Skip to main content

Main menu

  • Home
  • Content
    • First Release
    • Current
    • Archives
    • Collections
    • Audiovisual Rheum
    • COVID-19 and Rheumatology
    • 50th Volume Reprints
  • Resources
    • Guide for Authors
    • Submit Manuscript
    • Payment
    • Reviewers
    • Advertisers
    • Classified Ads
    • Reprints and Translations
    • Permissions
    • Meetings
    • FAQ
    • Policies
  • Subscribers
    • Subscription Information
    • Purchase Subscription
    • Your Account
    • Terms and Conditions
  • About Us
    • About Us
    • Editorial Board
    • Letter from the Editor
    • Duncan A. Gordon Award
    • Privacy/GDPR Policy
    • Accessibility
  • Contact Us
  • JRheum Supplements
  • Services

User menu

  • My Cart
  • Log In

Search

  • Advanced search
The Journal of Rheumatology
  • JRheum Supplements
  • Services
  • My Cart
  • Log In
The Journal of Rheumatology

Advanced Search

  • Home
  • Content
    • First Release
    • Current
    • Archives
    • Collections
    • Audiovisual Rheum
    • COVID-19 and Rheumatology
    • 50th Volume Reprints
  • Resources
    • Guide for Authors
    • Submit Manuscript
    • Payment
    • Reviewers
    • Advertisers
    • Classified Ads
    • Reprints and Translations
    • Permissions
    • Meetings
    • FAQ
    • Policies
  • Subscribers
    • Subscription Information
    • Purchase Subscription
    • Your Account
    • Terms and Conditions
  • About Us
    • About Us
    • Editorial Board
    • Letter from the Editor
    • Duncan A. Gordon Award
    • Privacy/GDPR Policy
    • Accessibility
  • Contact Us
  • Follow jrheum on Twitter
  • Visit jrheum on Facebook
  • Follow jrheum on LinkedIn
  • Follow jrheum on YouTube
  • Follow jrheum on Instagram
  • Follow jrheum on RSS
Research ArticleOMERACT 12 — International Consensus Conference on Outcome Measures in Rheumatology, Budapest, Hungary, May 7–11, 2014

Evaluation of Minimally Invasive, Ultrasound-guided Synovial Biopsy Techniques by the OMERACT Filter — Determining Validation Requirements

Frances Humby, Stephen Kelly, Serena Bugatti, Antonio Manzo, Andrew Filer, Arti Mahto, Joao Eurico Fonseca, Bernard Lauwerys, Maria-Antonietta D’Agostino, Esperanza Naredo, Rik Lories, Carlomaurizio Montecucco, Paul Peter Tak, Oliver Fitzgerald, Malcolm D. Smith, Douglas J. Veale, Ernest H. Choy, Vibeke Strand and Costantino Pitzalis
The Journal of Rheumatology January 2016, 43 (1) 208-213; DOI: https://doi.org/10.3899/jrheum.141199
Frances Humby
From the Centre for Experimental Medicine and Rheumatology, William Harvey Research Institute at Barts, and the London School of Medicine and Dentistry, Queen Mary University of London, London, UK; Rheumatology and Translational Immunology Research Laboratories (LaRIT), Division of Rheumatology, IRCCS Policlinico San Matteo Foundation/University of Pavia, Pavia, Italy; Rheumatology Research Group, School of Immunity and Infection, College of Medical and Dental Sciences, University of Birmingham, Edgbaston, Birmingham, UK; Rheumatology Research Unit, Instituto de Medicina Molecular, Faculdade de Medicina da Universidade de Lisboa, and Rheumatology Department, Lisbon Academic Medical Centre, Lisbon, Portugal; Institut de Recherche Expérimentale et Clinique, Université Catholique de Louvain and Department of Rheumatology, Cliniques Universitaires Saint-Luc, Brussels, Belgium; Rheumatology Department, Ambroise Paré Hospital, APHP, Université Versailles Saint Quentin en Yvelines, Inserm U987, Boulogne-Billancourt, France; Rheumatology Department, Hospital Universitario Severo Ochoa, Madrid, Spain; Laboratory for Skeletal Development and Joint Disorders, Department of Development and Regeneration, KU Leuven, Leuven, Belgium; University of Cambridge, Cambridge, UK; GlaxoSmithKline Research and Development, Stevenage, UK; School of Medicine and Medical Science, St. Vincent’s University Hospital, Dublin, Ireland; Rheumatology Research Unit, Repatriation General Hospital, Daw Park, South Australia; Dublin Academic Medical Centre, The Conway Institute of Biomedical and Biomolecular Research, University College Dublin, Dublin, Ireland; Cardiff Institute of Infection and Immunity, Cardiff Regional Experimental Arthritis Treatment and Evaluation Centre, Cardiff, UK; Division of Immunology/Rheumatology, Stanford University School of Medicine, Stanford, California, USA.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stephen Kelly
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Serena Bugatti
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Antonio Manzo
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Andrew Filer
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Arti Mahto
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joao Eurico Fonseca
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Bernard Lauwerys
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Maria-Antonietta D’Agostino
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Esperanza Naredo
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rik Lories
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Carlomaurizio Montecucco
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Paul Peter Tak
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Oliver Fitzgerald
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Malcolm D. Smith
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Douglas J. Veale
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ernest H. Choy
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Vibeke Strand
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Costantino Pitzalis
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: c.pitzalis@qmul.ac.uk
  • Article
  • Figures & Data
  • Info & Metrics
  • References
  • PDF
  • eLetters
PreviousNext
Loading

