ABSTRACT

Objective:

To analyze the spatial behavior of hepatitis A, measles, mumps, and rubella (MMR), and varicella vaccination coverage in children and its relationship with socioeconomic determinants in the state of Minas Gerais.

Methods:

This ecological study investigated records of doses administered to children, extracted from the Immunization Information System of 853 municipalities in Minas Gerais, in 2020. We analyzed the vaccination coverage and socioeconomic factors. Spatial scan statistics were used to identify spatial clusters and measure the relative risk based on the vaccination coverage indicator and the Bivariate Moran Index, and thus detect socioeconomic factors correlated with the spatial distribution of vaccination. We used the cartographic base of the state and its municipalities and the ArcGIS and SPSS software programs.

Results:

Hepatitis A (89.0%), MMR (75.7%), and varicella (89.0%) showed low vaccination coverage. All vaccines analyzed had significant clusters. The clusters most likely to vaccinate their population were mainly located in the Central, Midwest, South Central, and Northwest regions, while the least likely were in the North, Northeast, and Triângulo do Sul regions. The municipal human development index, urbanization rate, and gross domestic product were spatially dependent on vaccination coverage.

Conclusions:

The spatial behavior of hepatitis A, MMR, and varicella vaccination coverage is heterogeneous and associated with socioeconomic factors. We emphasize that vaccination records require attention and should be continuously monitored to improve the quality of information used in services and research.

Keywords:
Immunization programs; Vaccines; Vaccination coverage; Health information systems; Spatial analysis; Public health nursing

INTRODUCTION

Considered a priority intervention, vaccination prevents infant mortality and reduces hospitalization and vaccine-preventable diseases, avoiding up to 2.5 million deaths worldwide every year¹1 World Health Organization. Immunization agenda 2030: a global strategy to leave no one behind. Geneva: World Health Organization; 2020.–³3 World Health Organization. Immunization. Geneva: World Health Organization; 2019.. This intervention is regarded as one of the greatest achievements of humanity, recognized as the best cost-benefit public health investment³3 World Health Organization. Immunization. Geneva: World Health Organization; 2019.,⁴4 Diniz MO, Ferreira LCS. Biotecnologia aplicada ao desenvolvimento de vacinas. Estudos Avançados 2010; 24: 19-30. https://doi.org/10.1590/S0103-40142010000300003
https://doi.org/10.1590/S0103-4014201000... .

Currently, the Immunization Agenda 2030 global strategy foresees a world where people of all ages and places benefit fully from the vaccines offered to improve the population's health and well-being. This intervention proposes to maintain the positive vaccination results achieved and recover the losses caused by SARS-CoV-2 (COVID-19)⁵5 Organização Pan-Americana da Saúde. Pandemia de COVID-19 leva a grande retrocesso na vacinação infantil, mostram novos dados da OMS e UNICEF [Internet]. 2021 [cited on Oct 21, 2022]. Available at: https://www.paho.org/pt/noticias/15-7-2021-pandemia-covid-19-leva-grande-retrocesso-na-vacinacao-infantil-mostram-novos
https://www.paho.org/pt/noticias/15-7-20... .

However, less than two-thirds of all countries have reached optimal coverage⁶6 Peck M, Gacic-Dobo M, Diallo MS, Nedelec Y, Sodha SS, Wallace AS. Global routine vaccination coverage, 2018. MMWR Morb Mortal Wkly Rep 2019; 68(42): 937-42. https://doi.org/10.15585/mmwr.mm6842a1
https://doi.org/10.15585/mmwr.mm6842a1... . Among the vaccines offered to children, the measles, mumps, and rubella (MMR) and varicella vaccines are experiencing a decrease in coverage. These diseases are highly contagious and have several associated clinical complications⁷7 Di Pietrantonj C, Rivetti A, Marchione P, Debalini MG, Demicheli V. Vaccines for measles, mumps, rubella, and varicella in children. Cochrane Database Syst Rev 2020; 4: CD004407. https://doi.org/10.1002/14651858.CD004407.pub4
https://doi.org/10.1002/14651858.CD00440... . The hepatitis A vaccine also stands out, with a drop in vaccination coverage in all Brazilian states after 2015⁸8 Brito WI, Souto FJD. Universal hepatitis A vaccination in Brazil: analysis of vaccination coverage and incidence five years after program implementation. Rev Bras Epidemiol 2020: e200073. https://doi.org/10.1590/1980-549720200073
https://doi.org/10.1590/1980-54972020007... . The disease has mild clinical manifestations in childhood and rarely progresses into the severe condition of fulminant failure.

In 2020, about 23 million children missed essential vaccines — 3.7 million more than in 2019⁵5 Organização Pan-Americana da Saúde. Pandemia de COVID-19 leva a grande retrocesso na vacinação infantil, mostram novos dados da OMS e UNICEF [Internet]. 2021 [cited on Oct 21, 2022]. Available at: https://www.paho.org/pt/noticias/15-7-2021-pandemia-covid-19-leva-grande-retrocesso-na-vacinacao-infantil-mostram-novos
https://www.paho.org/pt/noticias/15-7-20... . Around 3 million children did not receive the first dose of the measles vaccine, contributing to the increase in outbreaks, such as those that occurred in Venezuela (2017), Madagascar, the Philippines, and Brazil (2018 and 2019)⁹9 Organização Pan-Americana da Saúde. Dados preliminares da OMS apontam que casos de sarampo em 2019 quase triplicaram em relação ao ano passado [Internet]. 2019 [cited on Oct 21, 2022]. Available at: https://www.paho.org/pt/noticias/12-8-2019-dados-preliminares-da-oms-apontam-que-casos-sarampo-em-2019-quase-triplicaram-em
https://www.paho.org/pt/noticias/12-8-20... ,¹⁰10 Fundo das Nações Unidas para a Infância. Surto global de sarampo, uma ameaça crescente para crianças [Internet]. 2019 [cited on Oct 21, 2022]. Available at: https://www.unicef.org/brazil/comunicados-de-imprensa/surto-global-de-sarampo-uma-ameaca-crescente-para-criancas
https://www.unicef.org/brazil/comunicado... . Vaccination coverage has been dropping in European countries since 2016, with measles and diphtheria, tetanus, and pertussis (DTP) vaccines showing the highest decreasing rates, reaching almost 14 million children not fully immunized in 2019¹¹11 Organização Pan-Americana da Saúde. OMS e UNICEF alertam para declínio na vacinação durante pandemia de COVID-19 [Internet]. 2020 [cited on Oct 21, 2022]. Available at: https://www.paho.org/pt/noticias/15-7-2020-oms-e-unicef-alertam-para-declinio-na-vacinacao-durante-pandemia-covid-19
https://www.paho.org/pt/noticias/15-7-20... . In Montana, United States, less than two out of five children aged 24 months are fully immunized with vaccines administered in childhood¹²12 Newcomer SR, Freeman RE, Wehner BK, Anderson SL, Daley MF. Timeliness of early childhood vaccinations and undervaccination patterns in Montana. Am J Prev Med 2021; 61(1): e21-e29. https://doi.org/10.1016/j.amepre.2021.01.038
https://doi.org/10.1016/j.amepre.2021.01... .

