key: cord-0899634-epyr0l03
authors: Kofoed, Poul‐Erik; Timm, Signe
title: The impact of COVID‐19 lockdown on glycaemic control and use of health services among children followed at a Danish diabetes clinic
date: 2021-10-05
journal: Acta Paediatr
DOI: 10.1111/apa.16128
sha: 6bb713b879fd89c0d33540dbf018ed6bac82574f
doc_id: 899634
cord_uid: epyr0l03

AIM: During COVID‐19 restrictions, the paediatric clinic only accepted essential outpatient visits, schools closed, sports activities and social life were limited. Most employees worked at home. This quasi‐experiment evaluates how this affected glycaemic control and use of health services among children with diabetes. METHODS: Paired t‐tests were used to compare HbA1c‐values before, during and after lockdown. Sub‐analyses were stratified by pre‐lockdown HbA1c‐values. RESULTS: Overall mean HbA1c decreased from 58.3 to 56.9 mmol/mol (p = 0.025) from pre‐ to post‐lockdown, a decrease also seen during the same season the previous year. HbA1c decreased by −4.2 mmol/mol (p = 0.002) for patients with pre‐lockdown HbA1c > 59 mmol/mol, but increased slightly by 0.8 mmol/mol (p = 0.176) for patients with HbA1c < 52 mmol/mol. HbA1c measured 8 months post‐lockdown increased again, most pronounced for patients with lowest HbA1c. During lockdown, virtual contacts increased from 0.1 to 0.5 contacts/patient/month and stayed post‐lockdown at 0.3 contacts/patient/month. CONCLUSION: Compared to 2019, overall the COVID‐19 restrictions did not influence the glycaemic control negatively. However, patients with pre‐lockdown HbA1c < 52 mmol/mol experienced a deterioration, whereas those with HbA1c > 59 mmol/mol experienced an improvement. Less stress and more contact with parents may contribute to the last‐mentioned finding. The lockdown enforced more virtual contacts between patients and the clinic.

during the initial national lockdown, 1 8% were send home temporarily. 2 Furthermore, the unemployment rate increased to 6%. 3 Thus, more than half of the Danish workforce was home full-or part-time.

On April 15th, the kindergartens re-opened, and children in The number of visits to diabetes clinics is a significant predictor of HbA1c, 4 and frequent attendance at outpatient clinics leads to improved glycaemic control. 5, 6 Corroborating this, both reducing the number of clinical contacts and having a high rate of cancelations or no-shows have been shown to lead to higher HbA1c levels, 7-10 and a strike among health staff at a diabetes clinic led to an increase in HbA1c levels, mainly in patients with better glycaemic control. 11 Due to the evidence of the importance of frequent and regular contact with the paediatric diabetic clinics, both the International Society for Paediatric and Adolescent Diabetes (ISPAD) and the Danish health authorities recommend that children and adolescents with diabetes be seen at least every 3 months. 12, 13 To evaluate the impact of the COVID-19 lockdown and the resulting restrictions and adjustments in health care on the glycaemic control of the children and adolescents with diabetes type 1, we made use of this natural quasi-experiment and investigated the changes in HbA1c and the use of the services offered by the diabetes clinic before, during and after the nationwide lockdown. Because of the COVID-19 restrictions, only outpatient visits considered to be essential by the paediatrician or the diabetes specialist nurse were accepted at the department from March 15th to May 15th resulting in much less patients being invited to come physically to the clinic. Furthermore, even in these cases, some patients/parents cancelled the appointments, as they were afraid of contracting COVID-19 at the hospital. During the lockdown period, the clinic offered telephone and video consultations as a replacement for faceto-face consultations.

The study population included patients with type 1 diabetes diagnosed before 2020 and not moving or being transferred to an adult diabetic clinic before November 1st 2020. Information on which patients used insulin pumps and continuous glucose monitors (CGM) and flash glucose monitors (FGM) were drawn from the patients' medical records.

The routinely measured HbA1c from just prior to lockdown (last measurement on or before March 14th 2020, but no earlier than December 15th 2019: HbA1c(3)) and just after the lockdown of the outpatient clinic (first measurement on or after May 15th but no later than August 14th 2020: HbA1c(4)) was registered. For comparison, the HbA1c measured in the same periods 1 year previously were used (December 15th 2018-March 14th 2019: HbA1c(1) and

May 15th-August 14th 2019: HbA1c(2)). Finally, the last HbA1c measured before January 14th 2021, but no earlier than October 1th 2020 (HbA1c(5)), was registered ( Figure 1 ). to January 14th 2020 (period 2)) ( Figure 1 ). In addition, virtual contacts and visits at the diabetes clinic during the periods prior to the lockdown (periods 1 and 2), during the lockdown (period 3), and following the lockdown (period 4) were presented as descriptive statistics (median, minimum and maximum number of contacts/patient/month).

