Generalizability of Patients With Rheumatoid Arthritis in Biologic Agent Clinical Trials

Arthritis Care and Research

Volumn 68, Issue 10, 2016, Pages 1478-1488

  Vashisht, Priyanka ^a   Sayles, Harlan ^a   Cannella, Amy C ^a   Mikuls, Ted R ^a   Michaud, Kaleb ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b National Databank for Rheumatic Diseases   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; ADALIMUMAB; BIOLOGICAL PRODUCT; CERTOLIZUMAB PEGOL; ETANERCEPT; GOLIMUMAB; INFLIXIMAB; PREDNISONE; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; RITUXIMAB; TOCILIZUMAB; TOFACITINIB;

ADULT; AGE; AGED; ARTICLE; CONTROLLED STUDY; CRITERION VARIABLE; DAS28; DISEASE ACTIVITY; DISEASE ACTIVITY SCORE; DISEASE DURATION; DISEASE REGISTRY; DRUG APPROVAL; DRUG EFFICACY; ERYTHROCYTE SEDIMENTATION RATE; FEMALE; FOOD AND DRUG ADMINISTRATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MULTICENTER STUDY (TOPIC); OBSERVATIONAL STUDY; PATIENT PARTICIPATION; PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RHEUMATOID ARTHRITIS; YOUNG ADULT;

EID: 84988966734     PISSN: 2151464X     EISSN: 21514658     Source Type: Journal    
DOI: 10.1002/acr.22860     Document Type: Article

References (69)