In Brazil, vaccination coverage is not evenly distributed, with reduced rates for some vaccines offered in the National Immunization Program (Programa Nacional de Imunizações — PNI) schedule¹³13 Sato APS. What is the importance of vaccine hesitancy in the drop of vaccination coverage in Brazil? Rev Saude Publica 2018; 52: 96. https://doi.org/10.11606/S1518-8787.2018052001199
https://doi.org/10.11606/S1518-8787.2018... –¹⁵15 Braz RM, Domingues CMAS, Teixeira AMS, Luna EJA. Classification of transmission risk of vaccine-preventable diseases based on vaccination indicators in Brazilian municipalities. Epidemiol Serv Saude 2016; 25(4): 745-54. https://doi.org/10.5123/S1679-49742016000400008
https://doi.org/10.5123/S1679-4974201600... . From 2006 to 2016, some states, such as Goiás, Mato Grosso, and Minas Gerais, had a reduced number of children vaccinated with MMR¹⁵15 Braz RM, Domingues CMAS, Teixeira AMS, Luna EJA. Classification of transmission risk of vaccine-preventable diseases based on vaccination indicators in Brazilian municipalities. Epidemiol Serv Saude 2016; 25(4): 745-54. https://doi.org/10.5123/S1679-49742016000400008
https://doi.org/10.5123/S1679-4974201600... ,¹⁶16 Arroyo LH, Ramos ACV, Yamamura M, Weiller TH, Crispim JA, Cartagena-Ramos D, et al. Áreas com queda da cobertura vacinal para BCG, poliomielite e tríplice viral no Brasil (2006-2016): mapas da heterogeneidade regional. Cad Saude Publica 2020; 36: e00015619. https://doi.org/10.1590/0102-311X00015619
https://doi.org/10.1590/0102-311X0001561... . Since 2015, hepatitis A vaccination coverage decreased among Brazilian municipalities, ranging from 60% to 82%⁸8 Brito WI, Souto FJD. Universal hepatitis A vaccination in Brazil: analysis of vaccination coverage and incidence five years after program implementation. Rev Bras Epidemiol 2020: e200073. https://doi.org/10.1590/1980-549720200073
https://doi.org/10.1590/1980-54972020007... . Varicella had a mean coverage of 78.0% in 2016, a rate that has been declining ever since, reaching 34.3% in 2019¹⁷17 Manetti CL, Fernandes B, Oliveira DK, Banovski DC, Araújo SP, Brusque CEP, et al. Varicela grave: uma análise das notificações compulsórias, Brasil 2012 a 2019. Res Soc Dev 2021; 10(2): e7510212026. https://doi.org/10.33448/RSD-V10I2.12026
https://doi.org/10.33448/RSD-V10I2.12026... .

Low vaccination coverage is often related to the population's geographic conditions and socioeconomic status¹⁸18 Hortal M, Di Fabio JL. Rechazo y gestión en vacunaciones: sus claroscuros. Rev Panam Salud Publica 2019; 43: e54. https://doi.org/10.26633/RPSP.2019.54
https://doi.org/10.26633/RPSP.2019.54... –²⁰20 Hu Y, Chen Y. Evaluating childhood vaccination coverage of NIP vaccines: coverage survey versus zhejiang provincial immunization information system. Int J Environ Res Public Health 2017; 14(7): 758. https://doi.org/10.3390/ijerph14070758
https://doi.org/10.3390/ijerph14070758... , structural conditions, supply and access to health services¹⁴14 Silveira MF, Buffarini R, Bertoldi AD, Santos IS, Barros AJD, Matijasevich A, et al. The emergence of vaccine hesitancy among upper-class Brazilians: results from four birth cohorts, 1982-2015. Vaccine 2020; 38(3): 482-8. https://doi.org/10.1016/J.VACCINE.2019.10.070
https://doi.org/10.1016/J.VACCINE.2019.1... ,¹⁹19 Guzman-Holst A, DeAntonio R, Prado-Cohrs D, Juliao P. Barriers to vaccination in Latin America: a systematic literature review. Vaccine 2020; 38(3): 470-81. https://doi.org/10.1016/j.vaccine.2019.10.088
https://doi.org/10.1016/j.vaccine.2019.1... ,²¹21 Figueiredo A, Johnston IG, Smith DMD, Agarwal S, Larson HJ, Jones NS. Forecasted trends in vaccination coverage and correlations with socioeconomic factors: a global time-series analysis over 30 years. Lancet Glob Health 2016; 4(10): e726-35. https://doi.org/10.1016/S2214-109X(16)30167-X
https://doi.org/10.1016/S2214-109X(16)30... , lack of awareness of the strategies recommended by the immunization program²²22 Duarte DC, Oliveira VC, Guimarães EAA, Viegas SMF. Vaccination access in Primary Care from the user's perspective: senses and feelings about healthcare services. Esc Anna Nery 2019; 23: e20180250. https://doi.org/10.1590/2177-9465-EAN-2018-0250
https://doi.org/10.1590/2177-9465-EAN-20... –²⁴24 Ferreira AV, Freitas PHB, Viegas SMF, Oliveira VC. Access to the vaccine room of the family health strategy: organization aspects. J Nurs UFPE on line 2017; 11(10): 3869-77. https://doi.org/10.5205/reuol.12834-30982-1-SM.1110201722
https://doi.org/10.5205/reuol.12834-3098... , vaccine hesitancy¹³13 Sato APS. What is the importance of vaccine hesitancy in the drop of vaccination coverage in Brazil? Rev Saude Publica 2018; 52: 96. https://doi.org/10.11606/S1518-8787.2018052001199
https://doi.org/10.11606/S1518-8787.2018... ,¹⁴14 Silveira MF, Buffarini R, Bertoldi AD, Santos IS, Barros AJD, Matijasevich A, et al. The emergence of vaccine hesitancy among upper-class Brazilians: results from four birth cohorts, 1982-2015. Vaccine 2020; 38(3): 482-8. https://doi.org/10.1016/J.VACCINE.2019.10.070
https://doi.org/10.1016/J.VACCINE.2019.1... and, more recently, the COVID-19 pandemic²⁵25 Bramer CA, Kimmins LM, Swanson R, Kuo J, Vranesich P, Jacques-Carroll LA, et al. Decline in child vaccination coverage during the COVID-19 pandemic — Michigan Care Improvement Registry, May 2016-May 2020. MMWR Morb Mortal Wkly Rep 2022; 69(20): 630-1. https://doi.org/10.15585/MMWR.MM6920E1
https://doi.org/10.15585/MMWR.MM6920E1... ,²⁶26 Sato APS. Pandemic and vaccine coverage: challenges of returning to schools. Rev Saude Publica 2020; 54: 115. https://doi.org/10.11606/S1518-8787.2020054003142
https://doi.org/10.11606/S1518-8787.2020... . The last one has aggravated pre-existing health inequities, exposing social inequalities, discrimination, and health gradients in human populations, both between and within countries²⁷27 Mujica OJ, Brown CE, Victora CG, Goldblatt P, Silva Jr JB. Health inequity focus in pandemic preparedness and response plans. Bull World Health Organ 2022; 100(2): 91. https://doi.org/10.2471/BLT.21.287580
https://doi.org/10.2471/BLT.21.287580... .

