Covid-19 impacts: Ethnic and regional inequalities in sickle cell disease patient care in Brazil

Abstract

Brazil is a continental country with significant socioeconomic and ethnic inequalities. It is important to understand how these differences are reflected in health care, especially during the COVID-19 pandemic. We investigated the potential impacts of the reduced number Transcranial Doppler Ultrasound (TCD) tests performed in Brazil during the COVID-19 pandemic, and its reflections according to region and race/color for patients with Sickle Cell Disease (SCD). This study performed data queries from the Brazilian Ministry of Health, literature research, and quantitative analysis using descriptive statistical analysis. We found evidence for a decrease in the number of TCD tests performed during the pandemic (−83 %) relative to the same non-pandemic period, and disparities in tests given in five regions in Brazil. Our data show, that in absolute numbers, most people with SCD are brown, but the highest prevalence of cases was among blacks. We also found evidence for racial discrimination when performing TCD test, which leads us to believe that the Brazilian Unified Health System (SUS) may be susceptible to racism when treating this disease. The implications of these findings serve as a warning to other countries with high indices of mixed ancestry in formulating health care policies for patients with SCD.

1. Introduction

It is estimated that 5 % of the world's population has hemoglobin disorders. Sickle Cell Disease (SCD) is the most prevalent hereditary hematological disease in the world and in Brazil [[1], [2], [3]]. In Brazil, it is estimated that of the more than 100,000 patients with SCD, most are of African descendancy [3].

Data from the National Newborn Screening Program in Brazil records an average of 1107 children with SCD per year. The neonatal diagnosis is essential for beginning treatment for SCD, especially with respect to stroke (CVA), with a mortality rate at 20 % for untreated patients, reaching levels up to 50 % for cases of hemorrhaging [3].

One of the main ways to track strokes is by performing Transcranial Doppler (TCD) tests, which measure blood velocity in the main arteries of organs. These tests detect risks for stroke, enabling early treatment for the patient [4].

In children with SCD, increased flow velocity in the cerebral arteries is associated with the risk of stenosis, silent cerebral infarctions, and stroke, which if occurs, can lead to motor and neurocognitive sequelae [5,6] or death.

In 2005, Brazil established guidelines for the National Policy for the Comprehensive Care of People with Sickle Cell Disease and other Hemoglobinopathies [7] within the Unified Health System (SUS). Furthermore, in 2013, Brazil implemented a protocol for utilizing TCD tests as an outpatient procedure to identify SCD patients at risk of developing cerebrovascular disease [3].

The guidelines for the policy seek to ensure comprehensive care to patients, aiming to increase life expectancy and quality of life via multidisciplinary treatment within the SUS. SCD has a high lethality rate in Brazil, significantly reducing patients' life expectancy. A recent study revealed an average annual death rate of 517 patients between 2000 and 2018 in Brazil, with SCD being the underlying cause in 70.5 % of deaths and an associated cause of death in 29.5 % of cases. The average age at death was 29.4 years for men and 33.3 years for women [8].

Studies show that mortality rates for COVID-19 have been different according to geographic region and patient ethnicity, disproportionately affecting black populations [[9], [10], [11]]. A study conducted in Brazil by Baqui et al. (2020) [9] confirmed these findings and concluded that greater socioeconomic vulnerabilities among brown and black populations leave them proportionally more exposed to risk factors related to COVID-19.

The high prevalence of stroke among patients with SCD and its serious consequences demonstrate the extreme necessity to use the TCD tests as a first step to detecting patients at high risk. Therefore, this paper highlights the impacts of reduced TCD tests amid the COVID-19 pandemic, drawing attention to regional and race/color disparities.

2. Methodology

2.1. Study Design

We conducted a retrospective cohort study evaluating the effects of COVID-19 and patient demographics on TCD performance rates for patients up to 19 years of age. The time series patient data were obtained from the Ministry of Health to consolidate the systematically collected variables e.g., number of patients registered by the Federated Unit, age group, and race/color.

Data on TCD exams came from the SUS Outpatient Information System (SIA/SUS), available using the Tabnet application [12], a tool for disseminating and accessing data on SUS health services. This data can be accessed by selecting ICD-10 code D57. The data were analyzed in the Tabwin [13] software program. Both options are publicly available via the SUS Computer Department (DATASUS).

The data collection was performed between September and October/2020, getting data from January to August, from 2016 to 2020, with a month cut-off, since 2020 data on performed exams were available only up to August.

