Skip to main content
Top
Published in: BMC Infectious Diseases 1/2022

Open Access 01-12-2022 | Tuberculosis | Research

Risk-prone territories for spreading tuberculosis, temporal trends and their determinants in a high burden city from São Paulo State, Brazil

Authors: Thaís Zamboni Berra, Antônio Carlos Vieira Ramos, Luiz Henrique Arroyo, Felipe Mendes Delpino, Juliane de Almeida Crispim, Yan Mathias Alves, Felipe Lima dos Santos, Fernanda Bruzadelli Paulino da Costa, Márcio Souza dos Santos, Luana Seles Alves, Regina Célia Fiorati, Aline Aparecida Monroe, Dulce Gomes, Ricardo Alexandre Arcêncio

Published in: BMC Infectious Diseases | Issue 1/2022

Login to get access

Abstract

Objectives

To identify risk-prone areas for the spread of tuberculosis, analyze spatial variation and temporal trends of the disease in these areas and identify their determinants in a high burden city.

Methods

An ecological study was carried out in Ribeirão Preto, São Paulo, Brazil. The population was composed of pulmonary tuberculosis cases reported in the Tuberculosis Patient Control System between 2006 and 2017. Seasonal Trend Decomposition using the Loess decomposition method was used. Spatial and spatiotemporal scanning statistics were applied to identify risk areas. Spatial Variation in Temporal Trends (SVTT) was used to detect risk-prone territories with changes in the temporal trend. Finally, Pearson's Chi-square test was performed to identify factors associated with the epidemiological situation in the municipality.

Results

Between 2006 and 2017, 1760 cases of pulmonary tuberculosis were reported in the municipality. With spatial scanning, four groups of clusters were identified with relative risks (RR) from 0.19 to 0.52, 1.73, 2.07, and 2.68 to 2.72. With the space–time scan, four clusters were also identified with RR of 0.13 (2008–2013), 1.94 (2010–2015), 2.34 (2006 to 2011), and 2.84 (2014–2017). With the SVTT, a cluster was identified with RR 0.11, an internal time trend of growth (+ 0.09%/year), and an external time trend of decrease (− 0.06%/year). Finally, three risk factors and three protective factors that are associated with the epidemiological situation in the municipality were identified, being: race/brown color (OR: 1.26), without education (OR: 1.71), retired (OR: 1.35), 15 years or more of study (OR: 0.73), not having HIV (OR: 0.55) and not having diabetes (OR: 0.35).