Abstract

Objective. Because limited data currently support the clinical utility of peripherally expressed biomarkers in guiding treatment decisions for patients with rheumatoid arthritis, the search has turned to the disease tissue. The strategic aim of the Outcome Measures in Rheumatology (OMERACT) synovitis working group over the years has been to develop novel diagnostic and prognostic synovial biomarkers. A critical step in this process is to refine and validate minimally invasive, technically simple, robust techniques to sample synovial tissue, for use both in clinical trials and routine clinical practice. The objective of the synovitis working group (SWG) at OMERACT 12 (2014) was to examine whether recently developed ultrasound (US)-guided synovial biopsy techniques could be validated according to the OMERACT filter for future clinical use recommendation.

Methods The SWG examined whether current data reporting US-guided synovial biopsy of both large and small joints addressed the OMERACT filters of truth, discrimination, and feasibility.

Results. There are currently limited data examining the performance of US-guided synovial biopsy, mainly from observational studies. Thus, it remains critical to evaluate its performance, within the clinical trials context, against the current gold standard of arthroscopic biopsy, with particular reference to: (1) synovial tissue yield, (2) capacity to determine treatment response as measured by a validated synovial biomarker, and (3) tolerability of the procedure.

Conclusion. We summarize the discrete work packages agreed to as requirements to validate US-guided synovial biopsy and therefore lead to a global consensus on the use of synovial biopsy for research and clinical practice.

Key Indexing Terms:
  • SYNOVITIS
  • BIOPSY
  • RHEUMATOID ARTHRITIS
  • ULTRASOUND

In the past 2 decades the critical association between ongoing synovitis and structural damage in patients with rheumatoid arthritis (RA) has been recognized and has contributed to a paradigm shift in treatment with a sustained treat-to-target approach, now accepted as “gold standard” therapy1. In part fueled by the development of novel biologic agents, this approach has generated significant longterm improvements2. However, our ability to induce sustained remission and/or cure on an individual level remains limited, with insufficient information to guide selection of therapy based on prognosis and/or predicted response to treatment3. Because limited data currently support the clinical utility of peripherally expressed biomarkers4,5,6,7, focus has turned to the use of synovial tissue biomarkers8,9,10,11,12,13. This is consistent with practice in other medical specialties such as oncology, where examination of pathobiological specimens from disease tissue have demonstrated prognostic value and are now integrated into standard care. In RA, however, synovial biopsy is not currently considered as a standard intervention in either routine care or in randomized controlled trials (RCT) for a variety of reasons14. Thus, the strategic aims and objectives of the Outcome Measures in Rheumatology (OMERACT) synovitis working group (SWG) are to develop a minimally invasive, simple, well-tolerated, and robust technique to sample synovial tissue from most patients/joints to use in turn to develop novel diagnostic/prognostic biomarkers15,16.

The objective of the SWG at OMERACT 12 (2014) was, therefore, to examine whether recently developed ultrasound (US)-guided synovial biopsy techniques could be validated and recommended for future use to monitor therapeutic responses in RCT and/or for patient stratification.

