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Published in: Clinical Rheumatology 8/2017

01-08-2017 | Original Article

Latent tuberculosis infection and tuberculosis in patients with rheumatic diseases treated with anti-tumor necrosis factor agents

Authors: Giovana Garziera, André Luis Bittencourt Morsch, Felipe Otesbelgue, Fernanda Luiza Staub, Penélope Esther Palominos, Claiton Viegas Brenol, Denise Rossato Silva

Published in: Clinical Rheumatology | Issue 8/2017

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Abstract

The introduction of biological agents, especially the tumor necrosis factor inhibitors (anti-TNF), for the treatment of rheumatic diseases increased the risk of developing tuberculosis (TB). Screening for latent TB infection (LTBI) is strongly recommended before starting therapy with anti-TNF agents. The objective of this study was to identify the prevalence of LTBI and TB among patients with rheumatic diseases on anti-TNF agents. This is a cross-sectional study. The electronic medical records of all adult patients (≥18 years old) undergoing anti-TNF treatment were reviewed. Every patient underwent tuberculin skin test (TST) before starting anti-TNF treatment. In total, 176 patients were included; the mean age was 51.9 ± 12.4 years, 34.7% were males, and 90.9% were white. The underlying diseases were rheumatoid arthritis (RA) in 50.6% (N = 89), ankylosing spondylitis (AS) in 27.8% (N = 49), and psoriatic arthritis (PsA) in 17.6% (N = 31). The prevalence of positive TST was 29.5%. Household contact with TB was significantly associated with a positive TST (p = 0.020). RA patients had lower TST reactions than AS patients (p = 0.022). There were six cases of TB (3.4%) diagnosed during anti-TNF therapy. We demonstrated a high prevalence of positive TST (29.5%) among patients with rheumatic diseases in a region with high TB prevalence. Our data corroborates the ACR’s recommendation that patients who live in high TB incidence settings should be tested annually for LTBI.
Literature
3.
go back to reference Mack U, Migliori GB, Sester M, Rieder HL, Ehlers S, Goletti D et al (2009) LTBI: latent tuberculosis infection or lasting immune responses to M. tuberculosis? A TBNET consensus statement. Eur Respir J 33:956–973CrossRefPubMed Mack U, Migliori GB, Sester M, Rieder HL, Ehlers S, Goletti D et al (2009) LTBI: latent tuberculosis infection or lasting immune responses to M. tuberculosis? A TBNET consensus statement. Eur Respir J 33:956–973CrossRefPubMed
4.
go back to reference Ishiguro T, Takayanagi N, Kagiyama N, Yanagisawa T, Sugita Y (2014) Characteristics of tuberculosis in patients with rheumatoid arthritis: a retrospective single-center study. Intern med 53:1291–1298CrossRefPubMed Ishiguro T, Takayanagi N, Kagiyama N, Yanagisawa T, Sugita Y (2014) Characteristics of tuberculosis in patients with rheumatoid arthritis: a retrospective single-center study. Intern med 53:1291–1298CrossRefPubMed
5.
go back to reference Alawneh KM, Ayesh MH, Khassawneh BY, Saadeh SS, Smadi M, Bashaireh K (2014) Anti-TNF therapy in Jordan: a focus on severe infections and tuberculosis. Biologics 8:193–198PubMedPubMedCentral Alawneh KM, Ayesh MH, Khassawneh BY, Saadeh SS, Smadi M, Bashaireh K (2014) Anti-TNF therapy in Jordan: a focus on severe infections and tuberculosis. Biologics 8:193–198PubMedPubMedCentral
6.
go back to reference Baronnet L, Barnetche T, Kahn V, Lacoin C, Richez C, Schaeverbeke T (2011) Incidence of tuberculosis in patients with rheumatoid arthritis. A systematic literature review. Joint Bone Spine 78:279–284CrossRefPubMed Baronnet L, Barnetche T, Kahn V, Lacoin C, Richez C, Schaeverbeke T (2011) Incidence of tuberculosis in patients with rheumatoid arthritis. A systematic literature review. Joint Bone Spine 78:279–284CrossRefPubMed
7.
