Recrudescence of tuberculosis in the state of São Paulo post-COVID-19: trends and clusters

Authors

DOI:

https://doi.org/10.11606/s15188787.2025059006987

Keywords:

Tuberculosis, COVID-19, Recrudescence, Trends, Public Health

Abstract

OBJECTIVE: To analyze the recrudescence of tuberculosis in the state of São Paulo after the COVID-19 pandemic, identifying temporal trends and spatial clusters of the disease. METHODS: An ecological study of tuberculosis cases reported on TBWeb in all São Paulo municipalities between January 2015 and December 2023. Time decomposition techniques, interrupted time series analysis by month and spatial analysis by municipality (global Moran index and Getis-Ord Gi*) were applied to identify trends, abrupt changes associated with the pandemic and clusters of high incidence, mortality, and treatment outcomes. The pre-pandemic (01/2015 to 01/2020), pandemic (02/2020 to 04/2022), and post-pandemic (05/2022 to 12/2023) periods were analyzed separately. RESULTS: There was an upsurge in tuberculosis in the post-pandemic period, with a 21.2% increase in the number of municipalities with an incidence > 110 cases per 100,000 inhabitants. T here was a progressive increase in the mortality trend of 0.0026 (95%CI: 0.0016 to 0.0035) deaths per 100,000 inhabitants per month after the pandemic. There was a gradual drop of 0.67% (95%CI: -1.099 to -0.246) per month in the proportion of people cured after the pandemic. High incidence clusters persisted in the Presidente Prudente region in all periods, and new clusters in Marília and Registro after the pandemic. Areas with high mortality rates persisted in the regions of Taubaté, Baixada Santista, Grande São Paulo, Registro, Sorocaba and Campinas in all periods. CONCLUSION: The recrudescence of tuberculosis in São Paulo in the post-pandemic context highlights the need for targeted strategies for early diagnosis, strengthening treatment and intensive monitoring in regions identified as clusters, especially those with vulnerable populations and structural challenges in health services.

References

1. Ministério da Saúde (BR). Brasil livre da tuberculose: plano nacional pelo fim da tuberculose como problema de saúde pública [Internet]. Brasília: Ministério da Saúde; 2017 [citado 2025 jun 26]. Disponível em: https://www.cosemssc.org.br/wp-content/ uploads/2022/03/brasil_livre_tuberculose_plano_nacional.pdf

2. World Health Organization. Global tuberculosis report 2024 [Internet]. Genebra: WHO; 2024 [citado 2025 jun 26]. Disponível em: https://www.who.int/publications/i/item/9789240077669

3. Ministério da Saúde (BR). Boletim Epidemiológico – Tuberculose 2025 [Internet]. Brasília: Ministério da Saúde; 2025 [citado 2025 jun 26]. Disponível em: https://www.gov.br/aids/pt-br/central-deconteudo/boletins-epidemiologicos/2025/boletim-epidemiologico-tuberculose-2025/view

4. Maciel EL, Golub JE, Silva JRL, Chaisson RE. Tuberculosis: a deadly and neglected disease in the COVID-19 era. J Bras Pneumol. 2022;48(3):e20220056. https://doi.org/10.36416/1806-3756/e20220056

5. Hino P, Yamamoto TT, Magnabosco GT, Bertolozzi MR, Taminato M, Fornari LF. Impact of COVID-19 on the control and reorganization of tuberculosis care. Acta Paul Enferm. 2021;34:eAPE002115. https://doi.org/10.37689/acta-ape/2021AR02115

6. Ministério da Saúde (BR). 2ª Reunião de Alto Nível pelo Fim da Tuberculose [Internet]. Brasília: Ministério da Saúde; 2023 [citado 2025 jun 26]. Disponível em: https://www.gov.br/aids/pt-br/ assuntos/tuberculose/Informativo2ReuniodeAltoNvelTB.pdf

7. Blume MC, Santoro I, Yamamura M, Croda J, Arakaki-Sanchez D, Oliveira GP, et al. 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 May;34:100765. https://doi.org/10.1016/j.lana.2024.100765

8. Pontes TAA, Fernandez-Llimos F, Wiens A. Impact of COVID-19 on tuberculosis notifications. Rev Inst Med Trop São Paulo. 2024 Jun;66:e37. https://doi.org/10.1590/S1678-9946202466037

