Tuberculosis infection in rheumatological patients receiving tumor necrosis factor – alpha inhibitors
https://doi.org/10.54921/2413-0346-2025-13-1-59-73
Abstract
Genetically engineered biological therapy has been widely introduced in the treatment of rheumatic diseases, lasting for decades until stable remission is achieved. Inhibitors of tumor necrosis factor alpha (TNF-α), a key cytokine, or its receptors are used to block autoimmune inflammation.
Interruption of cytokine cascade reactions can lead to defects in immune defense, inadequacy of new or destabilization of previously existing granulomas, and development of tuberculosis infection. Without screening procedures, the risks of tuberculosis increase significantly. In this regard, regular phthisiatric support is required for the entire period of therapy with TNF-α inhibitors.
The review examines in detail the role of TNF-α in the immunological response to tuberculosis, the effect of drugs that block this cytokine, the risks of developing tuberculosis when taking them in patients with rheumatological pathology, and the possibilities of reducing this risk through screening, monitoring, and preventive therapy.
About the Author
N. V. MakarovaRussian Federation
Moscow
References
1. Борисов С.Е., Лукина Г.В. Рекомендации по скринингу и мониторингу туберкулезной инфекции у больных, получающих генно-инженерные биологические препараты / клинические рекомендации [Электронный ресурс]. – 2018. – URL: https://www.rheumatolog.ru/experts/klinicheskie-rekomendacii/ (дата обращения 20.12.2024)
2. Борисов С.Е., Лукина Г.В., Слогоцкая Л.В., Кочетков Я.А., Гунтупова Л.Д. Куликовская Н.В. Скрининг и мониторинг туберкулезной инфекции у ревматологических больных, получающих генно-инженерные биологические препараты // Туберкулез и болезни легких. – 2011. – № 6. – С. 42-50.
3. Генно-инженерные биологические препараты в лечении ревматоидного артрита / под ред. Е.Л. Насонова. – М.: ИМА-ПРЕСС, 2013. – 549 с.
4. Диагностика туберкулезной инфекции при планировании и проведении терапии блокаторами ФНО-α (пособие для врачей) / под ред. акад. М.И. Перельмана и акад. Е.Л. Насонова. – М., 2008. – 40 С.
5. Зинина Е.П., Царенко С.В., Логунов Д.Ю. и др. Роль провоспалительных и противовоспалительных цитокинов при бактериальной пневмонии: обзор литературы //Вестник интенсивной терапии им. А.И. Салтанова. – 2021. – № 1. – С. 77-89. DOI: 10.21320/1818-474X-2021-1-77-89
6. Каратеев Д.Е. Вопросы безопасности терапии ингибиторами ФНО-а // Современная ревматология. – 2009. – № 3. – С. 33-37. – URL: https://cyberleninka.ru/article/n/voprosy-bezopasnosti-terapii-ingibitorami-fno-a (дата обращения: 29.03.2025).
7. Кочетков Я.А. Скрининг и мониторинг туберкулезной инфекции у ревматологических больных при лечении ингибиторами фактора некроза опухоли альфа: Дисс. ... канд. мед. наук. – М., 2012. – С. 129.
8. Кудлай Д. А. Биомаркеры и иммунологические тесты. Экспериментально-клинические параллели латентной туберкулезной инфекции // Туберкулез и болезни легких. – 2020. – Т. 98, № 8.– С. 63-74. http://doi.org/10.21292/2075-1230-2020-98-8-63-74
9. Лечение аутоиммунных заболеваний: продукция компании Biocad. URL: https://biocad.ru/products/autoimmune (дата обращения 23.12.2024)
10. Литвинов В.И. Латентная туберкулезная инфекция: свойства возбудителя; реакции макроорганизма; эпидемиология и диагностика (IGRA-тесты, Диаскинтест и другие подходы), лечение. – Москва: МНПЦ борьбы с туберкулезом, 2016. – 194 с.
11. Лукина Г.В., Сигидин Я.А., Насонов Е.Л. Применение инфликсимаба у больных ревматоидным артритом в клинической практике (по данным Российского регистра) // Терапевтический архив. – 2009. − № 8. – С. 15.
