Effect of COVID-19 lockdown on Moroccan patients with type 1 and type 2 diabetes

The implementation of coronavirus disease of 2019 (COVID-19) lockdown has affected the daily practices of subjects with chronic diseases such as diabetes and caused negative impact on their lifestyle and habits such as physical activity, dietary habits and accessibility to medications. Diabetic people are considered the most vulnerable groups to COVID-19, and the lockdown measure has disturbed the diabetes self-management. In our study, we aimed to assess, for the first time at the regional level (Souss Massa Region), the COVID-19 lockdown impact on HbA1c levels in patients with type 1 diabetes (T1D) and type 2 diabetes (T2D). We carried out a cross-sectional quantitative analysis at the health center of the industrial district in Agadir City. We found a significant improvement in post-lockdown mean ± SD HbA1c in 150 subjects suffering from T1D and T2D; p = 0.005). Our analysis revealed a significant association of HbA1c deviation with educational level and medical coverage (p = 0.01). No significant association was detected between HbA1c deviation and age, gender, weight, height, current BMI status, fasting blood sugar, family history, urban or rural areas, marital status, professional activity, socioeconomic income, type of diabetes, dietary, comorbidities, diabetic complications, housing, adherence to the dietary recommendations, physical activity, medical appointments, stopping medication, self-monitoring, fasting and anxiety about getting COVID-19. COVID-19 lockdown had no deleterious effect on HbA1c levels in Moroccan patients with T1D and T2D.


Background
In December 2019, a new beta coronavirus of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) had emerged in Wuhan City, China. The transmission rate of the infection, termed COVID-19 by World Health Organization (WHO), was extremely high and it spread rapidly worldwide leading to a global pandemic. On March 11, 2020, WHO had declared COVID-19 as a pandemic. Globally, 216,229,741 coronavirus-confirmed cases and 4,496,681 deaths have been reported in August 2021 according to WHO declarations. In Morocco, COVID-19 led to 853,373 cases and claimed 12,437 lives in August 2021, according to   Dashboard (WHO 2021). In order to mitigate and slow the spread of the disease, public health authorities applied exceptional measures in many parts of the world; social distancing and lockdowns. On March 20, 2020, Morocco established a highly strict lockdown until June 10, 2020, and citizens were advised to remain indoors except for limited necessities such as emergency medical help or alimentary shopping (Cucinotta and Vanelli 2020;Moroccan-Ministry-of-Health;WHO). The implementation of COVID-19 lockdown has affected the daily practices of subjects with chronic diseases such as

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Bulletin of the National Research Centre diabetes and caused negative impact on their lifestyle and habits such as physical activity, dietary habits and accessibility to medications. Diabetes is defined as a chronic metabolic disorder characterized by elevated blood glucose, which includes T1D and T2D. The chronic hyperglycemia is associated with several complications and pathological implications. The major indicator for diabetes assessment is glycated hemoglobin or HbA1c. HbA1c values signify the levels of blood sugar over the previous 2-3 months. Diabetic complications are associated with higher HBA1c (Orban and Ichai 2008). In 2019, WHO estimated 463 million diabetics aged 19 to 79 worldwide (9% for women-9.6% for men) and 1.5 million deaths were directly caused by diabetes. In Morocco, the prevalence in the adult population is 12.4%. Diabetes kills over 12,000 people a year (WHO 2021).

Objectives
Diabetic people are considered the most vulnerable groups to COVID-19, and the lockdown measure has disturbed the diabetes self-management. Within this context, we aimed to assess, for the first time at the regional level (Souss Massa Region), the COVID-19 lockdown impact on HbA1c levels in patients with T1D and T2D.

Study design
Our cross-sectional quantitative analysis was carried out from April 9, 2021, to June 6, 2021, at the health center of the industrial district in Agadir City. According to eligibility criteria, 150 patients were included in this study.

Data collection
Anonymized data were generated from a structured questionnaire created in Sphinx software by taking into consideration the education level of the interviewed patients.
The validated questionnaire consisted of four parts: • Part 1: socio-demographic characteristics including twelve questions (sex, place of residence, age, weight before and after lockdown, height, BMI, level of education, family status, occupation, medical and socioeconomic level according to annual income). • Part 2: disease characteristics including seventeen questions (type and duration of diabetes, therapeutic regimen including dosage and information about therapeutic agents, HbA1c and fasting blood sugar values before and after lockdown, comorbidity, complications and the frequency of monitoring

Participants: inclusion criteria
• Confirmed T1D or T2D based on medical records; fasting blood sugar > 126 mg/dl; HbA1C > 7% • Aged ≥ 18 years with a ≥ 1 year T1D and T2D diagnosis • Recruited and monitored at the Health Center of the industrial district in Agadir City.

Exclusion criteria
• Incomplete medical records • No HBA1c records in the last 3 months • Change of antidiabetic treatment at least 6 months before the lockdown and during the lockdown • Pregnancy • Active oncological illness (confirmed malignancy; under immunotherapy or chemotherapy) • Comorbidity with psychiatric, neurological disorders and non-communicable diseases

Data analysis
Anonymized data were divided according to two different periods: pre-lockdown and post-lockdown. Statistical analysis was performed using IBM SPSS Statistics 23 software. The degree of association was assessed using odds ratio (OR) (95% confidence intervals). A p value ≤ 0.05 was considered statistically significant.

Ethical consideration
• The study was conducted in accordance with Helsinki Declaration. Authorization was obtained by Souss Massa Regional Direction of Health before starting the study while respecting the confidentiality of the data and the respect of anonymity in the processing of the data. All participants gave verbal informed consent to answer the anonymous questionnaire.

