key: cord-333487-zem2d4y6
authors: Thomaz Ugliara Barone, Mark; Bega Harnik, Simone; Vieira de Luca, Patrícia; Letícia de Souza Lima, Bruna; José Pineda Wieselberg, Ronaldo; Ngongo, Belinda; Cordeiro Pedrosa, Hermelinda; Pimazoni-Netto, Augusto; Reis Franco, Denise; de Fatima Marinho de Souza, Maria; Carvalho Malta, Deborah; Giampaoli, Viviana
title: The Impact of COVID-19 on People with Diabetes in Brazil
date: 2020-07-03
journal: Diabetes Res Clin Pract
DOI: 10.1016/j.diabres.2020.108304
sha: 
doc_id: 333487
cord_uid: zem2d4y6

Abstract The present study aims atidentifying main barriers faced by people living with diabetes in Brazil during the COVID-19 pandemic. Methods In a convenience sampling study, data were collected from 1701 individuals, aged 18 or above; 75.54% female participants; 60.73% T1D and 30.75% T2D, between April 22nd and May 4th, using an anonymous and untraceable survey containing 20 multiple choice questions (socio-demographic; health status and habits of life during COVID-19 pandemic). Relationship between variables was established using the multiple correspondence analysis technique. Results 95.1% of respondents reduced their frequency of going outside of their homes; among those who monitored blood glucose at home during the pandemic (91.5%), the majority (59.4%) experienced an increase, a decrease or a higher variability in glucose levels; 38.4% postponed their medical appointments and/or routine examinations; and 59.5% reduced their physical activity. T1D, the youngest group, was more susceptible to presenting COVID-19 symptoms despite not being testing; whilst the TD2 group had higher frequency of comorbidities that are additional risk factors for COVID-19 severity. Conclusions This study provides a firsthand revelation of the severity of COVID-19 on individuals with diabetes in Brazil, altering their habits, which impacted their glycemia, potentially increasing their risk of poor outcomes if infected by SARS-CoV-2.

The outbreak COVID-19 has led to an unprecedented global health crisis which is testing health systems' preparedness and ability to cope with a pandemic response [1] [2] [3] [4] . . Brazilexperienced a similar situation. Thefirst SARS-Cov-2 case was officially reported in December 2019 in Wuhan,China, and rapidly spread in the entire country and beyond within 30 days [5] [6] [7] . The first suspected case in Latin America was reported on January 27th in Brazil and the first case confirmed in Brazil on February 26th of 2020 [2, 3, 7] . A series of measures were put in place p to prepare Brazil for the anticipated health crisis prior to the declaration of COVID-19 as being Public Health Emergency of International Concern, on January 30th [2] , and then a pandemic, on March 11th [8] . Following these international alerts,less than a month after the first confirmed case, on March 20th, the Brazilian Ministry of Health recognized that community transmission was already happening in Brazil [2] . Infection by SARS-Cov-2 causes major disruptions and threats ,in addition to the loss of human lives, with case fatality rate ranging from 0.2% in Germany, to 7.7%in Italy [9] , The impact of COVID-19 is beyond imagination and is sparkling a global mourning,booming afeeling of unsafety and uncertainty. On June 9th, according to the World Health Organization (WHO), 7,127,753 cases and 407,159 deaths duetoCOVID-19 were confirmed in 216 countries [10] . FCases and mortality in Brazil reached 739,503 and 38,406 respectively,with a case fatality rate of 5.2% [11] . While this is the highest number of cases and one of the highest case fatality rate in Latin America [12] , scientists argue that cases and mortality are extremely underscored due to the low number of tests performed among other reasons [1, 4, 12, 13] by possible 14-20 times the official reported figures [14] .

Authors of the first Chinese and Italian reports alerted for the worse prognosis of individuals with diabetes and other noncommunicable disease (NCDs), in comparison with populations of the same age group without those chronic conditions [5, [15] [16] [17] [18] . Further retrospective studies have revealed that, within this group of patients, hyperglycemia was associated with higher severity and mortality rates [15, 19, 20, 21] , for reasons under investigation [22, 23] . Additionally, usual comorbidities such as hypertension, cardiovascular disease, older age, and gender (male) also complement increased severity and mortality risks of individuals with diabetes hospitalized due to COVID-19 [24] .

