Risk of Reactivation of Latent Tuberculosis in Psoriasis Patients on Biologic Therapies: A Retrospective Cohort from a Tertiary Care Centre in Northern Italy
DOI:
https://doi.org/10.2340/actadv.v102.1982Keywords:
tuberculosis, biologics, psoriasis, infectionsAbstract
Psoriatic patients with latent tuberculosis infection and properly treated active tuberculosis need careful management when prescribing modern biological drugs. Although data and guidelines regarding tumour necrosis factor-α inhibitors advise caution and initiation of prophylactic therapy in patients with latent tuberculosis infection, the same indications do not seem to find equal force for interleukin (IL)-23 and IL-17 inhibitors. In order to evaluate the risk of reactivation in patients with latent tuberculosis infection or properly treated active tuberculosis, an observational retrospective study was conducted on the population referred to our centre at Dermatologic Clinic of University of Turin, Italy. In the last 10 years at the clinic 19 psoriatic patients were found to be at risk of tuberculosis reactivation: 10 patients were QuantiFERON- TB-positive at baseline, 2 became positive during treatment, 6 reported prior tuberculous infection, and 1 was QuantiFERON-TB-negative at baseline and developed disseminated tuberculosis during treatment with anti-tumour necrosis factor-α. Overall, 10.5% of this group of patients developed active tuberculosis; however, stratifying by biologic therapy, zero cases were observed among patients treated with anti-IL-17, -23, or -12/23 over a relatively long follow-up (48.1 months) A review of the available literature following our experience confirms the increased risk of tuberculosis reactivation with tumour necrosis factor-α inhibitors. Concerning anti-IL-23 and IL-17 drugs, available data showed high safety in patients at risk of tuberculosis reactivation. Screening of patients who should be taking IL-17 and IL-23 inhibitors is recommended for public health purposes. In case of a positive result with these therapies, consulting with an infectious diseases specialist is suggested in order to weigh up the risks and benefits of prophylactic treatment.
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Dapavo P, Siliquini N, Mastorino L, Avallone G, Merli M, Agostini A, et al. Efficacy, safety, and drug survival of IL-23, IL-17, and TNF-alpha inhibitors for psoriasis treatment: a retrospective study. J Dermatolog Treat 2022; 33: 2352-2357.
https://doi.org/10.1080/09546634.2021.1961998 DOI: https://doi.org/10.1080/09546634.2021.1961998
Cariti C, Dapavo P, Mastorino L, Ortoncelli M, Siliquini N, Merli M, et al. Comparison of secukinumab and ixekizumab in psoriasis: a real-life cohort study on the efficacy and drug survival of 445 patients. J Eur Acad Dermatol Venereol 2022; 36: e233-e235.
https://doi.org/10.1111/jdv.17766 DOI: https://doi.org/10.1111/jdv.17766
Greb JE, Goldminz AM, Elder JT, Lebwohl MG, Gladman DD, Wu JJ, et al. Psoriasis. Nat Rev Dis Primers 2016; 2: 16082.
https://doi.org/10.1038/nrdp.2016.82 DOI: https://doi.org/10.1038/nrdp.2016.82
Nast A, Smith C, Spuls PI, Avila Valle G, Bata-Csörgö Z, Boonen H, et al. EuroGuiDerm guideline on the systemic treatment of psoriasis vulgaris - part 1: treatment and monitoring recommendations. J Eur Acad Dermatol Venereol 2020; 34: 2461-2498.
https://doi.org/10.1111/jdv.16915 DOI: https://doi.org/10.1111/jdv.16915
Solovan C, Chiticariu E. Psoriasis, anti-tumor necrosis factor therapy, and tuberculosis: report of three challenging cases and literature review. Infect Dis Ther 2013; 2: 59-73.
https://doi.org/10.1007/s40121-013-0003-9 DOI: https://doi.org/10.1007/s40121-013-0003-9
Ribero S, Licciardello M, Quaglino P, Dapavo P. Efficacy and safety of secukinumab in patients with plaque psoriasis and latent tuberculosis. Case Rep Dermatol 2019; 11: 23-28.