1. Wolfe F, Michaud K. The loss of health status in rheumatoid arthritis and the effect of biologic therapy: a longitudinal observational study. Arthritis Res Ther 2010;12:R35.
2. Greenberg JD, Kremer JM, Curtis JR, Hochberg MC, Reed G, Tsao P, et al. Tumour necrosis factor antagonist use and associated risk reduction of cardiovascular events among patients with rheumatoid arthritis. Ann Rheum Dis 2011;70:576–82.
3. Singh JA, Furst DE, Bharat A, Curtis JR, Kavanaugh AF, Kremer JM, et al. 2012 update of the 2008 American College of Rheumatology recommendations for the use of disease-modifying antirheumatic drugs and biologic agents in the treatment of rheumatoid arthritis. Arthritis Care Res (Hoboken) 2012;64:625–39.
4. Smolen JS, Landewe R, Breedveld FC, Buch M, Burmester G, Dougados M, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis 2014;73:492–509.
5. Curtis JR, Singh JA. Use of biologics in rheumatoid arthritis: current and emerging paradigms of care. Clin Ther 2011;33:679–707.
6. Barnabe C, Thanh NX, Ohinmaa A, Homik J, Barr SG, Martin L, et al. Healthcare service utilisation costs are reduced when rheumatoid arthritis patients achieve sustained remission. Ann Rheum Dis 2013;72:1664–8.
7. Harrold LR, Peterson D, Beard AJ, Gurwitz JH, Briesacher BA. Time trends in medication use and expenditures in older patients with rheumatoid arthritis. Am J Med 2012;125:e9–15.
8. Welsing PM, Bijl M, van Bodegraven AA, Lems WF, Prens E, Bijlsma JW. Cost effectiveness of biologicals: high costs are the other face of success. Ned Tijdschr Geneeskd. 2011;155:A3026. In Dutch.
9. Genovese MC, Bathon JM, Martin RW, Fleischmann RM, Tesser JR, Schiff MH, et al. Etanercept versus methotrexate in patients with early rheumatoid arthritis: two-year radiographic and clinical outcomes. Arthritis Rheum 2002;46:1443–50.
10. St.Clair EW, Wagner CL, Fasanmade AA, Wang B, Schaible T, Kavanaugh A, et al. The relationship of serum infliximab concentrations to clinical improvement in rheumatoid arthritis: results from ATTRACT, a multicenter, randomized, double-blind, placebo-controlled trial. Arthritis Rheum 2002;46:1451–9.
11. Sokka T, Pincus T. Eligibility of patients in routine care for major clinical trials of anti–tumor necrosis factor α agents in rheumatoid arthritis. Arthritis Rheum 2003;48:313–8.
12. Simsek I, Yazici Y. Incomplete reporting of recruitment information in clinical trials of biologic agents for the treatment of rheumatoid arthritis: a review. Arthritis Care Res (Hoboken) 2012;64:1611–6.
13. Rothwell PM. External validity of randomised controlled trials: “To whom do the results of this trial apply?” Lancet 2005;365:82–93.
14. Wolfe F, Michaud K, Dewitt EM. Why results of clinical trials and observational studies of antitumour necrosis factor (anti-TNF) therapy differ: methodological and interpretive issues. Ann Rheum Dis 2004;63Suppl2: ii13–7.
15. Wolfe F, Michaud K. Towards an epidemiology of rheumatoid arthritis outcome with respect to treatment: randomized controlled trials overestimate treatment response and effectiveness. Rheumatology (Oxford) 2005;44 Suppl 4:iv18–22.
16. Gibofsky A, Palmer WR, Goldman JA, Lautzenheiser RL, Markenson JA, Weaver A, et al. Real-world utilization of DMARDs and biologics in rheumatoid arthritis: the RADIUS (rheumatoid arthritis disease-modifying anti-rheumatic drug intervention and utilization study) study. Curr Med Res Opin 2006;22:169–83.
17. Weaver AL, Lautzenheiser RL, Schiff MH, Gibofsky A, Perruquet JL, Luetkemeyer J, et al. Real-world effectiveness of select biologic and DMARD monotherapy and combination therapy in the treatment of rheumatoid arthritis: results from the RADIUS observational registry. Curr Med Res Opin 2006;22:185–98.
18. Zink A, Strangfeld A, Schneider M, Herzer P, Hierse F, Stoyanova-Scholz M, et al. Effectiveness of tumor necrosis factor inhibitors in rheumatoid arthritis in an observational cohort study: comparison of patients according to their eligibility for major randomized clinical trials. Arthritis Rheum 2006;54:3399–407.
19. Mikuls TR, Kazi S, Cipher D, Hooker R, Kerr GS, Richards JS, et al. The association of race and ethnicity with disease expression in male US veterans with rheumatoid arthritis. J Rheumatol 2007;34:1480–4.
20. Mikuls TR, Andreas Reimold M, Kerr GS, Cannon GW. Insights and implications of the VA rheumatoid arthritis registry. Fed Pract 2015;32:24–29.
21. England BR, Sayles H, Mikuls TR, Johnson DS, Michaud K. Validation of the Rheumatic Disease Comorbidity Index. Arthritis Care Res (Hoboken) 2015;67:865–72.
22. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis and Rheum 1988;31:315–24.
23. Prevoo ML, van 't Hof MA, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL. Modified disease activity scores that include twenty-eight–joint counts: development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum 1995;38:44–8.
24. Fuchs HA, Brooks RH, Callahan LF, Pincus T. A simplified twenty-eight–joint quantitative articular index in rheumatoid arthritis. Arthritis Rheum 1989;32:531–7.
