The Temporal Trends of Mortality Due to Tuberculosis in Brazil: Tracing the Coronavirus Disease 2019 (COVID-19) Pandemic’s Effect Through a Bayesian Approach and Unmasking Disparities
Abstract
1. Introduction
2. Materials and Methods
2.1. Design and Setting of This Study
2.2. Population, Data Sources, and Selection Criteria
2.3. Data Analysis
2.3.1. Calculation of the Mortality Rate
2.3.2. Trend Estimation
2.3.3. Detection of Structural Changes
2.3.4. Calculation of Percentage Change
2.3.5. Calculation of Averages
2.3.6. Assessment of Causal Effect
2.4. Ethics Statement
3. Results
3.1. Trends and Structural Changes
3.2. Mean and AMPC
3.3. Causal Effect Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
TB | Tuberculosis |
SIM | Mortality Information System |
WHO | World Health Organization |
DATASUS | Department of Informatics of the Unified Health System |
IBGE | Brazilian Institute of Geography and Statistics |
STL | Seasonal-Trend Decomposition by Loess |
BSTS | Bayesian Structural Time Series |
ARIMA | Autoregressive Integrated Moving Average |
CAAE | Certificate of Presentation for Ethical Appreciation |
SDG | Sustainable Development Goal |
CI | Confidence interval |
AIC | Akaike Information Criterion |
ICD-10 | International Classification of Diseases |
References
- Ministry of Health. Boletim Epidemiológicol; Ministry of Health: Brasília, Brazil, 2025. Available online: https://www.gov.br/aids/pt-br/central-de-conteudo/boletins-epidemiologicos/2025/boletim-epidemiologico-tuberculose-2025/@@download/file (accessed on 29 April 2025).
- World Health Organization. Global Tuberculosis Report, 2024. Available online: https://iris.who.int/bitstream/handle/10665/363752/9789240061729eng.pdf?sequence=1 (accessed on 29 April 2025).
- Hino, P.; Yamamoto, T.T.; Magnabosco, G.T.; Bertolozzi, M.R.; Taminato, M. Impacto da COVID-19 no controle E reorganização da atenção à tuberculose. Acta Paul. Enferm. 2021, 34, eAPE002115. [Google Scholar] [CrossRef]
- Berra, T.Z.; Ramos, A.C.V.; Alves, Y.M.; Tavares, R.B.V.; Tartaro, A.F.; do Nascimento, M.C.; Moura, H.S.D.; Delpino, F.M.; de Almeida Soares, D.; Silva, R.V.D.S.; et al. Impact of COVID-19 on Tuberculosis Indicators in Brazil: A Time Series and Spatial Analysis Study. Trop. Med. Infect. Dis. 2022, 7, 247. [Google Scholar] [CrossRef] [PubMed]
- Blumea, M.C.; Waldmanb, E.A.; Lindosoc, A.A.B.P.; Rújulac, M.J.P.; Orlandic, G.M.; de Lourdes Viude Oliveirac, M.; Guimarãesa, A.M.S. The impact of the SARS-CoV-2 pandemic on tuberculosis notifications and deaths in the state of São Paulo, Brazil: A cross-sectional study. Lancet Reg. Health Am. 2024, 34, 100765. [Google Scholar] [CrossRef] [PubMed]
- Cortez, A.O.; Melo, A.C.; Neves, L.O.; Resende, K.A.; Camargo, P. Tuberculosis in Brazil: One country, multiple realities. J. Bras. Pneumol. 2021, 47, e20200119. [Google Scholar] [CrossRef]
- de Souza, C.D.F.; Neto, E.R.D.; Matos, T.S.; Ferreira, A.C.F.; Bezerra-Santos, M.; da Silva Junior, A.G.; Carmo, R.F.D. Bridging the Gaps: Investigating the Complex Impact of the COVID-19 Pandemic on Tuberculosis Records in Brazil. Trop. Med. Infect. Dis. 2023, 8, 454. [Google Scholar] [CrossRef]
- Tavares, R.B.V.; Berra, T.Z.; Alves, Y.M.; Popolin, M.A.P.; Ramos, A.C.V.; Tártaro, A.F.; de Souza, C.F.; Arcêncio, R.A. Unsuccessful tuberculosis treatment outcomes across Brazil’s geographical landscape before and during the COVID-19 pandemic: Are we truly advancing toward the sustainable development/end TB goal? Infect Dis. Poverty 2024, 13, 17. [Google Scholar] [CrossRef]
- Hentringer, I.M.B.; da Mata Ribeiro, J.A.; de Jesus Brandão Barreto, I.; de Santana Cabral Silva, A.P. Effect of COVID-19 Pandemic on New Cases of Tuberculosis in Brazil: A Temporal and Spatial Analysis. Mundo Saude 2022, 47, e13912022. [Google Scholar] [CrossRef]
- Antunes, J.L.F.; Cardoso, M.R.A. Using time series analysis in epidemiological studies. SciELO 2015, 24, 565–576. [Google Scholar]
- Martinez, E.Z.; Achcar, J.A. Trends in epidemiology in the 21st century: Time to adopt bayesian methods. Cad. Saude Publica 2014, 30, 703–714. [Google Scholar] [CrossRef]
- World Health Organization. The End TB Strategy, 2015. Available online: https://iris.who.int/bitstream/handle/10665/331326/WHO-HTM-TB-2015.19eng.pdf?sequence=1 (accessed on 10 August 2024).