Results
Overall ,  The interviewed participants (T1D and T2D) had suffered from diabetes for an average of 11.29 ± 8.73 years with a dominance of T2D for 53.3% (Table 1).

Secondary outcomes
No significant association was detected between HbA1c deviation and age, gender, weight, height, current BMI status, fasting blood sugar, family history, urban or rural areas, marital status, professional activity, socioeconomic income, type of diabetes, dietary, comorbidities, diabetic complications and housing.
No effect of lockdown on weight (kg) was observed: 72.43 ± 14.83 (pre-lockdown) versus 72.24 ± 14.49 (post-lockdown). On the other hand, we observed a slight decrease in adherence to dietary guidelines from 75.3% (pre-lockdown) to 70.7% (post-lockdown). The majority respected the dietary recommendations during the lockdown period. According to the recommendations of the Francophone Diabetes Society, (minimum level ≥ three times 30 min per week) (Duclos et al. 2013), we also reported a slight drop  (Tables 1 and 3). No significant association was detected between HbA1c deviation and adherence to the dietary recommendations, physical activity, medical appointments, stopping medication, self-monitoring, fasting, and anxiety about getting COVID-19. However, a significant association was observed of HbA1c deviation with educational level and medical coverage (p = 0.01).

Discussion
In our original study, we aimed to assess the COVID-19 lockdown impact on HbA1c levels in Moroccan patients with T1D and T2D. We detected an overall improvement in HbA1c value by the end of lockdown time compared to pre-lockdown period. The pre-lockdown mean ± SD HbA1c was 8.35% ± 1.97 versus 7.97% ± 1.57 after the lockdown. The HbA1c deviation was independent of the age, gender, weight, height, current BMI status, fasting blood sugar, family history, urban or rural areas, marital status, professional activity, socioeconomic income, type of diabetes, dietary, comorbidities, diabetic complications, housing, adherence to the dietary recommendations, physical activity, medical appointments, stopping medication, self-monitoring, fasting and anxiety about getting COVID-19. Our findings are consistent with several studies that demonstrated no effect of the COVID-19 lockdown on HbA1c. A study carried out by Anjana et al. in 2020 revealed an improvement in HbA1c (n = 205 T2D): post-lockdown HbA1c = 7.7 ± 1.7 versus 8.2 ± 1.9%, p < 0.001 (Anjana et al. 2020). A meta-analysis performed by Psoma et al. (2020) showed a decrease in HbA1c (%) (n = 380 T2D): pre-lockdown HbA1c (%) 6.9 ± 1.3 versus post-lockdown HbA1c (%) 6.7 ± 0.9; p = 0.015 (Psoma et al. 2020). A pre-and post-lockdown data from 110 adults with T2D noted no significant change in mean HbA1c (Sankar et al. 2020). Retrospective analysis conducted by Pla et al. (2020) detected an improvement in glycemic control in patients with T1D during COVID-19 lockdown (HbA1c: 7.21 ± 0.78% vs 6.83 ± 0.71%, p = 0.0005). Fernández et al. (2020) detected, after the lockdown, that the mean glucose declined from 166.89 ± 29.4 to 158.0 ± 29.0 mg/dL in patients with T1D (n = 307), and their HbA1c decreased from 7.4 ± 1.0 to 7.1 ± 1.0% (54 ± 10.9 vs 57 ± 10.9 mmol/ mol; p < 0.001). In contrary, other studies described a deleterious effect of lockdowns on glycemic control. Recently, Khare and Jindal found a 0.51% increase in mean HbA1c values after home confinement (Khare and Jindal 2021). A study of 101 patients with T2D reported an increase in HbA1c value (from 7.67 ± 1.76 to 8.11 ± 2.48) (Önmez et al. 2020). The reported discoveries, although similar to our present study, demonstrated that the COVID-19 lockdown, regardless of the other risk factors, had no effect on diabetic state and related factors. Possible reasons cited for the decrease in HbA1c levels in our study during lockdown were a more regular lifestyle: stability at home, spending more time with family, less stress due to teleworking conditions, less exposure to pollution, more time to prepare healthy meals, meals on time, increased contribution to household chores, better sleep and awareness of more serious risks complications of COVID-19 and comorbidities.
Difficulties in accessing exercise centers or outdoor exercise could explain the slight decrease in physical activity offset by household chores. The majority of participants maintained self-monitoring and compliance with dietary recommendations during the confinement period, which compensated for the difficulties in traveling to health centers for medical appointments.
Our finding reported a significant association in HbA1c deviation according to educational level and medical coverage. Moderate and high level of education could improve the glycemic control. Several studies have recorded the negative impact of low educational level on diabetic state (Larsson et al. 1999;Kim et al. 2017;Fiseha et al. 2018). The majority of patients have medical insurance, which facilitates access to care and ensures good patient care. Medical coverage can contribute significantly to improving glycemic levels. The cross-sectional study conducted by Canedo et al. 2018 explained the negative impact of the lack of insurance coverage on the quality of diabetes control (Canedo et al. 2018). Glantz et al. (2020) determined that health insurance influences the glycemic control (Glantz et al. 2020). These findings are consistent with our results; the lack of medical coverage constitutes a risk factor for diabetes management. Despite the application of strict confinement and the interruption of health care, patients with T1D and T2D did not experience a worsening of glycemic control, but rather an improvement.

Conclusion
To conclude, the confinement due to COVID-19 did not cause a main disturbance in glycemic balance. Short duration of home confinement might be sufficient to affect significantly the glycemic control and other risk factors. Further work with larger study samples is needed to identify the metabolic changes that occurred after the strict lock-in period. Nonetheless, the slight improvement recorded implies an improvement in public health policies aiming at encouraging telemedicine and raising awareness about maintaining a healthy lifestyle.