https://doi.org/10.1159/000501989 DOI: https://doi.org/10.1159/000501989
Nast A, Smith C, Spuls PI, Avila Valle G, Bata-Csörgö Z, Boonen H, et al. EuroGuiDerm guideline on the systemic treatment of psoriasis vulgaris - Part 2: specific clinical and comorbid situations. J Eur Acad Dermatol Venereol 2021; 35: 281-317.
https://doi.org/10.1111/jdv.16926 DOI: https://doi.org/10.1111/jdv.16926
Bassukas ID, Gaitanis G, Constantopoulos SH. Diagnosis of tuberculosis in patients with psoriasis: the need for a modified approach. Eur Respir J 2011; 38: 231-232; author reply 232-233.
https://doi.org/10.1183/09031936.00016611 DOI: https://doi.org/10.1183/09031936.00016611
Ahn CS, Dothard EH, Garner ML, Feldman SR, Huang WW. To test or not to test? An updated evidence-based assessment of the value of screening and monitoring tests when using systemic biologic agents to treat psoriasis and psoriatic arthritis. J Am Acad Dermatol 2015; 73: 420-428.e1.
https://doi.org/10.1016/j.jaad.2015.06.004 DOI: https://doi.org/10.1016/j.jaad.2015.06.004
Barry CE, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 2009; 7: 845-855.
https://doi.org/10.1038/nrmicro2236 DOI: https://doi.org/10.1038/nrmicro2236
Ernst JD. The immunological life cycle of tuberculosis. Nat Rev Immunol 2012; 12: 581-591.
https://doi.org/10.1038/nri3259 DOI: https://doi.org/10.1038/nri3259
Lin PL, Flynn JL. Understanding latent tuberculosis: a moving target. J Immunol 2010; 185: 15-22.
https://doi.org/10.4049/jimmunol.0903856 DOI: https://doi.org/10.4049/jimmunol.0903856
Sia JK, Rengarajan J. Immunology of mycobacterium tuberculosis infections. Microbiol Spectr 2019; 7: 10.1128/microbiolspec.GPP3-0022-2018.
https://doi.org/10.1128/microbiolspec.GPP3-0022-2018 DOI: https://doi.org/10.1128/microbiolspec.GPP3-0022-2018
Mohan VP, Scanga CA, Yu K, Scott HM, Tanaka KE, Tsang E, et al. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect Immun 2001; 69: 1847-1855.
https://doi.org/10.1128/IAI.69.3.1847-1855.2001 DOI: https://doi.org/10.1128/IAI.69.3.1847-1855.2001
Méndez-Samperio, P. Role of interleukin-12 family cytokines in the cellular response to mycobacterial disease. Int J Infect Dis 2010; 14: e366-371.
https://doi.org/10.1016/j.ijid.2009.06.022 DOI: https://doi.org/10.1016/j.ijid.2009.06.022
Khader SA, Cooper AM. IL-23 and IL-17 in tuberculosis. Cytokine 2008; 41: 79-83.
https://doi.org/10.1016/j.cyto.2007.11.022 DOI: https://doi.org/10.1016/j.cyto.2007.11.022
Ottenhoff THM, Verreck FAW, Lichtenauer-Kaligis EGR, Hoeve MA, Sanal O, van Dissel JT. Genetics, cytokines and human infectious disease: lessons from weakly pathogenic mycobacteria and salmonellae. Nat Genet 2002; 32: 97-105.
https://doi.org/10.1038/ng0902-97 DOI: https://doi.org/10.1038/ng0902-97
Cooper AM, Kipnis A, Turner J, Magram J, Ferrante J, Orme IM. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 P40 subunit is present. J Immunol 2002; 168: 1322-1327.
https://doi.org/10.4049/jimmunol.168.3.1322 DOI: https://doi.org/10.4049/jimmunol.168.3.1322
Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, Jelley-Gibbs DM, et al. IL-23 Compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses If IL-12p70 is available. J Immunol 2005; 175: 788-795.