- Agency for Healthcare Research and Quality. National Healthcare Quality and Disparities Report; Agency for Healthcare Research and Quality: Rockville, MD, USA, 2021. Available online: https://www.ncbi.nlm.nih.gov/books/NBK578529/ (accessed on 20 January 2025).
- Duarte, R.; Lönnroth, K.; Carvalho, C.; Lima, F.; Carvalho, A.C.C.; Muñoz-Torrico, M.; Centis, R. Tuberculosis, social determinants and co-morbidities (including HIV). Pulmonology 2018, 24, 115–119. [Google Scholar] [CrossRef]
- Morgenstern, H. Ecologic studies in epidemiology: Concepts, principles, and methods. Annu. Rev. Public Health 1995, 16, 61–81. [Google Scholar] [CrossRef] [PubMed]
- Brazilian Institute of Geography and Statistics (IBGE). Brazil em Síntese; Brazilian Institute of Geography and Statistics (IBGE): Brasília, Brazil, 2022. Available online: https://brasilemsintese.ibge.gov.br/ (accessed on 26 July 2024).
- Ministry of Health. Manual de Recomendações para o Controle da Tuberculose no Brasil Brasília; Ministry of Health: Rio de Janeiro, Brazil, 2019. Available online: https://www.gov.br/saude/pt-br/assuntos/saude-de-a-a-z/t/tuberculose/publicacoes/manual-de-recomendacoes-para-o-controle-da-tuberculose-no-brasil.pdf/@@download/file (accessed on 10 July 2024).
- Brazilian Institute of Geography and Statistics (IBGE). População; Brazilian Institute of Geography and Statistics (IBGE): Brasília, Brazil, 2022. Available online: https://www.ibge.gov.br/estatisticas/sociais/populacao.html (accessed on 26 July 2024).
- Brazilian Institute of Geography and Statistics (IBGE). Censo Demográfico 2022. Identificação Étnico-Racial Da População, Por Sexo E Idade; Brazilian Institute of Geography and Statistics (IBGE): Brasília, Brazil, 2022. Available online: https://agenciadenoticias.ibge.gov.br/media/com_mediaibge/arquivos/13ee0337cffc1de37bf0cd4da3988e1f.pdf (accessed on 26 July 2024).
