The assistance gaps in combating COVID-19 in Brazil: for whom, where and when vaccination occurs | BMC Infectious Diseases | Full Text

The spacial and temporal profiling of the vaccination for COVID-19 in Brazil is key to understanding who, where, and when immunisation is occurring in the country. Vaccination in Brazil presents a distinguished historical scenario, with its National Vaccination Programme (PNI) being an example for the world [24]. However, the pandemic of COVID-19 brought numerous challenges. The setback imposed by the pandemic is evident in the drop in life expectancy of the population by approximately 2 years, going to 74.8, putting Brazil back to the numbers reached in 2013 [25].

One of the criteria for defining the elderly population group as a parameter of priority in vaccination against the coronavirus was the high morbidity and mortality in this group [9, 26]. This phenomenon occurs given the increased vulnerability to infectious diseases with unfavourable prognoses, added to associated comorbidities [27,28,29], as evidenced in April 2021, when 69.3% of SARS deaths were in individuals over 60 years of age, of which 61% had at least one comorbidity. Heart disease and diabetes were the most frequent conditions, and most of those who died and presented some comorbidities were 60 years or older [30].

In Brazil, by the end of April 2021, the first dose of CoronaVac or AstraZeneca vaccines had been administered to 24,768,325 individuals over 60 years, corresponding to 82.02% of the population estimate of the national COVID-19 vaccination campaign for this group [9]. In comparison with the United States, by 10 April 2021, 79.1% of the population above 65 years had initiated their vaccination [31]. This significant percentage of vaccinated elderly, with possible hospitalisation prevention of up to 94% with AstraZeneca [32] and 87.5% for CoronaVac [33], may be a relevant cause of the demographic shift in the profile of those affected by COVID-19 in 2021, with young and middle-aged adults representing a larger share of hospitalised cases and deaths. As shown in the Fiocruz epidemiological bulletin for weeks 16–17 of that year [34], the mean age of hospitalisation reduced from 62.7 to 57.1 and the mean age of deaths from 71.5 to 63.7 between epidemiological weeks 1 and 16.

Vaccination began in the Southeast region with the CoronaVac vaccine produced by Sinovac in partnership with the Butantan Institute. Such local production may explain why the Southeast region accounted for most of the vaccination by the elderly group (46.1%) and health workers (45.3%). The temporal distribution of vaccine doses followed the expected model, with clusters of high incidences of vaccination by EP occurring in epidemiological weeks 8 to 12, followed by high clusters of indigenous and quilombola group and health workers group, order of priority established by the national Ministry of Health [8]. Regarding the type of vaccine applied, the increase in high vaccination clusters was also due to the arrival of AstraZeneca/Oxford in Brazil on 21 March 2021 [35].

A decrease in the VR of CoronaVac was observed from week 14 to the last week analysed. It is important to point out that from May on, 72% of the vaccines distributed to the states were AstraZeneca type due to the decrease in the production of CoronaVac as a result of lack of inputs. This scarcity could be related to the diplomatic conflicts between the Brazilian government and the government of China, the leading supplier of Active Pharmaceutical Ingredient (API) to produce the CoronaVac vaccine [36]. The supply shortage can justify the predominance of high clusters of AstraZeneca vaccines over Coronavac across all groups starting on week 10, as evidenced in Fig. 1.

A possible cause pointed to the reduction in the vaccination rate for the EP was the inclusion of the group of comorbidities. This inclusion supposedly deviated the limited vaccine supplies to meet this new demand and could have caused the loss of vaccines since this group required medical statements before scheduling, which discouraged vaccination [37]. However, this argument becomes erroneous since, regardless of the recommended age range, chronic respiratory and cardiovascular diseases are presented as a high-risk factor for mortality by COVID-19 [8, 38]. Therefore, not including these groups in exchange for greater logistical ease would ignore the main objective of vaccination, which is to prevent severe cases and deaths.

Regarding the second dose, the elderly group in the Southeast region presented outstanding clusters of low rates for both vaccines, which can be related to the high number of people overdue for their second dose of vaccination in those states [39]. Furthermore, the difference in time between the first and second dose clusters, comparing the two vaccines, can be justified by the difference between the vaccination interval, which is 21 days between doses for CoronaVac and three months for AstraZeneca. Therefore, considering AstraZeneca’s inter-dose interval, the clusters of the second vaccination dose were affected, given the time frame adopted in the current study.

