The risk of deep fungal infections during biologic therapy for psoriasis

Journal of the European Academy of Dermatology and Venereology

Volumn 28, Issue 10, 2014, Pages 1277-1285

  Jourabchi, N ^a,b   Adelzadeh, L ^b   Wu, J J ^c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c KAISER PERMANENTE MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; ALEFACEPT; AMPHOTERICIN B; ANTIPSORIASIS AGENT; CEFALEXIN; CREATININE; EFALIZUMAB; ETANERCEPT; FLUCONAZOLE; GRISEOFULVIN; INFLIXIMAB; METHOTREXATE; METRONIDAZOLE; PREDNISONE; USTEKINUMAB; IMMUNOLOGIC FACTOR;

ADOLESCENT; ADULT; CASE REPORT; COMPUTER ASSISTED TOMOGRAPHY; CREATININE BLOOD LEVEL; DEEP FUNGAL INFECTION; DRUG SAFETY; FEMALE; FOLLOW UP; HISTOPLASMA CAPSULATUM; HUMAN; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; INCIDENCE; MALE; MYCOSIS; PATHOGENESIS; PREVALENCE; PSORIASIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; TREATMENT DURATION; BIOLOGICAL THERAPY; MYCOSES; PROGNOSIS;

BIOLOGICAL THERAPY; HUMANS; IMMUNOLOGIC FACTORS; INCIDENCE; MYCOSES; PROGNOSIS; PSORIASIS; RISK FACTORS;

EID: 84908099429     PISSN: 09269959     EISSN: 14683083     Source Type: Journal    
DOI: 10.1111/jdv.12508     Document Type: Review

References (74)

