Impact of biologic therapies on risk of major adverse cardiovascular events in patients with psoriasis: systematic review and meta-analysis of randomized controlled trials

British Journal of Dermatology

Volumn 176, Issue 4, 2017, Pages 890-901

  Rungapiromnan, W ^a   Yiu, Z Z N ^a,b   Warren, R B ^b   Griffiths, C E M ^b   Ashcroft, D M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; ETANERCEPT; INFLIXIMAB; IXEKIZUMAB; METHOTREXATE; PLACEBO; SECUKINUMAB; USTEKINUMAB; BIOLOGICAL FACTOR; IL17A PROTEIN, HUMAN; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR;

ADVERSE OUTCOME; BIOLOGICAL THERAPY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; COCHRANE LIBRARY; COMPARATIVE STUDY; DISEASE ASSOCIATION; DRUG DOSE COMPARISON; DRUG INDUSTRY; EMBASE; EUROPEAN MEDICINES AGENCY; FOOD AND DRUG ADMINISTRATION; HIGH RISK PATIENT; HUMAN; MEDLINE; META ANALYSIS; ONLINE ANALYSIS; PRIORITY JOURNAL; PSORIASIS VULGARIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK ASSESSMENT; RISK FACTOR; SYSTEMATIC REVIEW; SYSTEMIC THERAPY; ADULT; ANTAGONISTS AND INHIBITORS; CEREBROVASCULAR ACCIDENT; CHEMICALLY INDUCED; DEATH, SUDDEN, CARDIAC; FEMALE; HEART INFARCTION; MALE; MIDDLE AGED; PSORIASIS;

ADULT; ANTIBODIES, MONOCLONAL; BIOLOGICAL FACTORS; CARDIOVASCULAR DISEASES; DEATH, SUDDEN, CARDIAC; FEMALE; HUMANS; INTERLEUKIN-12; INTERLEUKIN-17; INTERLEUKIN-23; MALE; MIDDLE AGED; MYOCARDIAL INFARCTION; PSORIASIS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK FACTORS; STROKE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85015165581     PISSN: 00070963     EISSN: 13652133     Source Type: Journal    
DOI: 10.1111/bjd.14964     Document Type: Review

References (68)