go back to reference Arkema EV, Jonsson J, Baecklund E, Bruchfeld J, Feltelius N, Askling J (2015) Are patients with rheumatoid arthritis still at an increased risk of tuberculosis and what is the role of biological treatments? Ann Rheum dis 74:1212–1217CrossRefPubMed Arkema EV, Jonsson J, Baecklund E, Bruchfeld J, Feltelius N, Askling J (2015) Are patients with rheumatoid arthritis still at an increased risk of tuberculosis and what is the role of biological treatments? Ann Rheum dis 74:1212–1217CrossRefPubMed
8.
go back to reference Askling J, Fored M, Brandt L, Baecklund E, Bertilisson L (2005) Risk and case characteristics of tuberculosis in rheumatoid arthritis associated with tumor necrosis factor antagonists in Sweden. Arthritis Rheum 52:1986–1992CrossRefPubMed Askling J, Fored M, Brandt L, Baecklund E, Bertilisson L (2005) Risk and case characteristics of tuberculosis in rheumatoid arthritis associated with tumor necrosis factor antagonists in Sweden. Arthritis Rheum 52:1986–1992CrossRefPubMed
9.
go back to reference Carmona L, Hernandez-Garcia C, Vadillo C, Pato E, Balsa A, Gonzalez-Alvaro I et al (2003) Increased risk of tuberculosis in patients with rheumatoid arthritis. J Rheumatol 30:1436–1439PubMed Carmona L, Hernandez-Garcia C, Vadillo C, Pato E, Balsa A, Gonzalez-Alvaro I et al (2003) Increased risk of tuberculosis in patients with rheumatoid arthritis. J Rheumatol 30:1436–1439PubMed
10.
go back to reference Scrivo R, Armignacco O (2014) Tuberculosis risk and anti-tumour necrosis factor agents in rheumatoid arthritis: a critical appraisal of national registry data. Int J Rheum dis 17:716–724CrossRefPubMed Scrivo R, Armignacco O (2014) Tuberculosis risk and anti-tumour necrosis factor agents in rheumatoid arthritis: a critical appraisal of national registry data. Int J Rheum dis 17:716–724CrossRefPubMed
11.
go back to reference Seong SS, Choi CB, Woo JH, Bae KW, Joung CL, Uhm WS et al (2007) Incidence of tuberculosis in Korean patients with rheumatoid arthritis (RA): effects of RA itself and of tumor necrosis factor blockers. J Rheumatol 34:706–711PubMed Seong SS, Choi CB, Woo JH, Bae KW, Joung CL, Uhm WS et al (2007) Incidence of tuberculosis in Korean patients with rheumatoid arthritis (RA): effects of RA itself and of tumor necrosis factor blockers. J Rheumatol 34:706–711PubMed
12.
go back to reference Singh JA, Furst DE, Bharat A, Curtis JR, Kavanaugh AF, Kremer JM et al (2012) 2012 update of the 2008 American College of Rheumatology recommendations for the use of disease-modifying antirheumatic drugs and biologic agents in the treatment of rheumatoid arthritis. Arthritis Care res (Hoboken ) 64:625–639CrossRef Singh JA, Furst DE, Bharat A, Curtis JR, Kavanaugh AF, Kremer JM et al (2012) 2012 update of the 2008 American College of Rheumatology recommendations for the use of disease-modifying antirheumatic drugs and biologic agents in the treatment of rheumatoid arthritis. Arthritis Care res (Hoboken ) 64:625–639CrossRef
13.
go back to reference Ponce de LD, Acevedo-Vasquez E, Sanchez-Torres A, Cucho M, Alfaro J, Perich R et al (2005) Attenuated response to purified protein derivative in patients with rheumatoid arthritis: study in a population with a high prevalence of tuberculosis. Ann Rheum dis 64:1360–1361CrossRef Ponce de LD, Acevedo-Vasquez E, Sanchez-Torres A, Cucho M, Alfaro J, Perich R et al (2005) Attenuated response to purified protein derivative in patients with rheumatoid arthritis: study in a population with a high prevalence of tuberculosis. Ann Rheum dis 64:1360–1361CrossRef
14.
