Glycemic Control in People With Type 2 Diabetes Mellitus Seen in Primary Care During the Covid-19 Pandemic

Purpose: In Brazil, diabetes mellitus represents 8.8% of the population between 20 and 79 years of age. Disease control is associated with adherence to healthy lifestyle habits, promoting adequate glycemic control monitored by glycated hemoglobin. Therefore, the objective of this study was to analyze the glycemic control of people with Type 2 Diabetes Mellitus during the COVID-19 pandemic. Material and methods: The present research was a cross-sectional descriptive study. Through glycated hemoglobin, it evaluated the glycemic control of people with Type 2 Diabetes Mellitus during two periods of the pandemic. The �rst period was from March 2020 to June 2021, and the second was from July 2021 to February 2022. Results: There was a signi�cant reduction in glycated hemoglobin from 8.4% in the pandemic period to 8% (p=0.035) in the stabilization period. This reduction was most evident in the group with glycated hemoglobin ≥ 7 in the pandemic period (p=0.007) and among women (p=0.008). The group who reduced their consumption of ultra-processed foods lowered a glycated hemoglobin from 8.3% to 7.6% (p=0.010), and those who used antidepressants decreased it from 7.6% to 7% (p=0.032). Conclusion:


INTRODUCTION
Type 2 Diabetes Mellitus (T2DM) is a pathology triggered by the decreased functionality of pancreatic β cells and the presence of insulin resistance in muscle, liver, and adipose tissues, encompassing 90-95% of Diabetes cases [1].In 2021, 537 million adults around the world had diabetes mellitus.In Central and South America, there was one person with diabetes mellitus for every eleven adults.In Brazil, diabetes mellitus represented 8.8% of the population aged 20 to 79 years in the same year [2].
Diabetes mellitus is associated with factors related to the epidemiological and nutritional transition of recent decades, such as rapid urbanization, sedentary lifestyle, overweight, the increased life expectancy of the population, and the increased survival of individuals with T2DM.In this sense, the treatment consists of adopting healthy living and eating habits, which may be associated with pharmacological treatment [1,3].
Since Primary Health Care is responsible for more than 90% of the care of people with T2DM, actions such as watching their lifestyle habits, monitoring blood glucose levels, and making adjustments to pharmacological treatment are regular activities of primary care professionals.This care re ects directly on the clinical control of people with Diabetes Mellitus [4].
In December 2019, the rst case of SARS-CoV-2 infection was identi ed in China; due to its rapid contagion, the COVID-19 pandemic situation was declared in the early months of 2020.This disease has impacted global health, and the numbers of infected people and deaths have exceeded 100 million and 2 million, respectively, in approximately one year.Currently, these numbers have more than doubled, with 33.5 million positive cases and 676,217 deaths reported in Brazil alone [5][6].
Before the onset of a viral pandemic, the diabetes mellitus pandemic already presented numerous challenges in controlling its increasing rates.With COVID-19, it was observed that coping measures for coronavirus, such as social distancing, negatively impacted the health of diabetic individuals [7].
This occurred due to reduced access to health services and increased exposure to situations of stress and anxiety associated with changes in the eating behavior of these individuals.Aspects were present in the NutriNet Brazil cohort, due to the increased intake of ultra-processed foods in countries with lower economic development and low education [8][9].
Therefore, an environment of high levels of anxiety and depression, resulting from the loss of loved ones and nancial and food insecurity, can worsen the clinical condition of people with T2DM [10].In this sense, and considering the above facts, the present research became relevant since there is no known information of this nature regarding the access to health care offered in populations of small municipalities to people with T2DM during the COVID-19 pandemic.Therefore, the objective of this study was to analyze the glycemic control of people with T2DM seen in primary care during the COVID-19 pandemic.