This procedure, carried out by municipal, state or Federal District institutions within the scope of the SUS, is paid with a specific amount made available by the Ministry of Health.1

2.2. Study Setting

In Brazil, the SCD is significant due to an estimated number of 100,000 patients, one of the highest in the world [14] and the efforts made in the treatment of the disease, making the country a reference in healthcare for these individuals. Since 2014, the Brazilian Federal Government has been expanding the registration and systematic monitoring of these cases through a national database called Hemovida Web Hemoglobinopathies System, which includes social, clinical, and epidemiological data.

The country established guidelines for the National Policy of Comprehensive Care for People with Sickle Cell Disease and other Hemoglobinopathies within the scope of the Unified Health System in August 2005 [7]. In 2013, the Brazilian Ministry of Health established the protocol for the use of Transcranial Doppler (TCD) as a systematic outpatient procedure for primary stroke prevention in individuals with SCD between 2 and 16 years old, based on the Stroke Prevention Trial in Sickle Cell Anemia (STOP) study. Therefore, the examination should be performed and interpreted according to the parameters established by the STOP study [3].

The number of patients with hemoglobinopathies monitored by the Ministry of Health in 2016 was 25,449 individuals. Among them, 61.94 % were homozygous for sickle cell disease (HbSS), 25.80 % had sickle cell trait (HbSC), and 12.26 % had other hemoglobinopathies,2 which was the last year of data systematized by the agency at the time of our data collection.

It is relevant to point out that distribution of TCD equipment in Brazil is poor and uneven. According to a survey by the Ministry of Health, between 2018 and 2020, six states of the federation did not have the equipment in the SUS, 04 of them in the North region (Acre, Tocantins, Roraima, and Rondônia) and two from Central-West (Mato Grosso and Mato Grosso do Sul).3

2.3. Data processing

25,449 patients affected with hemoglobinopathies were treated by the Ministry of Health in 2016, the year in which data were collected by the ministry. Therefore, all analyses used this number of people as an initial reference, and this was the first national systematization of data published by the ministry. For the analysis of data from 2017 to 2020, an annual growth rate of 10 % was estimated for each Federal State and region.

To track SCD patients, Table 1 was created to display the number of patients and TCD exams. However, the initial dataset (from 2016) contained null records in the field age. Therefore, only 21,259 records were used to generate the table before filtering by age. This selection was necessary to accurately trace all SCD patients under 19.

Table 1.

Annual Frequency and percentage distribution of TCDs among population under 19 in Brazil by region and race/color, 2019–2020.

Region - Race/color	2019*				2020*
	People with DF		Exams performed		People with DF		Exams performed
	nº	%	nº	%	nº	%	nº	%
Brazil	15,090	100 %	3072	100.0 %	16,599	100 %	1675	100.00 %
Central-West	2170	100 %	230	100.0 %	2386	100 %	117	100.0 %
Yellow	17	0.8 %	0	0.0 %	19	0.8 %	3	2.6 %
White	100	4.6 %	8	3.5 %	110	4.6 %	9	7.7 %
Indigenous	0	0.0 %	0	0.0 %	0	0.0 %	0	0.0 %
Brown	510	23.5 %	184	80.0 %	561	23.5 %	93	79.5 %
Black	84	3.9 %	14	6.1 %	92	3.9 %	7	6.0 %
No information	1459	67.2 %	24	10.4 %	1605	67.2 %	5	4.3 %
Northeast	2818	100.0 %	1441	100.0 %	3099	100.0 %	702	100.0 %
Yellow	23	0.8 %	176	12.2 %	25	0.8 %	123	17.5 %
White	100	3.5 %	158	11.0 %	110	3.5 %	77	11.0 %
Indigenous	1	0.0 %	2	0.1 %	1	0.0 %	0	0.0 %
Brown	1206	42.8 %	786	54.5 %	1326	42.8 %	330	47.0 %
Black	101	3.6 %	70	4.9 %	111	3.6 %	51	7.3 %
No information	1387	49.2 %	249	17.3 %	1526	49.2 %	121	17.2 %
North	1410	100.0 %	1	100.0 %	1550	100.0 %	0	0.0 %
Yellow	4	0.3 %	0	0.0 %	4	0.3 %	0	0.0 %
White	17	1.2 %	0	0.0 %	19	1.2 %	0	0.0 %
Indigenous	0	0.0 %	0	0.0 %	0	0.0 %	0	0.0 %
Brown	253	18.0 %	1	100.0 %	278	18.0 %	0	0.0 %
Black	12	0.9 %	0	0.0 %	13	0.9 %	0	0.0 %
No information	1123	79.9 %	0	0.0 %	1236	79.9 %	0	0.0 %
Southeast	8372	100.0 %	1123	100.0 %	9209	100.0 %	707	100.0 %
Yellow	0	0.0 %	1	0.1 %	0	0.0 %	0	0.0 %
White	327	3.9 %	284	25.3 %	360	3.9 %	177	25.0 %
Indigenous	1	0.0 %	0	0.0 %	1	0.0 %	1	0.1 %
Brown	277	3.3 %	521	46.4 %	305	3.3 %	295	41.7 %
Black	71	0.8 %	170	15.1 %	78	0.8 %	81	11.5 %
No information	7696	91.9 %	147	13.1 %	8465	91.9 %	153	21.6 %
South	325	100.00 %	277	100.0 %	357	100.00 %	149	100.00 %
Yellow	0	0.0 %	0	0.0 %	0	0.0 %	0	0.0 %
White	117	36.1 %	209	75.5 %	129	36.1 %	92	61.7 %
Indigenous	0	0.0 %	0	0.0 %	0	0.0 %	0	0.0 %
Brown	59	18.0 %	20	7.2 %	64	18.0 %	23	15.4 %
Black	75	23.0 %	20	7.2 %	82	23.0 %	6	4.0 %
No information	75	23.0 %	28	10.1 %	82	23.0 %	28	18.8 %