- Cleveland, R.B.; Cleveland, W.S. STL: A Seasonal-Trend Decomposition Procedure Based on Loess. J. Off. Stat. 1990, 6, 3–33. [Google Scholar]
- Brockwell, P.J.; Davis, R.A. Introduction to Time Series and Forecasting, 2nd ed.; Springer: New York, NY, USA, 2002. [Google Scholar]
- Zeileis, A.; Kleiber, C.; Krämer, W.; Hornik, K. Testing and dating of structural changes in practice. Comput. Stat. Data Anal. 2003, 44, 109–123. [Google Scholar] [CrossRef]
- Brodersen, K.H.; Gallusser, F.; Koehler, J.; Remy, N.; Scott, S.L. Inferring causal impact using Bayesian structural time-series models. Ann. Appl. Stat. 2015, 9, 247–274. [Google Scholar] [CrossRef]
- Box, G.E.P.; Jenkins, G.M. Time Series Analysis: Forecasting and Control, 5th ed.; Wiley: Hoboken, NJ, USA, 1976; p. 712. [Google Scholar]
- Nalunjogi, J.; Mucching-Toscano, S.; Sibomana, J.P.; Centis, R.; D'Ambrosio, L.; Alffenaar, J.W.; Denholm, J.; Blanc, F.X.; Borisov, S.; Danila, E.; et al. Impact of COVID-19 on diagnosis of tuberculosis, multidrug-resistant tuberculosis, and on mortality in 11 countries in Europe, Northern America, and Australia. A Global Tuberculosis Network study. Int. J. Infect Dis. 2023, 130, S25–S29. [Google Scholar] [CrossRef]
- Brito, A.B.; Magalhães, W.B.; de Paiva, J.P.S.; de Leal, T.C.; Silva, L.F.; da Santos, L.G.; Santana, G.B.A.; Fernandes, T.R.M.O.; Souza, C.D.F. Tuberculosis in Northeastern Brasil (2001–2016): Trend, clinical profile, and prevalence of risk factors and associated comorbidities. Rev. Assoc. Med. Bras. 2020, 66, 1196–1202. [Google Scholar] [CrossRef]
- Szwarcwald, C.L.; Morais Neto, O.L.; Frias, P.G.; Souza, P.R.B., Jr.; Cortez-Escalante, J.J.; Lima, R.B.; Viola, R.C. Busca ativa de óbitos e nascimentos no Nordeste e na Amazônia Legal: Estimação das coberturas do SIM e do SINASC nos municípios brasileiros. In Departamento de Análise de Situação de Saúde, Secretaria de Vigilância em Saúde, Ministério da Saúde, Organizadores. Saúde Brasil, 2010: Uma Análise Da Situação de Saúde E de Evidências Selecionadas de Impacto de ações de Vigilância Em Saúde; Ministério da Saúde: Brasília, Brazil, 2011; pp. 79–98. [Google Scholar]
- UN Women. The Impact of COVID-19 on Women; United Nations: New York, NY, USA, 2020; Available online: https://www.unwomen.org/en/digital-library/publications/2020/04/policy-brief-the-impact-of-covid-19-on-women (accessed on 5 May 2025).
- Horton, K.C.; MacPherson, P.; Houben, R.M.G.J.; White, R.G.; Corbett, E.L. Sex Differences in Tuberculosis Burden and Notifications in Low- and Middle-Income Countries: A Systematic Review and Meta-Analysis. PLoS Med. 2016, 13, e1002119. [Google Scholar] [CrossRef]
- de Sousa Viana, P.V.; Paiva, N.S.; Villela, D.A.M.; Bastos, L.S.; de Souza Bierrenbach, A.L. Paulo Cesar Basta Factors associated with death in patients with tuberculosis in Brazil: Competing risks analysis. PLoS ONE 2020, 15, e0240090. [Google Scholar]
- Brazil Brazilian Institute of Geography Statistics (I.B.G.E.). Pessoas Pretas e Pardas Continuam Com Menor Acesso a Emprego Educação Segurança e Saneamento; Brazil Brazilian Institute of Geography Statistics (I.B.G.E.): Brasília, Brazil, 2023. Available online: https://agenciadenoticias.ibge.gov.br/agencia-noticias/2012-agencia-de-noticias/noticias/35467-pessoas-pretas-e-pardas-continuam-com-menor-acesso-a-emprego-educacao-seguranca-e-saneamentO (accessed on 26 August 2024).
