 mmol/L, and ketonuria or ketonemia.
To assess changes in glycemic control before and after the COVID-19 lockdown, we selected HbA1c measurements performed within 3 months before and after March 2020 to allow evaluation of blood glucose regulation before and after the lockdown period. In addition, to evaluate long-term effects, we calculated the mean of all HbA1c values obtained during 1- and 3-year intervals before and after March 2020, followed by a comparative analysis.
3. Statistical analysis
All statistical analyses were performed using IBM SPSS Statistics ver. 28.0 (IBM Co., Armonk, NY, USA). Quantitative variables were expressed as mean±standard deviation. A paired t-test was used to assess significant differences between the periods before and after the lockdown and compare the means of different groups and subgroups. When analyzing changes in HbA1c levels before and after lockdown, independent t-tests were used for categorical variables and linear regression analysis was used for continuous variables. Statistical significance was set at P<0.05.
Results
The present study included 47 patients (23 females and 24 males) with a mean age of 15.08±3.03 years and a median T1DM duration of 8.16±3.34 years (Table 1). Among the patients, 31.9% (15) received continuous subcutaneous insulin infusion (CSII) and 68.1% received multiple daily injections. In addition, 63.8% (30) used continuous glucose monitoring (CGM).
General characteristics of the study subjects (n=47)
The average age of the participants before the COVID-19 lockdown was 11.65±3.03 years. The mean HbA1c before the lockdown was 8.22%±1.69%, with 11 participants (23.4%) in the well-controlled group (displaying HbA1c levels < 7%). The obesity status of the participants was assessed using BMI z-scores, revealing an average of -0.13±1.24 before the lockdown period (Table 2).
Age, HbA1c, and BMI before COVID-19 lockdown
Fig. 1 shows the changes in HbA1c and BMI z-scores before and after the COVID-19 lockdown. A significant reduction in HbA1c was observed during the lockdown period, decreasing from 8.22%±1.69% to 7.86%±1.57% (P=0.001). However, the BMI z-score showed a slight increase during the pre- and postlockdown periods, from -0.13±1.24 to 0.03±1.24 (P=0.020).
HbA1c and BMI before lockdown (orange) and after lockdown (yellow). HbA1c, glycated hemoglobin; BMI, body mass index.
When analyzing the factors influencing the difference in HbA1c levels before and after the lockdown, we observed a significantly greater reduction in HbA1c among patients with poorly controlled levels (HbA1c ≥7%) compared with subjects with well-controlled levels (Table 3). Patients using CGM or CSII showed better glycemic control pre- and postlockdown than nonusers. However, a larger reduction in HbA1c was observed among patients not using CGM or CSII. Based on univariate linear regression analysis, higher prelockdown HbA1c levels and older age were associated with a more significant reduction in HbA1c levels during the lockdown period (Table 4). Furthermore, multivariate analysis using the stepwise method was conducted on the same independent variables; age and HbA1c levels before the lockdown significantly influenced the difference in HbA1c levels before and after the lockdown.
Differences in the change in HbA1c between the preand postlockdown periods
Univariate and multivariate linear regression analysis of possible factors influencing differences in HbA1c
Upon examining the long-term effects of the COVID-19 lockdown on glycemic control, we observed no significant changes in average HbA1c levels over the 3 years before and after the lockdown or within 1 year before and after the lockdown (Fig. 2).
Comparison of HbA1c averages 3 years and 1 year before (orange) and after (yellow) the COVID-19 lockdown period. HbA1c, glycated hemoglobin; COVID-19, coronavirus disease 2019.
Discussion
During the COVID-19 lockdown period, an analysis of blood glucose levels in 47 pediatric patients with T1DM revealed a significant decrease in average blood glucose levels. In this study, HbA1c decreased from 8.22% to 7.86% after the lockdown period. This outcome enhances the understanding of medical and healthcare strategies during emergencies such as COVID-19 and could aid in developing approaches necessary for disease control and prevention. Furthermore, the reduction in HbA1c was more pronounced in patients with high HbA1c levels before the lockdown, older age, and subjects not utilizing technological aids such as CGM and CSII, typically indicative of poor glycemic management. These findings provide an important foundation for seeking more effective strategies in the management of pediatric diabetes.
Factors including patient age, T1DM duration, treatment modality, use of technologies such as CGM and CSII, accessibility to healthcare facilities, and time spent with parents can influence glycemic control in T1DM [12-16]. The nationwide social distancing measures to prevent the spread of COVID-19 increased the time spent at home and brought about overall lifestyle changes, including alterations in eating habits, physical activity, and emotional well-being [17-19]. Although studies on the effect of changes caused by the COVID-19 lockdown on glycemic control in patients with T1DM have been published, the findings have been inconsistent [4,6-9,20-23]. Eberle et al. [24] conducted a systematic review of 25 papers and found that 18 (72%) showed significant improvements in glycemic outcomes, with a meta-analysis indicating a mean HbA1c reduction of 0.05% attributable to the lockdown. Our present study demonstrated similar results, and the diverse outcomes across studies are thought to be influenced by variations in lockdown methods in different countries and potential ethnic differences.
