Biologics or tofacitinib for people with rheumatoid arthritis unsuccessfully treated with biologics: a systematic review and network meta-analysis

doi:10.1002/14651858.CD012591

Review

. 2017 Mar 10;3(3):CD012591.

doi: 10.1002/14651858.CD012591.

Biologics or tofacitinib for people with rheumatoid arthritis unsuccessfully treated with biologics: a systematic review and network meta-analysis

Affiliations

¹ Department of Medicine, Birmingham VA Medical Center, Faculty Office Tower 805B, 510 20th Street South, Birmingham, AL, USA, 35294.
² Cardiovascular Research Methods Centre, University of Ottawa Heart Institute, 40 Ruskin Street, Room H-2265, Ottawa, ON, Canada, K1Y 4W7.
³ Bruyère Research Institute, University of Ottawa, 43 Bruyère St, Annex E, room 302, Ottawa, ON, Canada, K1N 5C8.
⁴ Department of Medicine - Rheumatology, University of Alabama at Birmingham, Birmingham, USA.
⁵ Centre for Practice-Changing Research (CPCR), Ottawa Hospital Research Institute (OHRI), The Ottawa Hospital - General Campus, 501 Smyth Road, Box 711, Ottawa, ON, Canada, K1H 8L6.
⁶ Monash Department of Clinical Epidemiology, Cabrini Hospital, Department of Epidemiology and Preventive Medicine, School of Public Health and Preventive Medicine, Monash University, Suite 41, Cabrini Medical Centre, 183 Wattletree Road, Malvern, Victoria, Australia, 3144.
⁷ Department of General Internal Medicine, The University of Texas, M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1465, Houston, Texas, USA, 77030.
⁸ Department of Medicine, Faculty of Medicine, University of Ottawa, Ottawa, ON, Canada, K1H 8M5.
⁹ Department of Epidemiology and Community Medicine, University of Ottawa, Room H1281, 40 Ruskin Street, Ottawa, ON, Canada, K1Y 4W7.

PMID: 28282491
PMCID: PMC6472522
DOI: 10.1002/14651858.CD012591

Review

Biologics or tofacitinib for people with rheumatoid arthritis unsuccessfully treated with biologics: a systematic review and network meta-analysis

Jasvinder A Singh et al. Cochrane Database Syst Rev. 2017.

. 2017 Mar 10;3(3):CD012591.

doi: 10.1002/14651858.CD012591.

Affiliations

¹ Department of Medicine, Birmingham VA Medical Center, Faculty Office Tower 805B, 510 20th Street South, Birmingham, AL, USA, 35294.
² Cardiovascular Research Methods Centre, University of Ottawa Heart Institute, 40 Ruskin Street, Room H-2265, Ottawa, ON, Canada, K1Y 4W7.
³ Bruyère Research Institute, University of Ottawa, 43 Bruyère St, Annex E, room 302, Ottawa, ON, Canada, K1N 5C8.
⁴ Department of Medicine - Rheumatology, University of Alabama at Birmingham, Birmingham, USA.
⁵ Centre for Practice-Changing Research (CPCR), Ottawa Hospital Research Institute (OHRI), The Ottawa Hospital - General Campus, 501 Smyth Road, Box 711, Ottawa, ON, Canada, K1H 8L6.
⁶ Monash Department of Clinical Epidemiology, Cabrini Hospital, Department of Epidemiology and Preventive Medicine, School of Public Health and Preventive Medicine, Monash University, Suite 41, Cabrini Medical Centre, 183 Wattletree Road, Malvern, Victoria, Australia, 3144.
⁷ Department of General Internal Medicine, The University of Texas, M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1465, Houston, Texas, USA, 77030.
⁸ Department of Medicine, Faculty of Medicine, University of Ottawa, Ottawa, ON, Canada, K1H 8M5.
⁹ Department of Epidemiology and Community Medicine, University of Ottawa, Room H1281, 40 Ruskin Street, Ottawa, ON, Canada, K1Y 4W7.

PMID: 28282491
PMCID: PMC6472522
DOI: 10.1002/14651858.CD012591

Abstract

Background: Biologic disease-modifying anti-rheumatic drugs (DMARDs: referred to as biologics) are effective in treating rheumatoid arthritis (RA), however there are few head-to-head comparison studies. Our systematic review, standard meta-analysis and network meta-analysis (NMA) updates the 2009 Cochrane overview, 'Biologics for rheumatoid arthritis (RA)' and adds new data. This review is focused on biologic or tofacitinib therapy in people with RA who had previously been treated unsuccessfully with biologics.

Objectives: To compare the benefits and harms of biologics (abatacept, adalimumab, anakinra, certolizumab pegol, etanercept, golimumab, infliximab, rituximab, tocilizumab) and small molecule tofacitinib versus comparator (placebo or methotrexate (MTX)/other DMARDs) in people with RA, previously unsuccessfully treated with biologics.