12. Муравьев Ю.В., Муравьева Л.А. Эволюция представлений о лекарственном туберкулезе при ревматоидном артрите // Научно-практическая ревматология. − 2010. – №2. − URL: https://cyberleninka.ru/article/n/evolyutsiya-predstavleniy-o-lekarstvennom-tuberkuleze-pri-revmatoidnom-artrite (дата обращения: 29.06.2023).
13. Постановление Главного государственного санитарного врача РФ от 28 января 2021 г. № 4 «Об утверждении санитарных правил и норм СанПиН 3.3686-21 «Санитарно-эпидемиологические требования по профилактике инфекционных болезней» (с изменениями и дополнениями): раздел VIII «Профилактика туберкулеза». URL: https://base.garant.ru/400342149/ (дата обращения 23.12.2024)
14. Приказ Министерства здравоохранения РФ от 21 марта 2017 г. № 124н «Об утверждении порядка и сроков проведения профилактических медицинских осмотров граждан в целях выявления туберкулеза» (с изменениями и дополнениями). URL: https://base.garant.ru/71688450/ (дата обращения 20.12.2024).
15. Салина Т.Ю. Значение фактора некроза опухолей в диагностике и течении туберкулезного процесса: Автореф. дисс... канд. мед. наук. – М., 1994. – 24 с.
16. Сартаева Г.Ш. Клинико-иммунологические особенности течения рецидивов туберкулеза органов дыхания у детей и подростков на современном этапе: Дисс. ... канд. мед. наук. – Алматы, 2010. – 86 с.
17. Справочник лекарственных средств Видаль. URL: https://www.vidal.ru/drugs/ (дата обращения 23.12.2024)
18. Терещенко И.В., Каюшев П.Е. Фактор некроза опухоли α и его роль в патологии // РМЖ. Медицинское обозрение. – 2022. – Т. 6, № 9. − С. 523-527. DOI: 10.32364/2587-6821-2022-6-9-523-527
19. Фролова К. С. Профилактика, выявление и лечение туберкулезной инфекции у больных с воспалительными заболеваниями кишечника на фоне лечения ингибиторами фактора некроза опухоли-альфа: Автореф. дисс. ... канд. мед. наук. – М., 2020. – 26 с.
20. Abitbol Y., Laharie D., Cosnes J., et al. GETAID. Negative screening does not rule out the risk of tuberculosis in patients with inflammatory bowel disease undergoing anti-TNF treatment: a descriptive study on the GETAID cohort // J Crohn’s Colitis. – 2016. – Vol. 10. – P. 1179-1185.
21. Acevedo-Vasquez E., Ponce de Leon D., Gamboa-Cardenas R. Latent infection and tuberculosis disease in rheumatoid arthritis patients // Rheum Dis Clin North Am. – 2009. – Vol. 35. – P. 163-71.
22. Aggarwal B.B., Gupta S.C., Kim J.H. Historical perspectives on tumor necrosis factor and its superfamily:25 years later, a golden journey // Blood. – 2012. – Vol.119, № 3. – Р. 651-665.
23. Antolín J., Azahara M., Hernández C., Blanco M., Mao L., Cigüenza R. Tuberculous peritonitis after treatment with adalimumab// Scand J Infect Dis. – 2008. – Vol. 40, № 8. – P. 677-8. doi: 10.1080/00365540701877320.
24. Azevedo V.F., Paiva E., Tosin T., et al. Splenic tuberculosis in a patient with ankylosing spondylitis treated with adalimumab // Reumatismo. – 2011. – Vol. 63, № 3. – Р. 171-4. doi: 10.4081/reumatismo.2011.171.
25. Azevedo V.F., Parchen C., Coelho S.A., Lacerda D.C., Hirth C.G. Tuberculous myositis in a patient with ankylosing spondylitis treated with adalimumab // Rheumatol Int. – 2009. – Vol. 29, № 11. – рР1381-4. doi: 10.1007/s00296-008-0837-8.
26. Balanescu A.R. et al. Tuberculosis in rheumatoid arthritis patients treated with infliximab — the Romanian experience// Arthr Rheum. – 2006. − Vol.54(Suppl. 9). – S405.
27. Bartalesi F., Vicidomini S., Goletti D. et al. QuantiFERON-TB Gold and the TST are both useful for latent tuberculosis infection screening in autoimmune diseases // European Respiratory Journal. – 2009. – Vol. 33, № 3. – P. 586-593.