, With a prevalence as high as 16.8 million people or 11.4% of the population between 20 and 79 years old, Brazil is among the top 5 countries with high prevalence of diabetes. Diabetes leads g to more than 135,000 deaths yearly [25] . Brazil struggles with the continuous treatment routine of impacted populations; only 28.8% are considered to be in target, having a glycated hemoglobin A1C below 7.0% (53mmol/mol) [26] . Consequently, 71.2% of Brazilians with diabetes belong to a subgroup more exposed to hyperglycemia , which makes them vulnerable to even higher risk of poor outcomes when infected by the SARS-CoV-2 virus.

This state of affairs calls fordeep commitments from the public health in all its forms and a concrete alignment with the WHO. Unfortunately, in the midst of the fight against this novel virus, Brazil experienced a troublesome atmosphere of political disputes, blinding authorities to make swift decisions aligned with the global technical recommendations [1, 4, 12] . This also harmed adjustments to continue the proper follow-up and management of other diseases, including both communicable and NCDs. For these reasons, the present study aims to investigate challenges encountered by people living with diabetes in Brazil during the COVID-19 pandemic.

Data from individuals with diabetes were collected through an anonymous and untraceable survey containing 20 multiple choice questions in portuguese. The authors shared this survey on social media including Facebook, through their affiliated institutions, co-ligated or partner entities, and diabetes social media groups. Hence, the convenience sampling nature of this study. In addition to being a person living with diabetes, individuals needed to be legally adults (above 18 years old) and accept the terms to share anonymous and untraceable answers. Survey responses were collected from April 22nd through May 4th.

The first question provided a complete overview of the questionnaire and required confirmation of the heath conditon (diabetes) by the respondent. . This was followed by socio-demographic questions related to age, gender, state of residence, capital/country/coast, education level, number of people living in the household, and nature of the health system which could be public, private or both. Subsequent questions served to identify the health status of the participants, asking about diabetes type, and presence and type of comorbidity. All remaining questions covered aspects attributed to the COVID-19 pandemic: frequency of going outside, strategies to protect from infection when outside, noted changes in the glycemic levels, access to medical care, changes in eating habits and physical activity, changes in smoking and drinking habits, and suspected or confirmed COVID-19 infection by the respondent or cohabitant family member. At the end of the survey, the respondent could leave a comment. Several questions and their answers were regarding subjective perceptions, such as "my blood glucose increased", "I am eating more" or "I am exercising much less" than before the pandemic. Therefore, answers should not be interpreted as objective measurements, but as subjective comparisons with the prepandemic states.

A multivariate analysis of dimensions of COVID-19 and types of diabetes (type 1 diabetes -T1D; type 2 diabetes -T2D; others: LADA, MODY, gestational; and unknown) was performed with multiple correspondence analysis (MCA) in R (version 3.6.1) and RStudio (version 1.1.453) [27] .