Note: period from January and August (0–19 years old).

Source: SUS Outpatient Information System (SIA/SUS).

The variables used in the study, regarding to patients and TCD exams were race/color, age group, region of residence, and the region where the exam was performed. These variables were used in the descriptive statistics to build a data set of the distribution of patients with SCD in Brazil considering their age and ethnicity and considering the distribution of number of exams among races during the COVID-19 pandemic period.

The categorization for the race/color variable has been defined by the Brazilian Institute of Geography and Statistics (IBGE) into five racial groups: white, brown, black, indigenous, and Asian.

To see where patients are geographically located (by federal state), data were standardized so states could be compared equally, regardless of the number of inhabitants in each state. Standardized was performed according to Formula 1, adding the number of people with sickle cell disease in each state, and dividing this by the number of inhabitants in the state. The result was multiplied by 1,000,000, allowing us to make comparisons among Brazilian states.

Formula 1: Standardized of the number of people with sickle cell disease per state.

$$\left(\frac{\sum _{i=1}^{n}sicklecellpatients}{population}\right)*\mathrm{1.000.000}$$

All patient records were used for the geographic location distribution and patient age groups. For the other analyses, we set an age cut-off, since the TCD protocol states that primary prevention should be performed for patients aged between 2 and 16 years old. The age cut-off considered patients aged 0–19 years old, since national data included the age groups <1 years old, 1–4 years old, 5–9 years old, 10–14 years old, and 15–19 years old, making a cutoff at patients aged 2–16 years old unfeasible, thereby extending data to patients up to 19 years old.

An index was calculated to better understand the prevalence of the disease by race/color in Brazil. The percentage of the Brazilian population was divided by the percentage of patients with SCD grouped by race. This prevalence index gives us a more concrete analysis since the absolute values may distort the real situation of the disease.

2.4. Significance tests and measurement methods

The chi-square (Χ²) test of independence was used to test statistical significance for the categories of race/color, specifically white and blacks, and the longitudinal categories of years, specifically 2019 and 2020. One Χ² test was performed to measure the statistical significance of the historical data over a race/color, and another Χ² was applied to measure the statistical significance among blacks and whites. The expected values of Χ² were derived through the existing data. One of the key assumptions to choose X² was the sufficiently large sample, except for the North region, which no hypothesis test could be generated because of shortage data, zero TCD test.

A method has been elaborated to measure the relative proportion of race/color differences considering the longitudinal data history. The measure of the relative longitudinal proportion of TCD tests for a given race/color was calculated by the SELR (Standardized Exam Longitudinal Rate), which is the ratio of the normalized number of TCD tests observed in a population over a given period to the number that would be expected over the previous period if the study population had the same rates as the standard TCD test population in the previous period.