28. Bekker L.G., Freeman S., Murray P.J., Ryffel B., Kaplan G. TNF-alpha controls intracellular mycobacterial growth by both inducible nitric oxide synthase-dependent and inducible nitric oxide synthase-independent pathways // J Immunol. – 2001. – Vol. 166. – P. 6728–34.
29. Blanco Pérez J.J., Aranda Torres A., Pego Reigosa J.M. et al. Tuberculosis pulmonar en relación con adalimumab: estudio de 3 casos [Pulmonary tuberculosis associated to adalimumab: a study of 3 cases] // Arch Bronconeumol. – 2010. – Vol. 46, №4. – Р. 203-5. doi: 10.1016/j.arbres.2009.07.007.
30. Brassard P., Lowe A.M., Bernatsky S. et al. Rheumatoid arthritis, its treatments, and the risk of tuberculosis in Quebec, Canada // Arthritis Rheum. – 2009. – Vol. 61, №3. – Р. 300-4. doi: 10.1002/art.24476.
31. Brehm T.T., Reimann M., Köhler N., Lange C. (Re-)introduction of TNF antagonists and JAK inhibitors in patients with previous tuberculosis: a systematic review // Clin Microbiol Infect. – 2024. – Vol. 30, № 8. – P. 989-998. doi: 10.1016/j.cmi.2024.04.011.
32. British Thoracic Society Standards of Care Committee. BTS recommendations for assessing risk and for managing Mycobacterium tuberculosis infection and disease in patients due to start anti-TNF-alpha treatment // Thorax. – 2005. – Vol. 60, №10: – Р. 800-5. doi: 10.1136/thx.2005.046797.
33. Brode S.K., Jamieson F.B., Ng R. et al. Increased risk of mycobacterial infections associated with anti-rheumatic medications // Thorax. – 2015ю – Vol. 70. – P. 677–682. pmid:25911222.
34. Cantini F., Nannini C., Niccoli L. et al. Guidance for the management of patients with latent tuberculosis infection requiring biologic therapy in rheumatology and dermatology clinical practice// Autoimmunity reviews. – 2015. – Vol. 14. – P. 503-509. pmid:25617816;
35. Capuano S.V., Croix D.A., Pawar S. et al. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection // Infect Immun. – 2003. – Vol. 71, №10. – P. 831-44. doi: 10.1128/IAI.71.10.5831-5844.2003.
36. Carmona L., Gómez-Reino J.J., Rodríguez-Valverde V. et al. Effectiveness of recommendations to prevent reactivation of latent tuberculosis infection in patients treated with tumor necrosis factor antagonists // Arthritis Rheum. – 2005. – Vol. 52, № 6. – P. 1766-72. doi: 10.1002/art.21043.
37. Carmona L., Hernandez-Garcia C., Vadillo C. et al. Increased risk of tuberculosis in patients with rheumatoid arthritis // J Rheumatol. – 2003. – Vol. 30. – P. 1436-9
38. Chen Y.H., Su W.J., Shen G.H. et al. Screening and management of tuberculosis infection in patients scheduled for tumor necrosis factor -alpha inhibitors: consensus recommendations from the Taiwan Rheumatology Association [Chinese] // Formosan Journal of Rheumatology. – 2012. – Vol. 26. – P. 8-14.
39. Cobelens F., Kik S., Esmail H. et al. From latent to patent: rethinking prediction of tuberculosis // Lancet Respir Med. – 2016. – URL: pii:S2213-2600(16)30419-2.
40. Consensus meeting report: development of a Target Product Profile (TPP) and a framework for evaluation for a test for predicting progression from tuberculosis infection to active disease. Geneva: World Health Organization; 2017 (WHO/HTM/TB/2017.18). - URL: https://apps.who.int/iris/bitstream/handle/10665/259176/WHO-HTM-TB-2017.18-eng.pdf
41. da Silva M. V. , Figueiredo A. A., Machado J. R. et al. T cell activation and proinflammatory cytokine production in clinically cured tuberculosis are time-dependent and accompanied by upregulation of IL-10 // PloS One. – 2013. – Vol. 8, № 6. – e65492.
42. Diel R., Hauer B., Loddenkemper R. et al. Recommendations for tuberculosis screening before initiation of TNF-alpha-inhibitor treatment in rheumatic diseases // Pneumologie. – 2009. – Vol. 63. – P. 329-34.
