Abstract
Objective: Carry out a spatial-temporal characterization of the incidence of tuberculosis (TB) in Maputo, Mozambique. Method: a descriptive ecological study of tuberculosis cases reported in an information system. The annual mean incidence rate and the number of TB notification cases in the municipality of Maputo from 2011 to 2016 were analyzed. Descriptive statistics were used with calculations of measures of central tendency (mean) and an application of the Poisson linear regression model. Trimester notifications were stratified by district, clinical form, and age group. The quarterly average temperature of the evaluated area was added as a covariate in the model seasonal. Results: 34,623 TB cases were notified from 2011 to 2016, with a trimester average of 1,443 cases. The average annual incidence was higher in the Kampfumo district, with 909.8 per 100 thousand inhabitants (95% CI 854.1 - 968.2); almost twice as much as the incidence of the municipality of Maputo, 527.8 (95% CI 514, 3-541.6), and the country of Mozambique, 551 (95% CI 356 - 787). The clinical diagnosis of the tested cases was higher concerning the bacteriological diagnosis; 44%, and 35%, respectively. Conclusion: Maputo had similar incidence rates to the country of Mozambique, however, there was a heterogeneity rate by district and a reduction in the number of TB cases in both the general population (not co-infected with HIV) and those over 15 years old, being higher in the first trimester.
References
Abebe, G., Deribew A., Apers, L., Woldemichael, K., Shiffa, J., Tesfaye, M., Abdissa, A., ... and Colebunders, R. (2010). Knowledge, Health Seeking Behavior and Perceived Stigma towards Tuberculosis among Tuberculosis Suspects in a Rural Community in Southwest Ethiopia. PLoS ONE, 5(10), 1–7. doi: 10.1371/journal.pone.0013339.
Ane-Anyangwe, I. N., Akenji, T. N., Mbacham, W. F., Penlap, V. N., and Titanji, V. P. K. (2006). Seasonal Variation and Prevalence of Tuberculosis among Health Seekers in the South Western Cameroon. East African Medical Journal, 83(11), 588–95. doi: 10.4314/eamj.v83i11.9474.
Avilov, K. K., Romanyukha, A. A., Borisov, S. E., Belilovsky, E. M., Nechaeva O. B., and Karkach, A. S. (2015). An Approach to Estimating Tuberculosis Incidence and Case Detection Rate from Routine Notification Data. International Journal of Tuberculosis and Lung Disease, 19(3), 288–94. doi: 10.5588/ijtld.14.0317.
Berg, S., Schelling, E., Hailu, E., Firdessa, R., Gumi, B., Erenso, G., Gadisa, E., ... and Aseffa, A. (2015). Investigation of the High Rates of Extrapulmonary Tuberculosis in Ethiopia Reveals No Single Driving Factor and Minimal Evidence for Zoonotic Transmission of Mycobacterium Bovis Infection. BMC Infectious Diseases, 15(1), 1–10. doi: 10.1186/s12879-015-0846-7.
Bhaskaran, K., Gasparrini, A., Hajat, S., Smeeth, L., and Armstrong, B. (2013). Time Series Regression Studies in Environmental Epidemiology. International Journal of Epidemiology, 42(4), 1187–95. doi: 10.1093/ije/dyt092.
Borgdorff, M.W., Sebek, M., Geskus, R.B., Kremer, K., Kalisvaart, N., and van Soolingen, N. (2011). The Incubation Period Distribution of Tuberculosis Estimated with a Molecular Epidemiological Approach. International Journal of Epidemiology, 40(4), 964–70. doi: 10.1093/ije/dyr058.
Bos, J. C., Smalbraak, L., Macome, A.C., Gomes, E., van Leth, F., and Prins, J.M. (2013). TB Diagnostic Process Management of Patients in a Referral Hospital in Mozambique in Comparison with the 2007 WHO Recommendations for the Diagnosis of Smear-Negative Pulmonary TB and Extrapulmonary TB. International Health, 5(4), 302–8. doi: 10.1093/inthealth/iht025.