go back to reference Conde MB, Melo FA, Marques AM et al (2009) III Brazilian thoracic association guidelines on tuberculosis. J Bras Pneumol 35:1018–1048CrossRefPubMed Conde MB, Melo FA, Marques AM et al (2009) III Brazilian thoracic association guidelines on tuberculosis. J Bras Pneumol 35:1018–1048CrossRefPubMed
16.
go back to reference Callado MR, Lima JR, Nobre CA, Vieira WP (2011) Low prevalence of reactive PPD prior to infliximab use: comparative study on a population sample of Hospital Geral de Fortaleza. Rev Bras Reumatol 51:40–52CrossRefPubMed Callado MR, Lima JR, Nobre CA, Vieira WP (2011) Low prevalence of reactive PPD prior to infliximab use: comparative study on a population sample of Hospital Geral de Fortaleza. Rev Bras Reumatol 51:40–52CrossRefPubMed
17.
go back to reference Bonfiglioli KR, Ribeiro AC, Moraes JC, Saad CG, Souza FH, Calich AL et al (2014) LTBI screening in rheumatoid arthritis patients prior to anti-TNF treatment in an endemic area. Int J Tuberc Lung dis 18:905–911PubMed Bonfiglioli KR, Ribeiro AC, Moraes JC, Saad CG, Souza FH, Calich AL et al (2014) LTBI screening in rheumatoid arthritis patients prior to anti-TNF treatment in an endemic area. Int J Tuberc Lung dis 18:905–911PubMed
18.
go back to reference Agarwal S, Das SK, Agarwal GG, Srivastava R (2014) Steroids decrease prevalence of positive tuberculin skin test in rheumatoid arthritis: implications on anti-TNF therapies. Interdiscip Perspect Infect dis 2014:430134CrossRefPubMedPubMedCentral Agarwal S, Das SK, Agarwal GG, Srivastava R (2014) Steroids decrease prevalence of positive tuberculin skin test in rheumatoid arthritis: implications on anti-TNF therapies. Interdiscip Perspect Infect dis 2014:430134CrossRefPubMedPubMedCentral
19.
go back to reference Saidenberg-Kermanac'h N, Semerano L, Naccache JM, Brauner M, Falgarone G, Dumont-Fischer D et al (2012) Screening for latent tuberculosis in anti-TNF-alpha candidate patients in a high tuberculosis incidence setting. Int J Tuberc Lung dis 16:1307–1314CrossRefPubMed Saidenberg-Kermanac'h N, Semerano L, Naccache JM, Brauner M, Falgarone G, Dumont-Fischer D et al (2012) Screening for latent tuberculosis in anti-TNF-alpha candidate patients in a high tuberculosis incidence setting. Int J Tuberc Lung dis 16:1307–1314CrossRefPubMed
20.
go back to reference Bartalesi F, Goletti D, Spinicci M, Cavallo A, Attala L, Mencarini J et al (2013) Serial QuantiFERON TB-gold in-tube testing during LTBI therapy in candidates for TNFi treatment. J Inf Secur 66:346–356 Bartalesi F, Goletti D, Spinicci M, Cavallo A, Attala L, Mencarini J et al (2013) Serial QuantiFERON TB-gold in-tube testing during LTBI therapy in candidates for TNFi treatment. J Inf Secur 66:346–356
21.
go back to reference Emery P, Panayi G, Symmons D, Brown G (1984) Mechanisms of depressed delayed-type hypersensitivity in rheumatoid arthritis: the role of protein energy malnutrition. Ann Rheum dis 43:430–434CrossRefPubMedPubMedCentral Emery P, Panayi G, Symmons D, Brown G (1984) Mechanisms of depressed delayed-type hypersensitivity in rheumatoid arthritis: the role of protein energy malnutrition. Ann Rheum dis 43:430–434CrossRefPubMedPubMedCentral
22.