1. Shear NH,. Fulfilling an unmet need in psoriasis: do biologicals hold the key to improved tolerability? Drug Saf 2006; 29: 49-66.
2. Balato N, Di Costanzo L, Ayala F, Balato A, Sanduzzi A, Bocchino M,. Psoriatic disease and tuberculosis nowadays. Clin Dev Immunol 2012; 2012: 747204.
3. Lee JH, Slifman NR, Gershon SK, et al,. Life-threatening histoplasmosis complicating immunotherapy with tumor necrosis factor alpha antagonists infliximab and etanercept. Arthritis Rheum 2002; 46: 2565-2570.
4. FDA. U.S. Food and Drug Administration: Postmarket Drug Safety Information for Patients and Providers-Information for Healthcare Professionals: Cimzia (certolizumab pegol), Enbrel (etanercept), Humira (adalimumab), and Remicade (infliximab). Silver Spring, MD: U.S. Food and Drug Administration; 2010 [updated 1/25/10; cited 2012 Dec. 9]; Available at: http://www.fda.gov/Drugs/DrugSafety/PostmarketDrugSafetyInformationforPatientsandProviders/ucm124185.htm (last accessed: 12 September 2012).
5. Bordignon V, Bultrini S, Prignano G, 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.
6. Ramagopalan SV, Goldacre R, Skingsley A, Conlon C, Goldacre MJ,. Associations between selected immune-mediated diseases and tuberculosis: record-linkage studies. BMC Med 2013; 11: 97.
7. Tsai TF, Wang TS, Hung ST, et al,. Epidemiology and comorbidities of psoriasis patients in a national database in Taiwan. J Dermatol Sci 2011; 63: 40-46.
8. Wakkee M, de Vries E, van den Haak P, Nijsten T,. Increased risk of infectious disease requiring hospitalization among patients with psoriasis: a population-based cohort. J Am Acad Dermatol 2011; 65: 1135-1144.
9. Salmon-Ceron D, Tubach F, Lortholary O, et al,. Drug-specific risk of non-tuberculosis opportunistic infections in patients receiving anti-TNF therapy reported to the 3-year prospective French RATIO registry. Ann Rheum Dis 2011; 70: 616-623.
10. Tsiodras S, Samonis G, Boumpas DT, Kontoyiannis DP,. Fungal infections complicating tumor necrosis factor alpha blockade therapy. Mayo Clin Proc 2008; 83: 181-194.
11. Algood HM, Lin PL, Flynn JL,. Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis. Clin Infect Dis 2005; 1 (41 Suppl 3): S189-S193.
12. Arnold TM, Sears CR, Hage CA,. Invasive fungal infections in the era of biologics. Clin Chest Med 2009; 30: 279-286, vi.
13. Krulig E, Gordon KB,. Ustekinumab: an evidence-based review of its effectiveness in the treatment of psoriasis. Core Evid 2010; 5: 11-22.
14. Koutruba N, Emer J, Lebwohl M,. Review of ustekinumab, an interleukin-12 and interleukin-23 inhibitor used for the treatment of plaque psoriasis. Ther Clin Risk Manag 2010; 6: 123-141.
15. Kagami S, Rizzo HL, Kurtz SE, Miller LS, Blauvelt A,. IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans. J Immunol 2010; 185: 5453-5462.
16. REMICADE (infliximab). Remicade (infliximab) Full Prescribing Information. In, Janssen Biotech I, ed. Janssen Biotech, Inc., Horsham, PA, 2013: 1-18.
17. ENBREL(etanercept). Enbrel (etanercept) Prescribing Information. In, Corporation I, ed. Amgen Inc and Pfizer Inc, Thousand Oaks, CA, 2012: 1-29.
18. Kerensky TA, Gottlieb AB, Yaniv S, Au SC,. Etanercept: efficacy and safety for approved indications. Expert Opin Drug Saf 2012; 11: 121-139.
19. Bagel J, Lynde C, Tyring S, Kricorian G, Shi Y, Klekotka P,. Moderate to severe plaque psoriasis with scalp involvement: a randomized, double-blind, placebo-controlled study of etanercept. J Am Acad Dermatol 2012; 67: 86-92.
20. Leonardi CL, Powers JL, Matheson RT, et al,. Etanercept as monotherapy in patients with psoriasis. N Engl J Med 2003; 349: 2014-2022.
21. Tyring S, Gottlieb A, Papp K, et al,. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet 2006; 367: 29-35.
22. van de Kerkhof PC, Segaert S, Lahfa M, et al,. Once weekly administration of etanercept 50 mg is efficacious and well tolerated in patients with moderate-to-severe plaque psoriasis: a randomized controlled trial with open-label extension. Br J Dermatol 2008; 159: 1177-1185.
23. Gottlieb AB, Matheson RT, Lowe N, et al,. A randomized trial of etanercept as monotherapy for psoriasis. Arch Dermatol. 2003; 139: 1627-1632. discussion 32.
24. Yang HZ, Wang K, Jin HZ, et al,. Infliximab monotherapy for Chinese patients with moderate to severe plaque psoriasis: a randomized, double-blind, placebo-controlled multicenter trial. Chin Med J (Engl) 2012; 125: 1845-1851.
25. Chaudhari U, Romano P, Mulcahy LD, Dooley LT, Baker DG, Gottlieb AB,. Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial. Lancet 2001; 357: 1842-1847.
26. Gottlieb AB, Evans R, Li S, et al,. Infliximab induction therapy for patients with severe plaque-type psoriasis: a randomized, double-blind, placebo-controlled trial. J Am Acad Dermatol 2004; 51: 534-542.
27. Reich K, Nestle FO, Papp K, et al,. Infliximab induction and maintenance therapy for moderate-to-severe psoriasis: a phase III, multicentre, double-blind trial. Lancet 2005; 366: 1367-1374.
