409
Views
14
CrossRef citations to date
0
Altmetric
Review

Synovial biopsies in inflammatory arthritis: precision medicine in rheumatoid arthritis

ORCID Icon & ORCID Icon
Pages 315-325 | Received 08 Aug 2019, Accepted 18 Dec 2019, Published online: 07 Jan 2020

References

  • Smith MD, Wechalekar MD. The synovium. In: Hochberg MC, Silman AJ, Smolen JS, et al. editors. Rheumatology (Sixth Edition). Philadelphia, Mosby, Ltd. 2015. 27–32.
  • Parker RH, Pearson CM. A simplified synovial biopsy needle. Arthritis Rheum. 1963 Apr;6:172–176.
  • Humby FC. Synovial tissue sampling in rheumatological practice-past developments and future perspectives. Front Med (Lausanne). 2019;6:4.
  • Veale DJ. Synovial tissue biopsy research. Front Med (Lausanne). 2019;6:72.
  • Vordenbaumen S, Joosten LA, Friemann J, et al. Utility of synovial biopsy. Arthritis Res Ther. 2009;11(6):256.
  • Smith MD, Baeten D, Ulfgren AK, 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 Jan;65(1):93–100.
  • Just SA, Humby F, Lindegaard H, et al. Patient-reported outcomes and safety in patients undergoing synovial biopsy: comparison of ultrasound-guided needle biopsy, ultrasound-guided portal and forceps and arthroscopic-guided synovial biopsy techniques in five centres across Europe. RMD Open. 2018;4(2):e000799–e000799.
  • Kane D, Veale DJ, FitzGerald O, et al. Survey of arthroscopy performed by rheumatologists. Rheumatology (Oxford). 2002 Feb;41(2):210–215.
  • Humby F, Romao VC, Manzo A, et al. A multicenter retrospective analysis evaluating performance of synovial biopsy techniques in patients with inflammatory arthritis: arthroscopic versus ultrasound-guided versus blind needle biopsy. Arthritis Rheumatol (Hoboken). 2018 May;70(5):702–710.
  • Scott DG, Porto LO, Lovell CR, et al. Chronic sarcoid synovitis in the Caucasian: an arthroscopic and histological study. Ann Rheum Dis. 1981 Apr;40(2):121–123.
  • Schumacher HR Jr. Pathology of crystal deposition diseases. Rheum Dis Clin North Am. 1988 Aug;14(2):269–288.
  • Matta Ramos RF, Cancian L, Calcagnotto F, et al. Synovial tuberculosis of the hand: an ancient disease in an unusual localisation. Indian J Plast Surg. 2017 May-Aug;50(2):130–137.
  • Gokhale N, Purohit S, Bhosale PB. Pigmented villonodular synovitis presenting as a popliteal cyst. J Orthop Case Rep. 2015 Jul-Sep;5(3):63–65.
  • Smith MD. The normal synovium. Open Rheumatol J. 2011;5:100–106.
  • Kondo Y, Suzuki K, Inoue Y, et al. Significant association between joint ultrasonographic parameters and synovial inflammatory factors in rheumatoid arthritis. Arthritis Res Ther. 2019;21(1):14.
  • de Hair MJH, van de Sande MGH, Ramwadhdoebe TH, et al. Features of the synovium of individuals at risk of developing rheumatoid arthritis: implications for understanding preclinical rheumatoid arthritis. Arthritis Rheumatol. 2014;66(3):513–522.
  • Kraan MC, Haringman JJ, Post WJ, et al. Immunohistological analysis of synovial tissue for differential diagnosis in early arthritis. Rheumatology (Oxford). 1999 Nov;38(11):1074–1080.
  • Ulfgren AK, Grondal L, Lindblad S, et al. Interindividual and intra-articular variation of proinflammatory cytokines in patients with rheumatoid arthritis: potential implications for treatment. Ann Rheum Dis. 2000 Jun;59(6):439–447.
  • van der Pouw Kraan TCTM, van Gaalen FA, Kasperkovitz PV, et al. Rheumatoid arthritis is a heterogeneous disease: evidence for differences in the activation of the STAT-1 pathway between rheumatoid tissues. Arthritis Rheum. 2003;48(8):2132–2145.
  • Weyand CM, Klimiuk PA, Goronzy JJ. Heterogeneity of rheumatoid arthritis: from phenotypes to genotypes. Springer Semin Immunopathol. 1998;20(1–2):5–22.
  • Orr C, Vieira-Sousa E, Boyle DL, et al. Synovial tissue research: a state-of-the-art review. Nat Rev Rheumatol. 2017 Aug;13(8):463–475.
  • Pitzalis C, Kelly S, Humby F. New learnings on the pathophysiology of RA from synovial biopsies. Curr Opin Rheumatol. 2013 May;25(3):334–344.
  • Astorri E, Nerviani A, Bombardieri M, et al. Towards a stratified targeted approach with biologic treatments in rheumatoid arthritis: role of synovial pathobiology. Curr Pharm Des. 2015;21(17):2216–2224.
  • Armitage JO, Weisenburger DD. New approach to classifying non-Hodgkin’s lymphomas: clinical features of the major histologic subtypes. Non-Hodgkin’s lymphoma classification project. J Clin Oncol. 1998 Aug;16(8):2780–2795.