Another measurement method elaborated was the proportion of TCD test among a race/color related to other ethnicities. The SER (Standardized Exam Rate) can be calculated by the ratio of the number of TCD tests observed in a population over a given period to the number that would be expected over the same period if the study population had the same rates as the standard ethnicities population.

2.5. Ethical guidelines

These data were obtained from the public organization, Health Ministry, and references do not violate or infringe upon ethical guidelines, and they are in accordance with Resolution of the National Health Council No. 510, dated April 7, 2016, Article 1, Section V, which states that ‘databases containing aggregated information without the possibility of individual identification,' given that the requested and granted access pertains solely to the aggregated dataset and does not allow for individual or personal information to be detailed, and it does not involve any patient records.

3. Results

For the analyzed period, the largest number of patients with SCD were concentrated in Tocantins and Bahia states. Bahia had the most patients with SCD in the period analyzed, at 6112 people, constituting 24.02 % of all cases in the northeast. The southeast had 50.59 % patients, followed by the northeast at 34.43 %. These data are shown in Fig. 1.

Fig. 1.

Geographic distribution of people with sickle cell disease in Brazil per 1,000,000 inhabitants.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus. Data considering the ratio between the number of people with SD in 2020 and the number of inhabitants per Brazilian state with data from IBGE 2010, multiplying the result by 1,000,000, according to Formula 1 in the methodology section.

Graph 1 shows the distribution of patients with SCD by age group. There is a high level of young patients aged between 20 and 29 years old. 48 % of all patients were aged between 15 and 39 years old.

Graph 1.

Patients with sickle cell disease per age group in Brazil.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus. Data of people with SCD in 2020.

Graph 2 shows the distribution of patients by race/color according to the regions in Brazil in 2016. One can see that the absolute number of people with the SCD are brown. However, it is important to note that most of the Brazilian population is brown, and therefore Graph 3 shows the prevalence of the disease by race/color.

Graph 2.

Patients with sickle cell disease per region in Brazil.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus.

Graph 3.

Brazilian population and population with sickle cell disease.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus.The data on Brazilian population is from IBGE4

In four of the regions in absolute numbers most patients were brown, followed by black. In the Southern region, the majority were black, followed by white. The rate of unidentified patients (race/color) is pronounced, at more than 60 % in the southeast, the most populated part of the country, and at about 50 % in the central-western region.

Graph 3 shows the relationship between the percentage of the Brazilian population and the percentage of the population with sickle cell disease, demonstrating the prevalence of the disease per each race.

Given this comparative analysis we saw that the highest prevalence of the disease was among the black population, although the highest absolute number of patients with sickle cell disease were of mixed race. In Graph 3, Asians and indigenous peoples had population percentages added to data collected from IBGE [15] for comparison's sake.

Analyzing the data one can obtain the prevalence index for the disease, which is equal to 3.5 among the black population, 1.15 among brown ethnicities, 0.85 among indigenous peoples and Asians, and 0.29 among the white population.

Graph 4 shows that there was an annual increase in the number of exams performed in almost all regions of Brazil from 2016 to 2019, except in the north. In 2020 there was a decrease in TCD exams, at 1952. In 2019 3655 TCD exams were performed.

Graph 4.

TCD exams performed per region in Brazil, 2016–2020.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus. Note: period from January to August. Data from the north were omitted from the chart since they contained only values equal to 1, 3, and 1 for 2016, 2017, and 2019 respectively.

Comparing data from the first eight months of the year, starting with 2016 and going to 2020, as shown in Graph 5, we can see an increase in TCD tests performed in recent years, except for 2020, when there was a significant decrease in exams at −83 %, probably due to the COVID-19 pandemic. Once again, the northern region stands out for having performed only 5 TCD tests between 2016 and 2020, highlighting a serious regional inequality. A −83 % decrease in number of TCD tests performed in 2020 is quite significant (Graph 5), since 48.78 % of all people with SCD are in the 0–19 age group (Graph 1).

Graph 5.

TCD exams performed for the age group 0–19 years old in Brazil from 2016 to 2020.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus. Note: Period from January to August.

Graph 6 shows the exams performed grouped by race/color for the age range that should be checked according to the TCD Protocol. This shows that there was a progressive increase in the number of tests performed in recent years for all population segments, and a sharp drop in 2020. A high degree of underreporting tests was noticeable, although this has decreased in recent years.

Graph 6.

TCD exams performed on patients 0–19 age, grouped by race.