Current Status on Synovial Tissue Acquisition

Acquisition of synovial tissue using an arthroscopic approach in RCT is currently recommended14 based on: (1) extensive data confirming the safety and tolerability of the procedure17,18,19, (2) its ability to sample synovial tissue from multiple sites within the joint, and (3) the means to sample joints with minimal synovitis20. However, outside of highly specialized centers, routine arthroscopic sampling of synovial tissue has not been widely adopted. This is due to a number of factors: technical training required for the procedure19, economic cost of the required equipment and capacity/infrastructure19,21, and the general acceptability of a relatively invasive technique to patients and/or their rheumatologists. Importantly, based on the recognition that small joint involvement is often prominent in early arthritis22, and large joint involvement is associated with more severe and established disease23, there is increasing interest in acquiring synovial tissue from small synovial joints24,25 to understand the early stages of disease pathogenesis by clearly distinguishing mechanistic pathways, as well as to ensure the recruitment of representative RA cohorts into RCT. However, even with small-bore arthroscopy26, the limitations of the procedure remain. Unless less-invasive techniques are validated, synovial biopsy is unlikely to be widely adopted.

Thus techniques using US to direct synovial tissue sampling are attractive: they are minimally invasive, applicable to both large and small joints, relatively inexpensive to perform, and technically simple. Two principal techniques for performance have been described: a portal and forceps (P&F) approach27 and more recently, adaptation using a quick core needle28. Both techniques use US to locate a suitable area of synovial tissue to biopsy. The P&F approach uses a 14–16G introducer, guide wire, and coaxial sheath. The coaxial sheath remains in situ during the procedure and facilitates repeated introduction of biopsy forceps to the joint. Conversely, the US-needle biopsy (NB) technique uses either a 14- or 16-G needle repeatedly entered into the joint without requiring insertion of a relatively larger coaxial sheath (Figure 1).

Figure 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 1.

US-guided synovial biopsy. A. US-guided needle biopsy (NB) of the metacarpophalangeal (MCP) joint; inset shows transverse US image of biopsy needle (BN) insertion into MCP joint space (MH, metacarpal head). B. US-guided NB of wrist joint. Inset illustrates transverse image of biopsy needle insertion into wrist joint under extensor digitorum (ED) tendon. C. US-guided synovial biopsy of knee joint. Inset illustrates transverse image of biopsy needle insertion into suprapatellar pouch (SPP; P: patellar). US: ultrasound.

Although US-guided biopsies may offer distinct advantages over arthroscopic sampling (Table 1), this approach cannot be recommended for use within RCT until it has been shown to fulfill the OMERACT filter of truth, discrimination, and feasibility.

View this table:
  • View inline
  • View popup
Table 1.

Relative merits of techniques currently used in clinical trials to sample synovial tissue.

MATERIALS AND METHODS

The SWG met at OMERACT 12 (2014) to discuss currently available data examining the performance of US-guided synovial biopsy against the OMERACT filters of truth, discrimination, and feasibility and to define future discrete work packages to validate the technique for use in clinical trials.

RESULTS

OMERACT Filter “Truth”

Synovial biopsy of large joints

US-guided synovial biopsies of large joints using a P&F29,30 and NB approaches have been reported with success rates of 89–93%28,30 for histopathological analyses and extraction of good-quality RNA from all samples reported. To overcome the heterogeneity of synovial tissue sampling in large joints, current OMERACT recommendations include acquisition from separate sites of at least 6 biopsies for histopathological and gene expression analysis, respectively14. Such a standard has not been evaluated for either US-guided technique. Given the distinct differences in biopsy tools (i.e., forceps vs needle), it is also critical to evaluate the yield of synovial tissue (histopathological and RNA) between each technique and to compare these data against the current gold standard of arthroscopy.

Small joint biopsy

Data support the use of US-guided biopsy of small joints using both the P&F27 and NB techniques28. However, in comparison with extensive validation data available for large joint biopsies, limited data are available for small joints. One report indicates that US-P&F biopsy of small joints28 provides sufficient tissue for reliable histopathological assessment; however, this validation exercise was restricted to defining the biopsy area (rather than biopsy number) and therefore is difficult to extrapolate to routine practice. Further, given the interest in sampling small joints with minimal synovitis, particularly following effective treatment, it is also important to recognize that serial sampling using US-NB has been reported to be feasible28 whereas US-P&F approach has not, primarily because of the challenge of inserting a larger coaxial sheath into minimally inflamed joints. As with large joints, currently there has been no systematic examination of overall yield of synovial tissue sampled using US-NB from small joints.

