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Meta-Analysis
. 2015 Apr 18;2015(4):CD005468.
doi: 10.1002/14651858.CD005468.pub2.

TNF-alpha inhibitors for ankylosing spondylitis

Lara J Maxwell  1 , Jane Zochling, Annelies Boonen, Jasvinder A Singh, Mirella M S Veras, Elizabeth Tanjong Ghogomu, Maria Benkhalti Jandu, Peter Tugwell, George A Wells
Affiliations
Meta-Analysis

TNF-alpha inhibitors for ankylosing spondylitis

Lara J Maxwell et al. Cochrane Database Syst Rev. .

Abstract

Background: TNF (tumor necrosis factor)-alpha inhibitors block a key protein in the inflammatory chain reaction responsible for joint inflammation, pain, and damage in ankylosing spondylitis.

Objectives: To assess the benefit and harms of adalimumab, etanercept, golimumab, and infliximab (TNF-alpha inhibitors) in people with ankylosing spondylitis.

Search methods: We searched the following databases to January 26, 2009: MEDLINE (from 1966); EMBASE (from 1980); the Cochrane Central Register of Controlled Trials (CENTRAL; 2008, Issue 4); ACP Journal Club; CINAHL (from 1982); and ISI Web of Knowledge (from 1900). We ran updated searches in May 2012, October 2013, and in June 2014 for McMaster PLUS. We searched major regulatory agencies for safety warnings and clinicaltrials.gov for registered trials.

Selection criteria: Randomized controlled trials (RCTs) comparing adalimumab, etanercept, golimumab and infliximab to placebo, other drugs or usual care in patients with ankylosing spondylitis, reported in abstract or full-text.

Data collection and analysis: Two authors independently assessed search results, risk of bias, and extracted data. We conducted Bayesian mixed treatment comparison (MTC) meta-analyses using WinBUGS software. To investigate a class-effect of harms across biologics, we pooled harms data using Review Manager 5.

Main results: We included twenty-one, short-term (24 weeks or less) RCTs with a total of 3308 participants; 18 contributed data to the MTC analysis: adalimumab (4 studies), etanercept (8 studies), golimumab (2 studies), infliximab (3 studies), and one head-to-head study (etanercept versus infliximab) which was unblinded and considered at a higher risk of bias. The risk of selection and detection bias was low or unclear for most of the studies. The risk of selective outcome reporting was low for most studies as they reported on outcomes recommended by the Assessment of SpondyloArthritis international Society. We found little heterogeneity and no significant inconsistency in the MTC analyses. The majority of the studies were funded by pharmaceutical companies. Most studies permitted concomitant therapy of stable doses of disease-modifying anti-rheumatic drugs, non-steroidal anti-inflammatory drugs, or corticosteroids, but allowances varied across studies.Compared with placebo, there was high quality evidence that patients on an anti-TNF agent were three to four times more likely to achieve an ASAS40 response (assessing spinal pain, function, and inflammation, as measured by the mean of intensity and duration of morning stiffness, and patient global assessment) by six months (adalimumab: risk ratio (RR) 3.53, 95% credible interval (Crl) 2.49 to 4.91; etanercept: RR 3.31, 95% Crl 2.38 to 4.53; golimumab: RR 2.90, 95% Crl 1.90 to 4.23; infliximab: RR 4.07, 95% Crl 2.80 to 5.74, with a 25% to 40% absolute difference between treatment and placebo groups. The number needed to treat (NNT) to achieve an ASAS 40 response ranged from 3 to 5.There was high quality evidence of improvement in physical function on a 0 to 10 scale (adalimumab: mean difference (MD) -1.6, 95% Crl -2.2 to -0.9; etanercept: MD -1.1, 95% CrI -1.6 to -0.6; golimumab: MD -1.5, 95% Crl -2.3 to -0.7; infliximab: MD -2.1, 95% Crl -2.7 to -1.4, with an 11% to 21% absolute difference between treatment and placebo groups. The NNT to achieve the minimally clinically important difference of 0.7 points ranged from 2 to 4.Compared with placebo, there was moderate quality evidence (downgraded for imprecision) that patients on an anti-TNF agent were more likely to achieve an ASAS partial remission by six months (adalimumab: RR 6.28, 95% Crl 3.13 to 12.78; etanercept: RR 4.24, 95% Crl 2.31 to 8.09; golimumab: RR 5.18, 95% Crl 1.90 to 14.79; infliximab: RR 15.41, 95% Crl 5.09 to 47.98 with a 10% to 44% absolute difference between treatment and placebo groups. The NNT to achieve an ASAS partial remission response ranged from 3 to 11.There was low to moderate level evidence of a greater reduction in spinal inflammation as measured by magnetic resonance imaging though the absolute differences were small and the clinical relevance of the difference was unclear: adalimumab (1 trial; -6% (95% confidence interval (CI) -12% to 0.05%); 1 trial: 53.6% mean decrease from baseline versus 9.4% mean increase in the placebo group), golimumab (1 trial; -2.5%, (95% CI -5.6% to -0.7%)), and infliximab (1 trial; -3% (95% CI -4% to -2.4%)).Radiographic progression was measured in one trial (N = 60) of etanercept versus placebo and it found that radiologic changes were similar in both groups (detailed data not provided).There were few events of withdrawals due to adverse events leading to imprecision around the estimates. When all the anti-TNF agents were combined against placebo, there was moderate quality evidence from 16 studies of an increased risk of withdrawals due to adverse events in the anti-TNF group (Peto odds ratio (OR) 2.44, 95% CI 1.26 to 4.72; total events: 38/1637 in biologic group; 7/986 in placebo) though the absolute increase in harm was small (1%; 95% CI 0% to 2%).Due to low event rates, evidence of the effect of individual TNF-inhibitors against placebo or for all four biologics pooled together versus placebo on serious adverse events is inconclusive (moderate quality; downgraded for imprecision). For all anti-TNF pooled versus placebo based on 16 studies: Peto OR 1.45, 95% CI 0.85 to 2.48; 51/1530 in biologic group; 18/878 in placebo; absolute difference: 1% (95% CI 0% to 2%).Using indirect comparison methodology, and one head-to-head study of etanercept versus infliximab, wide confidence intervals meant that results were inconclusive for evidence of differences in the major outcomes between different anti-TNF agents. Regulatory agencies have published warnings about rare adverse events of serious infections, including tuberculosis, malignancies and lymphoma.