Methods: On 22 June 2015 we searched for randomized controlled trials (RCTs) in CENTRAL, MEDLINE, and Embase; and trials registries (WHO trials register, Clinicaltrials.gov). We carried out article selection, data extraction, and risk of bias and GRADE assessments in duplicate. We calculated direct estimates with 95% confidence intervals (CI) using standard meta-analysis. We used a Bayesian mixed treatment comparison (MTC) approach for NMA estimates with 95% credible intervals (CrI). We converted odds ratios (OR) to risk ratios (RR) for ease of understanding. We have also presented results in absolute measures as risk difference (RD) and number needed to treat for an additional beneficial outcome (NNTB). Outcomes measured included four benefits (ACR50, function measured by Health Assessment Questionnaire (HAQ) score, remission defined as DAS < 1.6 or DAS28 < 2.6, slowing of radiographic progression) and three harms (withdrawals due to adverse events, serious adverse events, and cancer).

Main results: This update includes nine new RCTs for a total of 12 RCTs that included 3364 participants. The comparator was placebo only in three RCTs (548 participants), MTX or other traditional DMARD in six RCTs (2468 participants), and another biologic in three RCTs (348 participants). Data were available for four tumor necrosis factor (TNF)-biologics: (certolizumab pegol (1 study; 37 participants), etanercept (3 studies; 348 participants), golimumab (1 study; 461 participants), infliximab (1 study; 27 participants)), three non-TNF biologics (abatacept (3 studies; 632 participants), rituximab (2 studies; 1019 participants), and tocilizumab (2 studies; 589 participants)); there was only one study for tofacitinib (399 participants). The majority of the trials (10/12) lasted less than 12 months.We judged 33% of the studies at low risk of bias for allocation sequence generation, allocation concealment and blinding, 25% had low risk of bias for attrition, 92% were at unclear risk for selective reporting; and 92% had low risk of bias for major baseline imbalance. We downgraded the quality of the evidence for most outcomes to moderate or low due to study limitations, heterogeneity, or rarity of direct comparator trials. Biologic monotherapy versus placeboCompared to placebo, biologics were associated with clinically meaningful and statistically significant improvement in RA as demonstrated by higher ACR50 and RA remission rates. RR was 4.10 for ACR50 (95% CI 1.97 to 8.55; moderate-quality evidence); absolute benefit RD 14% (95% CI 6% to 21%); and NNTB = 8 (95% CI 4 to 23). RR for RA remission was 13.51 (95% CI 1.85 to 98.45, one study available; moderate-quality evidence); absolute benefit RD 9% (95% CI 5% to 13%); and NNTB = 11 (95% CI 3 to 136). Results for withdrawals due to adverse events and serious adverse events did not show any statistically significant or clinically meaningful differences. There were no studies available for analysis for function measured by HAQ, radiographic progression, or cancer outcomes. There were not enough data for any of the outcomes to look at subgroups. Biologic + MTX versus active comparator (MTX/other traditional DMARDs)Compared to MTX/other traditional DMARDs, biologic + MTX was associated with a clinically meaningful and statistically significant improvement in ACR50, function measured by HAQ, and RA remission rates in direct comparisons. RR for ACR50 was 4.07 (95% CI 2.76 to 5.99; high-quality evidence); absolute benefit RD 16% (10% to 21%); NNTB = 7 (95% CI 5 to 11). HAQ scores showed an improvement with a mean difference (MD) of 0.29 (95% CI 0.21 to 0.36; high-quality evidence); absolute benefit RD 9.7% improvement (95% CI 7% to 12%); and NNTB = 5 (95% CI 4 to 7). Remission rates showed an improved RR of 20.73 (95% CI 4.13 to 104.16; moderate-quality evidence); absolute benefit RD 10% (95% CI 8% to 13%); and NNTB = 17 (95% CI 4 to 96), among the biologic + MTX group compared to MTX/other DMARDs. There were no studies for radiographic progression. Results were not clinically meaningful or statistically significantly different for withdrawals due to adverse events or serious adverse events, and were inconclusive for cancer. Tofacitinib monotherapy versus placeboThere were no published data. Tofacitinib + MTX versus active comparator (MTX)In one study, compared to MTX, tofacitinib + MTX was associated with a clinically meaningful and statistically significant improvement in ACR50 (RR 3.24; 95% CI 1.78 to 5.89; absolute benefit RD 19% (95% CI 12% to 26%); NNTB = 6 (95% CI 3 to 14); moderate-quality evidence), and function measured by HAQ, MD 0.27 improvement (95% CI 0.14 to 0.39); absolute benefit RD 9% (95% CI 4.7% to 13%), NNTB = 5 (95% CI 4 to 10); high-quality evidence). RA remission rates were not statistically significantly different but the observed difference may be clinically meaningful (RR 15.44 (95% CI 0.93 to 256.1; high-quality evidence); absolute benefit RD 6% (95% CI 3% to 9%); NNTB could not be calculated. There were no studies for radiographic progression. There were no statistically significant or clinically meaningful differences for withdrawals due to adverse events and serious adverse events, and results were inconclusive for cancer.