The survey was answered by 1701 individuals, 75.54% were female respondents, 70.78% between 18 and 50 years old, 64.96% of respondents were from Southeast of Brazil, and the main diabetes types were type 1 (60.73%) and type 2 (30.75%) (full socio-demographic profile in table 1). Among the main reported consequences of the COVID-19 pandemic were: 95.1% reduced frequency of going outside home (among them, 26.9% never went outside since the beginning of the pandemic); among the ones who monitored their blood glucose at home (91.5%), the majority (59.4%) experienced a deterioration, which included: 31.2% are reporting greater variability than before the pandemic, 20% higher glycemia and 8.2% lower glycemic levels. Moreover, 38.4% postponed medical appointments and/or routine exams, and 40.2% did not schedule a medical appointment since the onset of the pandemic. Among recommended habits, slated for diabetes treatment, physical activity was most impacted, with a reduction reported by 59.5% of the respondents (14.7% with a slight reduction and 44.8% with a great reduction). See table 2 for habits and behaviors. Regarding co-morbidities, for the current study and analysis, we opted to group them into the following: 1) "Mental Health" which includes the following conditions: depression, anxiety, bulimia, anorexia and diabulimia; and 2) "Cardiovascular Diseases" comprising : stroke, infarction, hypertension and dyslipidemia. Two other groups were already established in the survey as a single answer, which had a parenthesis to facilitate comprehension, the "Diabetes Related Complications" with: retinopathy, neuropathy and diabetic renal disease; and the "Respiratory": asthma and COPD (table 1) . The analysis revealed the association between age and the occurrence of symptoms of COVID-19, type of diabetes and some of the co-morbidities evaluated (figure 1). People with T1D were among the youngest and appeared in proximity to mental health diseases category, but also close to the no-cardiovascular conditions, no-obesity and no-respiratory disease categories. They were alarmingly close to the category that, despite having symptoms of COVID-19, had no testing for SARS-CoV-2. Not measuring the blood glucose is close to T2D and unknown diabetes type. T2D, not surprisingly, was more associated than other types with older age, cardiovascular diseases and obesity. It is also worth noting that T2D and older group were the closest to test positive for SARS-CoV-2. In opposition, individuals who had symptoms of COVID-19 and were not tested (125 people or 7.35%) presented higher proximity to increased blood glucose (Figure 1 ). Measuring blood glucose was related with food consumption and working out, as depicted on figure 2. Individuals that experienced decrease in blood glucose levels, increased physical activity and decreased food consumption. Meanwhile, higher food consumption and reduced physical activity were associated with higher blood glucose levels. While it seems that the pandemic had a higher impact on habits and glycemic levels of T1D individuals (right side of figure 2), with significant perceived changes, T2D respondents seem to have maintained most of their habits during this period. Individuals who exclusively use the Brazilian public health system (Unified Health System -SUS), which serves more than 70% of the Brazilian population [28] (in our case, 28.16% of the respondents), were who kept venturing out during the pandemic and experienced an increase of blood glucose levels, as shown in figure 3 . T1D individuals were the closest to the use of both health systems (SUS and private) and also experienced higher glycemic variability (ups and downs). They had the ability to have friends or relatives to buy or collect their medicines and medical supplies. Users of the private health system were closer to experience no glycemic changes during the pandemic, using their own stocks of medicine and medical supplies or ordering for home delivery from private pharmacies (Figure 3) . 

The results above unveil short, mid and long-term risks for individuals with diabetes in Brazil. While the federal government and some states made initial commitments and plans [2] , knowing the risks for poor prognosis among individuals living with diabetes and/or other NCDs if infected by SARS-CoV-2. Our data revealed that implemented measures did not cover most of this population. The strategy to distribute medicines and medical supplies for 90 days, as recommended by different organizations [29, 30] , in order to avoid monthly trips were effective for only 21% of the 64.5% who received their medication and supplies from SUS (or 13.5% of the total respondents). This provision of medicines and supplies for 3 months, avoiding the monthly rounds to public primary healthcare facilities or pharmacies, seemed to be the one of the only specific policies to protect individuals with diabetes and others living with NCDs in Brazil [31, 32] . Although limited, this would at least protect them from encountering infected people seeking care. . Meanwhile, at municipality level, certain locations successfully implemented alternative strategies, as hailed by one participant from an inland town: "my town adopted a delivery of medicine method for people with chronic diseases".

According to our data, especially individuals w exclusively depended on SUS were at higher risk, venturing out of home more often and experiencing an increase in blood glucose levels ( figure 3 ). While differences would not be expected, since Brazil prides itself for its Universal Health Coverage, and most people, including the ones with private insurance, rely on SUS to receive part or all their medicines and supplies. We hypothesise that this finding highlights the socioeconomic inequalities in the country, which obliges the less privileged to continue going to work during the pandemic and/or to access affordable food. .

Even though 44.3% of the individuals reported having a family member or friend going monthly to public pharmacies on their behalf to collect medicines and supplies, 49.9% went themselves, perhaps due to lack of direct support.. It is important to highlight that family member's or friend's support may reduce but not eliminate the risk of infection, especially if residing in the same location, acting as a potential vehicle of indirect transmission. Another uncomfortable answer came from 5.8% of the individuals who reported halting collection of their medicines and medical supplies and relying on personal stocks, which might be limited in quantity or expected to expire soon. This situation may place those who avoided leaving their homes during the pandemic in a risky untreated situation, a globally shared concern [15, 17, 33, 34, 35] .

