Skip to main content
Erschienen in: Clinical Rheumatology 5/2020

01.05.2020 | Original Article

Incidence of tuberculosis in patients receiving anti-TNF therapy for rheumatic diseases: a systematic review

verfasst von: Natália Sarzi Sartori, Nicole Pamplona Bueno de Andrade, Rafael Mendonça da Silva Chakr

Erschienen in: Clinical Rheumatology | Ausgabe 5/2020

Einloggen, um Zugang zu erhalten

Abstract

Introduction

The TNF inhibitors were the first immunobiologicals used to treat rheumatic diseases, but their use is associated with an increased risk of tuberculosis. The primary objective is to estimate the incidence of tuberculosis in patients with rheumatic diseases exposed to anti-TNF therapy. The secondary objectives are to evaluate the incidence of tuberculosis by region and subgroups of diseases, to review the presentation of tuberculosis in these patients, and to assess the time elapsed between onset of anti-TNF therapy and development of active granulomatous disease.

Methods

A systematic review of the literature was conducted in MEDLINE, the Cochrane Library, and LILACS. The primary endpoint was described as incidence and secondary outcomes, through subgroup analyses and comparisons of means.

Results

We included 52 observational studies. Among the exposed patients, 947 cases of tuberculosis were documented (62.2% pulmonary), with a cumulative incidence of 9.62 cases per 1000 patients exposed. TB incidence across different continents was distributed as follows: South America, 11.75 cases/1000 patients exposed; North America, 4.34 cases/1000 patients exposed; Europe, 6.28 cases/1000 patients exposed; and Asia, 13.47 cases/1000 patients exposed. There were no significant differences in TB incidence among the described diseases. The mean time elapsed from start of anti-TNF therapy until the endpoint was 18.05 months.