In view of the COVID-19 pandemic, which further exacerbated the population's vaccination status, surveillance becomes particularly important and necessary to reduce non-vaccinated population clusters and, consequently, avoid the risk of new epidemics of vaccine-preventable diseases. Systematic monitoring of vaccination coverage is a crucial management action to know not only what motivates vaccine delays and refusals but also the realities involved in this process¹⁹19 Guzman-Holst A, DeAntonio R, Prado-Cohrs D, Juliao P. Barriers to vaccination in Latin America: a systematic literature review. Vaccine 2020; 38(3): 470-81. https://doi.org/10.1016/j.vaccine.2019.10.088
https://doi.org/10.1016/j.vaccine.2019.1... ,²⁸28 Succi RCM. Vaccine refusal – what we need to know. J Pediatr (Rio J) 2018; 94(6): 574-81. https://doi.org/10.1016/J.JPED.2018.01.008
https://doi.org/10.1016/J.JPED.2018.01.0... –³⁰30 Rodrigues CMC, Plotkin SA. Impact of vaccines; health, economic and social perspectives. Front Microbiol 2020; 11: 1526. https://doi.org/10.3389/fmicb.2020.01526
https://doi.org/10.3389/fmicb.2020.01526... .

Knowing the spatial coverage distribution and its possible determinants allows the identification of interfering factors, essential for planning and implementing effective vaccination strategies. The specific contribution of using spatial analysis in the vaccine field has been discussed for years and has steadily increased since the mid-2000s³¹31 Fundo das Nações Unidas para a Infância. Improving vaccination coverage and reducing inequities: use of GIS in immunization programs. New York 25-26 October, 2016 [Internet]. 2017 [cited on Oct 21, 2022]. Available at: https://www.unicef.org/media/58031/file
https://www.unicef.org/media/58031/file... . This analysis has been used in Brazil; however, it needs to be strengthened, given the country's continental dimensions, population size, cultural and socioeconomic diversity, and the foundations of its regional differences³²32 Silva TPR, Gomes CS, Carmo AS, Mendes LL, Rezende EM, Velasquez-Melendez G, et al. Spatial analysis of vaccination against hepatitis B in pregnant women in an urban Brazilian area. Cien Saude Colet 2021; 26(3): 1173-82. https://doi.org/10.1590/1413-81232021263.28262018
https://doi.org/10.1590/1413-81232021263... .

Thus, this study aimed to analyze the spatial behavior of hepatitis A, MMR, and varicella vaccination coverage in children and its relationship with socioeconomic determinants in the state of Minas Gerais.

METHODS

This ecological study sought to determine the hepatitis A, MMR, and varicella vaccination coverage and its spatial distribution in Minas Gerais, in 2020.

Minas Gerais, Brazil's second most populous state, has an area of 586,528.293 km², an estimated population of 20,033,665 inhabitants, and a degree of urbanization of 85.29%³³33 Instituto Brasileiro de Geografia e Estatística. Contagem da população de 2008 [Internet]. 2017 [cited on Oct 21, 2022]. Available at: https://www.ibge.gov.br/
https://www.ibge.gov.br/... . Its territory is divided into 14 macro-regions (South, South Central, Central, Jequitinhonha, West, East, Vale do Aço, Southeast, North, Northwest, Eastern South, Northeast, Triângulo do Sul, Triângulo do Norte), covering 853 municipalities³⁴34 Instituto Brasileiro de Geografia e Estatística. Macrorregiões de Saúde de Minas Gerais [Internet]. 2021 [cited on Oct 21, 2022]. Available at: https://cidades.ibge.gov.br/brasil/mg/panorama
https://cidades.ibge.gov.br/brasil/mg/pa... . This study established the municipalities of the 14 Minas Gerais macro-regions as territorial units of analysis (Figure 1).

