Advertisement

Clinical Rheumatology

, Volume 30, Issue 12, pp 1535–1541 | Cite as

Interferon-γ release assay in the diagnosis of latent tuberculosis infection in arthritis patients treated with tumor necrosis factor antagonists in Korea

  • Boksoon Chang
  • Hye Yun Park
  • Kyeongman Jeon
  • Joong Kyong Ahn
  • Hoon-Suk Cha
  • Eun-Mi Koh
  • Eun-Suk Kang
  • Won-Jung Koh
Original Article

Abstract

The aim of this study was to evaluate the usefulness of the interferon-γ release assay (IGRA) for the diagnosis of latent tuberculosis infection (LTBI) in arthritis patients who received tumor necrosis factor (TNF) antagonist in Korea. The study involved 107 consecutive patients: 61 (57%) with ankylosing spondylitis and 46 (43%) with rheumatoid arthritis. Screening tests were performed including the tuberculin skin test (TST), the QuantiFERON-TB Gold In-Tube (QFT-IT) test, and chest radiography. A positive QFT-IT test result, regardless of TST results, was considered an indication for LTBI treatment. If the QFT-IT results were indeterminate, a positive TST was regarded as an indication for LTBI treatment. A Bacillus Calmette-Guérin (BCG) scar was found in 63 patients (59%). LTBI treatment was performed in 37 patients (35%), including 36 with positive QFT-IT results and one with indeterminate QFT-IT and positive TST results. No patients developed tuberculosis during a median of 18 months (range, 13–26 months) of TNF antagonist therapy. In 16 patients who had positive TST and negative QFT-IT results, TNF antagonists were given without LTBI treatment. Tuberculosis did not occur, even in these patients, during a median of 24.5 months (range, 15–33.5 months) of TNF antagonist therapy. IGRA may be used instead of TST for the diagnosis of LTBI in patients before starting TNF antagonists in countries where tuberculosis prevalence is intermediate and the BCG vaccination is mandatory at birth, such as in Korea.

Keywords

Ankylosing spondylitis Latent tuberculosis Rheumatoid arthritis Tuberculin test Tumor necrosis factor-alpha 

Notes

Acknowledgments

This work was supported by IN-SUNG Foundation for Medical Research (CA98051). We thank Ms. Sook Young Woo, statistician, Biostatistics Unit, Samsung Biomedical Research Institute, for assistance in the statistical analysis.

Disclosures

None.