Authors' conclusions: Biologic (with or without MTX) or tofacitinib (with MTX) use was associated with clinically meaningful and statistically significant benefits (ACR50, HAQ, remission) compared to placebo or an active comparator (MTX/other traditional DMARDs) among people with RA previously unsuccessfully treated with biologics.No studies examined radiographic progression. Results were not clinically meaningful or statistically significant for withdrawals due to adverse events and serious adverse events, and were inconclusive for cancer.

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Conflict of interest statement

JS ‐ JS has received research grants from Takeda and Savient and consultant fees from Savient, Takeda, Regeneron, Merz, Iroko, Bioiberica, Crealta and Allergan pharmaceuticals, WebMD, UBM LLC and the American College of Rheumatology. JS serves as the principal investigator for an investigator‐initiated study funded by Horizon pharmaceuticals through a grant to DINORA, Inc., a 501 (c)(3) entity. JS is a member of the executive of OMERACT, an organization that develops outcome measures in rheumatology and receives arms‐length funding from 36 companies; a member of the American College of Rheumatology's (ACR) Annual Meeting Planning Committee (AMPC); Chair of the ACR Meet‐the‐Professor, Workshop and Study Group Subcommittee; and a member of the Veterans Affairs Rheumatology Field Advisory Committee.

AH ‐ none

AM ‐ none

EG ‐ none

RB ‐ RB is a Principal Investigator and Chair of the Management Committee of the Australian Rheumatology Association Database (ARAD). The Australian Rheumatology Association receives ongoing unrestricted educational grants from Abbvie, AstraZeneca, Bristol‐Myers Squibb, Celgene, Pfizer and Sanofi to support ARAD.

ML ‐ Research grant from the Rheumatology Research Foundation.

LM ‐ none

MSA ‐ Research grant from Pfizer. Consultant fees from Pfizer.

PT ‐ grants/honoraria from Bristol Myers, Chiltern International, and UCB.

GW ‐ research grant and consultant fee from Bristol‐Myers Squibb.

Figures

2
Network diagram for ACR50 in people with RA who are biologic‐experienced

3
ACR50: biologic monotherapy vs. placebo

4
ACR50: biologic with MTX vs. MTX/DMARD

6
RA remission: biologic with MTX vs. MTX/DMARD

7
Withdrawals due to adverse events: biologic monotherapy vs. placebo

8
Withdrawals due to adverse events: biologic with MTX vs. MTX/DMARD

9
Serious adverse events: biologic with MTX vs. MTX/DMARD

See this image and copyright information in PMC

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[1] Bingham CO 3rd, Rizzo W, Kivitz A, Hassanali A, Upmanyu R, Klearman M. Humoral immune response to vaccines in patients with rheumatoid arthritis treated with tocilizumab: results of a randomised controlled trial (VISARA). Annals of the Rheumatic Diseases 2015;74(5):818‐22. - PMC - PubMed

[2] Bingham CO 3rd, Rizzo W, Kivitz A, Hassanali A, Upmanyu R, Klearman M. Humoral immune response to vaccines in patients with rheumatoid arthritis treated with tocilizumab: results of a randomised controlled trial (VISARA). Annals of the Rheumatic Diseases 2015;74(5):818‐22. - PMC - PubMed

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References

References to included reviews

Bingham 2015

Burmester 2013

Cohen 2006

Emery 2008a

Furst 2007

Genovese 2005

Keystone 2008

Moreland 2002

Schiff 2014b

Smolen 2009

Weinblatt 2007a

Weinblatt 2008

References to excluded reviews

Abe 2006

Axelsen 2015

Bae 2013

Bathon 2000

Bejarano 2008

Bonafede 2015

Boyle 2015

Breedveld 2006

Bresnihan 1998

Burmester 2014

Burmester 2015

Chen 2009

Cheng 2014

Choy 2012

Cohen 2002

Cohen 2003

Cohen 2004

Combe 2006

Combe 2009

Conaghan 2013

Conaghan 2014

Coombs 2010

Detert 2013

Dougados 2013

Dougados 2014

Doyle 2013

Durez 2004

Durez 2007

Edwards 2004

Emery 2006

Emery 2008b

Emery 2010

Emery 2014a

Emery 2014b

Eriksson 2015

Fleischmann 2003

Fleischmann 2009

Fleischmann 2012a

Fleischmann 2012b

Fleischmann 2013

Furst 2003

Furst 2015

Gabay 2013

Gashi 2014

Genovese 2002

Genovese 2004

Genovese 2008

Genovese 2011

Genovese 2014

Genovese 2015

Gherge 2014

Goekoop‐Ruiterman 2007

Haraoui 2014

Heimans 2014

Hobbs 2015

Huizinga 2015

Hørslev‐Petersen 2014

Iannone 2014

Jobanputra 2012

Johnsen 2006