According to the regional ethics committee of the Region of southern Denmark, no ethical approval was needed. Permission for evaluating the impact of the COVID-19 restrictions on the outcome of the diabetes patients was according to guidelines granted by the hospital management (21.08.2020).

In January 2020, a total of 220 type-1 diabetes patients were followed at the clinic. As 26 patients left the clinic before November 2020, 194 were included in the study. Among these, 23 Table 1 .

In paired t-test, comparing mean HbA1c levels before and after lockdown (HbA1c(4)-(3)) showed a mean HbA1c level of 58.3 ± 11.6 mmol/mol before and of 56.9 ± 12.2 mmol/mol after lockdown corresponding to a statistical significant decrease of (Table 3) .

Stratifying by age showed similar results for seasonal variation in the two age groups (data not shown).

Secondary analyses showed that when the diabetes clinic was back to normal operation, mean HbA1c levels increased (HbA1c (4) F I G U R E 1 A timeline illustrating the time points of HbA1c measurements and the periods during which the number of contacts to the diabetes clinic were counted. For HbA1c(1), HbA1c(3) and HbA1c (5), the latest value in the interval was registered and for HbA1c (2) and HbA1c(4), the first value in the interval was registered 

The importance of patients with diabetes being seen regularly has been confirmed by many studies. [4] [5] [6] [7] [8] [9] [10] [11] . We therefore expected that the reduced availability to the paediatric diabetes team would have caused deterioration in the glycaemic control. However, overall we found a significant improvement in mean HbA1c from before until after the period with restricted access to the diabetic clinic. As the lockdown took place during spring, the improvement in HbA1c could be explained by seasonal changes, which was confirmed by a comparison with the changes in HbA1c during the same period in 2019, indicating that overall the metabolic control of the patients followed at the clinic did not change due to the lockdown.

We have previously shown that the better the glycaemic control, the greater the negative effect of reducing the availability to the diabetic clinic. 11 A Spanish study in adults found an improvement during lockdown mainly in patients with poorer baseline control. 15 One of the few studies in children and adolescents comparing HbA1c from before until after lockdown also found an improvement, which was inversely correlated with HbA1c values measured just before lockdown. 16 A brief report from Sweden found an unchanged HbA1c during the first 7 months of 2020 compared to 2019. 17 Other studies comparing CGM or FGM readings in adults [18] [19] [20] and in children 21, 22 have shown overall improvements in glycaemic control during lockdown. However, as these studies did not take season into consideration, the improvement could be due to season.

Paired t-test comparing HbA1c(1) and HbA1c(2), in addition with paired t-test investigating the seasonal variation in HbA1c levels in 2019 (HbA1c(2)-(1)) and 2020 (HbA1c(4)- (3)) for all patients and stratified by pre-lockdown HbA1c (HbA1c (3) (2) 

As seen in Table 1 , the children with poorer glycaemic control before lockdown were older, which agrees with the fact that glycaemic control often deteriorates during the teenage years. We have previously shown that shortening the interval between visits to the diabetes clinic helped the children with higher HbA1c to improve their glycaemic control. 6 Nevertheless, for children with the poorer glycaemic control, HbA1c decreased from 69.9 to 65.7 mmol/ mol despite of not being seen at the clinic. Even though many children achieve the ability of self-care by the age of around 12 years, non-adherence is particularly an issue with adolescents. 23 During lockdown, the schools were closed for the children of approximately 12 years and above, and social activity outside the closest family was almost non-exciting. As around every second adult either worked from home full-or part-time or was unemployed, 1-3 most children and adolescents spend much more time than usual with one or both parents. The more regular lifestyle, the more regular and for some probably better quality meals combined with the possibility of more support and help from parents could explain the significant improvement in glycaemic control for this group of patients despite of probably less physical activity.

In contrast to the patients with the poorer glycaemic control, the children with the better glycaemic control did not improve their HbA1c during lockdown, if anything a slight deterioration was seen.