While it is hard to predict social, economic and health impact of a pandemic, specialists alert to the consequences of implementing only light measures [4, 12, 13, 36, 37, 38] , but, at the same time, also the harmful consequences of lockdowns, mobility restrictions and social distancing on the prevention and control of diabetes and other NCDs [17, 34, 39] . Barone et al. [39] reported an association between stricter measures against the pandemic and perceived challenges and fear in the diabetes community in South and Central American, which, when disconnected from information and educational strategies, would increase the pressure on the health systems [37, 39] .

Although decentralized (defined by states and municipalities) and delayed [1, 4, 12, 13, 40] , the measures to contain the SARS-CoV-2 spread in Brazil, and reflected on mobility reduction, was experienced by 95.1% of this study's respondents in different degrees (with 26.9% never going outside). Differently from Kluge et al.'s prediction [17] , in our case it was not associated with increased consumption of alcohol, tobacco and unhealthy foods. Notwithstanding, physical activity was affected, being reduced for 59.5% of the respondents. Other researchers have also reported physical activity reductions during the pandemic, and alerted for the potential negative consequences on metabolic, cardiovascular and musculoskeletal health [41, 42] . These effects were observed even after short periods of inactivity, are hard to recover and, not only increase premature mortality, but also favors the development of diabetes chronic complications [41, 42] . A strategy to minimize those consequences would be developing good channels and partnerships for informing these populations through the internet and TV broadcasting in a structured manner, focusing on preventive measures and maintenance or improvement of habits and behaviors, such as regular physical activity [17, 34, 41, 42, 43] . This recommendation is compatible with the present findings where 87.4% of the individuals maintained or increased their time watching TV and 90.7% maintained or increased their time on the internet.

Regarding treatment, the COVID-19 pandemic, as predicted and observed by different authors, is impacting availability and access to healthcare professionals (HCPs) for the routine care of people with diabetes, since they relocated to emergency rooms, testing sites, ICUs and other services to attend infected individuals [15, 17, 33, 34, 39] . COVID-19 transmission was found to be high among HCPs. . We investigated 38.4% of the individuals who postponed their medical appointments and/or examinations. We attributed these results to shortage of HCPs, as cited by 3 individuals, reporting appointment cancelation or absence of s physician, or personal decision because of the fear of getting infected at a hospital or clinic. Also identified, in other studies as one of the greatest fears of the population [39, 35] . The potential consequence of this phenomenon of fear during the pandemic was reported in a pediatric emergency department, in Italy, with reduction and delay in children's arrival, which included cases of severe ketoacidosis and hypoglycemia [35] .

Although online consultation and other telemedicine strategies were not investigated profoundly in the present study, one of the respondents commented that he/she was having online medical appointments. Brazilian laws and regulations became more flexible allowing this type of approach during the COVID-19 pandemic [44] . In alignment with other authors and international organizations, we highly recommend it [15, 33, 36, 45, 46, 47, 48] , reinforcing Primary Healthcare's role during the pandemic through ensuring close and timely monitoring of people with diabetes and other NCDs [37, 44, 49] The results show thatall types of diabetes were close to additional risk factors for poor prognosis of individuals infected by SARS-CoV-2. While T2D and unknown diabetes type (figure 1) appear near other NCDs (especially cardiovascular and obesity) [18, 24, 47, 50, 51] , T1D and other types (LADA, MODY and gestational grouped) presented close proximity to glycemic variability (figure 2) [5, 15, 52] . Therefore, we suggest that none of the types should feel safe. Although, not surprising, T2D was associated with "50 years and older" (figure 1), and it is known that the COVID-19 mortality and severity increase with age [5, 24, 53] .It was unfortunate the proximity of individuals reporting increased blood glucose levels and the presence of COVID-19 symptoms without testing (figure 1). The global shortage of tests for SARS-CoV-2 poses a grand challenge [2] [3] [4] , however, cognizant that high blood glucose increases the risk for infection severity and death [15, 19, 20, 21, 22, 23] , early testing efforts are recommended in this group. In addition, supporting them in intensifying their diabetes self-care practices to quickly bring their glycemia back on track must be prioritized [45, 51, 54] . Figure 2 depicts the importance of balancing food and exercise, since individuals who increased or decreased any of them experienced changes in their blood glucose levels, whereas those able to maintain exercise and food consumption avoided glycemic changes.