https://doi.org/10.4049/jimmunol.175.2.788 DOI: https://doi.org/10.4049/jimmunol.175.2.788
Ogongo P, Tezera LB, Ardain A, Nhamoyebonde S, Ramsuran D, Singh A, et al. Tissue-resident-like CD4+ T cells secreting IL-17 control mycobacterium tuberculosis in the human lung. J Clin Invest 2021; 131: e142014.
https://doi.org/10.1172/JCI142014 DOI: https://doi.org/10.1172/JCI142014
Megna M, Ferrillo M, Ruggiero A, Cinelli E, Gallo L, Fabbrocini G. QuantiFERON TB-gold conversion rate among psoriasis patients under biologics: a 9-year retrospective study. Int J Dermatol 2021; 60: 352-357.
https://doi.org/10.1111/ijd.15217 DOI: https://doi.org/10.1111/ijd.15217
Gisondi P, Pezzolo E, Lo Cascio G, Girolomoni G. Latent tuberculosis infection in patients with chronic plaque psoriasis who are candidates for biological therapy. Br J Dermatol 2014; 171: 884-890.
https://doi.org/10.1111/bjd.13130 DOI: https://doi.org/10.1111/bjd.13130
Ting SW, Ting SY, Lin YS, Lin MS, Kuo G. Association between different systemic therapies and the risk of tuberculosis in psoriasis patients: a population-based study. Int J Clin Pract 2021; 12: e15006.
https://doi.org/10.1111/ijcp.15006 DOI: https://doi.org/10.1111/ijcp.15006
Hernandez C, Cetner AS, Jordan JE, Puangsuvan SN, Robinson JK. Tuberculosis in the age of biologic therapy. J Am Acad Dermatol 2008; 59: 363-380; quiz 382-384.
https://doi.org/10.1016/j.jaad.2008.05.033 DOI: https://doi.org/10.1016/j.jaad.2008.05.033
Souto A, Maneiro JR, Salgado E, Carmona L, Gomez-Reino JJ. 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; 53: 1872-1885.
https://doi.org/10.1093/rheumatology/keu172 DOI: https://doi.org/10.1093/rheumatology/keu172
Minozzi S, Bonovas S, Lytras T, Pecoraro V, González-Lorenzo M, Bastiampillai AJ, et al. Risk of infections using anti-TNF agents in rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis: a systematic review and meta-analysis. Expert Opin Drug Saf 2016; 15: 11-34.
https://doi.org/10.1080/14740338.2016.1240783 DOI: https://doi.org/10.1080/14740338.2016.1240783
Snast I, Bercovici E, Solomon-Cohen E, Avni T, Shitenberg D, Hodak E, et al. Active tuberculosis in patients with psoriasis receiving biologic therapy: a systematic review. Am J Clin Dermatol 2019; 20: 483-491.
https://doi.org/10.1007/s40257-019-00432-y DOI: https://doi.org/10.1007/s40257-019-00432-y
Lau CS, Chen YH, Lim K, de Longueville M, Arendt C, Winthrop K. Tuberculosis and viral hepatitis in patients treated with certolizumab pegol in Asia-Pacific countries and worldwide: real-world and clinical trial data. Clin Rheumatol 2021; 40: 867-875.
https://doi.org/10.1007/s10067-020-05248-4 DOI: https://doi.org/10.1007/s10067-020-05248-4
Dantes E, Tofolean DE, Fildan AP, Craciun L, Dumea E, Tofolean IT, et al. Lethal disseminated tuberculosis in patients under biological treatment - two clinical cases and a short review. J Int Med Res 2018; 46: 2961-2969.
https://doi.org/10.1177/0300060518771273 DOI: https://doi.org/10.1177/0300060518771273
Megna M, Ruggiero A, Ferrillo M, Fabbrocini G. QuantiFERON-TB Gold conversion is not uncommon in patients with psoriasis undergoing anti-tumour necrosis factor-α therapy. Br J Dermatol 2020; 183: 977-978.
https://doi.org/10.1111/bjd.19310 DOI: https://doi.org/10.1111/bjd.19310
Narcisi A, Bernardini N, Orsini D, D'Agostino M, De Felice C, Di Stefani A, et al. Long-term safety and efficacy of adalimumab in psoriasis: a multicentric study focused on infections (connecting study). Postepy Dermatol Alergol 2020; 37: 428-434.