Obesity is an important factor in blood glucose control, although its effects may be smaller in T1DM than in T2DM patients [25]. After the COVID-19 lockdown, numerous studies have reported increased weight gain and a higher prevalence of obesity due to reduced physical activity, inappropriate diet, and insufficient exercise [19,26]. Such studies have been performed in Korea, noting the difference in obesity rates before and after the lockdown [27,28]. Although results showed some variation based on age and sex, these studies consistently revealed an increase in the prevalence of obesity. This present study observed an average increase of 0.16 in BMI z-scores before and after the lockdown, with no significant difference based on age or sex.
The groups that experienced significant changes in blood glucose levels before and after the COVID-19 lockdown were analyzed. A notable decrease in blood glucose levels was observed among older patients, those with higher HbA1c levels just before the lockdown, and subjects who did not utilize technologies such as CGM or CSII. These findings indicate a more significant improvement in blood glucose regulation during the lockdown period in the patient cohort, which was previously anticipated to exhibit poor glycemic outcomes as evidenced by earlier research [16,29,30].
The age of patients with T1DM is a crucial factor in blood glucose regulation [31]. In a previous study analyzing the impact of puberty progression on glycemic control in patients with T1DM, insulin resistance increased as puberty advanced, leading to an increase in the daily insulin dosage. In addition, both patients and caregivers showed a decrease in their efforts regarding blood glucose management [32]. In the present study, when examining HbA1c levels across age groups prior to the lockdown, patients <10 years of age had HbA1c levels of 7.48%±1.27%, subjects 10–13 years of age had levels of 8.22%±1.69%, and those ≥13 years of age had levels of 8.77%±1.97%. However, when analyzing the reduction in HbA1c levels before and after the lockdown, older age groups experienced a more significant decrease, which was interpreted as an increased effect of remote learning during the lockdown period and the extended time spent with caregivers, affecting adolescents who spent more time at school than younger children.
In managing blood glucose levels in patients with diabetes, CGM and CSII are evaluated as innovative technological advancements [33,34]. In Korea, the use of CGM has increased, and patients reportedly experience improvements in glycemic control through more frequent blood glucose measurements [35]. In the present study, patients using CGM or CSII showed significantly lower HbA1c levels before and after the lockdown. However, when analyzing the reduced HbA1c levels during the lockdown period, patients who did not use CGM or CISS showed a greater reduction. This suggests that CGM or CSII users frequently monitored blood glucose levels and adjusted insulin dosages before the COVID-19 outbreak and experienced fewer significant lifestyle changes due to the lockdown.
When analyzing the long-term effects of the COVID-19 lockdown on glycemic control in T1DM patients, significant changes were not observed in average HbA1c levels over the 3 years before and after the lockdown or within 1 year before and after the lockdown. These findings can be attributed to the gradual easing of COVID-19 isolation measures over time. Furthermore, decreased proactiveness in blood glucose control was interpreted as adaptation to the lockdown and return to usual lifestyle patterns.
This study had a few limitations. It was a single-center, retrospective observational study with a small sample size, diminishing the statistical significance. Furthermore, the analysis did not include CGM variables such as time in range as indicators of blood glucose control in T1DM patients, relying solely on HbA1c. Last, the limitation of confirming COVID-19 infection in subjects through medical records resulted in the inability to analyze the effect of COVID-19 infection on glycemic control in pediatric T1DM patients. These limitations hindered the ability to assess the exact degree of blood glucose regulation during the lockdown.
In conclusion, during the COVID-19 lockdown period, a significant decrease in HbA1c levels was observed in pediatric patients with T1DM. These reductions were more pronounced among patients with higher prelockdown HbA1c levels, older age, and subjects not using CGM or CSII. This indicates that lifestyle changes caused by the COVID-19 lockdown had a significant positive effect on glycemic control in patients struggling with glucose regulation. Healthcare providers should pay particular attention to pediatric patients with T1DM and anticipate challenges in glycemic control. Frequent blood glucose monitoring and adherence to regular routines can sufficiently facilitate adequate glycemic control for the patient and the caregiver.
Notes
Conflicts of interest
No potential conflicts of interest relevant to this article were reported.
Funding
This study received no specific grants from any funding agency in the public, commercial, or not-for-profit sectors.
Data availability
The data supporting the findings of this study can be provided by the corresponding author upon reasonable request.
Author Contribution
Conceptualization: MHC, YSS, HSL; Data curation: MHC; Formal analysis: MHC; Methodology: MHC; Writing original draft: MHC; Writing review and editing: MHC, YSS, and HSL.