Study design and ethics considerations
This was a cross-sectional descriptive study, approved by the Ethics Committee under no.5.047.012,which initially included all individuals with T2DM registered in the primary healthcare database of a small municipality located in the central region of Rio Grande do Sul, Brazil.The exclusion criteria were: 1) being bedridden, 2) living in a long-stay home, 3) missing appointments, 4) advanced cancer, 5) type 1 diabetes mellitus, or 6) being hospitalized (see Fig. 1).
This study was retrospective and prospective, with data collection at two timepoints.The retrospective period, known as the pandemic period, from March 2020 to June 2021, was characterized by exclusively using electronic medical record data.The prospective period was marked by the pandemic stabilization period, from July 2021 until February 2022, and was carried out through interviews, anthropometric evaluations, and consultation of the patients' electronic medical records.
The de nition of the periods occurred according to moments experienced during the pandemic.The pandemic period was characterized by a high number of cases and deaths, the overcrowding of clinical and ICU beds, the absence of vaccines, and the initial phase of the vaccination campaign for COVID-19 associated with stricter measures to combat the movement of people.The stabilization period was characterized by the loosening of restrictive measures, a signi cant increase in the number of people vaccinated against COVID-19, and a gradual reduction in the occupation of clinical and ICU beds.

Data Collection
The following data were collected during both periods: weight and height for calculating body mass index (BMI), glycated hemoglobin (HbA1c), total cholesterol (TC), high-density lipoprotein (HDL-c), low-density lipoprotein (LDL-c) and triglycerides (TG).
During the consultations, besides the collection of anthropometric data and the request for laboratory tests, a questionnaire on sociodemographic characteristics, lifestyle, and self-care habits was also applied to the current behavior of people with T2DM and the period before the pandemic, making it possible to compare these two moments.
The glycemic control of individuals was determined by HbA1c, according to therapeutic goal criteria for adults proposed by the American Diabetes Association [11].Values less than 7% were considered reasonable glycemic control, and values equal to or greater than this were deemed to indicate inadequate glycemic control [12].
While the lipid pro le was classi ed according to the V Brazilian Guideline on Dyslipidemia and the Prevention of Atherosclerosis [13], updated in 2017.The following classi cation criteria were considered for fasting collections: isolated hypercholesterolemia when LDL-c ≥ 160mg/dL; isolated hypertriglyceridemia in the isolated increase of TG at levels ≥ 150mg/dL; mixed hyperlipidemia in a concomitant increase of LDL-c (LDL-c ≥ 160 mg/dL) and triglycerides (TG ≥ 150 mg/dL) or even HDL-c ≥ 190 mg/dL, in cases where TG was ≥ 400mg/dL; and low HDL-c when levels were < 40 mg/dL in men and < 50 mg/dL in women in isolation or associated with increased LDL-c and TG [13].

Statistical Analysis
After collection, the data were analyzed with IBM SPSS version 25.The Kolmogorov-Smirnov and Shapiro-Wilk tests were performed to analyze normality.Next, the independent and paired samples T-test, according to their criteria.For categorical variables, McNemar's test was used.The results were considered statistically signi cant at p < 0.05.