References

  1. 1.
    Lipsky PE, van der Heijde DM, St Clair EW, Furst DE, Breedveld FC, Kalden JR, Smolen JS, Weisman M, Emery P, Feldmann M, Harriman GR, Maini RN (2000) Infliximab and methotrexate in the treatment of rheumatoid arthritis. Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. N Engl J Med 343:1594–1602PubMedCrossRefGoogle Scholar
  2. 2.
    Keat A, Barkham N, Bhalla A, Gaffney K, Marzo-Ortega H, Paul S, Rogers F, Somerville M, Sturrock R, Wordsworth P (2005) BSR guidelines for prescribing TNF-α blockers in adults with ankylosing spondylitis. Report of a working party of the British Society for Rheumatology. Rheumatology (Oxford) 44:939–947CrossRefGoogle Scholar
  3. 3.
    Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, Siegel JN, Braun MM (2001) Tuberculosis associated with infliximab, a tumor necrosis factor α-neutralizing agent. N Engl J Med 345:1098–1104PubMedCrossRefGoogle Scholar
  4. 4.
    Gomez-Reino JJ, Carmona L, Valverde VR, 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 48:2122–2127PubMedCrossRefGoogle Scholar
  5. 5.
    Askling J, Fored CM, Brandt L, Baecklund E, Bertilsson L, Coster L, Geborek P, Jacobsson LT, Lindblad S, Lysholm J, Rantapaa-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 52:1986–1992PubMedCrossRefGoogle Scholar
  6. 6.
    Carmona L, Gomez-Reino JJ, Rodriguez-Valverde V, Montero D, Pascual-Gomez E, Mola EM, Carreno L, Figueroa M (2005) Effectiveness of recommendations to prevent reactivation of latent tuberculosis infection in patients treated with tumor necrosis factor antagonists. Arthritis Rheum 52:1766–1772PubMedCrossRefGoogle Scholar
  7. 7.
    Furst DE, Keystone EC, Fleischmann R, Mease P, Breedveld FC, Smolen JS, Kalden JR, Braun J, Bresnihan B, Burmester GR, De Benedetti F, Dorner T, Emery P, Gibofsky A, Kavanaugh A, Kirkham B, Schiff MH, Sieper J, Singer N, Van Riel PL, Weinblatt ME, Weisman MH, Winthrop K (2010) Updated consensus statement on biological agents for the treatment of rheumatic diseases, 2009. Ann Rheum Dis 69(Suppl 1):i2–i29PubMedCrossRefGoogle Scholar
  8. 8.
    Solovic I, Sester M, Gomez-Reino JJ, Rieder HL, Ehlers S, Milburn HJ, Kampmann B, Hellmich B, Groves R, Schreiber S, Wallis RS, Sotgiu G, Scholvinck EH, Goletti D, Zellweger JP, Diel R, Carmona L, Bartalesi F, Ravn P, Bossink A, Duarte R, Erkens C, Clark J, Migliori GB, Lange C (2010) The risk of tuberculosis related to tumour necrosis factor antagonist therapies: a TBNET consensus statement. Eur Respir J 36:1185–1206PubMedCrossRefGoogle Scholar
  9. 9.
    Mariette X, Salmon D (2003) French guidelines for diagnosis and treating latent and active tuberculosis in patients with RA treated with TNF blockers. Ann Rheum Dis 62:791PubMedCrossRefGoogle Scholar
  10. 10.
    British Thoracic Society Standards of Care Committee (2005) BTS recommendations for assessing risk and for managing Mycobacterium tuberculosis infection and disease in patients due to start anti-TNF-α treatment. Thorax 60:800–805CrossRefGoogle Scholar
  11. 11.
    Fonseca JE, Canhao H, Silva C, Miguel C, Mediavilla MJ, Teixeira A, Castelao W, Nero P, Bernardes M, Bernardo A, Mariz E, Godinho F, Santos MJ, Bogas M, Oliveira M, Saavedra MJ, Barcelos A, Cruz M, Santos RA, Mauricio L, Rodrigues M, Figueiredo G, Quintal A, Patto JV, Malcata A, da Silva JC, Araujo D, Ventura F, Branco J, Queiroz MV (2006) Tuberculosis in rheumatic patients treated with tumour necrosis factor alpha antagonists: the Portuguese experience. Acta Reumatol Port 31:247–253PubMedGoogle Scholar
  12. 12.
    Kavanagh PM, Gilmartin JJ, O'Donnell J, O'Flanagan D (2008) Tumour necrosis factor-α and tuberculosis: guidance from the National TB Advisory Committee. Ir Med J 101:6–7PubMedGoogle Scholar
  13. 13.
    Ponce de Leon D, Acevedo-Vasquez E, Sanchez-Torres A, Cucho M, Alfaro J, Perich R, Pastor C, Harrison J, Sanchez-Schwartz C (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 64:1360–1361PubMedCrossRefGoogle Scholar
  14. 14.
    Pai M, Zwerling A, Menzies D (2008) Systematic review: T-cell-based assays for the diagnosis of latent tuberculosis infection: an update. Ann Intern Med 149:177–184PubMedGoogle Scholar
  15. 15.
    Mori T (2009) Usefulness of interferon-gamma release assays for diagnosing TB infection and problems with these assays. J Infect Chemother 15:143–155PubMedCrossRefGoogle Scholar
  16. 16.
    Diel R, Goletti D, Ferrara G, Bothamley G, Cirillo D, Kampmann B, Lange C, Losi M, Markova R, Migliori GB, Nienhaus A, Ruhwald M, Wagner D, Zellweger JP, Huitric E, Sandgren A, Manissero D (2011) Interferon-γ release assays for the diagnosis of latent Mycobacterium tuberculosis infection: a systematic review and meta-analysis. Eur Respir J 37:88–99PubMedCrossRefGoogle Scholar
  17. 17.
    Sellam J, Hamdi H, Roy C, Baron G, Lemann M, Puechal X, Breban M, Berenbaum F, Humbert M, Weldingh K, Salmon D, Ravaud P, Emilie D, Mariette X (2007) Comparison of in vitro-specific blood tests with tuberculin skin test for diagnosis of latent tuberculosis before anti-TNF therapy. Ann Rheum Dis 66:1610–1615PubMedCrossRefGoogle Scholar
  18. 18.