43. Ehlers S., Benini J., Kutsch S.et al. Fatal granuloma necrosis without exacerbated mycobacterial growth in tumor necrosis factor receptor p55 gene-deficient mice intravenously infected with Mycobacterium avium //Infect Immun. – 1999. – Vol. 67. – 3571-9.
44. Emery P., Fleischmann R.M., Moreland L.W. et al. Golimumab, a human anti-tumor necrosis factor alpha monoclonal antibody, injected subcutaneously every four weeks in methotrexate-naive patients with active rheumatoid arthritis: twenty-four-week results of a phase III, multicenter, randomized, double-blind, placebo-controlled study of golimumab before methotrexate as first-line therapy for early-onset rheumatoid arthritis // Arthritis Rheum. – 2009. – Vol. 60, №8. – Р. 2272-83. doi: 10.1002/art.24638.
45. Esmail H., Thienemann F., Oni T. et al. QuantiFERON conversion following tuberculin administration is common in HIV infection and relates to baseline response // BMC Infect Dis. – 2016. – Vol.16. – P. 545
46. Esmail H., Wilkinson R.J. Minimizing tuberculosis risk in patients receiving anti-TNF therapy // Ann Am Thorac Soc. – 2017. – Vol. 14, №5. – Р. 621-623. doi: 10.1513/AnnalsATS.201701-055ED. P
47. Evangelatos G., Koulouri V., Iliopoulos A., Fragoulis G.E. Tuberculosis and targeted synthetic or biologic DMARDs, beyond tumor necrosis factor inhibitors // Ther Adv Musculoskelet Dis. – 2020. – Vol. 22. – P. 12:1759720X20930116. doi: 10.1177/1759720X20930116.
48. Flynn J.L., Chan J. Immunology of tuberculosis // Annual review of immunology. – 2001. – Vol. 19. – P. 93–129. pmid:11244032
49. Flynn J.L., Chan J. What‘s good for the host is good for the bug // Trends Microbiol. – 2005. – Vol. 13, № 3. – Р. 98-102. doi: 10.1016/j.tim.2005.01.005.
50. Flynn J.L., Goldstein M.M., Chan J., et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice // Immunity. – 1995. – Vol. 2. – P. 561-72.
51. Fuller C.L., Flynn J..L, Reinhart T.A. In situ study of abundant expression of proinflammatory chemokines and cytokines in pulmonary granulomas that develop in cynomolgus macaques experimentally infected with Mycobacterium tuberculosis // Infect Immun. – 2003. – Vol. 71, № 12. – P. 7023-34. doi: 10.1128/IAI.71.12.7023-7034.2003.
52. Furst D.E., Keystone E.C., Kirkman B. et al. Updated consensus statement on biological agents for the treatment of rheumatic diseases //Ann Rheum Dis. – 2008. – Vol. 67. – P. iii2-25.
53. Genovese M. C., Cohen S., Moreland L. et al. Combination therapy with etanercept and anakinra in the treatment of patients with rheumatoid arthritis who have been treated unsuccessfully with methotrexate // Arthritis Rheum. – 2004. – Vol. 50. – P. 1412.
54. Gin A., Dolianitis C. Multidrug resistant miliary tuberculosis during infliximab therapy despite tuberculosis screening // Australas J Dermatol. – 2014. – Vol. 55, № 2. – Р. 140-1. doi: 10.1111/ajd.12053.
55. Goletti D., Petruccioli E., Romagnoli A., Piacentini M., Fimia G.M. Autophagy in Mycobacterium tuberculosis infection: a passepartout to flush the intruder out? //Cytokine Growth Factor Reviews. – 2013. – Vol. 24, № 4. – P. 335–343.
56. Gómez-Reino J.J., Carmona L., Angel Descalzo M. Biobadaser Group. Risk of tuberculosis in patients treated with tumor necrosis factor antagonists due to incomplete prevention of reactivation of latent infection // Arthritis Rheum. – 2007. – Vol. 57. – P. 756-761.
57. Gutiérrez-Macías A., Lizarralde-Palacios E., Martínez-Odriozola P., Miguel-de la Villa F. Tuberculous peritonitis in a patient with rheumatoid arthritis treated with adalimumab // Clin Rheumatol. – 2007. – Vol. 26, № 3. – P. 452-3. doi: 10.1007/s10067-005-0164-3.
