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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Recurrence of TB has been associated with poor adherence to treatment&#44; smoking&#44; alcoholism&#44; unemployment&#44; drug abuse&#44; the severity of pulmonary cavitation&#44; HIV infection and duration of treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> However&#44; the risk factors can vary considerably across countries and between studies&#46; Since little is known about risk factors for recurrence in Portugal&#44; we aimed to identify predictors of treatment recurrence in the country&#46; Surveillance data on TB for the period of 2002&#8211;2009 was provided by SVIG-TB&#44; a database from the Portuguese National Health System&#46; For this analysis&#44; only cases of confirmed TB disease were considered&#44; and patients that had information on the first and second TB episodes&#46; The variables studied were chosen as TB risk factors according to previous reports about TB recurrence&#46; The existence of missing data was assessed and missing data characterised &#40;missingness between 0 and 10&#37;&#41;&#46; From this characterisation&#44; we chose to explore multiple imputation using random-forest based on multivariate imputation by chained equations&#46; We used a semi-parametric Cox regression model in which the event of interest was the second episode of TB&#44; with time being measured from the end of treatment for a first TB episode&#46; Patients without the second episode of TB before the end of the study were eliminated&#46; A total of 8364 individuals were analysed&#44; of which 145 &#40;1&#46;73&#37;&#41; had a recurrent TB episode during the time of the study&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Patients who defaulted TB treatment are ten times more likely to suffer a recurrent case of TB &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; As expected&#44;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> HIV was positively associated with recurrence of TB disease &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Alcohol use disorders have been associated with recurrent TB&#44; mostly by linkage to other confounding factors&#46;<a class="elsevierStyleCrossRefs" href="#bib0040"><span class="elsevierStyleSup">1&#44;2</span></a> We found that even when considering treatment default&#44; TB patients with an alcohol use disorder still had 86&#37; increase in the risk of TB recurrence &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Incarceration is a known risk factor for TB mainly due to overcrowding&#44; delayed diagnosis and&#47;or inadequate treatment&#46; Our study shows that in Portugal&#44; the risk of TB recurrence for prison inmates is four times higher &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The standard 6-month treatment regimen is often insufficient to prevent TB relapse&#44;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">3</span></a> nevertheless&#44; the study of treatment length as a risk factor has been mostly restricted to TB patients living with HIV&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a> Longer treatments are usually prescribed for patients with poor prognosis&#44; potentially confounding a beneficial effect&#46; We found a decrease of 10&#37; in the risk of recurrence per added month of treatment&#44; even accounting for the effect of other risk factors &#40;e&#46;g&#46; HIV&#41;&#44; which may suggest a need to reevaluate standard treatment regimens &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The inclusion of the clinical form in a study about recurrence is unusual&#46; Most studies discard extrapulmonary TB cases since this form is much less infectious&#44; contributing less to overall TB epidemics&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> Nevertheless&#44; we found that there is a two-fold increase in the risk of recurrence when suffering from an extrapulmonary form of the disease &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Driver et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a> showed that in TB patients living with HIV&#44; extrapulmonary disease increased the risk of recurrence&#44; and Millet et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">2</span></a> suggested that this was true irrespective of HIV status&#46; Interestingly&#44; some TB risk factors have been shown to be associated with the clinical form &#8211; i&#46;e&#46; having HIV or being young increases the chance of having an extrapulmonary infection&#44; while smoking and living with diabetes increases the chance of a pulmonary TB&#46; Regardless of the association between youth and extrapulmonary TB&#44; the role of age in TB recurrence is somewhat uncertain&#44; with some studies<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">5</span></a> indicating a decrease of risk for older people while others<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">6</span></a> suggest a reduction for younger individuals&#46; In Portugal&#44; we found that an increase of one year in the age of the patient leads to a decrease of 1&#37; in the risk of a recurrent episode &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The association between diabetes and TB incidence has been relatively established&#44; but the association with TB recurrence is unclear&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">3</span></a> Although the variable is not significant&#44; we have estimated a decrease of 80&#37; in the risk of a recurrent episode when having diabetes &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; In this study&#44; 55&#37; of recurrence occurred in the first 12 months after treatment completion&#44; suggesting that in Portugal most of TB recurrence