Conclusion

The importance of using spatial analysis tools in identifying areas that should be prioritized for TB control is highlighted, and greater attention is necessary for individuals who fit the profile indicated as “at risk” for the disease.
Appendix
Available only for authorised users
Literature
3.
go back to reference Moraga P, Kulldorff M. Detection of spatial variations in temporal trends with a quadratic function. Stat Methods Med Res. 2016;25(4):1422–37.CrossRef Moraga P, Kulldorff M. Detection of spatial variations in temporal trends with a quadratic function. Stat Methods Med Res. 2016;25(4):1422–37.CrossRef
4.
go back to reference Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic research: principles and quantitative Methods. 1st ed. USA: Wiley; 1982. Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic research: principles and quantitative Methods. 1st ed. USA: Wiley; 1982.
6.
go back to reference Galesi VMN. Data on tuberculosis in the state of São Paulo, Brazil. Rev Saúde Pública. 2007;41(1):121.CrossRef Galesi VMN. Data on tuberculosis in the state of São Paulo, Brazil. Rev Saúde Pública. 2007;41(1):121.CrossRef
7.
go back to reference Cleveland R, Cleveland W, McRee JE. Seasonal-trend decomposition procedure based on LOESS. J Offic Stat. 1990;6:3–73. Cleveland R, Cleveland W, McRee JE. Seasonal-trend decomposition procedure based on LOESS. J Offic Stat. 1990;6:3–73.
9.
go back to reference Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med. 1995;14(8):799–810.CrossRef Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med. 1995;14(8):799–810.CrossRef
11.
go back to reference Jaisankar R, Kesavan J. A study on spatial variations in temporal trends of dengue incidences In Tamil Nadu, India. Int J Sci Technol Res. 2019;8(09). Jaisankar R, Kesavan J. A study on spatial variations in temporal trends of dengue incidences In Tamil Nadu, India. Int J Sci Technol Res. 2019;8(09).
12.
go back to reference Zuur AF, Ieno EM, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol. 2010;1(1):3–14.CrossRef Zuur AF, Ieno EM, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol. 2010;1(1):3–14.CrossRef
13.
go back to reference Wagh YS, Kamalja KK. Zero-inflated models and estimation in zero-inflated Poisson distribution. Commun Stat Simul Comput. 2018;47(8):2248–65.CrossRef Wagh YS, Kamalja KK. Zero-inflated models and estimation in zero-inflated Poisson distribution. Commun Stat Simul Comput. 2018;47(8):2248–65.CrossRef
14.
go back to reference Berra TZ, Bruce ATI, Alves YM, Campoy LT, Arroyo LH, Crispim JA, et al. Related factors, time trend and spatial association of abandonment of treatment for tuberculosis in Ribeirão Preto-SP. Rev Eletr Enferm. 2020;22:1–10.CrossRef Berra TZ, Bruce ATI, Alves YM, Campoy LT, Arroyo LH, Crispim JA, et al. Related factors, time trend and spatial association of abandonment of treatment for tuberculosis in Ribeirão Preto-SP. Rev Eletr Enferm. 2020;22:1–10.CrossRef
17.
go back to reference Lima TM, Belotti NCU, Nardi SMT, Pedro HSP. GeneXpert MTB/RIF assay for diagnosis of tuberculosis. Rev Pan-Amaz Saude. 2017;8(2):67–78. Lima TM, Belotti NCU, Nardi SMT, Pedro HSP. GeneXpert MTB/RIF assay for diagnosis of tuberculosis. Rev Pan-Amaz Saude. 2017;8(2):67–78.
18.
go back to reference Shah W. To determine diagnostic accuracy of gene xpert and sputum Ziehl-Neelsen staining taking sputum culture as gold standard. Eur Respir J. 2016;48:PA2779.CrossRef Shah W. To determine diagnostic accuracy of gene xpert and sputum Ziehl-Neelsen staining taking sputum culture as gold standard. Eur Respir J. 2016;48:PA2779.CrossRef