25. Weinblatt ME, Keystone EC, Furst DE, Moreland LW, Weisman MH, Birbara CA, et al. Adalimumab, a fully human anti–tumor necrosis factor α monoclonal antibody, for the treatment of rheumatoid arthritis in patients taking concomitant methotrexate: the ARMADA trial. Arthritis Rheum 2003;48:35–45.
26. Furst DE, Schiff MH, Fleischmann RM, Strand V, Birbara CA, Compagnone D, et al. Adalimumab, a fully human anti tumor necrosis factor-α monoclonal antibody, and concomitant standard antirheumatic therapy for the treatment of rheumatoid arthritis: results of STAR (safety trial of adalimumab in rheumatoid arthritis). J Rheumatol 2003;30:2563–71.
27. Van de Putte LB, Atkins C, Malaise M, Sany J, Russell AS, van Riel PL, et al. Efficacy and safety of adalimumab as monotherapy in patients with rheumatoid arthritis for whom previous disease modifying antirheumatic drug treatment has failed. Ann Rheum Dis 2004;63:508–16.
28. Keystone EC, Kavanaugh AF, Sharp JT, Tannenbaum H, Hua Y, Teoh LS, et al. Radiographic, clinical, and functional outcomes of treatment with adalimumab (a human anti–tumor necrosis factor monoclonal antibody) in patients with active rheumatoid arthritis receiving concomitant methotrexate therapy: a randomized, placebo-controlled, 52-week trial. Arthritis Rheum 2004;50:1400–11.
29. Keystone E, van der Heijde D, Mason D Jr, Landewé R, van Vollenhoven R, Combe B, 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;58:3319–29.
30. Smolen J, Landewe RB, Mease P, Brzezicki J, Mason D, Luijtens K, 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;68:797–804.
31. Fleischmann R, Vencovsky J, van Vollenhoven RF, Borenstein D, Box J, Coteur G, et al. Efficacy and safety of certolizumab pegol monotherapy every 4 weeks in patients with rheumatoid arthritis failing previous disease-modifying antirheumatic therapy: the FAST4WARD study. Ann Rheum Dis 2009;68:805–11.
32. Moreland LW, Schiff MH, Baumgartner SW, Tindall EA, Fleischmann RM, Bulpitt KJ, et al. Etanercept therapy in rheumatoid arthritis: a randomized, controlled trial. Ann Intern Med 1999;130:478–86.
33. Keystone EC, Genovese MC, Klareskog L, Hsia EC, Hall ST, Miranda PC, et al. Golimumab, a human antibody to tumour necrosis factor α given by monthly subcutaneous injections, in active rheumatoid arthritis despite methotrexate therapy: the GO-FORWARD study. Ann Rheum Dis 2009;68:789–96.
34. Emery P, Fleischmann RM, Moreland LW, Hsia EC, Strusberg I, Durez P, et al. Golimumab, a human anti–tumor necrosis factor α 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;60:2272–83.
35. Smolen JS, Kay J, Landewe RB, Matteson EL, Gaylis N, Wollenhaupt J, et al. Golimumab in patients with active rheumatoid arthritis who have previous experience with tumour necrosis factor inhibitors: results of a long-term extension of the randomised, double-blind, placebo-controlled GO-AFTER study through week 160. Ann Rheum Dis 2012;71:1671–9.
36. Maini R, St.Clair EW, Breedveld F, Furst D, Kalden J, Weisman M, et al, and the ATTRACT Study Group. Infliximab (chimeric anti-tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial. Lancet 1999;354:1932–9.
37. St.Clair EW, van der Heijde DM, Smolen JS, Maini RN, Bathon JM, Emery P, et al. Combination of infliximab and methotrexate therapy for early rheumatoid arthritis: a randomized, controlled trial. Arthritis Rheum 2004;50:3432–43.
38. Genovese MC, Becker JC, Schiff M, Luggen M, Sherrer Y, Kremer J, et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor α inhibition. N Engl J Med 2005;353:1114–23.
39. Kremer JM, Genant HK, Moreland LW, Russell AS, Emery P, Abud-Mendoza C, et al. Effects of abatacept in patients with methotrexate-resistant active rheumatoid arthritis: a randomized trial. Ann Intern Med 2006;144:865–76.
40. Westhovens R, Robles M, Ximenes AC, Nayiager S, Wollenhaupt J, Durez P, et al. Clinical efficacy and safety of abatacept in methotrexate-naive patients with early rheumatoid arthritis and poor prognostic factors. Ann Rheum Dis 2009;68:1870–7.
41. Bresnihan B, Alvaro-Gracia JM, Cobby M, Doherty M, Domljan Z, Emery P, et al. Treatment of rheumatoid arthritis with recombinant human interleukin-1 receptor antagonist. Arthritis Rheum 1998;41:2196–204.
42. Cohen SB, Moreland LW, Cush JJ, Greenwald MW, Block S, Shergy WJ, et al. A multicentre, double blind, randomised, placebo controlled trial of anakinra (kineret), a recombinant interleukin 1 receptor antagonist, in patients with rheumatoid arthritis treated with background methotrexate. Ann Rheum Dis 2004;63:1062–8.
43. Cohen S, Hurd E, Cush J, Schiff M, Weinblatt ME, Moreland LW, et al. Treatment of rheumatoid arthritis with anakinra, a recombinant human interleukin-1 receptor antagonist, in combination with methotrexate: results of a twenty-four–week, multicenter, randomized, double-blind, placebo-controlled trial. Arthritis Rheum 2002;46:614–24.
44. Fleischmann RM, Schechtman J, Bennett R, Handel ML, Burmester GR, Tesser J, et al. Anakinra, a recombinant human interleukin-1 receptor antagonist (r-metHuIL-1ra), in patients with rheumatoid arthritis: a large, international, multicenter, placebo-controlled trial. Arthritis Rheum 2003;48:927–34.
45. Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572–81.
46. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, et al. Rituximab for rheumatoid arthritis refractory to anti–tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 2006;54:2793–806.
47. Genovese MC, McKay JD, Nasonov EL, Mysler EF, da Silva NA, Alecock E, et al. Interleukin-6 receptor inhibition with tocilizumab reduces disease activity in rheumatoid arthritis with inadequate response to disease-modifying antirheumatic drugs: the Tocilizumab in Combination With Traditional Disease-Modifying Antirheumatic Drug Therapy study. Arthritis Rheum 2008;58:2968–80.
48. Emery P, Keystone E, Tony HP, Cantagrel A, van Vollenhoven R, Sanchez A, et al. IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial. Ann Rheum Dis 2008;67:1516–23.
49. Smolen JS, Beaulieu A, Rubbert-Roth A, Ramos-Remus C, Rovensky J, Alecock E, et al. Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomised trial. Lancet 2008;371:987–97.
50. Jones G, Sebba A, Gu J, Lowenstein MB, Calvo A, Gomez-Reino JJ, et al. Comparison of tocilizumab monotherapy versus methotrexate monotherapy in patients with moderate to severe rheumatoid arthritis: the AMBITION study. Ann Rheum Dis 2010;69:88–96.
51. Kremer JM, Blanco R, Brzosko M, Burgos-Vargas R, Halland AM, Vernon E, et al. Tocilizumab inhibits structural joint damage in rheumatoid arthritis patients with inadequate responses to methotrexate: results from the double-blind treatment phase of a randomized placebo-controlled trial of tocilizumab safety and prevention of structural joint damage at one year. Arthritis Rheum 2011;63:609–21.
52. Burmester GR, Blanco R, Charles-Schoeman C, Wollenhaupt J, Zerbini C, Benda B, et al. Tofacitinib (CP-690,550) in combination with methotrexate in patients with active rheumatoid arthritis with an inadequate response to tumour necrosis factor inhibitors: a randomised phase 3 trial. Lancet 2013;381:451–60.
53. Fleischmann R, Kremer J, Cush J, Schulze-Koops H, Connell CA, Bradley JD, et al. Placebo-controlled trial of tofacitinib monotherapy in rheumatoid arthritis. N Engl J Med 2012;367:495–507.
54. Van Vollenhoven RF, Fleischmann R, Cohen S, Lee EB, Garcia Meijide JA, Wagner S, et al. Tofacitinib or adalimumab versus placebo in rheumatoid arthritis. N Engl J Med 2012;367:508–19.
55. Pincus T, Sokka T. Should contemporary rheumatoid arthritis clinical trials be more like standard patient care and vice versa? Ann Rheum Dis 2004;63Suppl2:ii32–9.
56. Pincus T, Sokka T. Clinical trials in rheumatic diseases: designs and limitations. Rheum Dis Clin North Am 2004;30:701–24.
57. Feinstein AR. An additional basic science for clinical medicine: II. The limitations of randomized trials. Ann Intern Med 1983;99:544–50.
58. Stein CM, Pincus T. Placebo-controlled studies in rheumatoid arthritis: ethical issues. Lancet 1999;353:400–3.
59. Pincus T. Limitations of randomized controlled clinical trials to depict accurately long-term outcomes in rheumatoid arthritis. Z Rheumatol 1998;57:46–9.
60. Nair SC, Kievit W, Janse RW, Bijlsma JW, Fransen J, Lafeber FP, et al. Generalization and extrapolation of treatment effects from clinical studies in rheumatoid arthritis. Arthritis Care Res (Hoboken) 2014;66:998–1007.
61. Khan NA, Lombeida JI, Singh M, Spencer HJ, Torralba KD. Association of industry funding with the outcome and quality of randomized controlled trials of drug therapy for rheumatoid arthritis. Arthritis Rheum 2012;64:2059–67.
62. Bergstrom U, Book C, Lindroth Y, Marsal L, Saxne T, Jacobsson L. Lower disease activity and disability in Swedish patients with rheumatoid arthritis in 1995 compared with 1978. Scand J Rheumatol 1999;28:160–5.
63. Genovese MC, Bathon JM, Martin RW, Fleischmann RM, Tesser JR, Schiff MH, et al. Etanercept versus methotrexate in patients with early rheumatoid arthritis: two-year radiographic and clinical outcomes. Arthritis Rheum 2002;46:1443–50.
64. Pincus T, Sokka T, Chung CP, Cawkwell G. Declines in number of tender and swollen joints in patients with rheumatoid arthritis seen in standard care in 1985 versus 2001: possible considerations for revision of inclusion criteria for clinical trials. Ann Rheum Dis 2006;65:878–83.
65. Hernandez-Avila M, Liang MH, Willett WC, Stampfer MJ, Colditz GA, Rosner B, et al. Exogenous sex hormones and the risk of rheumatoid arthritis. Arthritis Rheum 1990;33:947–53.
66. MacGregor AJ, Bamber S, Silman AJ. A comparison of the performance of different methods of disease classification for rheumatoid arthritis: results of an analysis from a nationwide twin study. J Rheumatol 1994;21:1420–6.
67. Khan NA, Singh M, Spencer HJ, Torralba KD. Randomized controlled trials of rheumatoid arthritis registered at ClinicalTrials.gov: what gets published and when. Arthritis Rheumatol 2014;66:2664–74.
68. Pincus T. Rheumatoid arthritis: disappointing long-term outcomes despite successful short-term clinical trials. J Clin Epidemiol 1988;41:1037–41.
69. Kingsley GH, Khoshaba B, Smith CM, Choy EH, Scott DL. Are clinical trials in rheumatoid arthritis generalizable to routine practice? A re-evaluation of trial entry criteria. Rheumatology (Oxford) 2005;44:629–32.