Therefore, key steps to be addressed before US-guided needle biopsy of small joints can be recommended in RA include: (1) to define the minimum number of biopsies required per procedure to ensure accurate histopathological assessment and adequate RNA yield; and (2) to systematically address whether US-guided biopsy reaches these defined standards for small joints.

OMERACT Filter “Discrimination”

The number of sublining CD68+ macrophages remains the only validated synovial biomarker recommended by OMERACT, with data to indicate that it varies according to clinical response31 and is not modulated by ineffective therapy32. Its performance, using arthroscopic biopsies within the setting of multicenter RCT, has been reported33,34. However, whether the sublining macrophage number obtained from synovial tissue using US-guided biopsies discriminates between clinical disease states and active therapy has not been reported, and examining this within the context of a clinical trial remains an important validation step.

OMERACT Filter “Feasibility”

When considering the feasibility for broad adoption of US-guided biopsy into RCT and routine clinical care, a crucial step will be determination of its acceptability to patients. Although there are data to support the safety of both US-NB28 and US-P&F30 and acceptable tolerability of US-NB in a small cohort28, both will require further evaluation, including through the application of patient questionnaires within large RCT. Further, examining a “learning curve” for clinicians undergoing training in US-guided synovial biopsy by defining numbers of observed/supervised procedures would be of critical importance to permit the development of robust training requirements for trainees.

Applying US-guided synovial biopsy to RCT

Evidence from observational studies already indicate that synovial biomarkers can predict responses to biologic therapy in RA9,35,36, and this hypothesis is currently being examined in 2 UK-wide RCT funded by: (1) the R4RA (National Institute for Health Research: Response, Relapse, Resistance to Rituximab study); and (2) STRAP (Stratification of Biologic Therapies for Rheumatoid Arthritis by Pathobiology study), jointly funded by the Medical Research Council and Arthritis Research UK. Such trials are critical to thoroughly examine whether synovial biopsy offers clinical utility in the unbiased environment of a RCT. This would address 1 of the core aims of the SWG, because US-guided biopsy is incorporated into both of the above RCT protocols, while the comparison of sampling methods with arthroscopy using descriptive, correlation, and reliability statistics will provide a unique platform to examine the performance of the procedures in the context of multicenter RCT. Critical research questions posed within the studies will also offer the opportunity to perform a resource use/economic impact assessment, as a core domain included within the recently revised OMERACT Filter 2.0 framework37.

The principal research agenda set by the SWG at OMERACT 12 is to deliver the discrete work packages that will lead to a global consensus on the use of synovial biopsy for research and clinical practice. Further, a systematic literature review of currently available synovial biopsy techniques in the context of clinical trials will be performed. The discrete work packages are summarized in Table 2 and focus on validation of a minimally invasive synovial biopsy technique for both small and large joints in RA — critical to facilitate the group’s overarching aim to identify synovial biomarkers for treatment response, diagnosis, and/or prognosis.

View this table:
  • View inline
  • View popup
Table 2.

Summary of planned validation exercises to evaluate US-guided synovial biopsy versus arthroscopy according to the OMERACT filter.