RESULTS
This study included 134 people with T2DM.Initially, the sample included 456 individuals registered with diabetes mellitus in the municipal health system, but 157 were not found through telephone contact or social networks.Later, it was necessary to exclude a further 165 individuals; of these, 77 were registered as having T2DM but did not have the disease, and 88 were omitted due to the following exclusion criteria: being bedridden (15), living in a long-stay home (9), missing appointments (58) and having at least one of the following conditions: cancer in advanced stages or type 1 diabetes mellitus, or being hospitalized (6).
Among the 134 people with T2DM who participated in this study, the median age was 62 years (52-70), 64.2% (n=86) were women, and 35.8% (n=48) were men; the majority were white (82.8%), with low education levels (67.91%), a per capita income of R$950.00, and with 70.9% being married and living in urban regions (82.1%), the median time since the diagnosis of T2DM was eight years, as seen in Table 1, along with the detailed categorization of the sample.
Regarding lifestyle habits, individuals who reported having a continuous sleep without waking up during the night showed a reduction in HbA1c from the pandemic period to the stabilization period of 8.4% (2.24) and 7.8% (1.67) (p=0.020),respectively, as shown in Table 2. On the other hand, people with T2DM who reported consuming fruits and vegetables frequently showed a non-signi cant reduction in HbA1c, from 8.2% (2.11) in the pandemic period to 7.8% (1.87) in the stabilization period (p=0.208).At the same time, those who mentioned avoiding the consumption of ultra-processed food showed a signi cant reduction in HbA1c from 8.3% (2.13) to 7.6% (1.43), respectively, from the pandemic period to the stabilization period (p=0.010), as shown in Table 2.
Regarding the use of insulin during the COVID-19 pandemic, there was a signi cant increase from 22.39% who used insulin before the pandemic to 30.60% (p=0.003;Table 3).As with insulin, there was also a substantial increase in the use of antidepressants; 32.84% of the individuals haf already used one of these drugs before the pandemic.This increased to 48.51% during the pandemic (p<0.001;Table 3).
In addition, individuals who used insulin showed a median HbA1c of 9.5% (7.8-11.6) in the pandemic period and 8.5% (7.5-10.4) in the stabilization period (p=0.135).On the other hand, individuals who did not use insulin but used antidepressants showed a signi cant reduction in HbA1c from 7.6% (1.95) to 7.0% (1.19), respectively, from the pandemic period to the stabilization period (p=0.032), as shown in Table 2. Some changes in the lifestyle habits of people with T2DM were observed after the COVID-19 pandemic emerged.It was shown that only 18.7% remained active (p<0.001)during the pandemic, while 48.9% of individuals remained active before the pandemic (p<0.001).The same occurred with the consumption of alcoholic beverages, which went from 30.8% to 17.9% during the pandemic (p<0.001)(Table 3).