cases were due to relapse since relapse occurs not long after the end of treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">7</span></a> Nevertheless&#44; future studies should consider the inclusion of mycobacterial DNA information to distinguish between relapse and exogenous reinfection&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">To the best of our knowledge&#44; this is the only study&#44; to date&#44; covering risk factors for TB recurrence in Portugal&#46; The study concerns the period 2002&#8211;2009 and&#44; although the situation may have changed over the last decade&#44; this cannot be assessed unless datasets linking multiple disease episodes at the individual level are made available to researchers&#46; Understanding risk factors for TB recurrence in Portugal can help to define new guidelines to reduce the prevalence of recurrence&#44; decreasing the chance of multi-drug resistant TB development&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Funding</span><p id="par0020" class="elsevierStylePara elsevierViewall">Cristina Rocha&#39;s research is partially supported by <span class="elsevierStyleGrantSponsor" id="gs1">FCT</span> &#40;Funda&#231;&#227;o para a Ci&#234;ncia e a Tecnologia&#41;&#44; Portugal&#44; through project UID&#47;MAT&#47;00006&#47;2019&#46; MGMG received funding from Funda&#231;&#227;o para a Ci&#234;ncia e a Tecnologia &#40;IF&#47;01346&#47;2014&#41;&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Conflict of interest</span><p id="par0025" class="elsevierStylePara elsevierViewall">The authors reported no conflict of interest&#46;</p></span></span>"
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                  \t\t\t\t">Prison&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">HIV&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">2&#46;34&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Clinical form&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Alcohol use&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Age&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">&#91;0&#46;98&#44; 0&#46;99&#93;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Length of treatment&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Diabetes&nbsp;\t\t\t\t\t\t\n
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                    0 => array:2 [
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                        0 => array:2 [
                          "etal" => false
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                      "titulo" => "Tuberculosis recurrence after completion treatment in a European city&#58; reinfection or relapse&#63;"
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                          "etal" => false
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                            3 => "M&#46; Casals"
                            4 => "J&#46;M&#46; Mir&#243;"
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                      "titulo" => "Risk factors for 1-year relapse of pulmonary tuberculosis treated with a 6-month daily regimen"
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                          "etal" => true
                          "autores" => array:6 [
                            0 => "K&#46;-W&#46; Jo"
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                            2 => "Y&#46; Hong"
                            3 => "J&#46;S&#46; Lee"
                            4 => "S&#46;-D&#46; Lee"
                            5 => "W&#46;S&#46; Kim"
                          ]
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                      "doi" => "10.1016/j.rmed.2014.01.010"
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                      "titulo" => "Relapse in persons treated for drug-susceptible tuberculosis in a population with high coinfection with human immunodeficiency virus in New York City"
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                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "C&#46;R&#46; Driver"
                            1 => "S&#46;S&#46; Munsiff"
                            2 => "J&#46; Li"
                            3 => "N&#46; Kundamal"
                            4 => "S&#46;S&#46; Osahan"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1086/323784"
                      "Revista" => array:6 [
                        "tituloSerie" => "Clin Infect Dis"
                        "fecha" => "2001"
                        "volumen" => "33"
                        "paginaInicial" => "1762"
                        "paginaFinal" => "1769"
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                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/11595988"
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                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Recurrent tuberculosis and exogenous reinfection&#44; Shanghai&#44; China"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "G&#46; Shen"
                            1 => "Z&#46; Xue"
                            2 => "X&#46; Shen"
                            3 => "B&#46; Sun"
                            4 => "X&#46; Gui"
                            5 => "M&#46; Shen"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.3201/eid1211.051207"
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                        "tituloSerie" => "Emerg Infect Dis"
                        "fecha" => "2006"
                        "volumen" => "12"
                        "paginaInicial" => "1776"
                        "paginaFinal" => "1778"
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                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/17283636"