19.
go back to reference Pandey P, Pant ND, Rijal KR, Shrestha B, Kattel S, Banjara MR, et al. Diagnostic accuracy of GeneXpert MTB/RIF assay in comparison to conventional drug susceptibility testing method for the diagnosis of multidrug-resistant tuberculosis. PLoS ONE. 2017;12(1): e0169798.CrossRef Pandey P, Pant ND, Rijal KR, Shrestha B, Kattel S, Banjara MR, et al. Diagnostic accuracy of GeneXpert MTB/RIF assay in comparison to conventional drug susceptibility testing method for the diagnosis of multidrug-resistant tuberculosis. PLoS ONE. 2017;12(1): e0169798.CrossRef
20.
go back to reference Macedo SM, Andrade RPS, Souza CRBA, Andrade ASS, Villa TCS, Pinto ESG. Estratégias para capacitação ao cuidado em tuberculose. Cogitare Enferm. 2016;21(3):01–8.CrossRef Macedo SM, Andrade RPS, Souza CRBA, Andrade ASS, Villa TCS, Pinto ESG. Estratégias para capacitação ao cuidado em tuberculose. Cogitare Enferm. 2016;21(3):01–8.CrossRef
21.
go back to reference Prado-Junior J, Medronho RA. Spatial analysis of tuberculosis cure in primary care in Rio de Janeiro, Brazil. BMC Public Health. 2021;21(1):1841.CrossRef Prado-Junior J, Medronho RA. Spatial analysis of tuberculosis cure in primary care in Rio de Janeiro, Brazil. BMC Public Health. 2021;21(1):1841.CrossRef
22.
go back to reference Santos BA, Cruz RPS, Lima SVMA, Santos AD, Duque AM, Araújo KCGM, et al. Tuberculosis among children and adolescents: an epidemiological and spatial analysis in the state of Sergipe, Brazil, 2001–2017. Cien Saude Colet. 2020;25(8):2939–48.CrossRef Santos BA, Cruz RPS, Lima SVMA, Santos AD, Duque AM, Araújo KCGM, et al. Tuberculosis among children and adolescents: an epidemiological and spatial analysis in the state of Sergipe, Brazil, 2001–2017. Cien Saude Colet. 2020;25(8):2939–48.CrossRef
23.
go back to reference Mendes MS, Oliveira ALS, Pimentel LMLM, Fiqueiredo TMRM, Schindler HC. Spatial analysis of tuberculosis in children under 15 years of age and socioeconomic risk: an ecological study in Paraíba, Brazil, 2007–2016. Epidemiol Serv Saude. 2021;30(3): e20201038.CrossRef Mendes MS, Oliveira ALS, Pimentel LMLM, Fiqueiredo TMRM, Schindler HC. Spatial analysis of tuberculosis in children under 15 years of age and socioeconomic risk: an ecological study in Paraíba, Brazil, 2007–2016. Epidemiol Serv Saude. 2021;30(3): e20201038.CrossRef
24.
go back to reference Andrade HLP, Ramos ACV, Crispim JA, Santos Neto M, Arroyo LH, Arcêncio RA. Spatial analysis of risk areas for the development of tuberculosis and treatment outcomes. Rev Bras Enferm. 2021;74(2): e20200564.CrossRef Andrade HLP, Ramos ACV, Crispim JA, Santos Neto M, Arroyo LH, Arcêncio RA. Spatial analysis of risk areas for the development of tuberculosis and treatment outcomes. Rev Bras Enferm. 2021;74(2): e20200564.CrossRef
25.
go back to reference Souza CDF, Paiva JPS, Silva LF, Leal TC, Magalhães MAFM. Trends in tuberculosis mortality in Brazil (1990–2015): joinpoint analysis. J Bras Pneumol. 2019;45(2): e20180393.CrossRef Souza CDF, Paiva JPS, Silva LF, Leal TC, Magalhães MAFM. Trends in tuberculosis mortality in Brazil (1990–2015): joinpoint analysis. J Bras Pneumol. 2019;45(2): e20180393.CrossRef
26.
go back to reference Berra TZ, Gomes D, Ramos ACV, Alves YM, Bruce ATI, Arroyo LH, et al. Effectiveness and trend forecasting of tuberculosis diagnosis after the introduction of GeneXpert in a city in south-eastern Brazil. PLoS ONE. 2021;16(5): e0252375.CrossRef Berra TZ, Gomes D, Ramos ACV, Alves YM, Bruce ATI, Arroyo LH, et al. Effectiveness and trend forecasting of tuberculosis diagnosis after the introduction of GeneXpert in a city in south-eastern Brazil. PLoS ONE. 2021;16(5): e0252375.CrossRef