28. Menter A, Feldman SR, Weinstein GD, et al,. A randomized comparison of continuous vs. intermittent infliximab maintenance regimens over 1 year in the treatment of moderate-to-severe plaque psoriasis. J Am Acad Dermatol 2007; 56: 31 e1-e15.
29. Torii H, Nakagawa H, Investigators JIS,. Infliximab monotherapy in Japanese patients with moderate-to-severe plaque psoriasis and psoriatic arthritis. A randomized, double-blind, placebo-controlled multicenter trial. J Dermatol Sci 2010; 59: 40-49.
30. Leonardi C, Langley RG, Papp K, et al,. Adalimumab for treatment of moderate to severe chronic plaque psoriasis of the hands and feet: efficacy and safety results from REACH, a randomized, placebo-controlled, double-blind trial. Arch Dermatol 2011; 147: 429-436.
31. Asahina A, Nakagawa H, Etoh T, Ohtsuki M, Adalimumab MSG,. Adalimumab in Japanese patients with moderate to severe chronic plaque psoriasis: efficacy and safety results from a Phase II/III randomized controlled study. J Dermatol 2010; 37: 299-310.
32. Gordon KB, Langley RG, Leonardi C, et al,. Clinical response to adalimumab treatment in patients with moderate to severe psoriasis: double-blind, randomized controlled trial and open-label extension study. J Am Acad Dermatol 2006; 55: 598-606.
33. Saurat JH, Stingl G, Dubertret L, et al,. Efficacy and safety results from the randomized controlled comparative study of adalimumab vs. methotrexate vs. placebo in patients with psoriasis (CHAMPION). Br J Dermatol 2008; 158: 558-566.
34. Menter A, Tyring SK, Gordon K, et al,. Adalimumab therapy for moderate to severe psoriasis: A randomized, controlled phase III trial. J Am Acad Dermatol 2008; 58: 106-115.
35. Leonardi CL, Kimball AB, Papp KA, et al,. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet 2008; 371: 1665-1674.
36. Tsai TF, Ho JC, Song M, et al,. Efficacy and safety of ustekinumab for the treatment of moderate-to-severe psoriasis: a phase III, randomized, placebo-controlled trial in Taiwanese and Korean patients (PEARL). J Dermatol Sci 2011; 63: 154-163.
37. Igarashi A, Kato T, Kato M, Song M, Nakagawa H,. Japanese Ustekinumab Study G. Efficacy and safety of ustekinumab in Japanese patients with moderate-to-severe plaque-type psoriasis: long-term results from a phase 2/3 clinical trial. J Dermatol 2012; 39: 242-252.
38. Krueger GG, Langley RG, Leonardi C, et al,. A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N Engl J Med 2007; 356: 580-592.
39. Gottlieb AB, Langley RG, Strober BE, et al,. A randomized, double-blind, placebo-controlled study to evaluate the addition of methotrexate to etanercept in patients with moderate to severe plaque psoriasis. Br J Dermatol 2012; 167: 649-657.
40. Zachariae C, Mork NJ, Reunala T, et al,. The combination of etanercept and methotrexate increases the effectiveness of treatment in active psoriasis despite inadequate effect of methotrexate therapy. Acta Derm Venereol 2008; 88: 495-501.
41. Barker J, Hoffmann M, Wozel G, et al,. Efficacy and safety of infliximab vs. methotrexate in patients with moderate-to-severe plaque psoriasis: results of an open-label, active-controlled, randomized trial (RESTORE1). Br J Dermatol 2011; 165: 1109-1117.
42. Griffiths CE, Strober BE, van de Kerkhof P, et al,. Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med 2010; 362: 118-128.
43. Leonardi C, Papp K, Strober B, et al,. The long-term safety of adalimumab treatment in moderate to severe psoriasis: a comprehensive analysis of all adalimumab exposure in all clinical trials. Am J Clin Dermatol 2011; 12: 321-337.
44. Reich K, Wozel G, Zheng H, van Hoogstraten HJ, Flint L,. Efficacy and Safety of Infliximab as Continuous or Intermittent Therapy in Patients With Moderate-to-Severe Plaque Psoriasis: Results of a Randomised, Long-Term Extension Trial (RESTORE2). Br J Dermatol 2013; 168: 1325-1334.
45. Pariser DM, Leonardi CL, Gordon K, et al,. Integrated safety analysis: short- and long-term safety profiles of etanercept in patients with psoriasis. J Am Acad Dermatol 2012; 67: 245-256.
46. Papp KA, Poulin Y, Bissonnette R, et al,. Assessment of the long-term safety and effectiveness of etanercept for the treatment of psoriasis in an adult population. J Am Acad Dermatol 2012; 66: e33-e45.
47. Gordon K, Papp K, Poulin Y, Gu Y, Rozzo S, Sasso EH,. Long-term efficacy and safety of adalimumab in patients with moderate to severe psoriasis treated continuously over 3 years: results from an open-label extension study for patients from REVEAL. J Am Acad Dermatol 2012; 66: 241-251.
48. Burmester GR, Panaccione R, Gordon KB, McIlraith MJ, Lacerda AP,. Adalimumab: long-term safety in 23 458 patients from global clinical trials in rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, psoriatic arthritis, psoriasis and Crohn's disease. Ann Rheum Dis 2013; 72: 517-524.