- Basta, P.C.; Marques, M.; de Oliveira, R.L.; Cunha, E.A.T.; da Costa Resendes, A.P.; Souza-Santos, R. Social inequalities and tuberculosis: An analysis by race/color in Mato Grosso do Sul, Brazil. Rev. Saúde Pública 2013, 47, 854–864. [Google Scholar] [CrossRef]
- Vaz, I.; Paiva, N.S.; Sousa, P.V. Spatial-temporal evolution of tuberculosis incidence rates in indigenous and non-indigenous people of Brazil, from 2011 to 2022. Rev. Bras. Epidemiol. 2023, 1, 26. [Google Scholar] [CrossRef]
- Satyanarayana, S.; Thekkur, P.; Kumar, A.M.V.; Lin, Y.; Dlodlo, R.A.; Khogali, M.; Zachariah, R.; Harries, A.D. An Opportunity to END TB: Using the Sustainable Development Goals for Action on Socio-Economic Determinants of TB in High Burden Countries in WHO South-East Asia and the Western Pacific Regions. Trop. Med. Infect. Dis. 2020, 5, 101. [Google Scholar] [CrossRef] [PubMed]
- Caraux-Paz, P.; Diamantis, S.; de Wazières, B.; Gallien, S. Tuberculosis in the Elderly. J. Clin. Med. 2021, 10, 5888. [Google Scholar] [CrossRef] [PubMed]
- Di Bari, V.; Cerva, C.; Libertone, R.; Carli, S.M.; Musso, M.; Goletti, D.; Aiello, A.; Mazzarelli, A.; Cannas, A.; Matusali, G.; et al. Impact of Severity of COVID-19 in TB Disease Patients: Experience from an Italian Infectious Disease Referral Hospital. Infect. Dis. Rep. 2025, 17, 11. [Google Scholar] [CrossRef] [PubMed]
- Casco, N.; Jorge, A.L.; Palmero, D.J.; Alffenaar, J.W.; Fox, G.J.; Ezz, W.; Cho, J.G.; Denholm, J.; Skrahina, A.; Solodovnikova, V.; et al. Long-term outcomes of the global tuberculosis and COVID-19 co-infection cohort. Eur. Respir. J. 2023, 62, 2300925. [Google Scholar]
Variable | Annual Mortality Rate (Deaths/100,000 Inhabitants) |
---|---|
Sex | |
Male | 3.50 |
Female | 1.11 |
Age group (Years) | |
0–14 | 0.09 |
15–59 | 2.05 |
>59 | 6.86 |
Race/skin color | |
White | 1.49 |
Black | 4.21 |
Mixed | 2.61 |
Indigenous | 5.58 |
Asian | 0.73 |
Region | |
North | 2.65 |
South | 1.66 |
Northeast | 2.53 |
Southeast | 2.36 |
Midwest | 1.50 |
Variable | Period (Month, Year) | AMPC (%) * | Mean |
---|---|---|---|
Sex | |||
Male | January 2012–April 2021 | 0.41 | 0.2829 |
May 2021–December 2022 | 0.72 | 0.3383 | |
Female | January 2012–April 2020 | 1.31 | 0.0907 |
May 2020–December 2022 | 2.80 | 0.0941 | |
Age group (Years) | |||
0–14 | January 2012–December 2022 | - | 0.0072 |
- | - | - | |
15–59 | January 2012–April 2020 | 0.65 | 0.1676 |
May 2020–December 2022 | 2.14 | 0.1833 | |
>59 | January 2012–April 2020 | 0.69 | 0.5800 |
May 2020–December 2022 | 1.58 | 0.5267 | |
Race/skin color | |||
White | January 2012–April 2020 | 0.90 | 0.1225 |
May 2020–December 2022 | 2.55 | 0.1383 | |
Black | January 2012–May 2019 | 1.86 | 0.3333 |
December 2019–December 2022 | 1.38 | 0.3654 | |
Mixed | January 2012–April 2020 | 0.72 | 0.2147 |
May 2020–December 2022 | 2.02 | 0.2312 | |
Indigenous | January 2012–March 2017 | - | 0.3968 |
March 2017–December 2022 | - | 0.4983 | |
Asian | January 2012–November 2020 | - | 0.0585 |
December 2020–December 2022 | - | 0.0892 | |
Region | |||
North | January 2012–April 2020 | 3.00 | 0.2192 |
May 2020–December 2022 | 4.64 | 0.2365 | |
South | January 2012–December 2022 | 2.85 | 0.1382 |
- | - | - | |
Northeast | January 2012–May 2020 | 0.89 | 0.2151 |
June 2020–December 2022 | 2.63 | 0.2011 | |
Southeast | January 2012–October 2018 | 0.53 | 0.1939 |
November 2018–December 2022 | 1.13 | 0.1962 | |
Midwest | January 2012–February 2019 | 6.33 | 0.1106 |