We analyzed records — obtained from the PNI Information System database — of hepatitis A (single dose), MMR (second dose), and varicella (first dose)³⁵35 Ministério da Saúde. e-SUS Atenção Primária à Saúde. Prontuário Eletrônico do Cidadão (PEC). Manual de uso – Versão 5 [Internet]. 2021 [cited on Oct 21, 2022]. Available at: https://cgiap-saps.github.io/Manual-eSUS-APS/docs/PEC
https://cgiap-saps.github.io/Manual-eSUS... vaccine doses administered to 15-month-old children from the 853 municipalities of Minas Gerais, in 2020. A spatial analysis was carried out to identify and evaluate clusters of vaccinated children³⁶36 Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med 1995; 14(8): 799-810. https://doi.org/10.1002/SIM.4780140809
https://doi.org/10.1002/SIM.4780140809... and possible socioeconomic factors associated with vaccination coverage. The MMR plus varicella (MMRV) vaccine was not included due to its shortage during the study period³⁷37 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Programa Nacional de Imunizações. Coberturas vacinais no Brasil: período 2010–2014 [Internet]. 2015 [cited on Oct 21, 2022]. Available at: https://siteal.iiep.unesco.org/sites/default/files/sit_accion_files/br_5113.pdf
https://siteal.iiep.unesco.org/sites/def... .

Considered the response variable, vaccination coverage was calculated as the total doses for full immunization of each vaccine analyzed in the numerator and the number of live births in the municipality (recorded in the Live Birth Information System, in 2019) in the denominator, multiplied by 100. According to the Live Birth Information System, 256,892 children were born in the state in 2019³⁸38 Brasil. Ministério da Saúde. DATASUS. Nascidos vivos – Brasil [Internet]. 2022 [cited on Oct 21, 2022]. Available at: http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinasc/cnv/nvuf.def
http://tabnet.datasus.gov.br/cgi/deftoht... , the fraction corresponding to the denominator used to calculate the vaccination coverage indicator for 2020. The PNI set a 95% target for the hepatitis A, MMR, and varicella vaccines³⁷37 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Programa Nacional de Imunizações. Coberturas vacinais no Brasil: período 2010–2014 [Internet]. 2015 [cited on Oct 21, 2022]. Available at: https://siteal.iiep.unesco.org/sites/default/files/sit_accion_files/br_5113.pdf
https://siteal.iiep.unesco.org/sites/def... .

The explanatory variables analyzed were grouped based on socioeconomic variables (municipal human development index; urbanization rate; gross domestic product per capita), extracted from the Brazilian Institute of Geography and Statistics and the João Pinheiro Foundation³⁹39 Fundação João Pinheiro. Estatística e informações: Minas Gerais [Internet]. 2019 [cited on Oct 21, 2022]. Available at: http://fjp.mg.gov.br/
http://fjp.mg.gov.br/... (Chart 1).

Clusters of vaccinated children were spatially identified and analyzed using the spatial analysis technique called scan statistics, developed by Kulldorff and Nagarwalla³⁶36 Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med 1995; 14(8): 799-810. https://doi.org/10.1002/SIM.4780140809
https://doi.org/10.1002/SIM.4780140809... . This analysis involves a gradual scan based on analysis windows with varying sizes throughout the territorial extension of the studied scenario. To this end, this research defined a circular analysis window, with its radius having a specific upper limit, established at 50% of the target population of vaccinated children in Minas Gerais. The intrinsic characteristic of this window is its high flexibility in both location and size, producing an infinite number of distinct geographic circles, each of them eligible as a cluster³⁶36 Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med 1995; 14(8): 799-810. https://doi.org/10.1002/SIM.4780140809
https://doi.org/10.1002/SIM.4780140809... .

Scan statistics uses different probability models. For the number of vaccinated children in the municipalities of Minas Gerais, we adopted the discrete Poisson model, considered the most suitable for rate modeling or count data. Each window has its null hypothesis (H0) tested against the alternative hypothesis (H1) — high risk for the event investigated (vaccination coverage) — compared to the outside window, that is, the remaining territory analyzed⁴⁰40 Lucena KDT, Silva ATMC, Moraes RM, Silva CC, Bezerra IMP. Análise espacial da violência doméstica contra a mulher entre os anos de 2002 e 2005 em João Pessoa, Paraíba, Brasil. Cad Saude Publica 2012; 28(6): 1111-21. https://doi.org/10.1590/S0102-311X2012000600010
https://doi.org/10.1590/S0102-311X201200... .

The analysis was processed by the SaTScan 9.6 software, setting non-overlapping clusters as parameter⁴¹41 Coulston JW, Riitters KH. Geographic analysis of forest health indicators using spatial scan statistics. Environ Manage 2003; 31(6): 764-73. https://doi.org/10.1007/s00267-002-0023-9
https://doi.org/10.1007/s00267-002-0023-... . The significance test for the identified clusters was based on the comparison between likelihood ratio test statistics and a null distribution, according to the Monte Carlo simulation. A higher number of replications in the Monte Carlo simulation affects the power of the respective test; thus, 999 replications were established to analyze the vaccination in the state³⁶36 Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med 1995; 14(8): 799-810. https://doi.org/10.1002/SIM.4780140809
https://doi.org/10.1002/SIM.4780140809... .

We considered the relative risk (RR) for significant clusters as a way of comparing information from dissimilar areas. RR is a non-negative epidemiological measure that represents how common the event is in the given spatial cluster. Taking into account the number of vaccinated children in Minas Gerais, RR values greater than 1 (RR>1) correspond to an increased probability of being vaccinated at a certain location, while values less than 1 (RR<1) mean the opposite, that is, a lower likelihood of being vaccinated in a region⁴²42 Lawson A. Bayesian disease mapping: hierarchical modeling in spatial epidemiology. 3rd ed. United Kingdom: Chapman and Hall/CRC; 2021.. This calculation is performed with the following mathematic formula:

In which c is the number of cases inside the cluster, C is the total number of cases in the dataset, E[c] is the number of cases expected inside the window under the null hypothesis. We also calculated 95% confidence intervals (95%CI) of RRs of significant spatial clusters⁴³43 Arroyo LH, Yamamura M, Protti-Zanatta ST, Fusco APB, Palha PF, Ramos ACV, et al. Identificação de áreas de risco para a transmissão da tuberculose no município de São Carlos, São Paulo, 2008 a 2013. Epidemiol Serv Saúde 2017; 26(3): 525-34. https://doi.org/10.5123/S1679-49742017000300010
https://doi.org/10.5123/S1679-4974201700... ,⁴⁴44 Assembleia Legislativa do Estado de São Paulo. Índice Paulista de Vulnerabilidade Social [Internet]. 2013 [cited on Oct 21, 2022]. Available at: http://ipvs.seade.gov.br/view/index.php
http://ipvs.seade.gov.br/view/index.php... .