Brouwer, M., Coelho, E., Mosse, C.D., Brondi, L., Winterton, L., and Leth, F.V. (2014). Health Care Workers Challenges in the implementation of prevention and control Measures in Mozambique. Plos One, 9(12), e114364. Retrieved from http://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0114364&type=printable
Dodd, Peter J., Elizabeth Gardiner, Renia Coghlan, and James A. Seddon. (2014). Burden of Childhood Tuberculosis in 22 High-Burden Countries: A Mathematical Modelling Study. The Lancet Global Health, 2(8), e453–59. doi: 10.1016/S2214-109X(14)70245-1.
Fares, A. (2011). Seasonality of tuberculosis. J Glob Infect Dis, 3(1), 46. Retrieved from http://www.jgid.org/text.asp?2011/3/1/46/77296
Fay, M.P., Feuer, E.J. (1997). Confidence intervals for directly standardized rates: a method based on the gamma distribution. Stat Med, 16(7), 791-801.
Freitas, I. M., Paschoal Popolin, M., Mosna Touso, M., Yamamura, M., Barbosa Bandeira Rodrigues, L., Santos Neto, M., ... and Arcêncio, R.A. (2015). Fatores Associados Ao Conhecimento Sobre Tuberculose e Atitudes Das Famílias de Pacientes Com a Doença Em Ribeirão Preto, São Paulo. Revista Brasileira de Epidemiologia, 18(2), 326–40. doi: 10.1590/1980-5497201500020004.
Fox, G. J., Barry, S., Britton W., and Marks, J.B. (2013). Contact Investigation for Tuberculosis: A Systematic Review and Meta-Analysis. European Respiratory Journal, 41(1), 140–56. doi: 10.1183/09031936.00070812.
García-Basteiro, A.L., López-Varela, E., Joaquim Augusto, O., Kizito Gondo, J.M., Jahit S., Marais, B., Alonso, P., and Ribó, J.L. (2015). Radiological Findings in Young Children Investigated for Tuberculosis in Mozambique. PLoS ONE, 10(5), 1–12. doi: 10.1371/journal.pone.0127323.
García-Basteiro, A. L., Miranda Ribeiro, R., Brew, J., Sacoor, C., Valencia, S., Bulo, H., Cobelens, F., and Macete, E. (2017). Tuberculosis on the Rise in Southern Mozambique (1997-2012). The European Respiratory Journal, 49(3). doi: 10.1183/13993003.01683-2016.
Gashu, Z. D., Jerene, D. G., Datiko, N., Hiruy, S., Negash, K., Melkieneh, D., ... and Hadgu, A. (2018). Seasonal Patterns of Tuberculosis Case Notification in the Tropics of Africa: A Six-Year Trend Analysis in Ethiopia. PLoS ONE, 13(11),1–12. doi: 10.1371/journal.pone.0207552.
Gelaw, Y., Yu, W., Magalhães, R.S., Assefa, Y., and Williams, G. (2019). Effect of temperature and altitude difference on tuberculosis notification: A systematic review. Glob. Infect. Dis, 11, 63. DOI: https://doi.org/10.4103/jgid.jgid_95_18
Ginestet, C. (2011). The R Project for Statistical Computing [Software]. Retrieved from http://www.r-project.org
Kumar, V., Abhay S., Mrinmoy, A., Shailaja, D., Khokhar, A., and Singh, S. (2014). Seasonality of Tuberculosis in Delhi, India: A Time Series Analysis. Tuberculosis Research and Treatment, 1–5. doi: 10.1155/2014/514093.
Liao, Ch. M., Nan, H. H., Tang, L. H., Yi, H. Ch., Yi, J. L., Chia, P. Ch., Szu, Ch. Ch., and Min, P. L. (2012). Assessing Trends and Predictors of Tuberculosis in Taiwan. BMC Public Health, 12(1). doi: 10.1186/1471-2458-12-29.