Conclusion

The incidence of TB in patients with rheumatic diseases exposed TNF inhibitor considering all countries was 9.62 cases per 1000 patients exposed. TB incidence was higher in South America and Asia compared with North America and Europe. Most cases occurred in the first XX months of use, and the pulmonary form predominated.
Key Points
Higher incidence of tuberculosis in patients exposed to anti-TNF compared with the general population.
• Higher incidence of TB in countries of South America and Asia compared with North America and Europe.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
3.
Zurück zum Zitat Firestein GS, Budd RC, Gabriel SE, McInnes IB, O’Dell J (2013) Kelley’s textbook of rheumatology. Vol Ninth. (Elsevier, ed.).Philadelphia Firestein GS, Budd RC, Gabriel SE, McInnes IB, O’Dell J (2013) Kelley’s textbook of rheumatology. Vol Ninth. (Elsevier, ed.).Philadelphia
4.
Zurück zum Zitat Hochberg MC, Silman AJ, Smolen JS, Weinblatt ME, Weisman M (2015) Rheumatology Vol Sixth. (Elsevier, ed.). Philadelphia Hochberg MC, Silman AJ, Smolen JS, Weinblatt ME, Weisman M (2015) Rheumatology Vol Sixth. (Elsevier, ed.). Philadelphia
8.
Zurück zum Zitat Dixon WG, Hyrich KL, Watson KD, Lunt M, Galloway J, Ustianowski A, B S R B R Control Centre Consortium, Symmons DP, BSR Biologics Register (2010) Drug-specific risk of tuberculosis in patients with rheumatoid arthritis treated with anti-TNF therapy: results from the British Society for Rheumatology Biologics Register (BSRBR). Ann Rheum Dis 69(3):522–528. https://doi.org/10.1136/ard.2009.118935 CrossRefPubMed Dixon WG, Hyrich KL, Watson KD, Lunt M, Galloway J, Ustianowski A, B S R B R Control Centre Consortium, Symmons DP, BSR Biologics Register (2010) Drug-specific risk of tuberculosis in patients with rheumatoid arthritis treated with anti-TNF therapy: results from the British Society for Rheumatology Biologics Register (BSRBR). Ann Rheum Dis 69(3):522–528. https://​doi.​org/​10.​1136/​ard.​2009.​118935 CrossRefPubMed
10.
Zurück zum Zitat Carmona L, Gómez-Reino JJ, Rodríguez-Valverde V, Montero D, Pascual-Gómez E, Mola EM, Carreño L, Figueroa M, BIOBADASER Group (2005) Effectiveness of recommendations to prevent reactivation of latent tuberculosis infection in patients treated with tumor necrosis factor antagonists. Arthritis Rheum 52(6):1766–1772. https://doi.org/10.1002/art.21043 CrossRefPubMed Carmona L, Gómez-Reino JJ, Rodríguez-Valverde V, Montero D, Pascual-Gómez E, Mola EM, Carreño L, Figueroa M, BIOBADASER Group (2005) Effectiveness of recommendations to prevent reactivation of latent tuberculosis infection in patients treated with tumor necrosis factor antagonists. Arthritis Rheum 52(6):1766–1772. https://​doi.​org/​10.​1002/​art.​21043 CrossRefPubMed
11.
Zurück zum Zitat Tubach F, Salmon D, Ravaud P, Allanore Y, Goupille P, Bréban M, Pallot-Prades B, Pouplin S, Sacchi A, Chichemanian RM, Bretagne S, Emilie D, Lemann M, Lortholary O, Mariette X, Research Axed on Tolerance of Biotherapies Group (2009) Risk of tuberculosis is higher with anti-tumor necrosis factor monoclonal antibody therapy than with soluble tumor necrosis factor receptor therapy: the three-year prospective French research axed on tolerance of biotherapies registry. Arthritis Rheum 60(7):1884–1894. https://doi.org/10.1002/art.24632 CrossRefPubMedPubMedCentral Tubach F, Salmon D, Ravaud P, Allanore Y, Goupille P, Bréban M, Pallot-Prades B, Pouplin S, Sacchi A, Chichemanian RM, Bretagne S, Emilie D, Lemann M, Lortholary O, Mariette X, Research Axed on Tolerance of Biotherapies Group (2009) Risk of tuberculosis is higher with anti-tumor necrosis factor monoclonal antibody therapy than with soluble tumor necrosis factor receptor therapy: the three-year prospective French research axed on tolerance of biotherapies registry. Arthritis Rheum 60(7):1884–1894. https://​doi.​org/​10.​1002/​art.​24632 CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Cagatay T, Bingol Z, Kıyan E, Yegin Z, Okumus G, Arseven O, Erkan F, Gulbaran Z, Erelel M, Ece T, Cagatay P, Kılıçaslan Z (2018) Follow-up of 1887 patients receiving tumor necrosis-alpha antagonists: tuberculin skin test conversion and tuberculosis risk. Clin Respir J 12(4):1668–1675. https://doi.org/10.1111/crj.12726 CrossRefPubMed Cagatay T, Bingol Z, Kıyan E, Yegin Z, Okumus G, Arseven O, Erkan F, Gulbaran Z, Erelel M, Ece T, Cagatay P, Kılıçaslan Z (2018) Follow-up of 1887 patients receiving tumor necrosis-alpha antagonists: tuberculin skin test conversion and tuberculosis risk. Clin Respir J 12(4):1668–1675. https://​doi.​org/​10.​1111/​crj.​12726 CrossRefPubMed
14.
Zurück zum Zitat Ai J-W, Zhang S, Ruan Q-L, Yu YQ, Zhang BY, Liu QH, Zhang WH (2015) The risk of tuberculosis in patients with rheumatoid arthritis treated with tumor necrosis factor- antagonist: a metaanalysis of both randomized controlled trials and registry/cohort studies. J Rheumatol 42(12):2229–2237. https://doi.org/10.3899/jrheum.150057 CrossRefPubMed Ai J-W, Zhang S, Ruan Q-L, Yu YQ, Zhang BY, Liu QH, Zhang WH (2015) The risk of tuberculosis in patients with rheumatoid arthritis treated with tumor necrosis factor- antagonist: a metaanalysis of both randomized controlled trials and registry/cohort studies. J Rheumatol 42(12):2229–2237. https://​doi.​org/​10.​3899/​jrheum.​150057 CrossRefPubMed