Bivariate Moran analysis was conducted to identify socioeconomic factors correlated with the spatial distribution of vaccination in Minas Gerais. This analysis is a global autocorrelation measure that estimates the influence of one variable on a neighboring one or the correlation between them⁴⁵45 Anselin L. The Moran scatterplot as an ESDA tool to assess local instability in spatial association. In: Fischer M, editor. Spatial analytical perspectives on GIS. London: Routledge; 2019. p. 111-26. https://doi.org/10.1201/9780203739051-8
https://doi.org/10.1201/9780203739051-8... .

The Bivariate Moran can be interpreted as a regression coefficient in a bivariate regression, in which p-values are generated with significant values (p<0.05)⁴⁵45 Anselin L. The Moran scatterplot as an ESDA tool to assess local instability in spatial association. In: Fischer M, editor. Spatial analytical perspectives on GIS. London: Routledge; 2019. p. 111-26. https://doi.org/10.1201/9780203739051-8
https://doi.org/10.1201/9780203739051-8... . The variables selected to analyze spatial correlation were those presented in the method: municipal human development index; urbanization rate, and gross domestic product per capita.

Both the analysis of global spatial autocorrelation (Moran index) and the Bivariate Moran (spatial correlation) were based on a queen contiguity matrix, in which municipalities that share borders are considered neighbors. These analyses were conducted in the Geoda 1.12 software.

Choropleth maps with results from the respective scanning analyses were prepared using the cartographic base of Minas Gerais and its respective municipalities, freely obtained from the website of the Brazilian Institute of Geography and Statistics and elaborated in the ArcGIS 10.8 software.

The study used public domain data with unrestricted access and anonymity for the individuals participating in the investigation; therefore, it did not require appreciation by the Research Ethics Committee.

RESULTS

In Minas Gerais, the vaccination coverage for hepatitis A (89.0%), varicella (89.0%), and MMR (75.7%) was low in 2020. Coverage reached 95.0% or more in only 57.2% (n=488) of the municipalities for hepatitis A, 56.2% (n=479) for varicella, and 35.3% (n=301) for MMR. Figure 2 reveals similarities in the spatial distribution of hepatitis A and varicella vaccination coverage. This pattern was not identified in the distribution of the MMR vaccine, which had a higher number of municipalities with coverage below 95% (n=552).

Spatial scan statistics detected statistically significant clusters for hepatitis A, MMR, and varicella vaccination coverage (Figure 3).

Clusters in the North and Northeast regions had the highest territorial extension (greater number of municipalities in the same cluster) and a lower likelihood of vaccinating their population with hepatitis A (cluster 4), MMR (cluster 5), and varicella (cluster 5) vaccines. The Triângulo do Sul region also presented a cluster with lower odds of vaccinating children against varicella (cluster 6). In contrast, the Central, Midwest, South Central (hepatitis A: cluster 5; MMR: cluster 6 and 7; varicella: cluster 7 and 8), and Northwest regions (MMR: cluster 9) showed the opposite behavior, that is, higher likelihood of vaccinating the population.

The hepatitis A vaccine had six clusters, four of them less likely to vaccinate the population. The MMR and varicella vaccines produced nine clusters. Both showed more clusters with lower odds of having their population vaccinated. Clusters with both higher and lower vaccination likelihood presented a similar pattern; namely, they were in neighboring regions, despite having different sizes, allowing the assumption that some characteristics lead municipalities to have similar coverage.

Table 1 shows results from analyses of the vaccination coverage in 2020 and the socioeconomic variables selected for the study in an attempt to identify factors that may have influenced the change in coverage values for the hepatitis A, MMR, and varicella vaccines in exploratory terms. The municipal human development index variable had a highly statistically significant positive spatial correlation with the coverage of the three vaccines analyzed. This result indicates that municipalities with higher percentages of vaccination coverage tend to be spatially correlated when municipal human development indices are higher in neighboring municipalities.

Also, the urbanization rate and gross domestic product per capita variables showed a low positive spatial correlation with hepatitis A and varicella vaccination coverage. We underline that, despite having a similar but very low trend in positive spatial correlation with these indices, the MMR vaccination coverage displays an important uniqueness in its spatial distribution. This finding is a strong indication that some external factor is influencing this spatial distribution. Nonetheless, this external factor was not included in this analysis, resulting in a different Bivariate Moran value for the hepatitis A and varicella vaccines.

DISCUSSION

The spatial analysis of vaccination coverage in pandemic times pointed to a heterogeneous behavior of the hepatitis A, MMR, and varicella vaccines among the macro-regions in this Brazilian state, a condition associated with socioeconomic factors.

Regional coverage variations are also found in Brazil and other countries. Such differences result from significant geographic, social, and cultural discrepancies between and within regions¹⁶16 Arroyo LH, Ramos ACV, Yamamura M, Weiller TH, Crispim JA, Cartagena-Ramos D, et al. Áreas com queda da cobertura vacinal para BCG, poliomielite e tríplice viral no Brasil (2006-2016): mapas da heterogeneidade regional. Cad Saude Publica 2020; 36: e00015619. https://doi.org/10.1590/0102-311X00015619
https://doi.org/10.1590/0102-311X0001561... ,⁴⁶46 World Health Organization. World Health Organization vaccination coverage cluster surveys: reference manual. Geneva: World Health Organization; 2018.–⁵⁰50 Melaku MS, Nigatu AM, Mewosha WZ. Spatial distribution of incomplete immunization among under-five children in Ethiopia: evidence from 2005, 2011, and 2016 Ethiopian Demographic and health survey data. BMC Public Health 2020; 20(1): 1362. https://doi.org/10.1186/s12889-020-09461-3
https://doi.org/10.1186/s12889-020-09461... . Brazil and Minas Gerais, for example, have large territories with unequal socioeconomic effects among their population groups⁵¹51 Domingues EP, Magalhães AS, Faria WR. Infraestrutura, crescimento e desigualdade regional: uma projeção dos impactos dos investimentos do Programa de Aceleração do Crescimento (PAC) em Minas Gerais. Pesqui Planej Econ 2009; 39(1): 121-58.. This inequality directly affects access to and care in health services, especially for the poorest or most vulnerable populations⁵²52 Perrett KP, Nolan TM. Immunization during pregnancy: impact on the infant. Paediatr Drugs 2017; 19(4): 313-24. https://doi.org/10.1007/s40272-017-0231-7
https://doi.org/10.1007/s40272-017-0231-... . The need for better governance regarding interdependencies between health, social, environmental, and economic systems to ensure public health equity has been increasingly recognized worldwide²⁷27 Mujica OJ, Brown CE, Victora CG, Goldblatt P, Silva Jr JB. Health inequity focus in pandemic preparedness and response plans. Bull World Health Organ 2022; 100(2): 91. https://doi.org/10.2471/BLT.21.287580
https://doi.org/10.2471/BLT.21.287580... .

