The national target of a 95% coverage of VAP was achieved only in 2011, 2012 and 2013. From 2014 to 2021, coverage progressively reduced from 101.3% in 2014, to 54.6% in 2021. The decrease trend of VAP coverage in Brazil and the formation of low-low spatial clusters from years 2011 to 2021, accounts for the high number of children susceptible to poliomyelitis, mainly in the North and Northeast regions of the country.
The existence of clusters of municipalities with low vaccination coverage surrounded by municipalities also with low vaccination coverage (low-low) demonstrates that this is not an isolated problem throughout municipalities, highlighting the common difficulties between cities and health regions in achieving vaccine coverage targets as recommended by the PNI. Clusters of municipalities with low coverage surrounded by municipalities with high coverage (low-high) and clusters of municipalities with high coverage surrounded by municipalities with low coverage appear as possibilities for intervention in these health regions by state and regional policy makers with the aim at strengthening the health care network in these municipalities.
Brazil has one of the most complete immunization programs in the world, widely recognized for its immunization strategies that have ensured the reduction in incidence rates and deaths from diseases such as measles, poliomyelitis and whooping cough [11,13]. It is noteworthy that for the prevention of poliomyelitis, the Brazilian National Immunization Program offers free OPV and IPV, which includes three doses of IVP (at 2, 4 and 6 months) and two boosters with OPV (at 15 months and at 4 years of age) [6]. For both vaccines, the PNI established an annual target of 95% vaccination coverage of the eligible population, as recommended by the WHO [13]. However, the national reduction in vaccination coverage rates, in recent years, has signaled a serious problem for herd immunity and the risk of resurgence of diseases once controlled or eradicated [22–24]. Many factors, contextual and individual, contributed to the drop in coverage of vaccines recommended during childhood, among them include national studies highlighting the implementation of the new SI-PNI, social and cultural aspects that affect vaccine acceptance, the introduction of several vaccines to the national vaccination schedule within a short period, the perception by parents and family members that infectious diseases do not represent a risk for children, since many of these diseases are under control or have been eliminated, and the inconsistency in the availability of immunobiologicals in Primary Care services [13,25–28].
In this study, VAP coverage was not homogeneous across Brazilian states and regions during the evaluated period. The North and Northeast regions, which have the worst social and economic indicators in the country [24,29], presented the worst indicators of VAP coverage in the evaluated study period, thus favoring the formation of pockets of individuals susceptible to Poliovirus in these regions. In Brazil, the regional inequality of human development and health indicators is historical [30,31]. The Southeast, South and Mid-West regions boast a greater Municipal Human Development Index (MHDI) than their neighbors of the North and Northeast regions [31]. The MHDI is an indicator comprised of three dimensions: longevity, education and income, which can vary from 0 to 1. A national study pointed to a trend towards a reduction in VAP coverage in the periods between 2006 to 2016 and the formation of clusters by municipalities with low vaccination coverage located in the North and Northeast regions, corroborating our results and reinforcing the historical discrepancy in vaccination coverage between the Regions of Brazil [14,24,32].
In addition to the worst social indicators, historical inequalities in the allocation of financial resources and investments to the health sector in the North region [14,25] negatively impacted on the structure and quality of primary care services, which in Brazil are responsible for the free provision of immunobiologicals [25]. A national study pointed out that the absence of exclusive refrigeration equipment for the conservation of immunobiologicals, thermal boxes and inadequate structure of vaccination facilities were more frequent in the North region when compared to other regions of the country. The study further reported that the were problemas with the supply chain resulting in the supply of the triple viral vaccine which prevents measles, mumps and rubella (MMR) [25]. Considering that the inaccessability of the vaccine, even for a short period of time, leads to a missed opportunity for vaccination, which may compromise the achievement of vaccine coverage goals and increase the number of susceptible individuals in certain áreas. Thus, strategies and health policies are necessary for improving the structure of primary care services in the Northern region of the country [25]. Finally, the inadequate structure necessary to maintain the cold chain network compromises the availability, not only of the triple viral vaccine (MMR) [25], but of all immunobiologicals, among them, VAP.
The progressive increase in the number of low-low clusters in the North and Northeast regions of the country, from 2016 to present, in contrast to the Southeast, South and Southeast regions, which demonstrated a predominance of high-high clusters during the same period, can be explained, in part, due to fiscal austerity measures that were adopted by the federal government from 2015 to present, in response to a national political and economic crisis [33]. As a result of the reduction in investment in the health sector and in income transfer programs, such as Bolsa Família [33], there was a worsening of social inequality in Brazil, an increase in income concentration and a deteriation of the population's health indicators, among them, vaccination coverage [33,34]. These factors may have acted synergistically, resulting in the worsening of the heterogeneity of vaccination coverage, with low-low clusters prevailing in the North and Northeast regions and a greater number of states with a tendency to decline in VAP coverage when compared to other regions of the country. It is also worth noting that the historic reduction in vaccination coverage in Brazil was exacerbated by the COVID-19 pandemic, especially in the North and Northeast regions, which suffered from the growing demand for beds for hospitalized patients with this disease, which resulted in the collapse of the health services in some states of these regions [11,35,36].