go back to reference Kim JH, Cho SK, Han M, Choi CB, Kim TH, Jun JB et al (2013) Factors influencing discrepancies between the QuantiFERON-TB gold in tube test and the tuberculin skin test in Korean patients with rheumatic diseases. Semin Arthritis Rheum 42:424–432CrossRefPubMed Kim JH, Cho SK, Han M, Choi CB, Kim TH, Jun JB et al (2013) Factors influencing discrepancies between the QuantiFERON-TB gold in tube test and the tuberculin skin test in Korean patients with rheumatic diseases. Semin Arthritis Rheum 42:424–432CrossRefPubMed
23.
go back to reference Laurindo IM, Seiscento M (2004) Bombardia Sea (Eds): diagnosis of latent tuberculosis in rheumatoid arthritis (RA) patients: tuberculin test (PPD) assessment. Ann Rheum dis 63:179 Laurindo IM, Seiscento M (2004) Bombardia Sea (Eds): diagnosis of latent tuberculosis in rheumatoid arthritis (RA) patients: tuberculin test (PPD) assessment. Ann Rheum dis 63:179
24.
go back to reference Paimela L, Johansson-Stephansson EA, Koskimies S, Leirisalo-Repo M (1990) Depressed cutaneous cell-mediated immunity in early rheumatoid arthritis. Clin Exp Rheumatol 8:433–437PubMed Paimela L, Johansson-Stephansson EA, Koskimies S, Leirisalo-Repo M (1990) Depressed cutaneous cell-mediated immunity in early rheumatoid arthritis. Clin Exp Rheumatol 8:433–437PubMed
25.
go back to reference Panayi GS, Corrigall VM (2001) Pitzalis C: pathogenesis of rheumatoid arthritis. The role of T cells and other beasts. Rheum dis Clin N am 27:317–334CrossRef Panayi GS, Corrigall VM (2001) Pitzalis C: pathogenesis of rheumatoid arthritis. The role of T cells and other beasts. Rheum dis Clin N am 27:317–334CrossRef
26.
go back to reference Koker IH, Pamuk ON, Karlikaya C, Tuncbilek N, Cakir N (2007) A low prevalance of purified protein derivative test positivity in Turkish patients with rheumatoid arthritis. Association with clinical features and HRCT findings. Clin Exp Rheumatol 25:54–59PubMed Koker IH, Pamuk ON, Karlikaya C, Tuncbilek N, Cakir N (2007) A low prevalance of purified protein derivative test positivity in Turkish patients with rheumatoid arthritis. Association with clinical features and HRCT findings. Clin Exp Rheumatol 25:54–59PubMed
27.
go back to reference Marques CDL, Duarte ALBP, Lorena VMB, Souza JR, Souza W, Gomes YM et al (2009) Resposta atenuada ao PPD no diagnóstico de infecção tuberculosa latente em pacientes com artrite reumatóide. Rev Bras Reumatol 49:121–125CrossRef Marques CDL, Duarte ALBP, Lorena VMB, Souza JR, Souza W, Gomes YM et al (2009) Resposta atenuada ao PPD no diagnóstico de infecção tuberculosa latente em pacientes com artrite reumatóide. Rev Bras Reumatol 49:121–125CrossRef
29.
go back to reference Fuchs I, Avnon L, Freud T, Abu-Shakra M (2009) Repeated tuberculin skin testing following therapy with TNF-alpha inhibitors. Clin Rheumatol 28:167–172CrossRefPubMed Fuchs I, Avnon L, Freud T, Abu-Shakra M (2009) Repeated tuberculin skin testing following therapy with TNF-alpha inhibitors. Clin Rheumatol 28:167–172CrossRefPubMed
30.
go back to reference Chan PC, Chang LY, Wu YC, Lu CY, Kuo HS, Lee CY et al (2008) Age-specific cut-offs for the tuberculin skin test to detect latent tuberculosis in BCG-vaccinated children. Int J Tuberc Lung dis 12:1401–1406PubMed Chan PC, Chang LY, Wu YC, Lu CY, Kuo HS, Lee CY et al (2008) Age-specific cut-offs for the tuberculin skin test to detect latent tuberculosis in BCG-vaccinated children. Int J Tuberc Lung dis 12:1401–1406PubMed
31.