9. Morgenstern H. Ecologic studies in epidemiology: concepts, principles, and methods. Annu Rev Public Health. 1995 May;16:61-81. https://doi.org/10.1146/annurev.pu.16.050195.000425

10. Villela EF de M, López RVM, Sato APS, Leite L, Oliveira FM, Waldman EA, et al. COVID-19 outbreak in Brazil: adherence to national preventive measures and impact on people’s lives, an online survey. BMC Public Health. 2021 Jan;21:152. https://doi.org/10.1186/s12889-021-10222-z

11. Ministério da Saúde (BR). Portaria GM/MS nº 913, de 22 de abril de 2022. Declara o encerramento da Emergência em Saúde Pública de Importância Nacional (ESPIN) em decorrência da Infecção Humana pelo novo coronavírus (SARS-CoV-2) [Internet]. Brasília: Ministério da Saúde; 2022 [citado 2025 jun 26]. Disponível em: https://bvsms.saude.gov.br/bvs/ saudelegis/gm/2022/prt0913_22_04_2022.html

12. Instituto Brasileiro de Geografia e Estatística. Cidades e estados: Brasil [Internet]. Brasília: IBGE; 2023 [citado 2025 jun 26]. Disponível em: https://www.ibge.gov.br/cidades-e-estados

13. Secretaria de Desenvolvimento Social do Governo do Estado de São Paulo. Informações Socioterritoriais [Internet]. São Paulo: SEDS-SP; 2010 [citado 2025 jun 26]. Disponível em: https:// www.desenvolvimentosocial.sp.gov.br/vigilancia-socioassistencial/informacoes-socioterritoriais/

14. Cleveland RB, Cleveland WS, McRee JE. Seasonal-trend decomposition procedure based on LOESS. J Official Stat [Internet]. 1990 [citado 2025 jun 26];6(1):3-73. Disponível em: https://www.math.unm.edu/~lil/Stat581/STL.pdf

15. Instituto Butantan. Retrospectiva 2021: segundo ano da pandemia é marcado pelo avanço da vacinação contra Covid-19 no Brasil [Internet]. São Paulo: Instituto Butantan; 2021 [citado 2025 jun 26]. Disponível em: https://butantan.gov.br/noticias/retrospectiva-2021segundo-ano-da-pandemia-e-marcado-pelo-avanco-da-vacinacao-contra-covid-19-no-brasil

16. Box GEP, Jenkins GM. Time Series Analysis: Forecasting and Control. 5th ed. Hoboken: Wiley; 1976.

17. Schaffer AL, Dobbins TA, Pearson SA. Interrupted time series analysis using autoregressive integrated moving average (ARIMA) models: a guide for evaluating large-scale health interventions. BMC Med Res Methodol. 2021 Mar;21(1):58. https://doi.org/10.1186/s12874-021-01235-8

18. Anselin L. Local Spatial Autocorrelation (3) [Internet]. GeoDa Center; 2020 [citado 2025 jun 26]. Disponível em: https://geodacenter.github.io/workbook/6c_local_multi/lab6c.html

19. Anselin L, Syabri I, Kho Y. GeoDa: an introduction to spatial data analysis. Geogr Anal. 2006 Jan;38(1):5-22. https://doi.org/10.1111/j.0016-7363.2005.00671.x

20. Getis A, Ord JK. The Analysis of Spatial Association by Use of Distance Statistics. In: Anselin L, Rey SJ, editors. Perspectives on Spatial Data Analysis. Berlin: Springer; 2010. p. 127-145. https://doi.org/10.1007/978-3-642-01976-0_10

21. Ribeiro ALP, Oliveira GP, Silva TF, Moreira CMM, Pescarini JM, Croda J, et al. Interrupção do diagnóstico de tuberculose durante a pandemia de COVID-19 no município do Rio de Janeiro: análise de séries temporais. Cad Saúde Pública. 2023;39(5):e00215622. https://doi.org/10.1590/0102-311x00215622

22. Gunsaru V, Henrion MYR, McQuaid CF. The impact of the COVID-19 pandemic on tuberculosis treatment outcomes in 49 high burden countries. BMC Med. 2024 Jul;22(1):312. https://doi.org/10.1186/s12916-024-03532-7

23. Migliori GB, Thong PM, Alffenaar JW, Denholm J, Tadolini M, Alyaquobi F, et al. Country-specific lockdown measures in response to the COVID-19 pandemic and its impact on tuberculosis control: a global study. J Bras Pneumol. 2022 Feb;48(2):e20220087. https://doi.org/10.36416/1806-3756/e20220087