While the present study focused only on diabetes, WHO's data show that other NCDs serviced in similar health systems and pandemic environment, are facing comparable challenges [55] . In terms of unattended needs of individuals with diabetes during this COVID-19 crisis, Brazil is not the only country with unaddressed demands. In a collection of testimonials from people with diabetes in different countries, the International Diabetes Federation exposed some similar issues whilst others different from the Brazilian context [56] . While the absence of specific measures to protect those with diabetes was reported in Greece and Spain, access to medicines was a challenge in Zimbabwe, Iran and India [56]. However, countries like Argentina, Italy, Portugal, and South Korea seemed to have adopted measures that made people with diabetes feel safer [48, 56] . It is urgent for Brazil to follow international best practices and recommendations, since, as stated by the WHO Regional Office for Europe, "the prevention and control of NCDs have a crucial role in the COVID-19 response and an adaptive response is required to account for the needs of people with NCDs" [17] .

imitations of the present study, although efforts were made to disseminate the survey as much as possible, this study's sample neither reflects the proportion of Brazilian population nor the fraction with diabetes. Thus, it is a convenience sample, without post-stratification weights. Questions about behaviors, habits and glycemic changes were subjective comparisons with the pre-pandemic state, therefore, we did not have access to objective data to validate the subjective responses. As an online survey, it is biased by individuals who have internet access. While 17% of the Brazilian population have a college degree [57] and 27.9% have private health insurance [28] , among the respondents of the present survey, 51.8% had at least one college degree and only 28.2% exclusively access care services through SUS.

Other demographic limitations related to the age groups distribution, younger than the general population with the great majority of the respondents from Sao Paulo state, which would be about 20% of the country, not 42.6% as in our group of respondents. We understand that one of the main factors leading to this bias is the network in which the authors are engaged, the geographic location of diabetes associations and the profile of their active members, tendency to have more individuals with T1D than T2D, mostly young and highly educated. Ann additional limitation is the number of choices for each question and the aggregation made for analysis purposes. This includes the fact that if separated, diseases aggregated in the Cardiovascular Disease group, for example, could behave differently in terms of proximity to other factors; moreover, increase or decrease of the blood glucose, interpreted as distancing from the target, would in fact have led the glycemic to target, while the ones who successfully maintained the blood glucose in pre-pandemic levels, may have kept it out of target.

As revealed for the first time in the current study, individuals with diabetes were not spared by the COVID-19 pandemic in Brazil. Measures and adjustments lacked or were insufficient, paving the way to unhealthy and unsafe behaviors such as postponing medical appointments, reducing physical activity and refraining from collecting medication and supplies, which led to a high percentage of glycemic worsen reports. Additionally, announced measures for prevention and mitigation of COVID-19 consequences on this population, such as supply of medicines for 3 months, worked just for a minority.

In conclusion, we see a pressing need from the Brazilian federal, states and municipal authorities to broaden the already implemented measures in order to reach more people, and partner with civil society, private sector and media channels to quickly improve the response and, this way, prevent a surge of individuals with diabetes infected by SARS-CoV-2 and of acute and chronic diabetes complications. Among the priorities measures to keep individuals healthy is by ensuring their glycemia is on target and they are at home as much as possible. We recommend that the public and the private health systems maintain and strengthen programs for the continuity of care of individuals with diabetes and other NCDs, and develop information and educational campaigns on how to access those measures. In addition to focusing on reducing the risk of infection and continuity of their healthcare, these measures should facilitate access to healthcare professionals' counseling for therapeutic adjustment.

Finally, as key measures we foresee are a) activemonitoring and response to communities' needs at primary heathcare level; b) high quality telehealth for consultations to monitoring and examining; c) distribution of medications and supplies for three or more months, ideally with home delivery; d) lab exams scheduled through home sampling, using mobile point-ofcare strategies or appointment in specific facilities with well established disinfection protocols. Consequently, we believe that the pandemic's challenges can be lessened if appropriate measures protecting individuals with diabetes and other chronic conditions are adopted, and investments are not solely directed to purchasing mechanical ventilators and equipping tertiary care.

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The authors acknowledge Vanessa Pirolo's support and assistance sharing the survey through her network and the non-governmental organizations ADJ Diabetes Brasil (ADJ), Institute for Children with Diabetes (ICD), Brazilian Diabetes Society (SBD), Brazilian Hypercholesterolemia Association (AHF), FórumDCNTs and their member and partner entities for assisting in sharing the survey and providing general support.