REFERENCES

  1. 1.↵
    1. Schoels M,
    2. Knevel R,
    3. Aletaha D,
    4. Bijlsma JW,
    5. Breedveld FC,
    6. Boumpas DT,
    7. et al.
    Evidence for treating rheumatoid arthritis to target: results of a systematic literature search. Ann Rheum Dis 2010;69:638–43.
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    1. Breedveld FC,
    2. Combe B
    . Understanding emerging treatment paradigms in rheumatoid arthritis. Arthritis Res Ther 2011;13:S3.
    OpenUrlPubMed
  3. 3.↵
    1. Choy EH,
    2. Kavanaugh AF,
    3. Jones SA
    . The problem of choice: current biologic agents and future prospects in RA. Nat Rev Rheumatol 2013;9:154–63.
    OpenUrlCrossRefPubMed
  4. 4.↵
    1. Sekiguchi N,
    2. Kawauchi S,
    3. Furuya T,
    4. Inaba N,
    5. Matsuda K,
    6. Ando S,
    7. et al.
    Messenger ribonucleic acid expression profile in peripheral blood cells from RA patients following treatment with an anti-TNF-alpha monoclonal antibody, infliximab. Rheumatology 2008;47:780–8.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Lequerre T,
    2. Gauthier-Jauneau AC,
    3. Bansard C,
    4. Derambure C,
    5. Hiron M,
    6. Vittecoq O,
    7. et al.
    Gene profiling in white blood cells predicts infliximab responsiveness in rheumatoid arthritis. Arthritis Res Ther 2006;8:R105.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Koczan D,
    2. Drynda S,
    3. Hecker M,
    4. Drynda A,
    5. Guthke R,
    6. Kekow J,
    7. et al.
    Molecular discrimination of responders and nonresponders to anti-TNF alpha therapy in rheumatoid arthritis by etanercept. Arthritis Res Ther 2008;10:R50.
    OpenUrlCrossRefPubMed
  7. 7.↵
    1. Marotte H,
    2. Maslinski W,
    3. Miossec P
    . Circulating tumour necrosis factor-alpha bioactivity in rheumatoid arthritis patients treated with infliximab: link to clinical response. Arthritis Res Ther 2005;7:R149–55.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Lindberg J,
    2. Wijbrandts CA,
    3. van Baarsen LG,
    4. Nader G,
    5. Klareskog L,
    6. Catrina A,
    7. et al.
    The gene expression profile in the synovium as a predictor of the clinical response to infliximab treatment in rheumatoid arthritis. PloS One 2010;5:e11310.
    OpenUrlCrossRefPubMed
  9. 9.↵
    1. Dennis G,
    2. Holweg C,
    3. Kummerfeld S,
    4. Choy D,
    5. Setiadi F,
    6. Hackney J,
    7. et al.
    Synovial phenotypes in rheumatoid arthritis correlate with response to biologic therapeutics. Arthritis Res Ther 2014;16:R90.
    OpenUrlCrossRefPubMed
  10. 10.↵
    1. Pitzalis C,
    2. Kelly S,
    3. Humby F
    . New learnings on the pathophysiology of RA from synovial biopsies. Current Opin Rheumatol 2013;25:334–44.
    OpenUrlCrossRefPubMed
  11. 11.↵
    1. Pitzalis C,
    2. Jones GW,
    3. Bombardieri M,
    4. Jones SA
    . Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nat Rev Immunol 2014;14:447–62.
    OpenUrlCrossRefPubMed
  12. 12.↵
    1. Wechalekar M,
    2. Smith M
    . Utility of arthroscopic guided synovial biopsy in understanding synovial tissue pathology in health and disease states. World J Orthop 2014;5:1–8.
    OpenUrlCrossRefPubMed
  13. 13.↵
    1. Wijbrandts CA,
    2. Dijkgraaf MG,
    3. Kraan MC,
    4. Vinkenoog M,
    5. Smeets TJ,
    6. Dinant H,
    7. et al.
    The clinical response to infliximab in rheumatoid arthritis is in part dependent on pretreatment tumour necrosis factor alpha expression in the synovium. Ann Rheum Dis 2008;67:1139–44.
    OpenUrlAbstract/FREE Full Text
  14. 14.↵
    1. van de Sande MG,