24. Nalunjogi J, Mucching-Toscano S, Sibomana JP, Centis R, D’Ambrosio L, Alffenaar JW, 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 May;130 Suppl 1:S25-9. https://doi.org/10.1016/j.ijid.2023.02.025

25. Ding W, Li Y, Bai Y, Li Y, Wang L, Wang Y. Estimating the effects of the COVID-19 outbreak on the reductions in tuberculosis cases and the epidemiological trends in China: a causal impact analysis. Infect Drug Resist. 2021 Nov;14:4641-55. https://doi.org/10.2147/IDR.S337473

26. Silva DR, Mello FCQ, Migliori GB. Effects of COVID-19 on tuberculosis control: past, present, and future. J Bras Pneumol. 2022;48(3):e20220102. https://doi.org/10.36416/1806-3756/e20220102

27. Revita NCT, Sukartini T, Makhfudli M, Acob JRU, Hasanudin H, Aini HN. The impact of COVID-19 pandemic on tuberculosis patient treatment adherence. J Respirasi. 2022 May;8(2):113-8. https://doi.org/10.20473/jr.v8-I.2.2022.113-118

28. Hamada Y, Quartagno M, Law I, Malik F, Bonsu FA, Adetifa IMO, et al. Association of diabetes, smoking, and alcohol use with subclinical-to-symptomatic spectrum of tuberculosis in 16 countries: an individual participant data meta-analysis of national tuberculosis prevalence surveys. eClinicalMedicine. 2023 Sep;63:102191. https://doi.org/10.1016/j.eclinm.2023.102191

29. Nascimento DR, Serpa SF, Bezerra-Santos M, do Carmo RF, Brito RJVC, Gomes OV. The impact of the COVID-19 pandemic on TB diagnosis in the Brazilian prison population, 2020-2021. Int J Tuberc Lung Dis. 2023 Sep;27(9):688-93. https://doi.org/10.5588/ijtld.22.0666

30. Pereira TV, Nogueira MC, Campos EMS. Spatial analysis of tuberculosis and its relationship with socioeconomic indicators in a medium-sized city in Minas Gerais. Rev Bras Epidemiol. 2021;24:e210021. https://doi.org/10.1590/1980-549720210021

31. Andrade HLP, Ramos ACV, Crispim JA, Neto MS, Arroyo LH, Arcêncio RA. Spatial analysis of risk areas for the development of tuberculosis and treatment outcomes. Rev Bras Enferm. 2021;74(2):e20200564. https://doi.org/10.1590/0034-7167-2020-0564

32. Secretaria da Administração Penitenciária do Estado de São Paulo. Complexos Penais [Internet]. São Paulo: Secretaria da Administração Penitenciária; [citado 2025 jun 26]. Disponível em: https://www1.sap.sp.gov.br/sp/unidades-prisionais/complexos-penais.html

33. Pinheiro Junior RVB, Carneiro Junior N, Sala A, Luppi CG, Schveitzer MC, Andrade MC, et al. Primary health care performance according to clusters of convergent municipalities in the state of São Paulo. Rev Bras Epidemiol. 2022 Jul;25:e220017. https://doi.org/10.1590/1980-549720220017.2

34. Secretaria de Desenvolvimento Social do Estado de São Paulo (BR). Atlas Digital da Situação da Pobreza e Extrema Pobreza no Estado de São Paulo, 2021 [Internet]. São Paulo: SEDS-SP; 2023 [citado 2025 jun 26]. Disponível em: https://www.desenvolvimentosocial.sp.gov.br/wpcontent/uploads/2023/06/atlas-digital-pobreza-e-extrema-pobreza-2021.pdf

Published

2025-12-04

Issue

Section

Original Articles

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How to Cite

Tavares, R. B. V., Zini, N., Alves, Y. M., Vinci, A. L. T., Ribeiro, N. M., Tártaro, A. F., Caripa, V. C. A., Pelodan, M. E. P., Souza, C. F. de, Monroe, A. A., Ballestero, J. G. de A., Pinto, I. C., Palha, P. F., & Arcêncio, R. A. (2025). Recrudescence of tuberculosis in the state of São Paulo post-COVID-19: trends and clusters. Revista De Saúde Pública, 59, 50. https://doi.org/10.11606/s15188787.2025059006987