Authors' conclusions: There is moderate to high quality evidence that anti-TNF agents improve clinical symptoms in the treatment of ankylosing spondylitis. More participants withdrew due to adverse events when on an anti-TNF agent but we did not find evidence of an increase in serious adverse events, though event rates were low and trials had a short duration. The short-term toxicity profile appears acceptable. Based on indirect comparison methodology, we are uncertain whether there are differences between anti-TNF agents in terms of the key benefit or harm outcomes.

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Conflict of interest statement

We received a National Institute for Health Research (NIHR) Cochrane Incentive Award to assist with the completion of this review.

  1. LJM: was an associate member of the Assessment of SpondyloArthritis international Society from 2005 to 2014.

  2. JZ: none known

  3. AB: Grants: to department only: Abbvie, Pfizer, Merck, Amgen Travel support to department: Janssen‐Cilag; Honorarium: part to department, part personally: Pfizer, UCB, Janssen‐Cilag, Abbvie

  4. JAS: received research grants from Takeda and Savient and consultant fees from Savient, Takeda, Regeneron and Allergan. JAS 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 Guidelines Subcommittee of the Quality of Care Committee; and a member of the Veterans Affairs Rheumatology Field Advisory Committee.

  5. ETG: none known.

  6. MV: none known.

  7. MBJ: none known.

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

  9. GW: none known

Figures

1
1
Study flow chart
 Note: October 2013 search included retrospective search for golimumab from database inception
2
2
Methodological quality summary: review authors' judgements about each methodological quality item for each included study.
3
3
ASAS40 Evidence Diagram
4
4
Forest Plot: ASAS40
5
5
Forest Plot: Withdrawals due to adverse events
6
6
ASAS40: Plot of Posterior Mean Deviance of the Individual Data Points in the Inconsistency Model against Their Posterior Mean Deviance in the Consistency Model
1.1
1.1. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 1 BASFI (0‐10 VAS).
1.2
1.2. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 2 ASAS 40.
1.3
1.3. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 3 ASAS partial remission.
1.4
1.4. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 4 MRI SPARCC score (lumbar spine; scale 0‐108).
1.5
1.5. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 5 MRI SPARCC score (sacroiliac joint; scale 0‐72)).
1.6
1.6. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 6 Withdrawals due to adverse events.
1.7
1.7. Analysis
Comparison 1 Adalimumab versus placebo, Outcome 7 Serious adverse events.
2.1
2.1. Analysis
Comparison 2 Infliximab versus placebo, Outcome 1 ASAS 40.
2.2
2.2. Analysis
Comparison 2 Infliximab versus placebo, Outcome 2 BASFI.
2.3
2.3. Analysis