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              "etiqueta" => "6"
              "referencia" => array:1 [
                0 => array:2 [
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                      "titulo" => "Why pulmonary tuberculosis recurs&#58; a population-based epidemiological study"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "A&#46;W&#46; Selassie"
                            1 => "D&#46;R&#46; Ph"
                            2 => "C&#46; Pozsik"
                            3 => "D&#46; Wilson"
                            4 => "P&#46;L&#46; Ferguson"
                          ]
                        ]
                      ]
                    ]
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                    0 => array:2 [
                      "doi" => "10.1016/j.annepidem.2005.03.002"
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                        "tituloSerie" => "Ann Epidemiol"
                        "fecha" => "2005"
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                      "titulo" => "Timing of relapse in short-course chemotherapy trials for tuberculosis"
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                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "J&#46; Nunn a"
                            1 => "P&#46;P&#46;J&#46; Phillips"
                            2 => "D&#46;A&#46; Mitchison"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Int J Tuberc Lung Dis"
                        "fecha" => "2010"
                        "volumen" => "14"
                        "paginaInicial" => "241"
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        "titulo" => "Acknowledgements"
        "texto" => "<p id="par0030" class="elsevierStylePara elsevierViewall">We thank the members of the Collective Dynamics Group of Instituto Gulbenkian de Ci&#234;ncia for help and discussion at various points in the project&#46; We also thank our collaborators from the Portuguese public health authorities&#44; namely&#44; Programa Nacional de Luta contra a Tuberculose&#44; and the reference laboratories&#44; Instituto Nacional de Sa&#250;de Ricardo Jorge and Administra&#231;&#227;o Regional de Sa&#250;de de Lisboa e Vale do Tejo&#46;</p>"
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Letter to the Editor
Insights into tuberculosis: A survival analysis of time to recurrence in Portugal, between 2002 and 2009
P. Soaresa,b,c,
Corresponding author
patseraos@gmail.com

Corresponding author.
, R. Duarted,e,f, M.G.M. Gomesg,h, C. Rochab,c, J.S. Lopesa,i
a Instituto Gulbenkian de Ciência, Oeiras, Portugal
b Departamento de Estatística e Investigação Operacional, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
c Centro de Estatística e Aplicações, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
d Serviço de Pneumologia, Centro Hospitalar de Vila Nova de Gaia/Espinho, Portugal
e Faculdade de Medicina, Universidade do Porto, Porto, Portugal
f EpiUnit, Instituto de Saúde Pública, Universidade do Porto, Porto, Portugal
g Liverpool School of Tropical Medicine, Liverpool, United Kingdom
h CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, and CMUP, Centro de Matemática da Universidade do Porto, Porto, Portugal
i Instituto Nacional de Estatística, Lisboa, Portugal
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Recurrence of TB has been associated with poor adherence to treatment&#44; smoking&#44; alcoholism&#44; unemployment&#44; drug abuse&#44; the severity of pulmonary cavitation&#44; HIV infection and duration of treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> However&#44; the risk factors can vary considerably across countries and between studies&#46; Since little is known about risk factors for recurrence in Portugal&#44; we aimed to identify predictors of treatment recurrence in the country&#46; Surveillance data on TB for the period of 2002&#8211;2009 was provided by SVIG-TB&#44; a database from the Portuguese National Health System&#46; For this analysis&#44; only cases of confirmed TB disease were considered&#44; and patients that had information on the first and second TB episodes&#46; The variables studied were chosen as TB risk factors according to previous reports about TB recurrence&#46; The existence of missing data was assessed and missing data characterised &#40;missingness between 0 and 10&#37;&#41;&#46; From this characterisation&#44; we chose to explore multiple imputation using random-forest based on multivariate imputation by chained equations&#46; We used a semi-parametric Cox regression model in which the event of interest was the second episode of TB&#44; with time being measured from the end of treatment for a first TB episode&#46; Patients without the second episode of TB before the end of the study were eliminated&#46; A total of 8364 individuals were analysed&#44; of which 145 &#40;1&#46;73&#37;&#41; had a recurrent TB episode during the time of the study&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Patients who defaulted TB treatment are ten times more likely to suffer a recurrent case of TB &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; As expected&#44;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> HIV was positively associated with recurrence of TB disease &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Alcohol use disorders have been associated with recurrent TB&#44; mostly by linkage to other confounding factors&#46;<a class="elsevierStyleCrossRefs" href="#bib0040"><span class="elsevierStyleSup">1&#44;2</span></a> We found that even when considering treatment default&#44; TB patients with an alcohol use disorder still had 86&#37; increase in the risk of TB recurrence &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Incarceration