    2. Gerlag DM,
    3. Lodde BM,
    4. van Baarsen LG,
    5. Alivernini S,
    6. Codullo V,
    7. et al.
    Evaluating antirheumatic treatments using synovial biopsy: a recommendation for standardisation to be used in clinical trials. Ann Rheum Dis 2011;70:423–7.
    OpenUrlAbstract/FREE Full Text
  15. 15.↵
    1. Bresnihan B,
    2. Baeten D,
    3. Firestein GS,
    4. Fitzgerald OM,
    5. Gerlag DM,
    6. Haringman JJ,
    7. et al.
    Synovial tissue analysis in clinical trials. J Rheumatol 2005;32:2481–4.
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    1. de Hair MJ,
    2. Harty LC,
    3. Gerlag DM,
    4. Pitzalis C,
    5. Veale DJ,
    6. Tak PP
    . Synovial tissue analysis for the discovery of diagnostic and prognostic biomarkers in patients with early arthritis. J Rheumatol 2011;38:2068–72.
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    1. Gerlag D,
    2. Tak PP
    . Synovial biopsy. Best Prac Res Clin Rheumatol 2005;19:387–400.
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Baeten D,
    2. Van den Bosch F,
    3. Elewaut D,
    4. Stuer A,
    5. Veys EM,
    6. De Keyser F
    . Needle arthroscopy of the knee with synovial biopsy sampling: technical experience in 150 patients. Clin Rheumatol 1999;18:434–41.
    OpenUrlCrossRefPubMed
  19. 19.↵
    1. Kane D,
    2. Veale DJ,
    3. FitzGerald O,
    4. Reece R
    . Survey of arthroscopy performed by rheumatologists. Rheumatology 2002;41:210–5.
    OpenUrlAbstract/FREE Full Text
  20. 20.↵
    1. van de Sande MG,
    2. de Hair MJ,
    3. van der Leij C,
    4. Klarenbeek PL,
    5. Bos WH,
    6. Smith MD,
    7. et al.
    Different stages of rheumatoid arthritis: features of the synovium in the preclinical phase. Ann Rheum Dis 2011;70:772–7.
    OpenUrlAbstract/FREE Full Text
  21. 21.↵
    1. Smith MD,
    2. Baeten D,
    3. Ulfgren AK,
    4. McInnes IB,
    5. Fitzgerald O,
    6. Bresnihan B,
    7. et al.
    Standardisation of synovial tissue infiltrate analysis: how far have we come? How much further do we need to go? Ann Rheum Dis 2006;65:93–100.
    OpenUrlAbstract/FREE Full Text
  22. 22.↵
    1. van Steenbergen HW,
    2. van Nies JA,
    3. Huizinga TW,
    4. Bloem JL,
    5. Reijnierse M,
    6. van der Helm-van Mil AH
    Characterising arthralgia in the preclinical phase of rheumatoid arthritis using MRI. Ann Rheum Dis 2014 April 9 (E-pub ahead of print).
  23. 23.↵
    1. Linn-Rasker SP,
    2. van der Helm-van Mil AH,
    3. Breedveld FC,
    4. Huizinga TW
    . Arthritis of the large joints - in particular, the knee - at first presentation is predictive for a high level of radiological destruction of the small joints in rheumatoid arthritis. Ann Rheum Dis 2007;66:646–50.
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    1. Veale DJ
    . The role of arthroscopy in early arthritis. Clin Exp Rheumatol 1999;17:37–8.
    OpenUrlPubMed
  25. 25.↵
    1. Kraan MC,
    2. Reece RJ,
    3. Smeets TJ,
    4. Veale DJ,
    5. Emery P,
    6. Tak PP
    . Comparison of synovial tissues from the knee joints and the small joints of rheumatoid arthritis patients: Implications for pathogenesis and evaluation of treatment. Arthritis Rheumatol 2002;46:2034–8.
    OpenUrlCrossRef
  26. 26.↵
    1. Andersen M,
    2. Boesen M,
    3. Ellegaard K,
    4. Christensen R,
    5. Soderstrom K,
    6. Soe N,
    7. et al.
    Synovial explant inflammatory mediator production corresponds to rheumatoid arthritis imaging hallmarks: a cross sectional study. Arthritis Res Ther 2014;16:R107.
    OpenUrlCrossRefPubMed