Source: Ministry of Health. General Coordination of Blood and Blood Products: Hemovida Web - Hemoglobinopathies and Formsus. Data from 2016 to 2020.

According to Graph 6, we can see that most people examined were brown. Very few Asians were examined. It is noteworthy that black people took fewer exams than white people. Indigenous peoples showed insignificant numbers.

Note: period from January to August. Data on indigenous peoples were omitted from the chart since they were equal to 2 and 1 in 2019 and 2020, respectively.

Table 1 shows the variables for age, race/color, and region where the exams were performed in the studied period.

The unique region that did not achieve statistical significance was the Central-West. The white SER in the Central-West was 1.27 (2019) and 1.31 (2020) times of the remaining ethnicities population. The black SER maintain the same proportion of the remaining ethnicities population in 2019 and 2020. The white SELR maintained the same proportion from 2019 to 2020, while the black SELR was reduced to 45 % of 2019 in the pandemic period (2020).

In the Northeast, there was a chi-square significance difference between black and whites’ exams. The SER for whites were always above the mean of the remaining ethnicities exams, 1.89 in 2019 and 2020. The relative ethnicities TCD tests for blacks were 0.83 and 1.24, 2019 and 2020, respectively. The black and white SELR were reduced to 66 % and 44 % in the pandemic period, respectively, with a significant chi-square test.

In that region, 11 % of exams conducted in 2019 and 2020 were performed on individuals of the white group, which represents 3.5 % of the patients under 19 years old.12.2 % and 17.5 % were performed on Asians, respectively, that are 0.8 %. 4.9 % and 7.3 % exams, respectively, were performed on blacks, who represent about 3.6 % of all patients under 19 and performed less than the other two population segments.

In the North, only 1 TCD test was performed in 2019, for a patient that is brown, even though there is an estimated population of 1406 people under 19 with SCD for that same year. No exams were performed in 2020. This region is home to a significant population of indigenous peoples affected by SCD i.e., 6.3 %, the highest rate in the country.

In the Southeast, there was a chi-square significance difference between black and whites’ exams related to their population. The relative ethnicities TCD tests from 2019 to 2020 for whites were below the average of the remaining ethnicities exam, 0.6 to 2019 and 2020. While black SER was above the remaining ethnicities with 1.65 and 1.39, 2019 and 2020, respectively. The white and black SELR were reduced to 56 % and 43 % in pandemic period, respectively, with a significant chi-square test.

The white population with SCD stands out once again, it was 25.3 % in 2019 and 25 % in 2020, while blacks performed 15.1 % and 11.5 % in 22019 and 2020, respectively.

The disparity of TCD tests between white and blacks continuous in the South, with chi-square significance. The black SER was reduced from 2019 to 2020, from 0.26 to 0.16, respectively, below the remaining ethnicities average. While the white SER was above the average, 1.79 and 1.62, between 2019 and 2020, respectively. The white and black SELR were reduced to 40 % and 27 % in the pandemic period, with a significant chi-square test.

The whites represent 36.1 % of all people under 19 with SCD, and blacks 23 %. Were performed on blacks 7.2 % of all exams in 2019 and 4 % in 2020, while were performed 75.5 % on whites of all exams in 2019 and 61.7 % in 2020.

The data are overwhelming, demonstrating the great disproportionality in performing exams when comparing these two population segments with SCD, demonstrated in Graph 2 combined with Table 1, with an indispensable highlight for the South region.

Despite the behavior differences between blacks and whites across regions, we can evidence the inferior proportional quantities of TCD tests performed by blacks when compared with whites in the country, with a significant chi-square test. The white SER for all the regions were the same 1.27 and 1.31 times in 2019 and 2020, respectively. While the black SER is the same as the remaining ethnicities population, between 2019 and 2020. These results showed that blacks and whites, in general, maintained the same proportion of TCD tests in pandemic period, regarding to the remaining ethnicities population. However, when considering the TCD tests over the study periods (2019-2010), the white and black SELR were reduced to 49 % and 48 % in the pandemic period, with a significant chi-square test.

Table 2 shows the performed Chi-square, SER and SELR tests. The details are in the supplemental material.

Table 2.

Chi-square, SER and SELR tests.