Concerning spatial analysis, for the elderly group vaccinated with CoronaVac, spatial clusters of high VR were detected in the country, emphasising Ceará, Rio Grande do Norte and Paraíba, the eastern of Minas Gerais, and the northeastern portion of Rio Grande do Sul. An important fact is that Ceará has prioritised the elderly over 75 years as a first phase vaccination goal by EP before including the group under 60 years and comorbidities [9]. With AstraZeneca, it was observed that the countryside of Pernambuco, Alagoas and Sergipe, the eastern border between Minas Gerais and São Paulo, had the highest concentration of high VR among the clusters found. To the same priority group, the second dose of AstraZeneca showed a cluster of high VR points only in the state of São Paulo. This phenomenon may be supported by the fact that AstraZeneca application began earlier and on a larger scale after the lack of CoronaVac.

About ten weeks after the period analysed in the present study, health scenarios indicated a return in the relative increase of deaths and hospitalisations among the elderly. According to the Fiocruz Bulletin of the epidemiological week (EW) 31–32, this group returned to present an average near the 70 years in deaths. Furthermore, the proportion of hospitalised cases among the elderly, at 27.1% in EW 23, grew to 43.6% [39]. This change is due to the shift generated by the achievement of broader vaccination coverage for the elderly in lower age groups, together with a possible reduction in the immunising power over time, associated with a reduction in the potential of the immune system with advancing age and the emergence of more transmissible, and new variants, such as the delta variant.

By the end of May 2021, 11,965,603 healthcare workers had received at least one dose of CoronaVac or AstraZeneca. This group’s pattern of vaccination distribution followed the expected demographic density arrangements in most of the country, with the Southeast leading the vaccinated contingent due to the higher number of healthcare workers (Table 1). The analyses of spatial clusters also detected this trend, especially for the state of São Paulo, where the Butantan Institute is located. This institute has successfully brought international partnerships for the development of tests and application of vaccines [41], highlighting the performance of CoronaVac, which generated, for both doses, spatial clusters of high vaccination rates in that state.

Right behind the Southeast, the Northeast region accounted for the second-highest number of vaccinated health workers in the country. However, for the North and South regions, the VRs observed with AstraZeneca were not higher than those expected for many HR. For its second dose, it was observed that healthcare workers remained leading in clusters of low VR in Brazil. This event was due, among other reasons, to the period covered by the study and to political and institutional disagreements [42,43,44], which ended up putting scientific negationism and ideological aspects ahead of vaccination objectives.

In addition, due to its continental dimensions and with multiple points of tension outside the political arena, Brazil needed to seek very efficient and coordinated logistical solutions for distribution and storage. In this sense, small failures accumulated throughout the process ended up causing delays and losses during the stages of immunisation, making the country quickly susceptible to the enormous human and material impacts of the pandemic during almost the entire year of 2020 [42,43,44]. This occurrence can be verified in the vaccination proportional to the population ranking [45], in which Brazil ranked 78th at the beginning of June 2021. Moreover, factors such as failures of shared management between the public administration levels; disparity and conflict between the healthcare capacity offered by public and private health systems; and actions that contributed to the country’s political and economic instability, hindering more accurate and anticipated decision-making [42,43,44].

Vaccination coverage among healthcare workers offers a simultaneous benefit to patients and workers themselves. Studies have shown that the risk of healthcare workers becoming infected with the novel coronavirus was high but reduced considerably in this population after immunisation [46]. However, a study identified disparities between vaccination rates among healthcare groups, with physicians more vaccinated, followed by nurses and technical assistants [47].

Worldwide, priority groups of older people and healthcare workers were the first to benefit, followed by those with severe comorbidities [48, 49]. However, during the early stages of vaccination, these priority groups encountered several difficulties arising from the challenges of concatenating a limited amount of vaccines for many people with closely related needs [48,49,50]. The VR observed among healthcare workers in Brazil in the first months of immunisation was negatively distinguished from other large-sized countries, for example, with the rate found in the USA [51]. This event was related to the Brazilian government’s difficulty in articulating the purchase of large quantities of vaccines in the first opportunities, which ended up not only delaying the vaccination for the priority groups but also overloading the vaccination sites, which had only CoronaVac available, therefore not meeting the massive demand [42,43,44].