49. Papp KA, Griffiths CE, Gordon K, et al,. Long-term safety of ustekinumab in patients with moderate-to-severe psoriasis: final results from 5 years of follow-up. Br J Dermatol 2013; 168: 844-854.
50. Gordon KB, Papp KA, Langley RG, et al,. Long-term safety experience of ustekinumab in patients with moderate to severe psoriasis (Part II of II): results from analyses of infections and malignancy from pooled phase II and III clinical trials. J Am Acad Dermatol 2012; 66: 742-751.
51. Garcia-Doval I, Carretero G, Vanaclocha F, et al,. Risk of serious adverse events associated with biologic and nonbiologic psoriasis systemic therapy: patients ineligible vs eligible for randomized controlled trials. Arch Dermatol 2012; 148: 463-470.
52. Schmitt-Egenolf M,. Psoriasis therapy in real life: the need for registries. Dermatology 2006; 213: 327-330.
53. Kimball AB, Pariser D, Yamauchi PS, et al,. OBSERVE-5 interim analysis: an observational postmarketing safety registry of etanercept for the treatment of psoriasis. J Am Acad Dermatol 2013; 68: 756-764.
54. Kerdel FA, Williams DA, Thaci D, Wolfgang J, Wang Y,. A 10-year postmarketing surveillance registry of adalimumab for moderate to severe psoriasis: Third-year interim results of ESPRIT. J Am Acad Dermatol 2013; 68: AB191.
55. van Lumig PP, Driessen RJ, Berends MA, Boezeman JB, van de Kerkhof PC, de Jong EM,. Safety of treatment with biologics for psoriasis in daily practice: 5-year data. J Eur Acad Dermatol Venereol 2012; 26: 283-291.
56. Leonardi C, Fiorentino D, Kalb R, et al,. Serious infection events in the psoriasis longitudinal assessment and registry (PSOLAR) study: Current status of observations. J Am Acad Dermatol 2013; 68 (Suppl 1): AB213.
57. Kamili Q, Menter A,. Atypical presentation of histoplasmosis in a patient with psoriasis and psoriatic arthritis on infliximab therapy. J Drugs Dermatol 2010; 9: 57-60.
58. Hoang JK, Burruss J,. Localized cutaneous Cryptococcus albidus infection in a 14-year-old boy on etanercept therapy. Pediatr Dermatol 2007; 24: 285-288.
59. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V,. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA 2006; 295: 2275-2285.
60. Leombruno JP, Einarson TR, Keystone EC,. The safety of anti-tumour necrosis factor treatments in rheumatoid arthritis: meta and exposure-adjusted pooled analyses of serious adverse events. Ann Rheum Dis 2009; 68: 1136-1145.
61. Furst DE,. The risk of infections with biologic therapies for rheumatoid arthritis. Semin Arthritis Rheum 2010; 39: 327-346.
62. Listing J, Strangfeld A, Kary S, et al,. Infections in patients with rheumatoid arthritis treated with biologic agents. Arthritis Rheum 2005; 52: 3403-3412.
63. Kroesen S, Widmer AF, Tyndall A, Hasler P,. Serious bacterial infections in patients with rheumatoid arthritis under anti-TNF-alpha therapy. Rheumatology (Oxford) 2003; 42: 617-621.
64. Favalli EG, Desiati F, Atzeni F, et al,. Serious infections during anti-TNFalpha treatment in rheumatoid arthritis patients. Autoimmun Rev 2009; 8: 266-273.
65. Peyrin-Biroulet L, Deltenre P, de Suray N, Branche J, Sandborn WJ, Colombel JF,. Efficacy and safety of tumor necrosis factor antagonists in Crohn's disease: meta-analysis of placebo-controlled trials. Clin Gastroenterol Hepatol 2008; 6: 644-653.
66. Wasko MC,. Comorbid conditions in patients with rheumatic diseases: an update. Curr Opin Rheumatol 2004; 16: 109-113.
67. Robinson MR, Korman BD, Korman NJ,. Combination immunosuppressive therapies: the promise and the peril. Arch Dermatol 2007; 143: 1053-1057.
68. Garcia-Doval I, Rustenbach SJ, Stern R, et al,. Systemic psoriasis therapy shows high between-country variation: a sign of unwarranted variation? Cross-sectional analysis of baseline data from the PSONET registries. Br J Dermatol 2013; 169: 710-714.
69. Wallis RS, Broder MS, Wong JY, Hanson ME, Beenhouwer DO,. Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin Infect Dis 2004; 38: 1261-1265.
70. Chu JH, Feudtner C, Heydon K, Walsh TJ, Zaoutis TE,. Hospitalizations for endemic mycoses: a population-based national study. Clin Infect Dis 2006; 42: 822-825.
71. Goodwin RA Jr, Shapiro JL, Thurman GH, Thurman SS, Des Prez RM,. Disseminated histoplasmosis: clinical and pathologic correlations. Medicine (Baltimore) 1980; 59: 1-33.
72. Assi MA, Sandid MS, Baddour LM, Roberts GD, Walker RC,. Systemic histoplasmosis: a 15-year retrospective institutional review of 111 patients. Medicine (Baltimore) 2007; 86: 162-169.
73. Wheat LJ, Connolly-Stringfield PA, Baker RL, et al,. Disseminated histoplasmosis in the acquired immune deficiency syndrome: clinical findings, diagnosis and treatment, and review of the literature. Medicine (Baltimore) 1990; 69: 361-374.
74. FDA. FDA: Manufacturers of TNF-Blocker Drugs Must Highlight Risk of Fungal Infections. Silver Spring: U.S. Food and Drug Administration; 2008 [updated 06/18/2009 cited 2012 Dec. 9]; Available at: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/2008/ucm116942.htm (last accessed: 9 December 2012).