Lisboa, M., Fronteira, I., Colove, E., Nhamonga, M., and Martins, M. R. (2019). Time Delay and Associated Mortality from Negative Smear to Positive Xpert MTB/RIF Test among TB/HIV Patients: A Retrospective Study. BMC Infectious Diseases, 19(1), 1–10. doi: 10.1186/s12879-018-3656-x.
Lundbye-Christensen, S., Dethlefsen, C., Gorst-Rasmussen, A., Fischer, F., Schønheyder, C., Rothman, J.K., and Sørensen, H.T. (2009). Examining Secular Trends and Seasonality in Count Data Using Dynamic Generalized Linear Modelling: A New Methodological Approach Illustrated with Hospital Discharge Data on Myocardial Infarction. European Journal of Epidemiology, 24(5), 225–30. doi: 10.1007/s10654-009-9325-z.
Mathema, B., Lewis, J. J., Connors, J., Chihota, V. N., Shashkina, E., van der Meulen, M., … and Churchyard, G. J. (2015). Molecular Epidemiology ofMycobacterium tuberculosisamong South African Gold Miners. Annals of the American Thoracic Society, 12(1), 12–20. doi:10.1513/annalsats.201404-150oc
Martineau, A. R., Shepherd, N., Tolu, O., Molebogeng, X., Rangaka, S. M, Nonzwakazi, B., Relebohile, T., Lizl, B., De Azevedo, V., Caldwell, J., Venton, T., Timms., P. M,. Wilkinson, K., and Wilkinson, R.J. (2011). Reciprocal Seasonal Variation in Vitamin D Status and Tuberculosis Notifications in Cape Town, South Africa. Proceedings of the National Academy of Sciences of the United States of America, 108(47), 19013–17. doi: 10.1073/pnas.1111825108.
Ministry of Health of Mozambique. (2013). Operational Strategic Plan 2014-2018. National Program for Tuberculosis Control (PNCT). Retrieved from http://gard-cplp.ihmt.unl.pt/Documentos/Paises/Mocambique/Plano_Estrategico_Operacional_Tuberculose_Mocambique_2014-2018.pdf
Ministry of Health of Mozambique. (2018). Survey on Indicators of Immunization, Malaria and HIV AIDS in Mozambique”. IMASIDA - 2015 (1st Ed.). Maputo, Mozambique: Republic of Mozambique.
Ministry of Health of Mozambique. (2014). National Program for Tuberculosis Control. Operational and strategic Plan (1st Ed.). Maputo, Mozambique: Republic of Mozambique.
Moiane, I., Adelina, M., Nuno, S., André, N., Osvaldo, I., Jan, H., Gunilla, K., Jakob, Z., and Correia-Neves, M. (2014). Prevalence of Bovine Tuberculosis and Risk Factor Assessment in Cattle in Rural Livestock Areas of Govuro District in the Southeast of Mozambique. PLoS ONE, 9(3). doi: 10.1371/journal.pone.0091527.
Muleia, Rachid, Makini Boothe, Osvaldo Loquiha, Marc Aerts, and Christel Faes. (2020). Spatial Distribution of HIV Prevalence among Young People in Mozambique. International Journal of Environmental Research and Public Health, 17(3),1–20. doi: 0.3390/ijerph17030885.
Munch, Z. Van Lill, S.W, Booysen, C.N, Zietsman, H.L, Enarson, D.A, Beyers, N. (2003). Tuberculosis transmission patterns in a high-incidence area: a spatial analysis. Int J Tuberc Lung Dis, 7(3), 271-277.
Narula, P., Praveer, S., Sarita, A., and Pietro, L. (2015). Analyzing Seasonality of Tuberculosis across Indian States and Union Territories. Journal of Epidemiology and Global Health, 5(4), 337–46. doi: 10.1016/j.jegh.2015.02.004.