DISCUSSION
Numerous aspects in uence the management of people with T2DM: environmental, psychosocial, and economic factors can both improve and impair the glycemic control of these individuals [16][17].In this sense, the COVID-19 pandemic brought unusual aspects to treating people with T2DM.In Brazil, decentralized management was adopted to contain the spread of the Sars-CoV-2 virus, leaving it to each Brazilian state to de ne the need or not to adopt a lockdown.In the state of Rio Grande do Sul, the municipalities had the autonomy to determine the degree of restriction of the measures to be adopted.
The municipality studied did not adopt a lockdown; however, people were strongly encouraged not to leave their homes.Public services were only available in remote mode, with only emergency services in primary health units and hospitals and restricted services in commercial establishments.
Given this scenario, a reduction in HbA1c was observed in the present study from the pandemic period to the stabilization period (p = 0.035), being more present among people with HbA1c ≥ 7% in the pandemic period.These showed a more signi cant reduction between the two periods (p = 0.007) compared to individuals who had reasonable glycemic control (HbA1c < 7).This suggests that the group that had more di culty achieving glycemic control may have bene ted from the change in pharmacological therapy between the two periods, as recommended by the current guidelines of the Brazilian Diabetes Society According to the research conducted in the state of Rio de Janeiro, Brazil, with people who had T2DM, they veri ed a reduction in HbA1c from 7.9-7.7%(p = 0.004) before and after lockdown, respectively, considering insulin as the only predictor associated with HbA1c decline and attributing the longer time for self-monitoring of insulin as possibly being responsible for the better glycemic control after lockdown [19].At the same time, a cohort study conducted in the south of this country evaluated individuals with Type 1 Diabetes mellitus using medical record records from 2019 to 2020 during the COVID-19 pandemic.
In the present study, individuals with T2DM who had continuous sleep showed a signi cant reduction in HbA1c from the period pandemic to the stabilization period compared to those who woke up during the night (p = 0.022).A meta-analysis published in 2017 suggests that intermittent sleep may hinder glycemic control, leading to increased HbA1c [21].At the same time, the American Diabetes Association recommends monitoring sleep quality and quantity as part of medical research in the care of persons with T2DM [22].
The group of women showed a reduction in HbA1c between the two periods of this study.According to previous studies, this result may be associated with the fact that women often have better self-care regarding T2DM when compared to men in aspects such as greater demand for medical care, more frequent blood glucose monitoring, and the adoption of healthier living and eating habits [23][24].
In this study, people with T2DM who avoided consuming ultra-processed foods also showed a signi cant reduction in HbA1c between the pandemic and stabilization periods (p = 0.010).This reinforces the importance of eating habits in treating T2DM, as recommended in the Brazilian Diabetes Society guidelines [4,3,1].
The fragility of the study population in maintaining self-care during the pandemic is of particular note, especially when factors such as income, education, and length of disease may have in uenced the individual coping with T2DM.These variables have already been associated with differences in self-care for people with T2DM in research conducted before the COVID-19 pandemic [25].Later, during the COVID-19 pandemic, the NutriNet Brazil cohort associated low education and income with the lower consumption of fruits and vegetables, corroborating the present study's ndings, which identi ed the reduced consumption of this food group during the COVID-19 pandemic [9].At the same time, studies conducted in high-income and educated populations recognize increased consumption of these foods [26][27].
However, the reduction in the consumption of ultra-processed foods was not con rmed in a secibd survey conducted in Brazil, by applying the online questionnaire during the COVID-19 pandemic, in which they found an increase in the consumption of sugary drinks and fast food: 13.25% and 20.42%, respectively [26].However, the study conducted by Negrão and colleagues was conducted with people mostly with undergraduate and graduate degrees and high income.The present research included only people with T2DM, who mostly had low education and revenue, from a small rural town in Rio Grande do Sul.
In addition, a decrease in physical activity was observed, as found in other studies conducted during the COVID-19 pandemic [26-28].It was possibly a direct re ection of the restrictions on the movement of people in the face of the COVID-19 pandemic.
Another aspect that may have in uenced the results of the present study was the increased use of insulin and antidepressants in the pandemic.Similar data were found to those reported in a study conducted in Japan, which indicated the use of insulin by 31.2% of people with T2DM during the pandemic [29].The restrictions on people's movements led to a broad psychological impact, which can be long-lasting and aggravated when associated with nancial di culties, traumatic stress such as job loss, or the loss of a family member [30].
Faced with the psychological impact mentioned above, the current research found that people with T2DM who used antidepressants without the concomitant use of insulin showed a signi cant reduction in HbA1c from the pandemic period to the stabilization period (p = 0.032), even presenting the lowest HbA1c levels (7.6%), in absolute values, compared to the other group strati cations performed in the study.
The population in this study was negatively impacted by the COVID-19 pandemic, mainly due to the reduced access to health services.On the other hand, they tried, as much as possible, to adopt healthier lifestyle habits.The better glycemic control observed in the stabilization period may be associated with the return to healthcare facilities and changes in pharmacological treatments.This is believed to be the rst study addressing the glycemic control of people with T2DM seen in primary care in a small municipality in the interior of Rio Grande do Sul, Brazil, amid the COVID-19 pandemic.Despite the numerous challenges faced when conducting research such as this, the ndings align with other studies conducted during the same period.
Considering that 90% of people with T2DM are assisted in primary care, which is the current space for receiving individuals with T2DM [4], conducting research similar to this seems relevant.Many of the limitations of this study can be mitigated in an environment of normality, outside the COVID-19 pandemic period, or by including individuals from more than one municipality with similar characteristics and geographically close.
Among the limitations, the sample size stands out due to the di culties with contacting patients and the many missed appointments.At the same time, the absence of information in the electronic medical record limited the number of analyses performed.

CONCLUSION
We conclude that there was a reduction in HbA1c in people with T2DM without glycemic control and in women from the pandemic period to the stabilization period during the COVID-19 pandemic.
Changes in dietary habits, such as the reduced consumption of healthy foods (fruits and vegetables), ultra-processed foods, and reduced physical activity, were noted, as were changes in pharmacological therapy.These changes may have in uenced glycemic control, but it is not possible to determine the degree of in uence of each of them.
It is understood that longer studies following people with T2DM are needed, making it possible to improve assistance to these individuals and its replication in similar populations.Determination of the sample and its exclusion criteria.

Declarations
Font: Author construction.

Table 1 :
Categorization of the sample, presenting sociodemographic and clinical information (n=134).

Table 2 :
HbA1c variation between periods, descriptive data, and analysis using paired t-test.

Table 3 :
Lifestyle habits, self-care with DM 2 and pharmacological therapy, comparative between: before and during pandemic (n=134).