	Chi-square 2019/2020 (p)	Chi-square Between 19/20 (p)	SER 2019 (Times)	SER 2020 (Times)	SELR 19/20 (Times)
Brazil
White	0.02*	0.00**	1.27	1.31	0.49
Black		0.00**	1.01	1.03	0.48
Central-West
White	0.42	0.96	0.27	0.57	1.02
Black		0.10	0.57	0.53	0.45
Northeast
White	0.00**	0.00**	1.89	1.89	0.44
Black		0.07	0.83	1.24	0.66
Southeast
White	0.00**	0.00**	0.60	0.66	0.56
Black		0.00**	1.65	1.39	0.43
South
White	0.00**	0.00**	1.79	1.62	0.40
Black		0.00*	0.26	0.16	0.27

* Statistical significance p < 0.05 ** Statistical significance p < 0.001.

PS: It is not possible to measure the chi-square for the North region because the data shortage for TCD tests.

4. Discussion

The data show a decrease in the number of TCD tests performed in Brazil in the months studied in 2020 for patients with SCD (−83 %). After the TCD Protocol process was consolidated, there were gradual increases in tests from 2016 to 2019, which leads us to believe that the decrease in the number of performed tests currently is linked to restrictions related to the pandemic.

Children with SCD, and with abnormal TCD measurements, who are not on regular blood transfusion therapy, have a stroke rate at 10.7 per 100 patients/year [16]. Roy et al. (2020) [17] understand that, even with all the restrictive measures, TCD testing in children with SCD " … should not be delayed, because the known risk of stroke outweighs the unknown risk of COVID-19 infection."

Imposing societal mobility restrictions and social distancing to contain or slow the spread of the COVID-19 pandemic disease [18,19] makes patients with SCD more vulnerable to stroke and its subsequent consequences and increases the chance of stroke in individuals who have simultaneously contracted COVID-19.

In the other hand, the Ministry of Health established as a goal of its National Health Plan 2020–2023, to increase the coverage of TCD for children with SCD aged 2 years to 60 % by the end of this period.5 Even if it is restricted to a specific audience, this makes the Ministry not only follow and monitor more closely the execution of the exams but also encourage their execution in general, offering some incentives, such as training for health professionals and the purchase of equipment. This action benefits everyone as it expands and qualifies the service offered at a time of various problems imposed by the pandemic.

Regional socioeconomic and racial/color disparities are reflected in the findings on the number of performed TCD test, and this will likely have relevant consequences for treating patients, and for patient survival. The race/color variable must be better studied, especially considering legislation that determines that this information must be recorded and given the implementation of the PNSIPN.

Low completeness levels for the race/color variable were found for all regions, which may be related to negligence or institutional racism, the latter being a concept first presented by Carmichael and Hamilton [20]. Even though legal obligations exist, sometimes they are not fulfilled.

Racism is present in Brazilian society and permeates the Brazilian social fabric, determining the way institutions and the State deal with the black population. Despite this, anti-racist legal frameworks alone cannot end racism, given the problems related to information involving issues of race/color.

Prejudice and discrimination stemming from institutional racism are present throughout legal frameworks, actions, and discriminatory behaviors in the day-to-day lives of people, making it difficult to advance services to people because of their race or color, or by failing to provide effective quality service, and consequently, generating more inequality [21].

This disparity becomes evident as black individuals with SCD underwent fewer TCD tests compared to their white counterparts in the three regions characterized by higher socioeconomic development and larger population concentrations (Southeast, Northeast, and South), despite the lower number of white individuals with SCD compared to black individuals with SCD.

In all regions, except for the South, most people with SCD are brown, in absolute number terms. However, in Brazil, our findings indicate that the highest prevalence of the disease is among blacks.

A study by Baqui et al. (2020) [9] on hospital mortality from COVID 19 in Brazil found evidence of increased mortality in the northern region, and significantly higher mortality of brown and black people compared to the white population, considering region, ethnicity, comorbidities, and symptoms, and brown individuals had the second risk factor for death, surpassed only by age. The black population compared to the white population, except for the older age groups, is less likely to survive COVID-19 in the south-central region.

In the North only 1 TCD test was conducted from 2016 to 2020. An important factor for this data is the lack of equipment to perform the exam in four of the seven states in this region. A study by Tavares and Betti [22] also showed that the north has the highest proportion of vulnerable people subject to COVID- 19 infection.

The factors related to regional socioeconomic development and ethnicity related to health care inequalities in Brazil has been widely discussed in literature [9, …,22]. Consequently, patients with SCD who face socioeconomic disparities and reduced access to health care services, and who are affected by COVID-19, have an increased risk of problems due to underlying diseases and conditions.