This study reveals a greater spatial correlation between vaccination coverage and the municipal human development index, a measure comprising indices related to three dimensions of human development: life expectancy, education, and income.

In Spain, children whose parents had a higher level of education were more likely to be vaccinated⁵³53 Mora T, Trapero-Bertran M. The influence of education on the access to childhood immunization: the case of Spain. BMC Public Health 2018; 18(1): 893. https://doi.org/10.1186/s12889-018-5810-1
https://doi.org/10.1186/s12889-018-5810-... . In Nigeria, a higher household income contributed to the children's full immunization⁵⁴54 Adebowale A, Obembe T, Bamgboye E. Relationship between household wealth and childhood immunization in core-North Nigeria. Afr Health Sci 2019; 19(1): 1582-93. https://doi.org/10.4314/ahs.v19i1.33
https://doi.org/10.4314/ahs.v19i1.33... . In Brazil, studies report that the higher the level of education⁵⁵55 Couto MT, Barbieri CLA. Cuidar e (não) vacinar no contexto de famílias de alta renda e escolaridade em São Paulo, SP, Brasil. Ciên Saúde Coletiva 2015; 20(1): 105-14. https://doi.org/10.1590/1413-81232014201.21952013
https://doi.org/10.1590/1413-81232014201... ,⁵⁶56 Smith PJ, Chu SY, Barker LE. Children who have received no vaccines: who are they and where do they live? Pediatrics 2004; 114(1): 187-95. https://doi.org/10.1542/peds.114.1.187
https://doi.org/10.1542/peds.114.1.187... and income of parents⁸8 Brito WI, Souto FJD. Universal hepatitis A vaccination in Brazil: analysis of vaccination coverage and incidence five years after program implementation. Rev Bras Epidemiol 2020: e200073. https://doi.org/10.1590/1980-549720200073
https://doi.org/10.1590/1980-54972020007... ,⁵⁷57 Cata-Preta BO, Santos TM, Mengistu T, Hogan DR, Barros AJD, Victora CG. Zero-dose children and the immunisation cascade: understanding immunisation pathways in low and middle-income countries. Vaccine 2021; 39(32): 4564-70. https://doi.org/10.1016/j.vaccine.2021.02.072
https://doi.org/10.1016/j.vaccine.2021.0... ,⁵⁸58 Barata RB, Ribeiro MCSA, Moraes JC, Flannery B, Vaccine Coverage Survey 2007 Group. Socioeconomic inequalities and vaccination coverage: results of an immunisation coverage survey in 27 Brazilian capitals, 2007-2008. J Epidemiol Community Health 2012; 66(10): 934-41. https://doi.org/10.1136/jech-2011-200341
https://doi.org/10.1136/jech-2011-200341... , the lower the probability of full immunization. This scenario may be associated with vaccine hesitancy⁸8 Brito WI, Souto FJD. Universal hepatitis A vaccination in Brazil: analysis of vaccination coverage and incidence five years after program implementation. Rev Bras Epidemiol 2020: e200073. https://doi.org/10.1590/1980-549720200073
https://doi.org/10.1590/1980-54972020007... ,²⁶26 Sato APS. Pandemic and vaccine coverage: challenges of returning to schools. Rev Saude Publica 2020; 54: 115. https://doi.org/10.11606/S1518-8787.2020054003142
https://doi.org/10.11606/S1518-8787.2020... ,⁵⁷57 Cata-Preta BO, Santos TM, Mengistu T, Hogan DR, Barros AJD, Victora CG. Zero-dose children and the immunisation cascade: understanding immunisation pathways in low and middle-income countries. Vaccine 2021; 39(32): 4564-70. https://doi.org/10.1016/j.vaccine.2021.02.072
https://doi.org/10.1016/j.vaccine.2021.0... ,⁵⁹59 Aps LRMM, Piantola MAF, Pereira SA, Castro JT, Santos FAO, Ferreira LCS. Adverse events of vaccines and the consequences of non-vaccination: a critical review. Rev Saude Publica 2018; 52: 40. https://doi.org/10.11606/S1518-8787.2018052000384
https://doi.org/10.11606/S1518-8787.2018... , which was more evident during the COVID-19 pandemic and exposed concerns about the quality and safety of vaccines⁸8 Brito WI, Souto FJD. Universal hepatitis A vaccination in Brazil: analysis of vaccination coverage and incidence five years after program implementation. Rev Bras Epidemiol 2020: e200073. https://doi.org/10.1590/1980-549720200073
https://doi.org/10.1590/1980-54972020007... ,²⁶26 Sato APS. Pandemic and vaccine coverage: challenges of returning to schools. Rev Saude Publica 2020; 54: 115. https://doi.org/10.11606/S1518-8787.2020054003142
https://doi.org/10.11606/S1518-8787.2020... ,⁵⁹59 Aps LRMM, Piantola MAF, Pereira SA, Castro JT, Santos FAO, Ferreira LCS. Adverse events of vaccines and the consequences of non-vaccination: a critical review. Rev Saude Publica 2018; 52: 40. https://doi.org/10.11606/S1518-8787.2018052000384
https://doi.org/10.11606/S1518-8787.2018... .