27.
go back to reference Roza DL, Caccia-Bava MCGG, Martinez EZ. Spatio-temporal patterns of tuberculosis incidence in Ribeirão Preto, State of São Paulo, southeast Brazil, and their relationship with social vulnerability: a Bayesian analysis. Rev Soc Bras Med Trop. 2012;45(5):607–15.CrossRef Roza DL, Caccia-Bava MCGG, Martinez EZ. Spatio-temporal patterns of tuberculosis incidence in Ribeirão Preto, State of São Paulo, southeast Brazil, and their relationship with social vulnerability: a Bayesian analysis. Rev Soc Bras Med Trop. 2012;45(5):607–15.CrossRef
28.
go back to reference Santos JA, Santos DT, Arcêncio RA, Nunes C. Space–time clustering and temporal trends of hospitalizations due to pulmonary tuberculosis: potential strategy for assessing health care policies. Eur J Public Health. 2021;31(1):57–62.CrossRef Santos JA, Santos DT, Arcêncio RA, Nunes C. Space–time clustering and temporal trends of hospitalizations due to pulmonary tuberculosis: potential strategy for assessing health care policies. Eur J Public Health. 2021;31(1):57–62.CrossRef
29.
go back to reference Giacomet CL, Santos MS, Berra TZ, Alves YM, Alves LS, Costa FBP, et al. Temporal trend of tuberculosis incidence and its spatial distribution in Macapá-Amapá. Rev Saude Publica. 2021;55:96.CrossRef Giacomet CL, Santos MS, Berra TZ, Alves YM, Alves LS, Costa FBP, et al. Temporal trend of tuberculosis incidence and its spatial distribution in Macapá-Amapá. Rev Saude Publica. 2021;55:96.CrossRef
30.
go back to reference Arcêncio RA, Berra TZ, Terena NFM, Rocha MP, Alecrim TFA, Kihara FMS, et al. Spatial clustering and temporal trend analysis of international migrants diagnosed with tuberculosis in Brazil. PLoS ONE. 2021;16(6): e0252712.CrossRef Arcêncio RA, Berra TZ, Terena NFM, Rocha MP, Alecrim TFA, Kihara FMS, et al. Spatial clustering and temporal trend analysis of international migrants diagnosed with tuberculosis in Brazil. PLoS ONE. 2021;16(6): e0252712.CrossRef
31.
go back to reference Santos JN, Sales CMM, Maciel EL. Factors associated with cure when treating tuberculosis in the state of Rio de Janeiro, Brazil, 2011–2014. Epidemiol Serv Saude. 2018;27(3): e2017464.PubMed Santos JN, Sales CMM, Maciel EL. Factors associated with cure when treating tuberculosis in the state of Rio de Janeiro, Brazil, 2011–2014. Epidemiol Serv Saude. 2018;27(3): e2017464.PubMed
32.
go back to reference Arcoverde MAM, Berra TZ, Alves LS, Santos DT, Belchior AS, Ramos ACV, et al. How do social-economic differences in urban areas affect tuberculosis mortality in a city in the tri-border region of Brazil, Paraguay and Argentina. BMC Public Health. 2018;18:795.CrossRef Arcoverde MAM, Berra TZ, Alves LS, Santos DT, Belchior AS, Ramos ACV, et al. How do social-economic differences in urban areas affect tuberculosis mortality in a city in the tri-border region of Brazil, Paraguay and Argentina. BMC Public Health. 2018;18:795.CrossRef
33.
go back to reference Maio MC. Raça, doença e saúde pública no Brasil: um debate sobre o pensamento higienista do século XIX. In: Maio MC, Santos RV, editors. Raça como questão: história, ciência e identidades no Brasil. Rio de Janeiro: Fiocruz; 2010. p. 51–82.CrossRef Maio MC. Raça, doença e saúde pública no Brasil: um debate sobre o pensamento higienista do século XIX. In: Maio MC, Santos RV, editors. Raça como questão: história, ciência e identidades no Brasil. Rio de Janeiro: Fiocruz; 2010. p. 51–82.CrossRef