is a known risk factor for TB mainly due to overcrowding&#44; delayed diagnosis and&#47;or inadequate treatment&#46; Our study shows that in Portugal&#44; the risk of TB recurrence for prison inmates is four times higher &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The standard 6-month treatment regimen is often insufficient to prevent TB relapse&#44;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">3</span></a> nevertheless&#44; the study of treatment length as a risk factor has been mostly restricted to TB patients living with HIV&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a> Longer treatments are usually prescribed for patients with poor prognosis&#44; potentially confounding a beneficial effect&#46; We found a decrease of 10&#37; in the risk of recurrence per added month of treatment&#44; even accounting for the effect of other risk factors &#40;e&#46;g&#46; HIV&#41;&#44; which may suggest a need to reevaluate standard treatment regimens &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The inclusion of the clinical form in a study about recurrence is unusual&#46; Most studies discard extrapulmonary TB cases since this form is much less infectious&#44; contributing less to overall TB epidemics&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> Nevertheless&#44; we found that there is a two-fold increase in the risk of recurrence when suffering from an extrapulmonary form of the disease &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Driver et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a> showed that in TB patients living with HIV&#44; extrapulmonary disease increased the risk of recurrence&#44; and Millet et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">2</span></a> suggested that this was true irrespective of HIV status&#46; Interestingly&#44; some TB risk factors have been shown to be associated with the clinical form &#8211; i&#46;e&#46; having HIV or being young increases the chance of having an extrapulmonary infection&#44; while smoking and living with diabetes increases the chance of a pulmonary TB&#46; Regardless of the association between youth and extrapulmonary TB&#44; the role of age in TB recurrence is somewhat uncertain&#44; with some studies<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">5</span></a> indicating a decrease of risk for older people while others<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">6</span></a> suggest a reduction for younger individuals&#46; In Portugal&#44; we found that an increase of one year in the age of the patient leads to a decrease of 1&#37; in the risk of a recurrent episode &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The association between diabetes and TB incidence has been relatively established&#44; but the association with TB recurrence is unclear&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">3</span></a> Although the variable is not significant&#44; we have estimated a decrease of 80&#37; in the risk of a recurrent episode when having diabetes &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; In this study&#44; 55&#37; of recurrence occurred in the first 12 months after treatment completion&#44; suggesting that in Portugal most of TB recurrence cases were due to relapse since relapse occurs not long after the end of treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">7</span></a> Nevertheless&#44; future studies should consider the inclusion of mycobacterial DNA information to distinguish between relapse and exogenous reinfection&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">To the best of our knowledge&#44; this is the only study&#44; to date&#44; covering risk factors for TB recurrence in Portugal&#46; The study concerns the period 2002&#8211;2009 and&#44; although the situation may have changed over the last decade&#44; this cannot be assessed unless datasets linking multiple disease episodes at the individual level are made available to researchers&#46; Understanding risk factors for TB recurrence in Portugal can help to define new guidelines to reduce the prevalence of recurrence&#44; decreasing the chance of multi-drug resistant TB development&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Funding</span><p id="par0020" class="elsevierStylePara elsevierViewall">Cristina Rocha&#39;s research is partially supported by <span class="elsevierStyleGrantSponsor" id="gs1">FCT</span> &#40;Funda&#231;&#227;o para a Ci&#234;ncia e a Tecnologia&#41;&#44; Portugal&#44; through project UID&#47;MAT&#47;00006&#47;2019&#46; MGMG received funding from Funda&#231;&#227;o para a Ci&#234;ncia e a Tecnologia &#40;IF&#47;01346&#47;2014&#41;&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Conflict of interest</span><p id="par0025" class="elsevierStylePara elsevierViewall">The authors reported no conflict of interest&#46;</p></span></span>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Hazard ratios and 95&#37; confidence intervals for TB recurrence&#46;</p>"
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        "texto" => "<p id="par0030" class="elsevierStylePara elsevierViewall">We thank the members of the Collective Dynamics Group of Instituto Gulbenkian de Ci&#234;ncia for help and discussion at various points in the project&#46; We also thank our collaborators from the Portuguese public health authorities&#44; namely&#44; Programa Nacional de Luta contra a Tuberculose&#44; and the reference laboratories&#44; Instituto Nacional de Sa&#250;de Ricardo Jorge and Administra&#231;&#227;o Regional de Sa&#250;de de Lisboa e Vale do Tejo&#46;</p>"
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Article information
ISSN: 25310437
Original language: English
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