https://doi.org/10.5114/ada.2020.96910 DOI: https://doi.org/10.5114/ada.2020.96910
Sánchez-Moya AI, Dauden E. Incidence of tuberculosis infection in psoriatic patients on anti-TNF therapy: report of a case series with 144 patients. J Eur Acad Dermatol Venereol 2011; 25: 730-733.
https://doi.org/10.1111/j.1468-3083.2010.03836.x DOI: https://doi.org/10.1111/j.1468-3083.2010.03836.x
Oh JH, Ham SP, Park HJ. Disseminated tuberculosis in a psoriasis patient under adalimumab treatment despite the chemoprophylaxis of latent tuberculosis: a case report. Ann Dermatol 2021; 33: 77-81.
https://doi.org/10.5021/ad.2021.33.1.77 DOI: https://doi.org/10.5021/ad.2021.33.1.77
Gori A, Fabroni C, Prignano F, Lotti T. Unusual presentation of tuberculosis in an infliximab-treated patient - which is the correct TB screening before starting a biologic? Dermatol Ther 2010; 23: S1-3.
https://doi.org/10.1111/j.1529-8019.2009.01278.x DOI: https://doi.org/10.1111/j.1529-8019.2009.01278.x
Tsai TF, Ho V, Song M, Szapary P, Kato T, Wasfi Y, et al. The safety of ustekinumab treatment in patients with moderate-to-severe psoriasis and latent tuberculosis infection. Br J Dermatol 2012; 167: 1145-1152.
https://doi.org/10.1111/j.1365-2133.2012.11142.x DOI: https://doi.org/10.1111/j.1365-2133.2012.11142.x
Lynch M, Roche L, Horgan M, Ahmad K, Hackett C, Ramsay B. Peritoneal tuberculosis in the setting of ustekinumab treatment for psoriasis. JAAD Case Rep 2017; 3: 230-232.
https://doi.org/10.1016/j.jdcr.2017.02.001 DOI: https://doi.org/10.1016/j.jdcr.2017.02.001
Errichetti E, Piccirillo A. Latent tuberculosis reactivation in a patient with erythrodermic psoriasis under treatment with ustekinumab and a low dose steroid, despite isoniazid chemoprophylaxis. Eur J Dermatol 2014; 24: 508-509.
https://doi.org/10.1684/ejd.2014.2386 DOI: https://doi.org/10.1684/ejd.2014.2386
Tsai TF, Chiu HY, Song M, Chan D. A case of latent tuberculosis reactivation in a patient treated with ustekinumab without concomitant isoniazid chemoprophylaxis in the PEARL trial. Br J Dermatol 2013; 168: 444-446.
https://doi.org/10.1111/j.1365-2133.2012.11162.x DOI: https://doi.org/10.1111/j.1365-2133.2012.11162.x
Hsiao CY, Chiu HY, Wang TS, Tsai TF. Serial QuantiFERON-TB Gold testing in patients with psoriasis treated with ustekinumab. PLoS One 2017; 12: e0184178.
https://doi.org/10.1371/journal.pone.0184178 DOI: https://doi.org/10.1371/journal.pone.0184178
Nogueira M, Warren RB, Torres T. Risk of tuberculosis reactivation with interleukin (IL)-17 and IL- 23 inhibitors in psoriasis - time for a paradigm change. J Eur Acad Dermatol Venereol 2021; 35: 824-834.
https://doi.org/10.1111/jdv.16866 DOI: https://doi.org/10.1111/jdv.16866
Shu D, Zhang Z, Zhou EY, Ma X, Zhao Y. Is chemoprophylaxis necessary for all latent tuberculosis infection patients receiving IL-17 inhibitors? A cohort study. Dermatol Ther 2020; 33: e14512.
https://doi.org/10.1111/dth.14512 DOI: https://doi.org/10.1111/dth.14512
Elewski BE, Baddley JW, Deodhar AA, Magrey M, Rich PA, Soriano ER, et al. Association of secukinumab treatment with tuberculosis reactivation in patients with psoriasis, psoriatic arthritis, or ankylosing spondylitis. JAMA Dermatol 2021; 157: 43-51.