35.
go back to reference Rodrigues MW, Mello AGNC. Tuberculose e escolaridade: Uma revisão da literatura. Rev Int Apoyo Inclusión, Logopedia, Sociedad y Multiculturalidad. 2018;4(2). Rodrigues MW, Mello AGNC. Tuberculose e escolaridade: Uma revisão da literatura. Rev Int Apoyo Inclusión, Logopedia, Sociedad y Multiculturalidad. 2018;4(2).
36.
go back to reference Bell LCK, Noursadeghi M. Pathogenesis of HIV-1 and Mycobacterium tuberculosis co-infection. Nat Rev Microbiol. 2018;16(2):80–90.CrossRef Bell LCK, Noursadeghi M. Pathogenesis of HIV-1 and Mycobacterium tuberculosis co-infection. Nat Rev Microbiol. 2018;16(2):80–90.CrossRef
37.
go back to reference Meintjes G, Brust JCM, Nuttall J, Maartens G. Management of active tuberculosis in adults with HIV. Lancet HIV. 2019;6(7):e463–74.CrossRef Meintjes G, Brust JCM, Nuttall J, Maartens G. Management of active tuberculosis in adults with HIV. Lancet HIV. 2019;6(7):e463–74.CrossRef
38.
go back to reference Tornheim JA, Dooley KE. Tuberculosis associated with HIV infection. Microbiol Spectr. 2017;5(1) Tornheim JA, Dooley KE. Tuberculosis associated with HIV infection. Microbiol Spectr. 2017;5(1)
39.
go back to reference Silva DR, Muñoz-Torrico M, Duarte R, Galvão T, Bonini EH, Arbex FF, et al. Fatores de risco para tuberculose: diabetes, tabagismo, álcool e uso de outras drogas. J Bras Pneumol. 2018;44(2):145–52.CrossRef Silva DR, Muñoz-Torrico M, Duarte R, Galvão T, Bonini EH, Arbex FF, et al. Fatores de risco para tuberculose: diabetes, tabagismo, álcool e uso de outras drogas. J Bras Pneumol. 2018;44(2):145–52.CrossRef
40.
go back to reference Pereira SM, Araújo GS, Santos CAST, Oliveira MG, Barreto ML. Associação entre diabetes e tuberculose: estudo caso controle. Rev Saúde Pública. 2016;50:82.PubMedPubMedCentral Pereira SM, Araújo GS, Santos CAST, Oliveira MG, Barreto ML. Associação entre diabetes e tuberculose: estudo caso controle. Rev Saúde Pública. 2016;50:82.PubMedPubMedCentral
41.
go back to reference Marais BJ, Lönnroth K, Lawn SD, Migliori GB, Mwaba P, Glaziou P, et al. Tuberculosis comorbidity with communicable and non-communicable diseases: integrating health services and control efforts. Lancet Infect Dis. 2013;13(5):436–48.CrossRef Marais BJ, Lönnroth K, Lawn SD, Migliori GB, Mwaba P, Glaziou P, et al. Tuberculosis comorbidity with communicable and non-communicable diseases: integrating health services and control efforts. Lancet Infect Dis. 2013;13(5):436–48.CrossRef
42.
go back to reference Ayelign B, Negash M, Genetu M, Wondmagegn T, Shibabaw T. Immunological impacts of diabetes on the susceptibility of Mycobacterium tuberculosis. J Immunol Res. 2019;2019:6196532.CrossRef Ayelign B, Negash M, Genetu M, Wondmagegn T, Shibabaw T. Immunological impacts of diabetes on the susceptibility of Mycobacterium tuberculosis. J Immunol Res. 2019;2019:6196532.CrossRef
43.
Metadata
Title
Risk-prone territories for spreading tuberculosis, temporal trends and their determinants in a high burden city from São Paulo State, Brazil
Authors
Thaís Zamboni Berra
Antônio Carlos Vieira Ramos
Luiz Henrique Arroyo
Felipe Mendes Delpino
Juliane de Almeida Crispim
Yan Mathias Alves
Felipe Lima dos Santos
Fernanda Bruzadelli Paulino da Costa
Márcio Souza dos Santos
Luana Seles Alves
Regina Célia Fiorati
Aline Aparecida Monroe
Dulce Gomes
Ricardo Alexandre Arcêncio
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2022
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-022-07500-5

Other articles of this Issue 1/2022

BMC Infectious Diseases 1/2022 Go to the issue