For these patients, the positive effect of spending more time with a parent was probably less, as they were younger and therefore tended to get more support at school and to have less social challenges and demands. 24, 25 We have previously seen a negative effect of not offering consultations during a period of 2 months for the children with better control. 11 Therefore, we speculate that the lack of physical consultations at the clinic could have had a negative effect on these patients, even though the number of virtual contacts increased considerably.

However, other factors were at play, one of the most important being the reduced opportunity for physical activity. Regular physical activity is recommended for all patients with diabetes, 26 and a meta-analysis has shown a significant reduction in HbA1c as a consequence of physical activity. 27 After the services at the hospital returned to normal and schools reopened, restrictions continued to varying degrees for the rest of 2020 hampering social life and limiting the possibility to participate in sport activities. 28 In fact, 8 months after the reopening, the mean HbA1c had increased significantly and had returned to or slightly above the pre-lockdown value while one would have expected the glycaemic control to continue to improve as has happened during recent years. 7, 29 The patients with the worse glycaemic control pre-lockdown not only had the best outcome during the initial lockdown period; they also had the smallest increase in HbA1c post-lockdown.

One can hypothesise that even though the restrictions imposed on their lives had a negative effect on physical activity, the more regular daily life and the more regular contact with the parents due to many still working at least part-time at home had the opposite effect and overall resulted in only a slight increase in HbA1c post lockdown. 22 Actually, these patients ended up having a better glycaemic control after the first 10 months of the pandemic than they had pre-lockdown.

The patients with the better pre-lockdown HbA1c-values had the largest increase post-lockdown, which may indicate that the restrictions imposed on their daily lives had a negative impact on the glycaemic control, where the lack of physical activity could be one of the factors. 27 The better opportunity of getting support from the diabetes clinic and of having closer contact to the parents might thus have been less important for this group of patients. This corroborate a recent Danish study finding that children with HbA1c < 59 mmol/ mol indicated having sufficient support from teachers and fellow students. 25 Before March 2020, the patients had a median of 0.5 face-toface consultations per months, which corresponds to what has previously been seen at the clinic. 7 As expected, very few consultations were performed during the lockdown period. It has been anticipated that the experience obtained in using telephone and video consultations during the COVID-19 pandemic will cause some face-to-face contacts to change to virtual contacts. 30 That the number of physical consultations after re-opening increased to pre-lockdown levels could be due to the patients and the clinicians going back to old habits, but is more likely due to a backlog following the 2 months closure of the clinic. Prior to lockdown, the number of virtual contacts was approximately 0.1 per patient per month 7 ; this increased to approximately 0.5 during lockdown, and decreased only slightly during the following 8 months indicating that a change in the contact pattern might actually have taken place. Considering the experience from the lockdown period and with the increased use of diabetes technologies, more face-to-face contacts could be expected to be replaced by telemedicine consultations. 30 However, we need to be cautious as face-to-face contacts between healthcare providers and patients are invaluable, especially when dealing with children and adolescents. 17, 25 A methodological strength of the study is the relatively high number of observations and the long follow-up time. A limitation is that HbA1c was measured using Afinion HbA1c DS 100 analyzers with a measurement variation of 2%. 14 However, we expect the measurement error to be random, and thus the precision is improved by investigating group means. In addition, we depended on HbA1c measurements from visits to the clinic why the intervals from which we accepted values are between 3-4 months. Furthermore, the number of included patients was predetermined by the number of patients followed at the clinic. Therefore, sub-analyses were performed with reduced power.

A limitation of this natural experiment is the potential risk of bias from residual confounding especially from dietary habits and physical activity, which we assume is associated with both lockdown and change in HbA1c-level from time point (3) to (4) . However, information on these parameters was not available. Another limitation is that the analyses did not include download data from insulin pumps and CGM or FGM, which could have given detailed information on the changes in the daily handling of the diabetes (number of insulin doses taken, the total insulin dosage, the time in range, number of scans and carbohydrates entered), whereas HbA1c gives an overall indication of the metabolic control. However, the day-to-day variation in handling of the diabetes was beyond the scope of this paper.

The The experience gained by patients, parents and staff using telemedicine during the lockdown seemed to be used also during the initial 8 months following the normalisation of the diabetic clinic and could be expected to have an impact on future consultations.

We thank Hans Jørn Refsgaard Jørgensen, specialist consultant, Lillebaelt Hospital, University Hospital of Southern Denmark, for helping draw data from the hospital registration system.

Poul-Erik Kofoed https://orcid.org/0000-0002-4854-5777

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