16.
21.
Zurück zum Zitat Kisacik B, Pamuk ON, Onat AM, Erer SB, Hatemi G, Ozguler Y, Pehlivan Y, Kilic L, Ertenli I, Can M, Direskeneli H, Keser G, Oksel F, Dalkilic E, Yilmaz S, Pay S, Balkarli A, Cobankara V, Cetin GY, Sayarlioglu M, Cefle A, Yazici A, Avci AB, Terzioglu E, Ozbek S, Akar S, Gul A (2016) Characteristics predicting tuberculosis risk under tumor necrosis factor-α inhibitors: report from a large multicenter cohort with high background prevalence. J Rheumatol 43(3):524–529. https://doi.org/10.3899/jrheum.150177 CrossRefPubMed Kisacik B, Pamuk ON, Onat AM, Erer SB, Hatemi G, Ozguler Y, Pehlivan Y, Kilic L, Ertenli I, Can M, Direskeneli H, Keser G, Oksel F, Dalkilic E, Yilmaz S, Pay S, Balkarli A, Cobankara V, Cetin GY, Sayarlioglu M, Cefle A, Yazici A, Avci AB, Terzioglu E, Ozbek S, Akar S, Gul A (2016) Characteristics predicting tuberculosis risk under tumor necrosis factor-α inhibitors: report from a large multicenter cohort with high background prevalence. J Rheumatol 43(3):524–529. https://​doi.​org/​10.​3899/​jrheum.​150177 CrossRefPubMed
24.
Zurück zum Zitat Rahman P, Choquette D, Bensen WG, Khraishi M, Chow A, Zummer M, Shaikh S, Sheriff M, Dixit S, Sholter D, Psaradellis E, Sampalis JS, Letourneau V, Lehman AJ, Nantel F, Rampakakis E, Otawa S, Shawi M (2016) Biologic treatment registry across Canada (BioTRAC): a multicentre, prospective, observational study of patients treated with infliximab for ankylosing spondylitis. BMJ Open 6(4):1–10. https://doi.org/10.1136/bmjopen-2015-009661 CrossRef Rahman P, Choquette D, Bensen WG, Khraishi M, Chow A, Zummer M, Shaikh S, Sheriff M, Dixit S, Sholter D, Psaradellis E, Sampalis JS, Letourneau V, Lehman AJ, Nantel F, Rampakakis E, Otawa S, Shawi M (2016) Biologic treatment registry across Canada (BioTRAC): a multicentre, prospective, observational study of patients treated with infliximab for ankylosing spondylitis. BMJ Open 6(4):1–10. https://​doi.​org/​10.​1136/​bmjopen-2015-009661 CrossRef
25.
Zurück zum Zitat Mourão AF, Santos MJ, Melo Gomes JA, Martins FM, Mendonça SC, Oliveira Ramos F, Fernandes S, Salgado M, Guedes M, Carvalho S, Costa JA, Brito I, Duarte C, Furtado C, Lopes A, Rodrigues A, Sequeira G, Branco JC, Fonseca JE, Canhão H (2016) Effectiveness and long-term retention of anti-tumour necrosis factor treatment in juvenile and adult patients with juvenile idiopathic arthritis: data from Reuma.pt. Pediatr Rheumatol Online J 55(4):697–703. https://doi.org/10.1093/rheumatology/kev398 CrossRef Mourão AF, Santos MJ, Melo Gomes JA, Martins FM, Mendonça SC, Oliveira Ramos F, Fernandes S, Salgado M, Guedes M, Carvalho S, Costa JA, Brito I, Duarte C, Furtado C, Lopes A, Rodrigues A, Sequeira G, Branco JC, Fonseca JE, Canhão H (2016) Effectiveness and long-term retention of anti-tumour necrosis factor treatment in juvenile and adult patients with juvenile idiopathic arthritis: data from Reuma.pt. Pediatr Rheumatol Online J 55(4):697–703. https://​doi.​org/​10.​1093/​rheumatology/​kev398 CrossRef
26.
Zurück zum Zitat Calzada-Hernández J, Anton-López J, Bou-Torrent R, Iglesias-Jiménez E, Ricart-Campos S, Martín de Carpi J, Carmen García de Vicuña Muñoz de la Nava, Torrente-Segarra V, Sánchez-Manubens J, Giménez-Roca C, Rozas-Quesada L, Juncosa-Morros MT, Fortuny C, Noguera-Julian A (2015) Tuberculosis in pediatric patients treated with anti-TNFα drugs: a cohort study. Pediatr Rheumatol Online J 13(1):54. https://doi.org/10.1186/s12969-015-0054-4 CrossRefPubMedPubMedCentral Calzada-Hernández J, Anton-López J, Bou-Torrent R, Iglesias-Jiménez E, Ricart-Campos S, Martín de Carpi J, Carmen García de Vicuña Muñoz de la Nava, Torrente-Segarra V, Sánchez-Manubens J, Giménez-Roca C, Rozas-Quesada L, Juncosa-Morros MT, Fortuny C, Noguera-Julian A (2015) Tuberculosis in pediatric patients treated with anti-TNFα drugs: a cohort study. Pediatr Rheumatol Online J 13(1):54. https://​doi.​org/​10.​1186/​s12969-015-0054-4 CrossRefPubMedPubMedCentral
28.
38.
Zurück zum Zitat He D, Bai F, Zhang S, Jiang T, Shen J et al (2013) High incidence of tuberculosis infection in rheumatic diseases and impact for chemoprophylactic prevention of tuberculosis activation during biologics therapy. Clin Vaccine Immunol 20(6):892–899. https://doi.org/10.1128/CVI.00049-13 CrossRef He D, Bai F, Zhang S, Jiang T, Shen J et al (2013) High incidence of tuberculosis infection in rheumatic diseases and impact for chemoprophylactic prevention of tuberculosis activation during biologics therapy. Clin Vaccine Immunol 20(6):892–899. https://​doi.​org/​10.​1128/​CVI.​00049-13 CrossRef
39.
48.
Zurück zum Zitat Titton DC, Silveira IG, Louzada-junior P et al (2011) Registro Brasileiro de Biológicos : preliminares do BiobadaBrasil. Rev Bras Reumatol 51(2):145–160 Titton DC, Silveira IG, Louzada-junior P et al (2011) Registro Brasileiro de Biológicos : preliminares do BiobadaBrasil. Rev Bras Reumatol 51(2):145–160
56.