National Institute of Statistic. (2007). Censuses - General of Popul. and Housing. Retrieved from http://www.ine.gov.mz/operacoes-estatisticas/censos/censo-2007/rgph-2007
National Institute of Statistic. (2011). District Statistics - Maputo City. General of Popul. and Housing. Retrieved from http://www.ine.gov.mz/estatisticas/estatisticas-territorias-distritais/maputo-cidade/2011/estatisticas-do-distrito-cidade-de-maputo-2011.pdf/view
National Institute of Statistic. (2017). Statistical Yearbook, Maputo City. Maputo, Mozambique. Retrieved from
http://www.ine.gov.mz/estatisticas/publicacoes/anuario/nacionais/anuario-estatistico-2017.pdf
Nguenha, N., Almiro, T., Mirela, P., Loira, M., Afonso, N., Germano, P., Edirsse, M., ... and Tufária, M. (2018). Clinical and Epidemiological Characterization of Influenza Virus Infections in Children with Severe Acute Respiratory Infection in Maputo, Mozambique: Results from the Implementation of Sentinel Surveillance, 2014 – 2016. PLoS ONE, 13(3), 1–14. doi: 10.1371/journal.pone.0194138.
Nunes, T., Cord, H., Jonathon, M., Sanchez, J., Thorn, R., Reiczigel, J., Robison-cox, J., Sebastiani, P., Solymos, P., Yoshida, K., Pirikahu, S., Firestone, S., Kyle, R., Jay, M., Reynard, C., and Stevenson, M.M. (2020). “Package ‘ EpiR .’”
Orlando, S, Triulzi I., Ciccacci F., Palla I., Palombi L., Marazzi M.C., Giuliano M., Floridia M., Mancinelli S., Mutemba E., and Turchetti G. (2018). Delayed Diagnosis and Treatment of Tuberculosis in HIV+ Patients in Mozambique: A Cost-Effectiveness Analysis of Screening Protocols Based on Four Symptom Screening, Smear Microscopy, Urine LAM Test and Xpert MTB/RIF. PLoS ONE, 13(7), 1–16.
Oliveira, Nathália França, and Maria Jacirema Ferreira Gonçalves. (2013). Social and Environmental Factors Associated with the Hospitalization of Tuberculosis Patients. Revista Latino-Americana de Enfermagem, 21(2), 507–14. doi: 10.1590/S0104-11692013000200006.
Oshi, Daniel C., Joseph N. Chukwu, Charles C. Nwafor, Anthony O. Meka, Nelson O. Madichie, Chidubem L. Ogbudebe, Ugochukwu U. Onyeonoro, Joy N. Ikebudu, Ngozi Ekeke, Moses C. Anyim, Kingsley N. Ukwaja, and Emmanuel N. Aguwa. (2016). Does Intensified Case Finding Increase Tuberculosis Case Notification among Children in Resource-Poor Settings? A Report from Nigeria. International Journal of Mycobacteriology, 5(1), 44–50. doi: 10.1016/j.ijmyco.2015.10.007.
Southern Africa Tuberculosis and Health Systems. (2017). Retrieved from https://www.satbhss.org/
Semá-Baltazar, Cynthia, Yara Voss DeLima, Helena Ricardo, Carlos Botão, Denise Chitsondzo Langa, Paulino Da Costa, Diosdélio Malamule, Angelo Augusto, Sofia Viegas, Nkechi Obisie-Nmehielle, Laura Tomm-Bonde, and Francis Bwambale Mulekya. (2020). HIV Prevalence and TB in Migrant Miners Communities of Origin in Gaza Province, Mozambique: The Need for Increasing Awareness and Knowledge. PLoS ONE, 15(4), 1–14. doi: 10.1371/journal.pone.0231303.
Telisinghe, Lilanganee, Salome Charalambous, Stephanie M. Topp, Michael E. Herce, Christopher J. Hoffmann, Peter Barron, Erik J. Schouten, Andreas Jahn, Rony Zachariah, Anthony D. Harries, Chris Beyrer, and Joseph J. Amon. (2016). HIV and Tuberculosis in Prisons in Sub-Saharan Africa. The Lancet, 388(10050), 1215–27. doi: 10.1016/S0140-6736(16)30578-5.