March 2019–December 2022 | 5.39 | 0.1436 |
Variable (p-Value) | Average | Cumulative |
---|---|---|
Brazil (p = 0.001) | ||
Actual | 0.2 | 6.7 |
Prediction (95% CI *) | 0.18 [0.18–0.19] | 6.10 [6.04–6.16] |
Absolute effect (95% CI) | 0.018 [0.016–0.02] | 0.601 [0.541–0.67] |
Relative effect (95% CI) | 9.9% [8.8–11%] | 9.9% [8.8–11%] |
Midwest (p = 0.001) | ||
Actual | 0.15 | 5.04 |
Prediction (95% CI) | 0.12 [0.11–0.12] | 3.88 [3.73–4.02] |
Absolute effect (95% CI) | 0.035 [0.031–0.04] | 1.169 [1.021–1.31] |
Relative effect (95% CI) | 30% [25–35%] | 30% [25–35%] |
Northeast (p = 0.045) | ||
Actual | 0.21 | 6.82 |
Prediction (95% CI) | 0.21 [0.21–0.21] | 6.92 [6.82–7.05] |
Absolute effect (95% CI) | −0.0031 [−0.0069–−0.00012] | −0.1021 [−0.2271–0.00387] |
Relative effect (95% CI) | −1.5% [−3.2–0.057%] | −1.5% [−3.2–0.057%] |
North (p = 0.004) | ||
Actual | 0.24 | 8.06 |
Prediction (95% CI) | 0.23 [0.23–0.24] | 7.74 [7.54–7.96] |
Absolute effect (95% CI) | 0.0095 [0.003–0.016] | 0.3136 [0.098–0.512] |
Relative effect (95% CI) | 4.1% [1.2–6.8%] | 4.1% [1.2–6.8%] |
Southeast (p = 0.001) | ||
Actual | 0.21 | 7.07 |
Prediction (95% CI) | 0.18 [0.18–0.19] | 6.10 [6.01–6.20] |
Absolute effect (95% CI) | 0.03 [0.026–0.032] | 0.97 [0.874–1.066] |
Relative effect (95% CI) | 16% [14–18%] | 16% [14–18%] |
South (p = 0.001) | ||
Actual | 0.17 | 5.47 |
Prediction (95% CI) | 0.15 [0.14–0.15] | 4.84 [4.71–4.96] |
Absolute effect (95% CI) | 0.019 [0.015–0.023] | 0.629 [0.506–0.756] |
Relative effect (95% CI) | 13% [10–16%] | 13% [10–16%] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tavares, R.B.V.; Gomes, D.; Berra, T.Z.; Alves, Y.M.; Ramos, A.C.V.; Popolin, M.A.P.; Abade, A.d.S.; Zini, N.; Tártaro, A.F.; Alves, J.D.; et al. The Temporal Trends of Mortality Due to Tuberculosis in Brazil: Tracing the Coronavirus Disease 2019 (COVID-19) Pandemic’s Effect Through a Bayesian Approach and Unmasking Disparities. Microorganisms 2025, 13, 1145. https://doi.org/10.3390/microorganisms13051145
Tavares RBV, Gomes D, Berra TZ, Alves YM, Ramos ACV, Popolin MAP, Abade AdS, Zini N, Tártaro AF, Alves JD, et al. The Temporal Trends of Mortality Due to Tuberculosis in Brazil: Tracing the Coronavirus Disease 2019 (COVID-19) Pandemic’s Effect Through a Bayesian Approach and Unmasking Disparities. Microorganisms. 2025; 13(5):1145. https://doi.org/10.3390/microorganisms13051145
Chicago/Turabian StyleTavares, Reginaldo Bazon Vaz, Dulce Gomes, Thaís Zamboni Berra, Yan Mathias Alves, Antônio Carlos Vieira Ramos, Marcela Antunes Paschoal Popolin, André da Silva Abade, Nathalia Zini, Ariela Fehr Tártaro, Josilene Dália Alves, and et al. 2025. "The Temporal Trends of Mortality Due to Tuberculosis in Brazil: Tracing the Coronavirus Disease 2019 (COVID-19) Pandemic’s Effect Through a Bayesian Approach and Unmasking Disparities" Microorganisms 13, no. 5: 1145. https://doi.org/10.3390/microorganisms13051145
APA StyleTavares, R. B. V., Gomes, D., Berra, T. Z., Alves, Y. M., Ramos, A. C. V., Popolin, M. A. P., Abade, A. d. S., Zini, N., Tártaro, A. F., Alves, J. D., Costa, F. B. P. d., Pelodan, M. E. P., Vigato, B. F., Pinheiro, D. d. M., Paiva, J. Q. R. d., Souza, C. F. d., & Arcêncio, R. A. (2025). The Temporal Trends of Mortality Due to Tuberculosis in Brazil: Tracing the Coronavirus Disease 2019 (COVID-19) Pandemic’s Effect Through a Bayesian Approach and Unmasking Disparities. Microorganisms, 13(5), 1145. https://doi.org/10.3390/microorganisms13051145