58. Hou J.K., Kramer J.R., Richardson P., Sansgiry S., El-Serag H.B. Tuberculosis screening and reactivation among a national cohort of patients with i nflammatory bowel disease treated with tumor necrosis factor alpha antagonists // Inflamm Bowel Dis. – 2017. – Vol. 23. – P. 254–260.
59. Inanc N., Aydin S.Z., Karakurt S.et al. 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. – 2009. – Vol. 36. – P. 2675-81. https://doi.org/10.3899/jrheum.090268.
60. Jahnich N., Arkwright P.D. Regional risk of tuberculosis and viral hepatitis with tumor necrosis factor-alpha inhibitor treatment: A systematic review // Front Pharmacol. – 2023. – Vol. 14. – P. 1046306. doi: 10.3389/fphar.2023.1046306.
61. Keane J., Gershon S., Wise R.P. et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent // N Engl J Med. – 2001. – Vol. 345, № 15. – P. 1098-104. doi: 10.1056/NEJMoa011110.
62. Keane J., Remold H.G., Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages // J Immunol. – 2000. – Vol. 164. – P. 2016-20.
63. Keystone E., Heijde Dv., Mason D Jr. et al. Certolizumab pegol plus methotrexate is significantly more effective than placebo plus methotrexate in active rheumatoid arthritis: findings of a fifty-two-week, phase III, multicenter, randomized, double-blind, placebo-controlled, parallel-group study // Arthritis Rheum. –2008. – Vol. 58, №11. – P. 3319-29. doi: 10.1002/art.23964.
64. Khelghati F., Rahmanian M., Eghbal E. et al. Risk of tuberculosis disease in patients receiving TNF-α antagonist therapy: A meta-analysis of randomized controlled trials // New Microbes New Infect. – 2024. – Vol. 62. – P. 101533. doi: 10.1016/j.nmni.2024.101533.
65. Kim E.M., Uhm W.S., Bae S.C. et al. Incidence of tuberculosis among korean patients with ankylosing spondylitis who are taking tumor necrosis factor blockers // J Rheumatol. – 2011. – Vol. 38, № 10. – P. 2218-23. doi: 10.3899/jrheum.110373.
66. Kim E.S., Song G.A., Cho K.B. et al. Significant risk and associated factors of active tuberculosis infection in Korean patients with inflammatory bowel disease using anti-TNF agents // World J Gastroenterol. – 2015. – Vol. 21. – P. 3308–3316.
67. Kim H.A., Yoo C.D., Baek H.J. et al. Mycobacterium tuberculosis infection in a corticosteroid-treated rheumatic disease patient population // Clin Exp Rheumatol. – 1998. – Vol. 16, № 1. – P. 9-13.
68. Laffitte E., Janssens J.P., Roux-Lombard P. et al. Tuberculosis screening in patients with psoriasis before antitumour necrosis factor therapy: comparison of an interferon-γ release assay vs. tuberculin skin test // Br J Dermatol. – 2009. – Vol. 161. – P. 797-800. https://doi.org/10.1111/j.1365-2133.2009.09331
69. Lee J., Kim E., Jang E.J. et al. Efficacy of treatment for latent tuberculosis in patients undergoing treatment with a tumor necrosis factor antagonist // Ann Am Thorac Soc. – 2017. – Vol. 14. – P. 690-697.
70. Lee S.H. Diagnosis and treatment of latent tuberculosis infection // Tuberc Respir Dis (Seoul). – 2015. – Vol. 78. – P. 56–63.
71. Liao T.L., Lin C.H., Chen Y.M. et al. Different risk of tuberculosis and efficacy of isoniazid prophylaxis in rheumatoid arthritis patients with biologic therapy: a nationwide retrospective cohort study in Taiwan // PLoS One. – 2016. – Vol. 11, № 4. – e0153217. doi: 10.1371/journal.pone.0153217.
72. Lim C.H., Chen H.H., Chen Y.H. et al. The risk of tuberculosis disease in rheumatoid arthritis patients on biologics and targeted therapy: A 15-year real world experience in Taiwan // PLoS One. – 2017. – Vol. 12, № 6. – e0178035. doi: 10.1371/journal.pone.0178035.