1. Gelfand JM, Neimann AL, Shin DB et al. Risk of myocardial infarction in patients with psoriasis. JAMA 2006; 296:1735–41.
2. Armstrong AW, Harskamp CT, Ledo L et al. Coronary artery disease in patients with psoriasis referred for coronary angiography. Am J Cardiol 2012; 109:976–80.
3. Armstrong AW, Lin SW, Chambers CJ et al. Psoriasis and hypertension severity: Results from a case-control study. PLOS One 2011; 6:e18227.
4. Samarasekera EJ, Neilson JM, Warren RB et al. Incidence of cardiovascular disease in individuals with psoriasis: a systematic review and meta-analysis. J Invest Dermatol 2013; 133:2340–6.
5. Parisi R, Rutter MK, Lunt M et al. Psoriasis and the risk of major cardiovascular events: cohort study using the Clinical Practice Research Datalink. J Invest Dermatol 2015; 135:2189–97.
6. Stern RS, Huibregtse A. Very severe psoriasis is associated with increased noncardiovascular mortality but not with increased cardiovascular risk. J Invest Dermatol 2011; 131:1159–66.
7. Wakkee M, Herings RM, Nijsten T. Psoriasis may not be an independent risk factor for acute ischemic heart disease hospitalizations: results of a large population-based Dutch cohort. J Invest Dermatol 2010; 130:962–7.
8. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352:1685–95.
9. 2 inhibitor darapladib on human coronary atherosclerotic plaque. Circulation 2008; 118:1172–82.
10. Libby P, Ridker P, Hansson GK. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol 2009; 54:2129–38.
11. Ridker PM. Testing the inflammatory hypothesis of atherothrombosis: scientific rationale for the cardiovascular inflammation reduction trial (CIRT). J Thromb Haemost 2009; 7 (Suppl. 1):332–9.
12. Menter A, Griffiths CEM. Current and future management of psoriasis. Lancet 2007; 370:272–84.
13. Gordon KB, Langley RG, Gottlieb AB et al. A phase III, randomized, controlled trial of the fully human IL-12/23 mAb briakinumab in moderate-to-severe psoriasis. J Invest Dermatol 2012; 132:304–14.
14. 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; 356:580–92.
15. Petrou I. Systemic medications for psoriasis therapy must be prescribed with caution. Available at: http://dermatologytimes.modernmedicine.com/dermatology-times/news/clinical/clinical-pharmacology/systemic-medications-psoriasis-therapy-must-be (last accessed 17 January 2017).
16. Moher D, Liberati A, Tetzlaff J et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annu Intern Med 2009; 151:264–9.
17. Lefebvre C, Manheimer E, Glanville J. Searching for studies. In: Cochrane Handbook for Systematic Reviews of Interventions. (Higgins JPT, Green S, eds). Chichester: John Wiley & Sons Ltd, 2008; 95–150.
18. Higgins JP, Altman DG. Assessing risk of bias in included studies. In: Cochrane Handbook for Systematic Reviews of Interventions (Higgins JPT, Green S, eds). Chichester: John Wiley & Sons Ltd, 2008; 187–242.
19. Bradburn MJ, Deeks JJ, Berlin JA, Russell Localio A. Much ado about nothing: a comparison of the performance of meta-analytical methods with rare events. Stat Med 2007; 26:53–77.
20. 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; 58:106–15.
21. Maari C, Bolduc C, Nigen S et al. Effect of adalimumab on sleep parameters in patients with psoriasis and obstructive sleep apnea: a randomized controlled trial. J Dermatolog Treat 2014; 25:57–60.
22. Gordon KB, Duffin KC, Bissonnette R et al. A phase 2 trial of guselkumab versus adalimumab for plaque psoriasis. N Engl J Med 2015; 373:136–44.
23. AbbVie. Safety and efficacy study of adalimumab in the treatment of plaque psoriasis. Available at: https://clinicaltrials.gov/show/NCT01646073 (last accessed 17 January 2017).
24. AbbVie. Adalimumab M13-606 clinical study report R&D/13/997. Available at: https://www.abbvie.com/wp-content/uploads/2016/10/adalimumab-M13-606.pdf (last accessed 17 January 2017).
25. 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; 158:558–66.
26. Gottlieb AB, Matheson RT, Lowe N et al. A randomized trial of etanercept as monotherapy for psoriasis. Arch Dermatol 2003; 139:1627–32.
27. 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.
28. van de Kerkhof PCM, 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; 159:1177–85.
29. Gottlieb A, Leonardi C, Kerdel F et al. Efficacy and safety of briakinumab vs. etanercept and placebo in patients with moderate to severe chronic plaque psoriasis. Br J Dermatol 2011; 165:652–60.
30. Strober BE, Crowley JJ, Yamauchi PS et al. Efficacy and safety results from a phase III, randomized controlled trial comparing the safety and efficacy of briakinumab with etanercept and placebo in patients with moderate to severe chronic plaque psoriasis. Br J Dermatol 2011; 165:661–8.
31. Bagel J, Lynde C, Tyring S et al. 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.
32. Bachelez H, van de Kerkhof PCM, Strohal R et al. Tofacitinib versus etanercept or placebo in moderate-to-severe chronic plaque psoriasis: A phase 3 randomised non-inferiority trial. Lancet 2015; 386:552–61.
33. Griffiths CEM, Reich K, Lebwohl M et al. Comparison of ixekizumab with etanercept or placebo in moderate-to-severe psoriasis (UNCOVER-2 and UNCOVER-3): results from two phase 3 randomised trials. Lancet 2015; 386:541–51.
34. Leonardi CL, Powers JL, Matheson RT et al. Etanercept as monotherapy in patients with psoriasis. N Engl J Med 2003; 349:2014–22.
35. Papp KA, Tyring S, Lahfa M et al. A global phase III randomized controlled trial of etanercept in psoriasis: safety, efficacy, and effect of dose reduction. Br J Dermatol 2005; 152:1304–12.