Furthermore, Northern region states of the country have some particularities, among them, are populations which reside along river banks and who require use of small wooden boats for mobility and who must navigate average distances of 60 km, for 4 hours, to access the nearest health services [37]. To reduce the challenges posed by theses distances, strategies and public policies are needed to ensure the riverbank population's have access to immunization services [37,38]. In addition to the geographical barriers, the extensive cross-border territory also poses challenges and, since 2016, the Northern region has received approximately 260,000 Venezuelan refugees who entered Brazil through the city of Pacaraíma, the Vanezuelan-Brazilian border located in the State of Roraima [39]. The political and economic instability in Venezuela has compromised the population's access to employment, health services and housing, triggering the migratory flow of Venezuelans to Latin American countries, especially to Brazil [39]. In February 2018, an outbreak of the genotype D8 measles virus was reported, which started in Roraima and spread to the states of the Northern region of the country [19]. Transmission occurred by contact between susceptible people and Venezuelans who contracted measles, and because of low MRR vaccine coverage by the population in the North, the result was the reintroduction of measles in the country [40].
This scenario becomes even more worrisome when analyzing the global geopolitical situation. In Afghanistan, the recent seizure of power by the Taliban, an Islamic fundamentalist militia group that, in 2019, banned polio campaigns in Afghanistan and Pakistan [41], resulting in a increase in Poliomyelitis cases and leaving these countries increasingly distant from certification of polio-free regions [6]. In addition to the political challenges, polio vaccination refusal by children's parents, illiteracy, poverty, the increasing number of children who are not immunized during vaccination campaigns, administration of polio vaccine after the deadline validity, the belief that the polio vaccine is not in accordance with the precepts of Islam and the dissemination of fake news on social media—are just some of reasons for the immunization campaign failures in Pakistan and Afghanistan [5–7,42].
It should be noted that, in the midst of the COVID-19 pandemic, immunization strategies against poliomyelitis were interrupted in these countries, especially those immunization strategies that were carried out door-to-door [6,7]. This interruption, even for a short period of time, has compromised polio vaccine coverage and represents a barrier to achieving a Polio Free World by 2026, a target set out in the Polio Eradication Strategy 2022–2026 [6,7]. In addition to facing the low vaccine coverage against poliomyelitis in these countries, it is worth mentioning that an increase in cases of acute flaccid paralysis was the result of a specific vaccine poliovirus, called the vaccine-derived poliovirus (VDPV) [2], which occurred between 2019 to 2020 [6,7].
The circulation of the VDPV (cVDPV) occurs when the Poliovirus contained in the OPV undergoes mutations that give the virus the ability to invade the central nervous system and cause acute flaccid paralysis in the same way as wild polioviruses [2,8]. Since 2018, there have been an increasing number of outbreaks of acute flaccid paralysis caused by cVDPV, with the majority of cases arising from the circulation of vaccine-derived Poliovirus 2 (cVDPV2) [43]. The low OPV coverage, added to the increased number of individuals susceptible to Poliovirus in certain areas, increases the chances of outbreaks of acute flaccid paralysis caused by cVDPV2 [2,8]. In 2020, 1,056 cVDPV2 cases were detected in Afghanistan, Pakistan, Chad, and the Democratic Republic of Congo, representing triple the number of cVDPV2 cases from the previous year [7,8], and by the end of 2021, cVDPV2 was isolated in stool samples from children with acute flaccid paralysis in Ukraine and Yemen [8,44,45]. In the same manner that immunization actions against Poliomyelitis were interrupted in these countries during the COVID-19 pandemic, the systematic Epidemiological Surveillance (EV) strategies of acute flaccid paralysis, which are essential for early detection of possible cases of poliomyelitis [10], also fell short of expectations, which motivated the Emergency Committee, in accordance to the International Health Regulations, to declare that there was a risk of international spread of Wild poliovirus and cVDPV, an outbreak that constituted a Public Health Emergency of International Concern (PHEIC) [7,8].
In this context, similar to migratory movements, added to the low coverage of the triple viral vaccine and triggered the measles outbreak in Brazil which began in the North region and spread throughout the country [19]. Civil war, economic and political instability in Pakistan and Afghanistan, the last bastions of the WP1 strain in the world [6], can contribute to the spread of Poliovirus to the rest of the world, affecting countries with low vaccination coverage and high risk of cVDPV emergence or importation of Poliovirus, among them, Brazil.
Limitations
This study was subject to information bias, since the researchers did not possess access to quality-controlled SI-PNI information records. However, the SI-PNI constitutes an important official source of information. Coordinated by the Ministry of Health, the SI-PNI is technically sound and, over the past 40 years, has allowed for vaccination monitoring coverage and provides technical assistance at the federal, state and local levels for guidance and decision-making necessary best choice health strategy practices aimed at preventing infectious diseases [13]. Therefore, the generalization of the results is relatively safe for national estimates.
Contributions
This study may contribute to the identification of territories that presented unsatifactory indicators on vaccination coverage targeting poliomyelitis in Brazil, which highlights the urgent need to prioritize vaccination strategies and efforts at increase coverage of vulnerable populations in theses regions. In addition to the territories that report vaccine coverage against poliomyelitis below the 95% target, those with a sharp drop in vaccination coverage in the evaluated period should also be prioritized. In this sense, vaccination strategies that address both the resident population and the population of travelers, migrants and refugees should be given full priority in these territories.