73. Lin P.L., Plessner H.L., Voitenok N.N., Flynn J.L. Tumor necrosis factor and tuberculosis // J Investig Dermatol Symp Proc. – 2007. – Vol. 12, № 1. – P. 22-5. doi: 10.1038/sj.jidsymp.5650027.
74. Lin P.L., Flynn J.L. Understanding latent tuberculosis: a moving target // J. Immunol. – 2010. – Vol. 185. – P. 15-22.
75. Mahmoud I., Dridi L., Saidane O. et al. Latent tuberculosis screening and management before biologic agents instauration and risk of reactivation: the experience of an endemic tuberculosis country //Annals of the Rheumatic Diseases. – 2013. – Vol. 72. – A987-A988.
76. Mandic D., Curcic R., Radosavljevic G. et al. Recommendations for tuberculosis screening before and during treatment with tumour necrosis factor inhibitors // Srp Arh Celok Lek. – 2009. – Vol. 137. – P. 211-216
77. McCann F.E., Perocheau D.P., Ruspi G. et al. Selective tumor necrosis factor receptor I blockade is antiinflammatory and reveals an immunoregulatory role for tumor necrosis factor receptor II in collagen-induced arthritis // Arthritis Rheum. – 2014. – Vol. 66. – P. 2728
78. McInnes I.B., Schett G. The pathogenesis of rheumatoid arthritis // N Engl J Med. – 2011. – Vol. 365, № 23. – P. 2205-19. doi: 10.1056/NEJMra1004965.
79. Mirzaei A., Mahmoudi H. Evaluation of TNF-α cytokine production in patients with tuberculosis compared to healthy people // GMS Hyg Infect Control. – 2018. – Vol. 13. Doc09. DOI: 10.3205/dgkh000315
80. Mohan V.P. , Scanga C.A., Yu K. et al. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology // Infection and Immunity. – 2001. – Vol. 69, № 3. – P. 1847-1855.
81. Molenaar E.T., Bultink I.E., Dijkmans B.A., Lems W.F. Development of fatal tuberculosis in a patient with rheumatoid arthritis after three years of treatment with infliximab: comment on the article by Wolfe et al. // Arthritis Rheum. – 2005. – Vol. 52, № 4. – P. 1334-6. doi: 10.1002/art.20973.
82. Monaco C., Nanchahal J., Taylor P., Feldmann M. Anti-TNF therapy: past, present and future // Int Immunol. – 2015. – Vol. 27, № 1. – Р. 55-62. doi: 10.1093/intimm/dxu102.
83. NHS UK. Biological and biosimilar medicines (biosimilars). – URL: www.nhs.uk/conditions/biological-and-biosimilar-medicines (дата обращения 23.05.2024].
84. Oh J.H., Ham S.P., Park H.J. Disseminated tuberculosis in a psoriasis patient under adalimumab treatment despite the chemoprophylaxis of latent tuberculosis: a case report // Ann Dermatol. – 2021. – Vol. 33, № 1. – P. 77-81. doi: 10.5021/ad.2021.33.1.77.
85. Ponce de Leon D., Acevedo-Vasquez E., Alvizuri S. et al. Comparison of an interferon-gamma assay with tuberculin skin testing for detection of tuberculosis (TB) infection in patients with rheumatoid arthritis in a TB-endemic population // J Rheumatol. – 2008. – Vol. 35, №5. – P. 776-81.
86. Ponce de Leon D., Acevedo-Vasquez E., Sanchez-Torres A. Attenuated response to purified protein derivative in patients with rheumatoid arthritis: study in a population with a high prevalence of tuberculosis // Ann Rheum Dis. – 2005. – Vol. 64. – P. 1360-1.
87. Ramos S., Nogueira A., Dias A., Gonçalves A.F., Gaio A.R., Duarte R. Tuberculosis screening in patients receiving biological therapy // Acta Reumatologica Portuguesa. – 2015. – Vol. 40. – P. 234-240
88. Roach D.R., Bean A.G., Demangel C., France M.P., Briscoe H., Britton W.J. TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection // J Immunol. – 2002. – Vol. 168. – P. 4620-7.