go back to reference Araujo Z, de Waard JH, de Larrea CF, Borges R, Convit J (2008) The effect of Bacille Calmette-Guerin vaccine on tuberculin reactivity in indigenous children from communities with high prevalence of tuberculosis. Vaccine 26:5575–5581CrossRefPubMed Araujo Z, de Waard JH, de Larrea CF, Borges R, Convit J (2008) The effect of Bacille Calmette-Guerin vaccine on tuberculin reactivity in indigenous children from communities with high prevalence of tuberculosis. Vaccine 26:5575–5581CrossRefPubMed
32.
go back to reference Rangaka MX, Wilkinson KA, Glynn JR, Ling D, Menzies D, Mwansa-Kambafwile J et al (2012) Predictive value of interferon-gamma release assays for incident active tuberculosis: a systematic review and meta-analysis. Lancet Infect dis 12:45–55CrossRefPubMed Rangaka MX, Wilkinson KA, Glynn JR, Ling D, Menzies D, Mwansa-Kambafwile J et al (2012) Predictive value of interferon-gamma release assays for incident active tuberculosis: a systematic review and meta-analysis. Lancet Infect dis 12:45–55CrossRefPubMed
33.
go back to reference Chen DY, Shen GH, Chen YM, Chen HH, Hsieh CW, Lan JL (2012) Biphasic emergence of active tuberculosis in rheumatoid arthritis patients receiving TNFalpha inhibitors: the utility of IFNgamma assay. Ann Rheum dis 71:231–237CrossRefPubMed Chen DY, Shen GH, Chen YM, Chen HH, Hsieh CW, Lan JL (2012) Biphasic emergence of active tuberculosis in rheumatoid arthritis patients receiving TNFalpha inhibitors: the utility of IFNgamma assay. Ann Rheum dis 71:231–237CrossRefPubMed
34.
go back to reference Hsia EC, Cush JJ, Matteson EL, Beutler A, Doyle MK, Hsu B et al (2013) Comprehensive tuberculosis screening program in patients with inflammatory arthritides treated with golimumab, a human anti-tumor necrosis factor antibody, in phase III clinical trials. Arthritis Care res (Hoboken ) 65:309–313CrossRef Hsia EC, Cush JJ, Matteson EL, Beutler A, Doyle MK, Hsu B et al (2013) Comprehensive tuberculosis screening program in patients with inflammatory arthritides treated with golimumab, a human anti-tumor necrosis factor antibody, in phase III clinical trials. Arthritis Care res (Hoboken ) 65:309–313CrossRef
35.
go back to reference Raval A, Akhavan-Toyserkani G, Brinker A, Avigan M (2007) Brief communication: characteristics of spontaneous cases of tuberculosis associated with infliximab. Ann Intern med 147:699–702CrossRefPubMed Raval A, Akhavan-Toyserkani G, Brinker A, Avigan M (2007) Brief communication: characteristics of spontaneous cases of tuberculosis associated with infliximab. Ann Intern med 147:699–702CrossRefPubMed
36.
go back to reference Westhovens R, Yocum D, Han J, Berman A, Strusberg I, Geusens P et al (2006) The safety of infliximab, combined with background treatments, among patients with rheumatoid arthritis and various comorbidities: a large, randomized, placebo-controlled trial. Arthritis Rheum 54:1075–1086CrossRefPubMed Westhovens R, Yocum D, Han J, Berman A, Strusberg I, Geusens P et al (2006) The safety of infliximab, combined with background treatments, among patients with rheumatoid arthritis and various comorbidities: a large, randomized, placebo-controlled trial. Arthritis Rheum 54:1075–1086CrossRefPubMed
Metadata
Title
Latent tuberculosis infection and tuberculosis in patients with rheumatic diseases treated with anti-tumor necrosis factor agents
Authors
Giovana Garziera
André Luis Bittencourt Morsch
Felipe Otesbelgue
Fernanda Luiza Staub
Penélope Esther Palominos
Claiton Viegas Brenol
Denise Rossato Silva
Publication date
01-08-2017
Publisher
Springer London
Published in
Clinical Rheumatology / Issue 8/2017
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-017-3714-6

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