Comparison 2 Infliximab versus placebo, Outcome 3 ASAS partial remission.
2.4
2.4. Analysis
Comparison 2 Infliximab versus placebo, Outcome 4 Serious adverse events.
2.5
2.5. Analysis
Comparison 2 Infliximab versus placebo, Outcome 5 Withdrawals due to adverse events.
2.6
2.6. Analysis
Comparison 2 Infliximab versus placebo, Outcome 6 Spinal inflammation (MRI activity score (0‐138)).
2.7
2.7. Analysis
Comparison 2 Infliximab versus placebo, Outcome 7 Spinal inflammation (MRI Activity score >1).
3.1
3.1. Analysis
Comparison 3 Golimumab versus placebo, Outcome 1 ASAS40.
3.2
3.2. Analysis
Comparison 3 Golimumab versus placebo, Outcome 2 BASFI.
3.3
3.3. Analysis
Comparison 3 Golimumab versus placebo, Outcome 3 ASAS partial remission.
3.4
3.4. Analysis
Comparison 3 Golimumab versus placebo, Outcome 4 ASspiMRI‐a change from baseline (spinal inflammation, score 0‐138)).
3.5
3.5. Analysis
Comparison 3 Golimumab versus placebo, Outcome 5 Withdrawals due to adverse events.
3.6
3.6. Analysis
Comparison 3 Golimumab versus placebo, Outcome 6 Serious adverse event.
4.1
4.1. Analysis
Comparison 4 Etanercept (25 mg twice weekly or 50mg once weekly) versus placebo, Outcome 1 ASAS 40.
4.2
4.2. Analysis
Comparison 4 Etanercept (25 mg twice weekly or 50mg once weekly) versus placebo, Outcome 2 BASFI (0‐10 scale, none to severe limitations).
4.3
4.3. Analysis
Comparison 4 Etanercept (25 mg twice weekly or 50mg once weekly) versus placebo, Outcome 3 ASAS Partial remission.
4.4
4.4. Analysis
Comparison 4 Etanercept (25 mg twice weekly or 50mg once weekly) versus placebo, Outcome 4 Withdrawals due to adverse events.
4.5
4.5. Analysis
Comparison 4 Etanercept (25 mg twice weekly or 50mg once weekly) versus placebo, Outcome 5 Serious adverse events.
5.1
5.1. Analysis
Comparison 5 Etanercept versus infliximab, Outcome 1 ASAS40 ‐ 12 weeks.
5.2
5.2. Analysis
Comparison 5 Etanercept versus infliximab, Outcome 2 BASFI ‐ 12 weeks.
6.1
6.1. Analysis
Comparison 6 Etanercept versus sulphasalazine, Outcome 1 ASAS40 ‐ 16‐week.
6.2
6.2. Analysis
Comparison 6 Etanercept versus sulphasalazine, Outcome 2 BASFI.
6.3
6.3. Analysis
Comparison 6 Etanercept versus sulphasalazine, Outcome 3 ASAS Partial remission.
6.4
6.4. Analysis
Comparison 6 Etanercept versus sulphasalazine, Outcome 4 Withdrawals due to adverse events.
6.5
6.5. Analysis
Comparison 6 Etanercept versus sulphasalazine, Outcome 5 Serious adverse events.
7.1
7.1. Analysis
Comparison 7 Infliximab + methotrexate versus placebo + methotrexate, Outcome 1 BASDAI.
7.2
7.2. Analysis
Comparison 7 Infliximab + methotrexate versus placebo + methotrexate, Outcome 2 ASAS20.
7.3
7.3. Analysis
Comparison 7 Infliximab + methotrexate versus placebo + methotrexate, Outcome 3 > 50% BASDAI.
8.1
8.1. Analysis
Comparison 8 TNF‐inhibitors versus placebo, Outcome 1 Withdrawals due to AE.
8.2
8.2. Analysis
Comparison 8 TNF‐inhibitors versus placebo, Outcome 2 Serious adverse events.
See this image and copyright information in PMC