89. Rotar Z., Svetina P., Tomsic M., Hočevar A, Prapotnik S. Tuberculosis among patients treated with TNF inhibitors for rheumatoid arthritis, ankylosing spondylitis and psoriatic arthritis in Slovenia: a cohort study // BMJ Open. – 2020. – Vol. 10, № 2. – e034356. doi: 10.1136/bmjopen-2019-034356.
90. Saag K.S., Teng G.G., Patkar N.M. et al. American College of Rheumatology 2008 Recommendations for the гse of nonbiologic and biologic diseasemodifying antirheumatic drugs in rheumatoid arthritis // Arthr Care and Research. – 2008. – Vol. 59. – P. 762-84.
91. Salvana E.M., Salata R.A. Infectious complications associated with monoclonal antibodies and related small molecules // Clin Microbiol Rev. – 2009. – Vol. 22, №2. – P. 274-90. doi: 10.1128/CMR.00040-08.
92. Sartori N. S., de Andrade N. P. B., da Silva Chakr R. M. Incidence of tuberculosis in patients receiving anti-TNF therapy for rheumatic diseases: A systematic review // Clin. Rheumatol. – 2020. – Vol. 39, № 5. – P. 1439-1447. 10.1007/s10067-019-04866-x.
93. Scallon B., Cai A., Solowski N. et al. Binding and functional comparisons of two types of tumor necrosis factor antagonists // J Pharmacol Exp Ther. – 2002. – Vol. 301, № 2. – P. 418-26. doi: 10.1124/jpet.301.2.418.
94. Scriba T.J., Fiore-Gartland A., Penn-Nicholson A. et al. CORTIS-01 Study Team. Biomarker-guided tuberculosis preventive therapy (CORTIS): a randomised controlled trial // Lancet Infect Dis. – 2021. – Vol. 21, № 3. – P. 354-365. doi: 10.1016/S1473-3099(20)30914-2.
95. Seong S.S., Choi C.B., Woo J.H. et al. Incidence of tuberculosis in Korean patients with rheumatoid arthritis (RA): effects of RA itself and of tumor necrosis factor blockers // J Rheumatol. – 2007. – Vol. 34, № 4. – P. 706-11.
96. Shim T.S. Diagnosis and treatment of latent tuberculosis infection due to initiation of anti-TNF therapy // Tuberc Respir Dis (Seoul). – 2014. – Vol. 76, № 6. – P. 261-8. doi: 10.4046/trd.2014.76.6.261.
97. Singanayagam A., Manalan K., Sridhar S. et al. Evaluation of screening methods for identification of patients with chronic rheumatological disease requiring tuberculosis chemoprophylaxis prior to commencement of TNF-α antagonist therapy // Thorax. – 2013. – Vol. 68. – P. 955–961
98. Smolen J.S., Landewé R.B., Mease P. et al. Efficacy and safety of certolizumab pegol plus methotrexate in active rheumatoid arthritis: the RAPID 2 study. A randomised controlled trial // Ann Rheum Dis. – 2009. – 68, № 6. – P. 797-804. doi: 10.1136/ard.2008.101659.
99. Soborg B., Ruhwald M., Hetland M.L. et al. Comparison of screening procedures for Mycobacterium tuberculosis infection among patients with inflammatory diseases // J Rheumatol. – 2009. – Vol. 36, № 9. – P. 1876-84. doi: 10.3899/jrheum.081292.
100. Solovic I., Sester M., Gomez-Reino J.J. et al. The risk of tuberculosis related to tumour necrosis factor antagonist therapies: a TBNET consensus statement // Eur Respir J. – 2010. – Vol. 36. – P. 1185-1206
101. Song X.Y., Fox F., Gallo M.A. et al. Effects of 2 different anti-tumor necrosis factor-alpha agents in a primate model of subcutaneous abscess formation // J Infect Dis. – 2002. – Vol. 185, 2. – P. 204-13. doi: 10.1086/338451.
102. Souto A., Maneiro J.R., Salgado E. et al. Risk of tuberculosis in patients with chronic immune-mediated inflammatory diseases treated with biologics and tofacitinib: a systematic review and meta-analysis of randomized controlled trials and long-term extension studies // Rheumatology (Oxford). – 2014. – Vol. 53. – P. 1872-1885.