Zurück zum Zitat Garcia-Vidal C, Rodríguez-Fernández S, Teijón S, Esteve M, Rodríguez-Carballeira M, Lacasa JM, Salvador G, Garau J (2009) Risk factors for opportunistic infections in infliximab-treated patients: the importance of screening in prevention. Eur J Clin Microbiol Infect Dis 28(4):331–337. https://doi.org/10.1007/s10096-008-0628-x CrossRefPubMed Garcia-Vidal C, Rodríguez-Fernández S, Teijón S, Esteve M, Rodríguez-Carballeira M, Lacasa JM, Salvador G, Garau J (2009) Risk factors for opportunistic infections in infliximab-treated patients: the importance of screening in prevention. Eur J Clin Microbiol Infect Dis 28(4):331–337. https://​doi.​org/​10.​1007/​s10096-008-0628-x CrossRefPubMed
59.
Zurück zum Zitat Takeuchi T, Tatsuki Y, Nogami Y, Ishiguro N, Tanaka Y, Yamanaka H, Kamatani N, Harigai M, Ryu J, Inoue K, Kondo H, Inokuma S, Ochi T, Koike T (2008) Postmarketing surveillance of the safety profile of infliximab in 5000 Japanese patients with rheumatoid arthritis. Ann Rheum Dis 67(2):189–194. https://doi.org/10.1136/ard.2007.072967 CrossRefPubMed Takeuchi T, Tatsuki Y, Nogami Y, Ishiguro N, Tanaka Y, Yamanaka H, Kamatani N, Harigai M, Ryu J, Inoue K, Kondo H, Inokuma S, Ochi T, Koike T (2008) Postmarketing surveillance of the safety profile of infliximab in 5000 Japanese patients with rheumatoid arthritis. Ann Rheum Dis 67(2):189–194. https://​doi.​org/​10.​1136/​ard.​2007.​072967 CrossRefPubMed
60.
Zurück zum Zitat Sichletidis L, Settas L, Spyratos D, Chloros D, Patakas D (2006) Tuberculosis in patients receiving anti-TNF agents despite chemoprophylaxis. Int J Tuberc Lung Dis 10(10):1127–1132PubMed Sichletidis L, Settas L, Spyratos D, Chloros D, Patakas D (2006) Tuberculosis in patients receiving anti-TNF agents despite chemoprophylaxis. Int J Tuberc Lung Dis 10(10):1127–1132PubMed
62.
Zurück zum Zitat Askling J, Fored CM, Brandt L, Baecklund E, Bertilsson L, Cöster L, Geborek P, Jacobsson LT, Lindblad S, Lysholm J, Rantapää-Dahlqvist S, Saxne T, Romanus V, Klareskog L, Feltelius N (2005) Risk and case characteristics of tuberculosis in rheumatoid arthritis associated with tumor necrosis factor antagonists in Sweden. Arthritis Rheum 52(7):1986–1992. https://doi.org/10.1002/art.21137 CrossRefPubMed Askling J, Fored CM, Brandt L, Baecklund E, Bertilsson L, Cöster L, Geborek P, Jacobsson LT, Lindblad S, Lysholm J, Rantapää-Dahlqvist S, Saxne T, Romanus V, Klareskog L, Feltelius N (2005) Risk and case characteristics of tuberculosis in rheumatoid arthritis associated with tumor necrosis factor antagonists in Sweden. Arthritis Rheum 52(7):1986–1992. https://​doi.​org/​10.​1002/​art.​21137 CrossRefPubMed
65.
Zurück zum Zitat Gómez-Reino JJ, Carmona L, Rodríguez Valverde V, Mola EM, Montero MD (2003) Treatment of rheumatoid arthritis with tumor necrosis factor inhibitors may predispose to significant increase in tuberculosis risk: a multicenter active-surveillance report. Arthritis Rheum 48(8):2122–2127. https://doi.org/10.1002/art.11137 CrossRefPubMed Gómez-Reino JJ, Carmona L, Rodríguez Valverde V, Mola EM, Montero MD (2003) Treatment of rheumatoid arthritis with tumor necrosis factor inhibitors may predispose to significant increase in tuberculosis risk: a multicenter active-surveillance report. Arthritis Rheum 48(8):2122–2127. https://​doi.​org/​10.​1002/​art.​11137 CrossRefPubMed
66.
Zurück zum Zitat Smolen JS, Schöls M, Braun J, Dougados M, FitzGerald O, Gladman DD, Kavanaugh A, Landewé R, Mease P, Sieper J, Stamm T, Wit M, Aletaha D, Baraliakos X, Betteridge N, Bosch FVD, Coates LC, Emery P, Gensler LS, Gossec L, Helliwell P, Jongkees M, Kvien TK, Inman RD, McInnes I, Maccarone M, Machado PM, Molto A, Ogdie A, Poddubnyy D, Ritchlin C, Rudwaleit M, Tanew A, Thio B, Veale D, Vlam K, van der Heijde D (2018) Treating axial spondyloarthritis and peripheral spondyloarthritis, especially psoriatic arthritis, to target: 2017 update of recommendations by an international task force. Ann Rheum Dis 77(1):3–17. https://doi.org/10.1136/annrheumdis-2017-211734 CrossRefPubMed Smolen JS, Schöls M, Braun J, Dougados M, FitzGerald O, Gladman DD, Kavanaugh A, Landewé R, Mease P, Sieper J, Stamm T, Wit M, Aletaha D, Baraliakos X, Betteridge N, Bosch FVD, Coates LC, Emery P, Gensler LS, Gossec L, Helliwell P, Jongkees M, Kvien TK, Inman RD, McInnes I, Maccarone M, Machado PM, Molto A, Ogdie A, Poddubnyy D, Ritchlin C, Rudwaleit M, Tanew A, Thio B, Veale D, Vlam K, van der Heijde D (2018) Treating axial spondyloarthritis and peripheral spondyloarthritis, especially psoriatic arthritis, to target: 2017 update of recommendations by an international task force. Ann Rheum Dis 77(1):3–17. https://​doi.​org/​10.​1136/​annrheumdis-2017-211734 CrossRefPubMed
Metadaten
Titel
Incidence of tuberculosis in patients receiving anti-TNF therapy for rheumatic diseases: a systematic review
verfasst von
Natália Sarzi Sartori
Nicole Pamplona Bueno de Andrade
Rafael Mendonça da Silva Chakr
Publikationsdatum
01.05.2020
Verlag
Springer London
Erschienen in
Clinical Rheumatology / Ausgabe 5/2020
Print ISSN: 0770-3198
Elektronische ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-019-04866-x