The NASEM (National Academies of Sciences, Engineering, and Medicine) and the WHO have recommended that policymakers prioritise racial and ethnic minorities for vaccination against COVID-19 [52]. An analysis of indigenous populations in 23 countries found worse health indicators outcomes in this group: life expectancy at birth, infant mortality rate, maternal mortality, low birth weight, infant malnutrition, obesity, and others [53]. In Brazil, infectious and parasitic diseases are among the most responsible for indigenous deaths, especially compared to the rest of the national population. A recent example is the H1N1 pandemic in 2009, when 1,567 deaths among indigenous peoples were recorded in Brazil, 4.5 times more affected than the general population [13].

In the current pandemic, the greater vulnerabilisation of certain racial and ethnic groups is a reality worldwide and nationally. For example, a study published in late 2020, which analysed 29,008 cases and 532 deaths of indigenous people in Brazil from COVID-19, found national incidence and mortality rates of 3,546.4 cases and 65.0 deaths per 100,000 inhabitants, respectively, and a case fatality rate of 1.8% in the group [14, 54]. Factors that explain the vulnerability produced to this group in the current pandemic in the country are: communal lifestyle; constant invasions of indigenous lands; missionary actions; absence of a protection policy by the federal government; lack of an adequate drinking water supply system; poor access to hygiene products and alcohol gel; limited access to health care, especially those of high complexity [13]; and reduced investments of the Mais Médicos program, which has resulted in the dismissal of more than 8.000 primary care physicians in 2019, mainly affecting indigenous communities in remote areas [54].

The present study found clusters of high vaccination rates with CoronaVac during the first seven epidemiological weeks and low vaccination rates in the following weeks. With AstraZeneca, high vaccination clusters occurred after the tenth week. This temporal pattern followed the expected trend for priority groups included in the first phases of vaccination in most state and municipal plans. Moreover, it was very similar to the temporal pattern found for healthcare workers. Among the groups analysed in this study, the indigenous and quilombola populations had the lowest vaccination rates, with a national rate of 0.62/100.

The percentages of complete vaccination schedules were also the lowest when comparing indigenous and quilombola to the other groups studied, not exceeding 2% in any of the five regions during the weeks studied. In the North region, for example, where 97.3% of demarcated indigenous lands in the country are concentrated [55], the vaccination rate for the group was 0.18/100 inhabitants, with 0.38% of individuals with a complete scheme. Some difficulties faced during the period studied for the vaccination of these ethnic and racial groups may explain such results: deficient national immunisation plan, highlighted by inconsistencies regarding the definition of priority groups; geographic isolation; problems with local management and vaccine hesitation.

Regarding the indigenous population, the Special Secretariat for Indigenous Health (SESAI) is responsible for the immunisation actions executed by 34 Special Indigenous Health Districts (DSEI) [55]. For the establishment of the National Plan for the Operationalisation of vaccination against COVID-19, the estimation of the indigenous population was based on data from the Department of Indigenous Health (DESAI), including those over 18 years of age served by the national public health system, living on demarcated lands.

According to the Plan, it was recommended that the vaccination should be carried out in agreement with the DSEI responsible for each municipality with which the indigenous lands are associated, including this population in the vaccination first phase [9]. There are 310 indigenous lands in stalled demarcation processes. Consequently, in this first stage, 379.5 thousand people, or 42.8% of the indigenous population, were left out of the first stage of the immunisation against coronavirus [55]. On 16 March 2021, the Federal Supreme Court (STF) accepted the appeal of the Association of the Indigenous Peoples of Brazil (APIB), determining that even “unallocated” indigenous people should be included in the General Plan of Confrontation of COVID-19 for Indigenous Peoples [56], leading to an increase in the vaccination following the decision.