Update of

  • doi: 10.1002/14651858.CD005468

References

References to studies included in this review

Bao 2014 {published data only}
    1. Bao C, Huang F, Khan MA, Fei K, Zhong W, Han C, et al. Safety and efficacy of golimumab in Chinese patients with active ankylosing spondylitis: 1‐year results of a multicentre, randomized, double‐blind, placebo‐controlled phase III trial. Rheumatology 2014;53:1654‐63. - PubMed
Barkham 2010 {published data only}
    1. Barkham N, Coates L, Keen H, Hensor E, Fraser A, Redmond A, et al. A double blind placebo controlled trial of etanercept in the prevention of work disability in ankylosing spondylitis. Rheumatology 2008;47:ii72. - PubMed
    1. Barkham N, Coates LC, Keen H, Hensor E, Fraser A, Redmond A, et al. Double‐blind placebo‐controlled trial of etanercept in the prevention of work disability in ankylosing spondylitis. Annals of the Rheumatic Diseases 2010;69(11):1926‐8. - PubMed
Brandt 2003 {published and unpublished data}
    1. Brandt J, Khariouzov A, Listing J, Haibel H, Sorensen H, Grassnickel L. Six‐month results of a double‐blind, placebo‐controlled trial of etanercept treatment in patients with active ankylosing spondylitis. Arthritis and Rheumatism 2003;48:1667‐75. - PubMed
Braun 2002 {published and unpublished data}
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Braun 2011 {published data only}
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    1. Sieper J, Moots R, Taylor A, Sato R, Singh A, Roberson D, et al. Assessment of patient‐reported outcomes from a randomized, double‐blind study of etanercept and sulphasalazine in patients with ankylosing spondylitis. Arthritis and Rheumatism. 2008; Vol. 58:S580.
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Dougados 2011 {published data only}
    1. Dougados M, Braun J, Szanto S, Combe B, Elbaz M, Geher P, et al. Efficacy of etanercept on rheumatic signs and pulmonary function tests in advanced ankylosing spondylitis: Results of a randomised double‐blind placebo‐controlled study (SPINE). Annals of the Rheumatic Diseases 2011;70:799‐804. [DOI: 10.1136/ard.2010.139261] - DOI - PMC - PubMed
Giardina 2009 {published data only}
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    1. Giardina AR, Ferrante A, Ciccia F, Impastato R, Miceli M, Principato A, et al. A 2‐year comparative open label randomized study of efficacy and safety of etanercept and infliximab in patients with ankylosing spondylitis. Rheumatology International 2009 October 23 [Epub ahead of print]. [DOI: 10.1007/s00296-009-1157-3] - DOI - PubMed
    1. Impastato R, Ciccia F, Ferrante A, Principato A, Giardina A, Cadelo M, et al. Infliximab and etanercept are both effective and safe in patients with ankylosing spondylitis. A two‐year randomised study. Annals of the Rheumatic Diseases 2007;66(Suppl II):399.
Gorman 2002 {published data only}
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Hu 2012 {published data only}
    1. Hu Z, Xu M, Qiuxia L, Zhiming L, Liao Z, Cao S, et al. Adalimumab significantly reduces inflammation and serumDKK‐1 level but increases fatty deposition in lumbar spine inactive ankylosing spondylitis. International Journal of Rheumatic Diseases 2012;15:358‐65. - PubMed
Huang 2008 {published data only}
    1. Huang F, MacPeek D, Shunle C, Li Z, Gu J, Wu D, et al. Etanercept is effective and well tolerated in Chinese patients with ankylosing spondylitis: 6‐week placebo‐controlled trial followed by 6‐week open‐label treatment. Annals of the Rheumatic Diseases. 2008; Vol. 67:Suppl II: 521.
    1. Huang F, Zhang J, Huang JL, Wu DH, Li ZG, Chen SL, et al. A multicenter, double‐blind, placebo‐controlled, randomized, phase III clinical study of etanercept in treatment of ankylosing spondylitis. Zhonghua Nei Ke Za Zhi (Chinese Journal of Internal Medicine) 2010;49:741–5. - PubMed
Huang 2014 {published data only}
    1. Huang F, Gu J, Zhu P, Bao C, Xu, J, Xu H, et al. Efficacy and safety of adalimumab in Chinese adults with active ankylosing spondylitis: results of a randomised, controlled trial. Annals of the Rheumatic Diseases 2014;73:587‐94. [DOI: 10.1136/annrheumdis-2012-202533] - DOI - PubMed
Inman 2008 {published data only}
    1. Braun J, Baraliakos X, Hermann KG, Heijde D, Inman RD, Deodhar AA, et al. Golimumab reduces spinal inflammation in ankylosing spondylitis: MRI results of the randomised, placebo‐controlled GO‐RAISE study. Annals of the Rheumatic Diseases 2012;71(6):878‐84. [DOI: 10.1136/annrheumdis-2011-200308] - DOI - PMC - PubMed