Gross domestic product and urbanization rate affect vaccination coverage and other socioeconomic factors because they can contribute to a poverty scenario⁸8 Brito WI, Souto FJD. Universal hepatitis A vaccination in Brazil: analysis of vaccination coverage and incidence five years after program implementation. Rev Bras Epidemiol 2020: e200073. https://doi.org/10.1590/1980-549720200073
https://doi.org/10.1590/1980-54972020007... ,⁵⁰50 Melaku MS, Nigatu AM, Mewosha WZ. Spatial distribution of incomplete immunization among under-five children in Ethiopia: evidence from 2005, 2011, and 2016 Ethiopian Demographic and health survey data. BMC Public Health 2020; 20(1): 1362. https://doi.org/10.1186/s12889-020-09461-3
https://doi.org/10.1186/s12889-020-09461... , thus impacting the organizational and geographic access to health services and their quality¹⁶16 Arroyo LH, Ramos ACV, Yamamura M, Weiller TH, Crispim JA, Cartagena-Ramos D, et al. Áreas com queda da cobertura vacinal para BCG, poliomielite e tríplice viral no Brasil (2006-2016): mapas da heterogeneidade regional. Cad Saude Publica 2020; 36: e00015619. https://doi.org/10.1590/0102-311X00015619
https://doi.org/10.1590/0102-311X0001561... ,¹⁸18 Hortal M, Di Fabio JL. Rechazo y gestión en vacunaciones: sus claroscuros. Rev Panam Salud Publica 2019; 43: e54. https://doi.org/10.26633/RPSP.2019.54
https://doi.org/10.26633/RPSP.2019.54... ,¹⁹19 Guzman-Holst A, DeAntonio R, Prado-Cohrs D, Juliao P. Barriers to vaccination in Latin America: a systematic literature review. Vaccine 2020; 38(3): 470-81. https://doi.org/10.1016/j.vaccine.2019.10.088
https://doi.org/10.1016/j.vaccine.2019.1... ,²²22 Duarte DC, Oliveira VC, Guimarães EAA, Viegas SMF. Vaccination access in Primary Care from the user's perspective: senses and feelings about healthcare services. Esc Anna Nery 2019; 23: e20180250. https://doi.org/10.1590/2177-9465-EAN-2018-0250
https://doi.org/10.1590/2177-9465-EAN-20... ,⁶⁰60 Mizuta AH, Succi GM, Montalli VAM, Succi RCM. Perceptions on the importance of vaccination and vaccine refusal in a medical school. Rev Paul Pediatr 2019; 37(1): 34-40. https://doi.org/10.1590/1984-0462/;2019;37;1;00008
https://doi.org/10.1590/1984-0462/;2019;... ,⁶¹61 My C, Danchin M, Willaby HW, Pemberton S, Leask J. Parental attitudes, beliefs, behaviours and concerns towards childhood vaccinations in Australia: a national online survey. Aust Fam Physician 2017; 46(3): 145-51. PMID: 28260278. Brazilian studies have identified that the place of residence influences the drop in vaccination coverage⁵⁷57 Cata-Preta BO, Santos TM, Mengistu T, Hogan DR, Barros AJD, Victora CG. Zero-dose children and the immunisation cascade: understanding immunisation pathways in low and middle-income countries. Vaccine 2021; 39(32): 4564-70. https://doi.org/10.1016/j.vaccine.2021.02.072
https://doi.org/10.1016/j.vaccine.2021.0... ,⁶²62 Gonçalves JS, Olivindo DDF. As coberturas vacinais no controle das doenças imunopreveniveis: uma revisão integrativa. Res Soc Dev 2021; 10(6): e59110616536. https://doi.org/10.33448/RSD-V10I6.16536
https://doi.org/10.33448/RSD-V10I6.16536... .

However, in addition to the socioeconomic inequalities detected in this study, other determinants associated with low vaccination coverage have been evidenced, such as difficult access to health services²²22 Duarte DC, Oliveira VC, Guimarães EAA, Viegas SMF. Vaccination access in Primary Care from the user's perspective: senses and feelings about healthcare services. Esc Anna Nery 2019; 23: e20180250. https://doi.org/10.1590/2177-9465-EAN-2018-0250
https://doi.org/10.1590/2177-9465-EAN-20... ,⁶³63 Escobar-Díaz F, Osorio-Merchán MB, De la Hoz-Restrepo F. Motivos de no vacunación en menores de cinco años en cuatro ciudades colombianas. Rev Panam Salud Publica 2017; 41: e123. https://doi.org/10.26633/RPSP.2017.123
https://doi.org/10.26633/RPSP.2017.123... , number of children⁶⁴64 Silva FS, Barbosa YC, Batalha MA, Ribeiro MRC, Simões VMF, Branco MRFC, et al. Incomplete childhood immunization with new and old vaccines and associated factors: BRISA birth cohort, São Luís, Maranhão State, Northeast Brazil. Cad Saude Publica 2018; 34(3): e00041717. https://doi.org/10.1590/0102-311X00041717
https://doi.org/10.1590/0102-311X0004171... ,⁶⁵65 Tauil MC, Sato APS, Costa AA, Inenami M, Ferreira VLR, Waldman EA. Vaccination coverage according to doses received and timely administered based on an electronic immunization registry, Araraquara-SP, Brazil, 2012-2014. Epidemiol Serv Saude 2017; 26(4): 835-46. https://doi.org/10.5123/S1679-49742017000400014
https://doi.org/10.5123/S1679-4974201700... , missed vaccination opportunities⁶⁶66 Olorunsaiye CZ, Langhamer MS, Wallace AS, Watkins ML. Missed opportunities and barriers for vaccination: a descriptive analysis of private and public health facilities in four African countries. Pan Afr Med J 2017; 27(Suppl 3): 6. https://doi.org/10.11604/pamj.supp.2017.27.3.12083
https://doi.org/10.11604/pamj.supp.2017.... ,⁶⁷67 Assad SGB, Corvino MPF, Valente GSC, Cortez EA, Santos SCP. Educação permanente e vacinação: minimizando oportunidades perdidas. Res Soc Dev 2020; 9(11): e59391110198. https://doi.org/10.33448/RSD-V9I11.10198
https://doi.org/10.33448/RSD-V9I11.10198... , underfunding of the health sector, and the complexity of the immunization schedule¹⁴14 Silveira MF, Buffarini R, Bertoldi AD, Santos IS, Barros AJD, Matijasevich A, et al. The emergence of vaccine hesitancy among upper-class Brazilians: results from four birth cohorts, 1982-2015. Vaccine 2020; 38(3): 482-8. https://doi.org/10.1016/J.VACCINE.2019.10.070
https://doi.org/10.1016/J.VACCINE.2019.1... . The COVID-19 pandemic has also aggravated pre-existing social inequalities in health, exposing deeply rooted social shortcomings, discrimination, and health gradients in human populations, between and within countries²⁷27 Mujica OJ, Brown CE, Victora CG, Goldblatt P, Silva Jr JB. Health inequity focus in pandemic preparedness and response plans. Bull World Health Organ 2022; 100(2): 91. https://doi.org/10.2471/BLT.21.287580
https://doi.org/10.2471/BLT.21.287580... .