This study was limited in some senses. The national database, which is managed at the national level, depends on the data inputs from the state level, from all Brazilian states. In 2016, for example, data from three states were not recorded, i.e., Acre, Mato Grosso do Sul, and Rio Grande do Sul. We were unable to determine if annual TCD tests were performed on a single patient to comply with the TCD Protocol, i.e., the percentage of performed tests is related to the number of procedures, and not individuals.

5. Conclusion

This study showed that there was a significant decrease in the number of TCD tests performed on people with Sickle Cell Disease (SCD) in Brazil during the period studied. Evidence was presented suggesting that this decrease was caused by mobility restrictions and social distancing caused by the COVID-19 pandemic. This may have consequences in the form of increased risk for strokes in patients with SCD.

The results of this study also show how national preventive public policies, like the policy for SCD, can vary among region in Brazil, disproportionately affecting ethnic groups. The study also shows how COVID-19 may have impacted this, not only in the number of possible deaths related to not conducting the exam, but also in the aftereffects of the disease.

We observed how incomplete preventive actions impact the needs and the fragilities of many children, adolescents and youngsters, and suspect potential setbacks in stroke prevention processes for patients with SCD due to the impacts of the COVID-19 pandemic.

It is possible to infer from this study that despite significant technical advancements in Brazil, like early diagnosis using neonatal screening, and cures using bone marrow transplantation, SCD care and medical assistance may be provided unequally for patients due to racial discrimination. Xavier Gomes et al. (2015) [23] point out that SCD "has been historically neglected in Brazil and in the world for being predominantly a black disease. However, due to the mixed ancestry of the Brazilian people and the presence of SCD in all races/ethnicities, even if prevalent in blacks, it is imperative that it be recognized as a common disease of Brazilians and not of African descendants."

The difference in TCD tests performed on black and white populations, as demonstrated in this study, corroborates the findings of Xavier Gomes et al. (2015) [23]. Specifically, when examining the South region, the study revealed that in 2019, 75.5 % of TCD exams were conducted on the white population, which accounts 36 % of the SCD population under 19 years old, whereas only 7.2 % of tests were performed on black individuals, who represents 23 % of the same population. In 2020, the numbers decreased to 61.7 % for whites and 4 % for black patients under 19 years old. These findings reinforce the significance of implementing the PNSIPN [24] program, which aims to "address racism, ethnic-racial inequalities, and institutional racism as social determinants of health to promote health equity."

The results of this study show that the race/color social determinants for health care were fundamental in identifying the number of TCD tests performed. We can infer that the origin of these inequalities in health care services is not only in function of race or color, but also in function of structural racism in Brazil.

Given this evidence, we can further state that advancements in implementing public policies for people with SCD in countries with a variety of racial groups, similar to Brazil, will require State policy decisions to promote greater technical and scientific advances in caring form and assisting these people.

Data availability statement

The datasets used in this study originate from the Brazilian Health Ministry, called Hemovida Web Hemoglobinopatias System e Formsus System. The data is available in our project's record on the REDCap platform of the Federal University of Tocantins, and the files can be accessed through the following links:

https://redcap.comais.uft.edu.br/surveys/?__file=SxcoY4Idn8QNxYQJ5s9pVtCu8LkWCqUhWe8STg32kU67epy8gzSMzp7IHcC8k9avnrR299MYju9TIGGTTwcJWdcK9KJwmp4EqW2S

https://redcap.comais.uft.edu.br/surveys/?__file=SxcoY4Idn8QNxYQJ5s9pVtCu8LkWCqUhWe8STg32kU67epy8gzSMzp7IHcC8k9avnrR299MYju9TIGGTTwcJWdcK9KJwmp4EqW2S.

CRediT authorship contribution statement

Rui Leandro Santos: Conceptualization, Investigation, Validation, Writing – original draft, Writing – review & editing. Waldecy Rodrigues: Conceptualization, Formal analysis, Investigation, Methodology, Project administration, Software, Supervision, Validation, Writing – original draft, Writing – review & editing. David Prata: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Daniela Trevisan: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing – original draft, Writing – review & editing. Paulo Henrique de Souza Bermejo: Conceptualization, Formal analysis, Validation, Writing – original draft, Writing – review & editing. Marina Figueiredo Moreira: Conceptualization, Formal analysis, Validation, Writing – original draft, Writing – review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.