  27. 27.↵
    1. Scire CA,
    2. Epis O,
    3. Codullo V,
    4. Humby F,
    5. Morbini P,
    6. Manzo A,
    7. et al.
    Immunohistological assessment of the synovial tissue in small joints in rheumatoid arthritis: validation of a minimally invasive ultrasound-guided synovial biopsy procedure. Arthritis Res Ther 2007;9:R101.
    OpenUrlCrossRefPubMed
  28. 28.↵
    1. Kelly S,
    2. Humby F,
    3. Filer A,
    4. Ng N,
    5. Di Cicco M,
    6. Hands RE,
    7. et al.
    Ultrasound-guided synovial biopsy: a safe, well-tolerated and reliable technique for obtaining high-quality synovial tissue from both large and small joints in early arthritis patients. Ann Rheum Dis 2015;74:611–7.
    OpenUrlAbstract/FREE Full Text
  29. 29.↵
    1. Kaiser MJ,
    2. Hauzeur JP,
    3. Blacher S,
    4. Foidart JM,
    5. Deprez M,
    6. Rossknecht A,
    7. et al.
    Contrast-enhanced coded phase-inversion harmonic sonography of knee synovitis correlates with histological vessel density: 2 automated digital quantifications. J Rheumatol 2009;36:1391–400.
    OpenUrlAbstract/FREE Full Text
  30. 30.↵
    1. Koski JM,
    2. Helle M
    . Ultrasound guided synovial biopsy using portal and forceps. Ann Rheum Dis 2005;6:926–9.
    OpenUrl
  31. 31.↵
    1. Haringman JJ,
    2. Gerlag DM,
    3. Zwinderman AH,
    4. Smeets TJ,
    5. Kraan MC,
    6. Baeten D,
    7. et al.
    Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 2005;64:834–8.
    OpenUrlAbstract/FREE Full Text
  32. 32.↵
    1. Wijbrandts CA,
    2. Vergunst CE,
    3. Haringman JJ,
    4. Gerlag DM,
    5. Smeets TJ,
    6. Tak PP
    . Absence of changes in the number of synovial sublining macrophages after ineffective treatment for rheumatoid arthritis: implications for use of synovial sublining macrophages as a biomarker. Arthritis Rheum 2007;56:3869–71.
    OpenUrlCrossRefPubMed
  33. 33.↵
    1. Bresnihan B,
    2. Pontifex E,
    3. Thurlings RM,
    4. Vinkenoog M,
    5. El-Gabalawy H,
    6. Fearon U,
    7. et al.
    Synovial tissue sublining CD68 expression is a biomarker of therapeutic response in rheumatoid arthritis clinical trials: consistency across centers. J Rheumatol 2009;36:1800–2.
    OpenUrlAbstract/FREE Full Text
  34. 34.↵
    1. Bresnihan B,
    2. Gerlag DM,
    3. Rooney T,
    4. Smeets TJ,
    5. Wijbrandts CA,
    6. Boyle D,
    7. et al.
    Synovial macrophages as a biomarker of response to therapeutic intervention in rheumatoid arthritis: standardization and consistency across centers. J Rheumatol 2007;34:620–2.
    OpenUrlAbstract/FREE Full Text
  35. 35.↵
    1. Rooney T,
    2. Roux-Lombard P,
    3. Veale DJ,
    4. FitzGerald O,
    5. Dayer JM,
    6. Bresnihan B
    . Synovial tissue and serum biomarkers of disease activity, therapeutic response and radiographic progression: analysis of a proof-of-concept randomised clinical trial of cytokine blockade. Ann Rheum Dis 2010;69:706–14.
    OpenUrlAbstract/FREE Full Text
  36. 36.↵
    1. Ducreux J,
    2. Durez P,
    3. Galant C,
    4. Nzeusseu Toukap A,
    5. Van den Eynde B,
    6. Houssiau FA,
    7. et al.
    Global molecular effects of tocilizumab therapy in rheumatoid arthritis synovium. Arthritis Rheumatol 2014;66:15–23.
    OpenUrlCrossRefPubMed
  37. 37.↵
    1. Boers M,
    2. Kirwan JR,
    3. Wells G,
    4. Beaton D,
    5. Gossec L,
    6. d’Agostino MA,
    7. et al.
    Developing core outcome measurement sets for clinical trials: OMERACT Filter 2.0. J Clin Epidemiol 2014;67:745–53.
    OpenUrlCrossRefPubMed
View Abstract
PreviousNext
Back to top