We can assume that an external factor is influencing the MMR vaccination coverage distribution. This factor may be related to the record of doses administered in the Brazilian Immunization Information System. The system change in Brazil (2014) altered how the system is populated, now based on nominal entries, complicating the process of recording the doses administered⁶⁸68 Silva BS, Guimarães EAA, Oliveira VC, Cavalcante RB, Pinheiro MMK, Gontijo TL, et al. National immunization program information system: implementation context assessment. BMC Health Serv Res 2020; 20(1): 333. https://doi.org/10.1186/s12913-020-05175-9
https://doi.org/10.1186/s12913-020-05175... ,⁶⁹69 Cruz A. A queda da imunização no Brasil. Consensus 2017; 20-9.. Currently, the doses administered are recorded in the Citizen's Electronic Health Record, software developed by the e-SUS Primary Health Care strategy³⁵35 Ministério da Saúde. e-SUS Atenção Primária à Saúde. Prontuário Eletrônico do Cidadão (PEC). Manual de uso – Versão 5 [Internet]. 2021 [cited on Oct 21, 2022]. Available at: https://cgiap-saps.github.io/Manual-eSUS-APS/docs/PEC
https://cgiap-saps.github.io/Manual-eSUS... .

The Brazilian child immunization schedule recommends an MMR dose at 12 months of age and a second MMR dose associated with the varicella component (MMRV) at 15 months³⁷37 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Programa Nacional de Imunizações. Coberturas vacinais no Brasil: período 2010–2014 [Internet]. 2015 [cited on Oct 21, 2022]. Available at: https://siteal.iiep.unesco.org/sites/default/files/sit_accion_files/br_5113.pdf
https://siteal.iiep.unesco.org/sites/def... . However, the MMRV vaccine is not systematically distributed to all Brazilian states. Minas Gerais has not received a supply of this vaccine since 2018⁷⁰70 Brasil. Ministério da Saúde. Coordenação-Geral do Programa Nacional de Imunizações. Nota informativa n° 135-SEI/2017-CGPNI/DEVIT/SVS/MS. Informa as mudanças no Calendário Nacional de Vacinação para o ano de 2018 [Internet]. 2017 [cited on Oct 21, 2022]. Available at: https://saude.es.gov.br/Media/sesa/Imuniza%C3%A7%C3%A3o/SEI_MS%20-%20Nota%20Informativa%20135%20-%20mudancas%20no%20calendario%20nacional%20de%20vacinacao%202018.pdf
https://saude.es.gov.br/Media/sesa/Imuni... . We can infer that some professionals might be recording a second MMR dose in the MMRV field. This assumption indicates underrated coverage, which agrees with the findings of this study, since the MMR vaccine showed a different spatial behavior from the other vaccines (hepatitis A and varicella), both administered at 15 months of age.

The use of the Immunization Information System became a complex and multidimensional process influenced by structural and process conditions, issues with technological components of the software, little experience of the health team with technological resources, and lack of training to use and understand the system, impacting the record of these data and, consequently, the vaccination coverage⁶⁸68 Silva BS, Guimarães EAA, Oliveira VC, Cavalcante RB, Pinheiro MMK, Gontijo TL, et al. National immunization program information system: implementation context assessment. BMC Health Serv Res 2020; 20(1): 333. https://doi.org/10.1186/s12913-020-05175-9
https://doi.org/10.1186/s12913-020-05175... ,⁷¹71 Oliveira VC, Guimarães EAA, Amaral GG, Silva TIM, Fabriz LA, Pinto IC. Acceptance and use of the information system of the national immunization program. Rev Lat Am Enfermagem 2020; 28: e3307. https://doi.org/10.1590/1518-8345.3360.3307
https://doi.org/10.1590/1518-8345.3360.3... ,⁷²72 Guimarães EAA, Morato YC, Carvalho DBF, Oliveira VC, Pivatti VMS, Cavalcante RB, et al. Evaluation of the usability of the immunization information system in Brazil: a mixed-method study. Telemed J E Health 2021; 27(5): 551-60. https://doi.org/10.1089/TMJ.2020.0077
https://doi.org/10.1089/TMJ.2020.0077... .

Although this study aimed to provide an overview of vaccination coverage correlates, regional variability might occur within the municipalities and also among other cluster sets. Study limitations include its ecological design based on secondary data, which may have inconsistencies related to the quality and quantity of information, due to incorrect filling and mistaken records of doses administered in the information system. Nevertheless, the choice of this type of source reduces operational costs and enables the performance of analyses. A consistency analysis of the database was carried out to minimize this limitation.

The results of this article can help health managers and professionals design interventions to structure immunization services and implement management actions (supervision, monitoring, evaluation) to increase vaccination coverage in places at higher risk of transmission of vaccine-preventable diseases. The research field must advance the knowledge of the practice of professionals working in the vaccination station regarding surveillance actions related to the child's vaccination status and confirm, using other methodological designs, the factors that impact vaccination coverage in the child population.

In addition, vaccination records and the quality of data from immunization information systems are issues that require attention and must be continuously monitored to improve these data and reduce the entry of mistaken information.

Lastly, this study aims to provide the basis for policies and promote the equitable expansion of access to and use of immunization services. To that end, further research is necessary.

ACKNOWLEDGEMENTS:

The authors thank the support of the Universidade Federal de São João del-Rei – Divinópolis (Minas Gerais) and the Minas Gerais State Health Department – Belo Horizonte.

REFERENCES

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