https://doi.org/10.1001/jamadermatol.2020.3257 DOI: https://doi.org/10.1001/jamadermatol.2020.3257
Leonardi C, Reich K, Foley P, Torii H, Gerdes S, Guenther L, et al. Efficacy and safety of ixekizumab through 5 years in moderate-to-severe psoriasis: long-term results from the UNCOVER-1 and UNCOVER-2 phase-3 randomized controlled Trials. Dermatol Ther (Heidelb) 2020; 10: 431-447.
https://doi.org/10.1007/s13555-020-00367-x DOI: https://doi.org/10.1007/s13555-020-00367-x
Yamaguchi Y, Takatsu N, Ootaki K, Nakagawa H. Long-term safety of brodalumab in Japanese patients with plaque psoriasis: an open-label extension study. J Dermatol 2020; 47: 569-577.
https://doi.org/10.1111/1346-8138.15343 DOI: https://doi.org/10.1111/1346-8138.15343
Blauvelt A, Leonardi CL, Gooderham M, Papp KA, Philipp S, Wu JJ, et al. Efficacy and safety of continuous risankizumab therapy vs treatment withdrawal in patients with moderate to severe plaque psoriasis: a phase 3 randomized clinical trial. JAMA Dermatol 2020; 156: 649-658.
https://doi.org/10.1001/jamadermatol.2020.0723 DOI: https://doi.org/10.1001/jamadermatol.2020.0723
Sundbaum JK, Arkema EV, Bruchfeld J, Jonsson J, Askling J, Baecklund E. Tuberculosis in biologic- naïve patients with rheumatoid arthritis: risk factors and tuberculosis characteristics. J Rheumatol 2021; 48: 1243-1250.
https://doi.org/10.3899/jrheum.201251 DOI: https://doi.org/10.3899/jrheum.201251
Bassukas ID, Kosmidou M, Gaitanis G, Tsiouri G, Tsianos E. Patients with psoriasis are more likely to be treated for latent tuberculosis infection prior to biologics than patients with inflammatory bowel disease. Acta Derm Venereol 2011; 91: 444-446.
https://doi.org/10.2340/00015555-1106 DOI: https://doi.org/10.2340/00015555-1106
Balato N, Di Costanzo L, Ayala F, Balato A, Sanduzzi A, Bocchino M. Psoriatic disease and tuberculosis nowadays. Clin Dev Immunol 2012; 2012: 747204.
https://doi.org/10.1155/2012/747204 DOI: https://doi.org/10.1155/2012/747204
Bordignon V, Bultrini S, Prignano G, Sperduti I, Piperno G, Bonifati C, et al. High prevalence of latent tuberculosis infection in autoimmune disorders such as psoriasis and in chronic respiratory diseases, including lung cancer. J Biol Regul Homeost Agents 2011; 25: 213-220.
Chen YJ, Wu CY, Shen JL, Chen TT, Chang YT. Association between traditional systemic antipsoriatic drugs and tuberculosis risk in patients with psoriasis with or without psoriatic arthritis: results of a nationwide cohort study from Taiwan. J Am Acad Dermatol 2013; 69: 25-33.
https://doi.org/10.1016/j.jaad.2012.12.966 DOI: https://doi.org/10.1016/j.jaad.2012.12.966
Filoni A, Vestita M, Congedo M, Giudice G, Tafuri S, Bonamonte D. Association between psoriasis and vitamin D: duration of disease correlates with decreased vitamin D serum levels: an observational case-control study. Medicine (Baltimore) 2018; 97: e11185.
https://doi.org/10.1097/MD.0000000000011185 DOI: https://doi.org/10.1097/MD.0000000000011185
Talat N, Perry S, Parsonnet J, Dawood G, Hussain R. Vitamin D deficiency and tuberculosis progression. Emerg Infect Dis 2010; 16: 853-855.
https://doi.org/10.3201/eid1605.091693 DOI: https://doi.org/10.3201/eid1605.091693
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