Weitere Artikel der Ausgabe 5/2020

Clinical Rheumatology 5/2020 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Echinokokkose medikamentös behandeln oder operieren?

06.05.2024 DCK 2024 Kongressbericht

Die Therapie von Echinokokkosen sollte immer in spezialisierten Zentren erfolgen. Eine symptomlose Echinokokkose kann – egal ob von Hunde- oder Fuchsbandwurm ausgelöst – konservativ erfolgen. Wenn eine Op. nötig ist, kann es sinnvoll sein, vorher Zysten zu leeren und zu desinfizieren. 

Umsetzung der POMGAT-Leitlinie läuft

03.05.2024 DCK 2024 Kongressbericht

Seit November 2023 gibt es evidenzbasierte Empfehlungen zum perioperativen Management bei gastrointestinalen Tumoren (POMGAT) auf S3-Niveau. Vieles wird schon entsprechend der Empfehlungen durchgeführt. Wo es im Alltag noch hapert, zeigt eine Umfrage in einem Klinikverbund.

Proximale Humerusfraktur: Auch 100-Jährige operieren?

01.05.2024 DCK 2024 Kongressbericht

Mit dem demographischen Wandel versorgt auch die Chirurgie immer mehr betagte Menschen. Von Entwicklungen wie Fast-Track können auch ältere Menschen profitieren und bei proximaler Humerusfraktur können selbst manche 100-Jährige noch sicher operiert werden.

Die „Zehn Gebote“ des Endokarditis-Managements

30.04.2024 Endokarditis Leitlinie kompakt

Worauf kommt es beim Management von Personen mit infektiöser Endokarditis an? Eine Kardiologin und ein Kardiologe fassen die zehn wichtigsten Punkte der neuen ESC-Leitlinie zusammen.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.