Tedijanto, C., Hermans, S., Cobelens, F., Wood, R., and Andrews, J.R. (2018). Drivers of Seasonal Variation in Tuberculosis Incidence: Insights from a Systematic Review and Mathematical Model. Epidemiology, 29, 857–866. DOI: https://doi.org/10.1097/EDE.0000000000000877
The World Bank. (2018). Incidence of tuberculosis (per 100,000 people) - South Africa, Mozambique. Incid. Tuberc. (per 100,000 people) Retrieved from https://data.worldbank.org/indicator/SH.TBS.INCD?end=2016&locations=ZA-MZ&start=2000&view=chart
Van’t Hoog, Anna H., Kayla F. Laserson, Willie A. Githui, Helen K. Meme, Janet A. Agaya, Lazarus O. Odeny, Benson G. Muchiri, Barbara J. Marston, Kevin M. DeCock, and Martien W. Borgdorff. (2011). High Prevalence of Pulmonary Tuberculosis and Inadequate Case Finding in Rural Western Kenya. American Journal of Respiratory and Critical Care Medicine, 183(9), 1245–53. doi: 10.1164/rccm.201008-1269OC.
Vynnycky, E., and P. E. M. Fine. 2000. Lifetime Risks, Incubation Period, and Serial Interval of Tuberculosis. American Journal of Epidemiology, 152(3), 247–63. doi: 10.1093/aje/152.3.247.
Wang, Yongbin, Chunjie Xu, Jingchao Ren, Weidong Wu, Xiangmei Zhao, Ling Chao, Wenjuan Liang, and Sanqiao Yao. (2020). Secular Seasonality and Trend Forecasting of Tuberculosis Incidence Rate in China Using the Advanced Error-Trend-Seasonal Framework. Infection and Drug Resistance, 13, 733–47. doi: 10.2147/IDR.S238225.
Wang, Xiaoqing, Zhenhua Yang, Yanyong Fu, Guoqin Zhang, Xu Wang, Yuhua Zhang, and Xiexiu Wang. (2014). Insight to the Epidemiology and Risk Factors of Extrapulmonary Tuberculosis in Tianjin, China during 2006-2011. PLoS ONE, 9(12),1–12. doi: 10.1371/journal.pone.0112213.
Wardani, D. W. S. R., and Wahono, E. P. (2020). Spatial-Temporal Dynamisc of Tuberculosis Clusters in Indonesia. Indian Journal of Community Medicine, 45(1), 43-47. doi: 10.4103/ijcm.IJCM_182_19
World Health Organization. (2019). Global tuberculosis report (Internet). Geneva: Author. Retrieved from https://apps.who.int/iris/bitstream/handle/10665/191102/9789241565059_eng.pdf?sequence=1&isAllowed=y
World Health Organization. (2018). Global tuberculosis report (1st Ed.). Geneva: Author. Retrieved from https://apps.who.int/medicinedocs/documents/s23553en/s23553en.pdf
Wubuli, Atikaimu, Yuehua Li, Feng Xue, Xuemei Yao, Halmurat Upur, and Qimanguli Wushouer. (2017). Seasonality of Active Tuberculosis Notification from 2005 to 2014 in Xinjiang, China. PLoS ONE, 12(7), 1–12. doi: 10.1371/journal.pone.0180226.
Yu, Ya, Bo Wu, Chengguo Wu, Qingya Wang, Daiyu Hu, and Wei Chen. (2020). Spatial-Temporal Analysis of Tuberculosis. BMC Infectious Diseases, 20, 1–12.
Zheng, Yan Ling, Li Ping Zhang, Xue Liang Zhang, Kai Wang, and Yu Jian Zheng. 2015. Forecast Model Analysis for the Morbidity of Tuberculosis in Xinjiang, China. PLoS ONE, 10(3),1–13. doi: 10.1371/journal.pone.0116832.
Zhu, Minmin, Guiyuan Han, Howard Eugene Takiff, Jian Wang, Jianping Ma, Min Zhang, and Shengyuan Liu. (2018). Times Series Analysis of Age-Specific Tuberculosis at a Rapid Developing Region. Scientific Reports, 8(1), 2011–16. doi: 10.1038/s41598-018-27024-w.