    1. Inman RD, Davis JC Jr, Heijde Dv, Diekman L, Sieper J, Kim SI, et al. Efficacy and safety of golimumab in patients with ankylosing spondylitis: results of a randomized, double‐blind, placebo‐controlled, phase III trial. Arthritis and Rheumatism 2008;58(11):3402‐12. - PubMed
Inman 2010 {published data only}
    1. Inman R, Maksymowych W, CANDLE group. A double‐blind, placebo‐controlled trial of low dose infliximab in ankylosing spondylitis. Journal of Rheumatology 2010;37(6):1‐8. [DOI: ] - PubMed
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    1. Maksymowych W, Salonen D, Inman R, Paul FL, Lambert RG. CANaDian evaluation of Low dosE Infliximab in Ankylosing Spondylitis (CANDLE) ‐ 12 week magnetic resonance imaging evaluation of spinal inflammation with the SPARCC MRI method. Journal of Rheumatology 2008;35(6):1211‐12.
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Lambert 2007 {published data only}
    1. Lambert RGW, Salonen D, Rahman P, Inman RD, Wong RL, Einstein SG, et al. Adalimumab significantly reduces both spinal and sacroiliac joint inflammation in patients with ankylosing spondylitis. Arthritis and Rheumatism 2007;56(12):4005‐14. - PubMed
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Marzo‐Ortega 2005 {published data only}
    1. Marzo‐Ortega H, McGonagle D, Jarrett S, Haugeberg G, Hensor E, O'Connor P, et al. Infliximab in combination with methotrexate in active ankylosing spondylitis: A clinical and imaging study. Annals of the Rheumatic Diseases 2005;64(11):1568‐75. - PMC - PubMed
Navarro‐Sarabia 2011 {published data only}
    1. Navarro‐Sarabia F, Fernandez‐Sueiro JL, Torre‐Alonso JC, Gratacos J, Queiro R, Gonzalez C, et al. High‐dose etanercept in ankylosing spondylitis: results of a 12‐week randomized, double blind, controlled multicentre study (LOADET study). Rheumatology 2011;50(10):1828‐37. - PubMed
van der Heijde 2005 {published data only}
    1. Braun J, Deodhar A, Dijkmans B, Geusens P, Sieper J, Williamson P, et al. Efficacy and safety of infliximab in patients with ankylosing spondylitis over a two‐year period. Arthritis and Rheumatism 2008;59:1270‐8. - PubMed
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van der Heijde 2006a {published and unpublished data}
    1. Davis Jr JC, Revicki D, Heijde DMF, Rentz AM, Wong RL, Kupper H, et al. Health‐related quality of life outcomes in patients with active ankylosing spondylitis treated with adalimumab: Results from a randomized controlled study. Arthritis Care and Research 2007; Vol. 57, issue 6:1050‐7. [DOI: 10.1002/art.22887] - DOI - PubMed
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    1. Heijde D, Dijkmans B, Schiff M, Kivitz A, Vlam K, Wordsworth P, et al. Maintenance of reduction in disease activity and partial remission in patients with ankylosing spondylitis (AS) ‐ 3 year results from the adalimumab (Humira) trial evaluating long‐term efficacy and safety in AS (ATLAS). Arthritis and Rheumatism. 2008:S579.
    1. Heijde D, Kivitz A, Schiff MH, Sieper J, Dijkmans BAC, Braun J, ATLAS study group. Efficacy and safety of adalimumab in patients with ankylosing spondylitis. Arthritis and Rheumatism 2006;54(7):2136‐46. - PubMed
    1. Heijde D, Schiff M, Sieper J, Kivitz A, Wong R, Kupper H, et al. Adalimumab effectiveness for the treatment of ankylosing spondylitis is maintained for up to 2 years: long‐term results from the ATLAS trial. Annals of the Rheumatic Diseases 2009;68:922‐9. - PMC - PubMed
van der Heijde 2006b {published data only}
    1. Braun J, McHugh N, Singh A, Wajdula JS, Sato R. Improvement in patient‐reported outcomes for patients with ankylosing spondylitis treated with etanercept 50 mg once‐weekly and 25 mg twice‐weekly. Rheumatology 2007;46(6):999‐1004. - PubMed
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References to studies excluded from this review

Barkham 2008b {published data only}
    1. Barkham N, Keen HI, Coates P, O'Connor EMA, Hensor AD, Fraser LS, et al. A randomized controlled trial of infliximab shows clinical and MRI efficacy in HLA B27 positive very early ankylosing spondylitis. Annals of the Rheumatic Diseases. 2008; Vol. 67:Suppl II:382.
Breban 2008 {published data only}
    1. Breban M, Ravaud P, Claudepierre P, Baron G, Henry Y‐D, Hudry C, et al. Maintenance of infliximab treatment in ankylosing spondylitis: Results of a one‐year randomized controlled trial comparing systematic versus on‐demand treatment. Arthritis and Rheumatism 2008;58(1):88‐97. [DOI: 10.1002/art.23167] - DOI - PubMed
Haibel 2008 {published data only}
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References to other published versions of this review

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