In this issue

The Journal of Rheumatology
Vol. 43, Issue 1
1 Jan 2016
  • Table of Contents
  • Table of Contents (PDF)
  • Index by Author
  • Editorial Board (PDF)
Print
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word about The Journal of Rheumatology.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Evaluation of Minimally Invasive, Ultrasound-guided Synovial Biopsy Techniques by the OMERACT Filter — Determining Validation Requirements
(Your Name) has forwarded a page to you from The Journal of Rheumatology
(Your Name) thought you would like to see this page from the The Journal of Rheumatology web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Evaluation of Minimally Invasive, Ultrasound-guided Synovial Biopsy Techniques by the OMERACT Filter — Determining Validation Requirements
Frances Humby, Stephen Kelly, Serena Bugatti, Antonio Manzo, Andrew Filer, Arti Mahto, Joao Eurico Fonseca, Bernard Lauwerys, Maria-Antonietta D’Agostino, Esperanza Naredo, Rik Lories, Carlomaurizio Montecucco, Paul Peter Tak, Oliver Fitzgerald, Malcolm D. Smith, Douglas J. Veale, Ernest H. Choy, Vibeke Strand, Costantino Pitzalis
The Journal of Rheumatology Jan 2016, 43 (1) 208-213; DOI: 10.3899/jrheum.141199

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero

 Request Permissions

Share
Evaluation of Minimally Invasive, Ultrasound-guided Synovial Biopsy Techniques by the OMERACT Filter — Determining Validation Requirements
Frances Humby, Stephen Kelly, Serena Bugatti, Antonio Manzo, Andrew Filer, Arti Mahto, Joao Eurico Fonseca, Bernard Lauwerys, Maria-Antonietta D’Agostino, Esperanza Naredo, Rik Lories, Carlomaurizio Montecucco, Paul Peter Tak, Oliver Fitzgerald, Malcolm D. Smith, Douglas J. Veale, Ernest H. Choy, Vibeke Strand, Costantino Pitzalis
The Journal of Rheumatology Jan 2016, 43 (1) 208-213; DOI: 10.3899/jrheum.141199
Reddit logo Twitter logo Facebook logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One
Bookmark this article

Jump to section

  • Article
    • Abstract
    • MATERIALS AND METHODS
    • RESULTS
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • References
  • PDF
  • eLetters

Keywords

SYNOVITIS
BIOPSY
RHEUMATOID ARTHRITIS
ULTRASOUND

Related Articles

Cited By...

More in this TOC Section

OMERACT 12 — International Consensus Conference on Outcome Measures in Rheumatology, Budapest, Hungary, May 7–11, 2014

  • Current Status of Efforts on Standardizing Magnetic Resonance Imaging of Juvenile Idiopathic Arthritis: Report from the OMERACT MRI in JIA Working Group and Health-e-Child
  • Development and Preliminary Validation of a Digital Overlay-based Learning Module for Semiquantitative Evaluation of Magnetic Resonance Imaging Lesions in Osteoarthritis of the Hip
  • Minimal Clinically Important Difference as Applied in Rheumatology: An OMERACT Rasch Working Group Systematic Review and Critique
Show more OMERACT 12 — International Consensus Conference on Outcome Measures in Rheumatology, Budapest, Hungary, May 7–11, 2014

Special Interest Groups II

  • Development of a Provisional Core Domain Set for Polymyalgia Rheumatica: Report from the OMERACT 12 Polymyalgia Rheumatica Working Group
  • Current Status of Efforts on Standardizing Magnetic Resonance Imaging of Juvenile Idiopathic Arthritis: Report from the OMERACT MRI in JIA Working Group and Health-e-Child
  • Development and Preliminary Validation of a Digital Overlay-based Learning Module for Semiquantitative Evaluation of Magnetic Resonance Imaging Lesions in Osteoarthritis of the Hip
Show more Special Interest Groups II

Similar Articles

Keywords

  • synovitis
  • biopsy
  • rheumatoid arthritis
  • ultrasound

Content

  • First Release
  • Current
  • Archives
  • Collections
  • Audiovisual Rheum
  • COVID-19 and Rheumatology

Resources

  • Guide for Authors
  • Submit Manuscript
  • Author Payment
  • Reviewers
  • Advertisers
  • Classified Ads
  • Reprints and Translations
  • Permissions
  • Meetings
  • FAQ
  • Policies

Subscribers

  • Subscription Information
  • Purchase Subscription
  • Your Account
  • Terms and Conditions

More

  • About Us
  • Contact Us
  • My Alerts
  • My Folders
  • Privacy/GDPR Policy
  • RSS Feeds
The Journal of Rheumatology
The content of this site is intended for health care professionals.
Copyright © 2022 by The Journal of Rheumatology Publishing Co. Ltd.
Print ISSN: 0315-162X; Online ISSN: 1499-2752
Powered by HighWire