For the quilombola population, data from the 2010 National Census were applied regarding individuals above 18 years of age, maintaining the recommendations for creating strategies at the municipal level [9]. The quilombola population also faces problems regarding the certification of their territories. The titling of lands belonging to the remaining quilombola peoples/communities is carried out by the National Institute of Colonisation and Agrarian Reform (Incra), and less than 7% of them are regularised. The populations of lands whose possessions are not regularised found, in the pandemic, the problem of access to vaccination, testing and medical assistance [57]. Moreover, in the 23 national states that have made available their vaccination plans, only 12 have included the quilombola population among the priority groups. The majority did not inform the phase in which the vaccine should be applied in this group [13].

Regarding both groups, geographic isolation imposes itself as another difficulty faced. The Associated Press, which accompanied the transport of vaccines by health workers to indigenous and quilombola communities, reported problems regarding the delivery of vaccines in locations with access only possible by boat, requiring several days of travel, highlighting the difficulty of maintaining the refrigeration of vaccines during transport [58]. For example, in the quilombo Kalunga do Mimoso, in the state of Tocantins, the community had to gather to purchase a refrigerator to store the vaccines since the municipality provided the doses but not the refrigeration equipment. In summary, the vaccination of ethnic priority groups in the country is hindered by local public administrators’ lack of political will [59].

According to the last national census (2010), the regions with the largest indigenous populations are the North, with 342,836 people and the Northeast, with 232,739 [60]. Concerning the quilombos, the states of Bahia (NE), Maranhão (N) and Minas Gerais (SE) concentrate more significant numbers; also highlighted are other states of the Northeast region, and the state of Rio Grande do Sul [61]. However, despite presenting higher concentrations of demarcated lands and people declared or considered indigenous, the North region did not present clusters of high or low vaccination rates. The absence of high vaccination clusters can be explained by the problems previously mentioned, especially in the Legal Amazon region.

Despite the significant indigenous and quilombola populations contingent, which could translate into lower vaccination rates due to the greater need for vaccines, the Northeast region presented high vaccination clusters for both vaccines. With the pandemic of COVID-19, the matter of vaccine hesitancy returned strongly to the scientific community’s interest, which moved new efforts to investigate the rates of vaccine intention [62]. Research involving healthcare workers showed that the rates of intention to be vaccinated among professionals varied throughout the pandemic between 27.7 and 77.3% [63]. Among the main issues involved in vaccine hesitancy are insecurity about its efficacy/quality and the political and organisational dissonance between governmental sectors, health entities and supranational bodies [63, 64]. This social behaviour may have reduced VR among health workers in some country areas.

For the elderly, a relevant issue directly related to the low demand for the second dose is the wide dissemination of fake news and the movement of anti-vaccine groups. Despite studies that prove the vaccine’s effectiveness, vaccine hesitation is still frequent, and anti-vaccine movements can find even greater ground among the elderly group since they also represent the age group with less access to education and high rates of functional illiteracy [64, 65].

In certain indigenous localities, vaccine hesitancy and resistance are of particular concern, especially in the states of the legal Amazon. According to SESAI, 70% of the indigenous people living in the Rio Tapajós basin villages (state of Pará) were doubtful or had refused to take the COVID-19 vaccine. In the region, 6,420 doses of the vaccine were made available by 25 March 2021. However, only 30.3% were applied, as 35.2% of the indigenous people refused to take it, and another 32% stated they were hesitant about accepting the immunisation [66]. The dissemination of fake news by evangelical religious groups has been pointed out as one of the main factors responsible for such hesitation, especially in the states of the legal Amazon, where these groups have spread in the last ten years. An analysis with community leaders, researchers, indigenous people, and non-governmental organisations showed that where there is a more significant presence of pastors opposed to vaccination, VRs were lower [67].

While collecting data for the study, some limitations were identified. The database used had some discrepancies in the notification, such as the non-matching of the number of doses applied and people associated with risk groups, making it difficult to interpret some vaccination behaviours, especially for the population over 80 years old in the South region. In addition, another limitation was the absence of demographic data for the year 2021, which was replaced by 2020 values. Likewise, the demographic data for indigenous and quilombola people for 2019 were used, the most up-to-date available. From the study period perspective, while this work was able to broadly overview the behaviour between doses of CoronaVac, the evaluation of the dynamics between doses of AstraZeneca was hampered, given that at the end of the 21st epidemiological week of 2021, this vaccine had not yet reached the second dose’s peak of administration.

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