36. Chaudhari U, Romano P, Mulcahy LD et al. Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial. Lancet 2001; 357:1842–7.
37. 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; 51:534–42.
38. 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; 366:1367–74.
39. 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.e1–15.
40. 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; 125:1845–51.
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; 165:1109–17.
42. Mrowietz U, Leonardi CL, Girolomoni G et al. Secukinumab retreatment-as-needed versus fixed-interval maintenance regimen for moderate to severe plaque psoriasis: a randomized, double-blind, noninferiority trial (SCULPTURE). J Am Acad Dermatol 2015; 73:27–36.
43. Langley RG, Elewski BE, Lebwohl M et al. Secukinumab in plaque psoriasis – results of two phase 3 trials. N Engl J Med 2014; 371:326–38.
44. Blauvelt A, Prinz JC, Gottlieb AB et al. Secukinumab administration by pre-filled syringe: efficacy, safety and usability results from a randomized controlled trial in psoriasis (FEATURE). Br J Dermatol 2015; 172:484–93.
45. Paul C, Lacour J-P, Tedremets L et al. Efficacy, safety and usability of secukinumab administration by autoinjector/pen in psoriasis: a randomized, controlled trial (JUNCTURE). J Eur Acad Dermatol Venereol 2015; 29:1082–90.
46. Tsai T-F, Ho J-C, 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; 63:154–63.
47. Zhu X, Zheng M, Song M et al. Efficacy and safety of ustekinumab in Chinese patients with moderate to severe plaque-type psoriasis: results from a phase 3 clinical trial (LOTUS). J Drugs Dermatol 2013; 12:166–74.
48. Lebwohl M, Strober B, Menter A et al. Phase 3 studies comparing brodalumab with ustekinumab in psoriasis. N Engl J Med 2015; 373:1318–28.
49. Papp KA, Langley RG, Lebwohl M et al. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 52-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 2). Lancet 2008; 371:1675–84.
50. Igarashi A, Kato T, Kato M et al. 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; 39:242–52.
51. 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; 371:1665–74.
52. Griffiths CEM, Strober BE, van de Kerkhof P et al. Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med 2010; 362:118–28.
53. ®) in participants with moderate to severe psoriasis. Available at: https://clinicaltrials.gov/ct2/show/NCT01276847 (last accessed 17 January 2017).
54. Goldminz AM, Suárez-Fariñas M, Wang AC et al. CCL20 and IL22 Messenger RNA expression after adalimumab vs methotrexate treatment of psoriasis: a randomized clinical trial. JAMA Dermatol 2015; 151:837–46.
55. Janssen Pharmaceutical K.K. An efficacy and safety study of ustekinumab (CNTO 1275) in participants with plaque psoriasis. Available at: https://clinicaltrials.gov/ct2/show/results/NCT00723528 (last accessed 17 January 2017).
56. Leonardi C, Blauvelt A, Langley RG et al. Maintenance of efficacy among patients who achieve sPGA (0, 1): 60-week results from UNCOVER-1, a phase 3 trial of ixekizumab for moderate-to-severe plaque psoriasis. Presented at the 74th American Academy of Dermatology Annual Meeting, Washington, D.C., U.S.A., 4–8 March 2016.
57. Gordon KB, Blauvelt A, Papp KA et al. Phase 3 trials of ixekizumab in moderate-to-severe plaque psoriasis. N Engl J Med 2016; 375:345–56.
58. Ryan C, Leonardi CL, Krueger JG et al. Association between biologic therapies for chronic plaque psoriasis and cardiovascular events: a meta-analysis of randomized controlled trials. JAMA 2011; 306:864–71.
59. Tzellos T, Kyrgidis A, Zouboulis CC. Re-evaluation of the risk for major adverse cardiovascular events in patients treated with anti-IL-12/23 biological agents for chronic plaque psoriasis: a meta-analysis of randomized controlled trials. J Eur Acad Dermatol Venereol 2013; 27:622–7.
60. Callen JP. Are major adverse cardiovascular events associated with anti–IL-12/23 therapies? Available at: http://www.jwatch.org/jd201109160000001/2011/09/16/are-major-adverse-cardiovascular-events (last accessed 17 January 2017).
61. Reddy M, Torres G, McCormick T et al. Positive treatment effects of ustekinumab in psoriasis: analysis of lesional and systemic parameters. J Dermatol 2010; 37:413–25.
62. Rauch G, Rauch B, Schüler S, Kieser M. Opportunities and challenges of clinical trials in cardiology using composite primary endpoints. World J Cardiol 2015; 7:1–5.
63. Taichman DB, Backus J, Baethge C et al. Sharing clinical trial data – a proposal from the International Committee of Medical Journal Editors. N Engl J Med 2016; 374:384–6.
64. Ahlehoff O, Skov L, Gislason G et al. Cardiovascular outcomes and systemic anti-inflammatory drugs in patients with severe psoriasis: 5-year follow-up of a Danish nationwide cohort. J Eur Acad Dermatol Venereol 2015; 29:1128–34.
65. Gottlieb AB, Kalb RE, Langley RG et al. Safety observations in 12095 patients with psoriasis enrolled in an international registry (PSOLAR): experience with infliximab and other systemic and biologic therapies. J Drugs Dermatol 2014; 13:1441–8.
66. Ray WA. Evaluating medication effects outside of clinical trials: new-user designs. Am J Epidemiol 2003; 158:915–20.
67. Wu JJ, Poon KY, Channual JC, Shen AY. Association between tumor necrosis factor inhibitor therapy and myocardial infarction risk in patients with psoriasis. Arch Dermatol 2012; 148:1244–50.
68. Moride Y, Abenhaim L. Evidence of the depletion of susceptibles effect in non-experimental pharmacoepidemiologic research. J Clin Epidemiol 1994; 47:731–7.