    Ponce de Leon D, Acevedo-Vasquez E, Alvizuri S, Gutierrez C, Cucho M, Alfaro J, Perich R, Sanchez-Torres A, Pastor C, Sanchez-Schwartz C, Medina M, Gamboa R, Ugarte M (2008) Comparison of an interferon-γ assay with tuberculin skin testing for detection of tuberculosis (TB) infection in patients with rheumatoid arthritis in a TB-endemic population. J Rheumatol 35:776–781PubMedGoogle Scholar
  19. 19.
    Matulis G, Juni P, Villiger PM, Gadola SD (2008) Detection of latent tuberculosis in immunosuppressed patients with autoimmune diseases: performance of a Mycobacterium tuberculosis antigen-specific interferon γ assay. Ann Rheum Dis 67:84–90PubMedCrossRefGoogle Scholar
  20. 20.
    Diel R, Hauer B, Loddenkemper R, Manger B, Kruger K (2009) Recommendations for tuberculosis screening before initiation of TNF-α-inhibitor treatment in rheumatic diseases. Pneumologie 63:329–334PubMedCrossRefGoogle Scholar
  21. 21.
    Beglinger C, Dudler J, Mottet C, Nicod L, Seibold F, Villiger PM, Zellweger JP (2007) Screening for tuberculosis infection before the initiation of an anti-TNF-α therapy. Swiss Med Wkly 137:620–622PubMedGoogle Scholar
  22. 22.
    Bartalesi F, Vicidomini S, Goletti D, Fiorelli C, Fiori G, Melchiorre D, Tortoli E, Mantella A, Benucci M, Girardi E, Cerinic MM, Bartoloni A (2009) QuantiFERON-TB Gold and the TST are both useful for latent tuberculosis infection screening in autoimmune diseases. Eur Respir J 33:586–593PubMedCrossRefGoogle Scholar
  23. 23.
    Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324PubMedCrossRefGoogle Scholar
  24. 24.
    van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 27:361–368PubMedCrossRefGoogle Scholar
  25. 25.
    Yun JW, Lim SY, Suh GY, Chung MP, Kim H, Kwon OJ, Cha HS, Koh EM, Koh WJ (2007) Diagnosis and treatment of latent tuberculosis infection in arthritis patients treated with tumor necrosis factor antagonists in Korea. J Korean Med Sci 22:779–783PubMedCrossRefGoogle Scholar
  26. 26.
    Comstock GW, Edwards LB, Philip RN, Winn WA (1964) A comparison in the United States of America of two tuberculins, Ppd-S and Rt 23. Bull World Health Organ 31:161–170PubMedGoogle Scholar
  27. 27.
    Rieder HL, Chadha VK, Nagelkerke NJ, van Leth F, van der Werf MJ (2011) Guidelines for conducting tuberculin skin test surveys in high-prevalence countries. Int J Tuberc Lung Dis 15(Suppl 1):S1–S25PubMedGoogle Scholar
  28. 28.
    Fleiss J (1981) Statistical methods for rates and proportions. Wiley, New York, pp 212–236Google Scholar
  29. 29.
    Valesini G, Montecucco C, Cutolo M (2006) Recommendations for the use of biologic (TNF-α blocking) agents in the treatment of rheumatoid arthritis in Italy. Clin Exp Rheumatol 24:413–423PubMedGoogle Scholar
  30. 30.
    Shovman O, Anouk M, Vinnitsky N, Arad U, Paran D, Litinsky I, Caspi D, Elkayam O (2009) QuantiFERON-TB Gold in the identification of latent tuberculosis infection in rheumatoid arthritis: a pilot study. Int J Tuberc Lung Dis 13:1427–1432PubMedGoogle Scholar
  31. 31.
    Soborg B, Ruhwald M, Hetland ML, Jacobsen S, Andersen AB, Milman N, Thomsen VO, Jensen DV, Koch A, Wohlfahrt J, Ravn P (2009) Comparison of screening procedures for Mycobacterium tuberculosis infection among patients with inflammatory diseases. J Rheumatol 36:1876–1884PubMedCrossRefGoogle Scholar
  32. 32.
    Diel R, Loddenkemper R, Niemann S, Meywald-Walter K, Nienhaus A (2011) Negative and positive predictive value of a whole-blood interferon-γ release assay for developing active tuberculosis: an update. Am J Respir Crit Care Med 183:88–95PubMedCrossRefGoogle Scholar
  33. 33.
    Brock I, Ruhwald M, Lundgren B, Westh H, Mathiesen LR, Ravn P (2006) Latent tuberculosis in HIV positive, diagnosed by the M. tuberculosis specific interferon-gamma test. Respir Res 7:56PubMedCrossRefGoogle Scholar
  34. 34.
    Ferrara G, Losi M, Meacci M, Meccugni B, Piro R, Roversi P, Bergamini BM, D'Amico R, Marchegiano P, Rumpianesi F, Fabbri LM, Richeldi L (2005) Routine hospital use of a new commercial whole blood interferon-γ assay for the diagnosis of tuberculosis infection. Am J Respir Crit Care Med 172:631–635PubMedCrossRefGoogle Scholar
  35. 35.
    Kobashi Y, Sugiu T, Mouri K, Obase Y, Miyashita N, Oka M (2009) Indeterminate results of QuantiFERON TB-2 G test performed in routine clinical practice. Eur Respir J 33:812–815PubMedCrossRefGoogle Scholar
  36. 36.
    Inanc N, Aydin SZ, Karakurt S, Atagunduz P, Yavuz S, Direskeneli H (2009) Agreement between Quantiferon-TB gold test and tuberculin skin test in the identification of latent tuberculosis infection in patients with rheumatoid arthritis and ankylosing spondylitis. J Rheumatol 36:2675–2681PubMedCrossRefGoogle Scholar

Copyright information

© Clinical Rheumatology 2011

Authors and Affiliations

  • Boksoon Chang
    • 1
  • Hye Yun Park
    • 1
  • Kyeongman Jeon
    • 1
  • Joong Kyong Ahn
    • 2
  • Hoon-Suk Cha
    • 2
  • Eun-Mi Koh
    • 2
  • Eun-Suk Kang
    • 3
  • Won-Jung Koh
    • 1
  1. 1.Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea
  2. 2.Division of Rheumatology, Department of Medicine, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea
  3. 3.Department of Laboratory Medicine and Genetics, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea

Personalised recommendations