103. Szeto T., Peterson J., Silva F. A case of tuberculous peritonitis in the United States in a patient with rheumatoid arthritis treated with adalimumab // J Clin Rheumatol. – 2010. – Vol. 16, № 3. – P. 135-7. doi: 10.1097/RHU.0b013e3181d56506.
104. Tubach F., Salmon D., Ravaud P. et al. Research axed on tolerance of biotherapies group. 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. – 2009. – Vol. 60, № 7. – P. 1884-94. doi: 10.1002/art.24632.
105. Vandiviere H.M., Loring W.E., Melvin I., Willis S. The treated pulmonary lesion and its tubercle bacillus. II. The death and resurrection // Am J Med Sci. – 1956. – Vol. 232, № 1. – P. 30-37. doi: 10.1097/00000441-195607000-00006.
106. Vassilopoulos D., Stamoulis N., Hadziyannis E., Archimandritis A.J. Usefulness of enzyme-linked immunospot assay (Elispot) compared to tuberculin skin testing for latent tuberculosis screening in rheumatic patients scheduled for anti-tumor necrosis factor treatment // J Rheumatol. – 2008. – Vol. 35, № 7. – P. 1271-6.
107. Vassilopoulos D., Tsikrika S., Hatzara C., et al. Comparison of two gamma interferon release assays and tuberculin skin testing for tuberculosis screening in a cohort of patients with rheumatic diseases starting anti-tumor necrosis factor therapy // Clin Vaccine Immunol. – 2011. – Vol. 18. – P. 2102-2108
108. Vonkeman H.E., van der Valk P.D., Mulder L., van de Laar M.A. Fatale miliaire tuberculose tijdens behandeling met infliximab [Fatal miliary tuberculosis during treatment with infliximab] // Ned Tijdschr Geneeskd. – 2002. – Vol. 146, № 25. – P. 1196-9.
109. Wallis R. S.Mathematical modeling of the cause of tuberculosis during tumor necrosis factor blockade // Arthritis Rheum. – 2008. – Vol. 58. – P. 947-952.
110. Weinblatt M., Schiff M., Goldman A. et al. Selective costimulation modulation using abatacept in patients with active rheumatoid arthritis while receiving etanercept: a randomised clinical trial // Ann. Rheum. Dis. – 2007. – Vol. 66. – P. 228.
111. Wejse C. Transcriptomic signatures have a place in short-term prediction of incident tuberculosis // Lancet Infect Dis. – 2021. – Vol. 21, №3. – P. 299-300. doi: 10.1016/S1473-3099(20)30980-4.
112. Winthrop K. L., Baxter R., Liu L., et al. Mycobacterial diseases and antitumour necrosis factor therapy in USA // Ann. Rheum. Dis. – 2013. – Vol. 72, № 1. – P. 37-42. 10.1136/annrheumdis-2011-200690
113. Wolfe F., Michaud K., Anderson J., Urbansky K. Tuberculosis infection in patients with rheumatoid arthritis and the effect of infliximab therapy. // Arthritis Rheum. – 2004. – Vol. 50, № 2. – P. 372-9. doi: 10.1002/art.20009.
114. World Health Organization (WHO) (2024). Global tuberculosis report 2024. Licence CC BY-NC-SA 3.0 IGO.
115. Xanthoulea S., Pasparakis M., Kousteni S. et al. Tumor necrosis factor (TNF) receptor shedding controls thresholds of innate immune activation that balance opposing TNF functions in infectious and inflammatory diseases //J. Exp. Med. – 2004. – Vol. 200. – P. 367
116. Xie X., Li F., Chen J.W., Wang J. Risk of tuberculosis infection in anti-TNF-alpha biological therapy: from bench to bedside. Journal of microbiology, immunology, and infection // Wei mian yu gan ran za zhi. – 2014. – Vol. 47. – P. 268-274. pmid:23727394
117. Yoo W.H. Multiple organ tuberculosis of lung, pleura, and peritoneum in ankylosing spondylitis during adalimumab therapy // Rheumatol Int. – 2012. – Vol. 32, № 3. – P. 787-90. doi: 10.1007/s00296-009-1357-x.
Review
For citations:
Makarova N.V. Tuberculosis infection in rheumatological patients receiving tumor necrosis factor – alpha inhibitors. Tuberculosis and socially significant diseases. 2025;13(1):59-73. (In Russ.) https://doi.org/10.54921/2413-0346-2025-13-1-59-73