  • Donlin LT, Rao DA, Wei K, et al. Methods for high-dimensonal analysis of cells dissociated from cyropreserved synovial tissue. Arthritis Res Ther. 2018 Jul 11;20(1):139.
  • Kuo D, Ding J, Cohn IS, et al. HBEGF(+) macrophages in rheumatoid arthritis induce fibroblast invasiveness. Sci Transl Med. 2019 May 8;11:491.
  • Mizoguchi F, Slowikowski K, Wei K, et al. Functionally distinct disease-associated fibroblast subsets in rheumatoid arthritis. Nat Commun. 2018 Feb 23;9(1):789.
  • Humby F, Lewis M, Ramamoorthi N, et al. Synovial cellular and molecular signatures stratify clinical response to csDMARD therapy and predict radiographic progression in early rheumatoid arthritis patients. Ann Rheum Dis. 2019 Jun;78(6):761–772.
  • Dennis G Jr., Holweg CT, Kummerfeld SK, et al. Synovial phenotypes in rheumatoid arthritis correlate with response to biologic therapeutics. Arthritis Res Ther. 2014;16(2):R90.
  • Humby F, Bombardieri M, Manzo A, et al. Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med. 2009 Jan 13;6(1):e1.
  • Wechalekar MD, Smith MD. Arthroscopic guided synovial biopsy in rheumatology: current perspectives. Int J Rheum Dis. 2017 Feb;20(2):141–144.
  • Just SA, Nielsen C, Werlinrud JC, et al. Six-month prospective trial in early and long-standing rheumatoid arthritis: evaluating disease activity in the wrist through sequential synovial histopathological analysis, RAMRIS magnetic resonance score and EULAR-OMERACT ultrasound score. RMD Open. 2019;5(2):e000951.
  • Croft AP, Campos J, Jansen K, et al. Distinct fibroblast subsets drive inflammation and damage in arthritis. Nature. 2019 Jun;570(7760):246–251.
  • Triaille C, Lauwerys BR. Synovial tissue: turning the page to precision medicine in arthritis. Front Med (Lausanne). 2019;6:46.
  • Wechalekar MD, Smith MD. Utility of arthroscopic guided synovial biopsy in understanding synovial tissue pathology in health and disease states. World J Orthop. 2014 Nov 18;5(5):566–573.
  • Stephenson W, Donlin LT, Butler A, et al. Single-cell RNA-seq of rheumatoid arthritis synovial tissue using low-cost microfluidic instrumentation. Nat Commun. 2018 Feb 23;9(1):791.
  • Rao DA, Gurish MF, Marshall JL, et al. Pathologically expanded peripheral T helper cell subset drives B cells in rheumatoid arthritis. Nature. 2017 Feb 1;542(7639):110–114.
  • Orr C, Najm A, Biniecka M, et al. Synovial immunophenotype and anti-citrullinated peptide antibodies in rheumatoid arthritis patients: relationship to treatment response and radiologic prognosis. Arthritis Rheumatol (Hoboken). 2017 Nov;69(11):2114–2123.
  • Ouboussad L, Burska AN, Melville A, et al. Synovial tissue heterogeneity in rheumatoid arthritis and changes with biologic and targeted synthetic therapies to inform stratified therapy [Mini Review]. Front Med (Lausanne). 2019 Mar 19;6(45). DOI: 10.3389/fmed.2019.00045
  • Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet. 2010 Sep 25;376(9746):1094–1108.
  • Walsh AM, Wechalekar MD, Guo Y, et al. Triple DMARD treatment in early rheumatoid arthritis modulates synovial T cell activation and plasmablast/plasma cell differentiation pathways. PloS One. 2017;12(9):e0183928.
  • Christensen AF, Sorensen GL, Junker K, et al. Site-specific absence of microfibrillar-associated protein 4 (MFAP4) from the internal elastic membrane of arterioles in the rheumatoid arthritis synovial membrane: an immunohistochemical study in patients with advanced rheumatoid arthritis versus osteoarthritis. APMIS. 2019 ;127(8):588–593.
  • Koppejan H, Jansen DTSL, Hameetman M, et al. Altered composition and phenotype of mucosal-associated invariant T cells in early untreated rheumatoid arthritis. Arthritis Res Ther. 2019;21(1):3.
  • Schmidt T, Najm A, Mussawy H, et al. General synovitis score and immunologic synovitis score reflect clinical disease activity in patients with advanced stage rheumatoid arthritis. Sci Rep. 2019;9(1):8448.
  • Wechalekar MD, Najm A, Veale DJ, et al. The 2018 OMERACT synovial tissue biopsy special interest group report on standardization of synovial biopsy analysis. J Rheumatol. 2019;46:1365–1368.
  • Choi IY, Karpus ON, Turner JD, et al. Stromal cell markers are differentially expressed in the synovial tissue of patients with early arthritis. PloS One. 2017;12(8):e0182751.
  • Van Landuyt KB, Jones EA, McGonagle D, et al. Flow cytometric characterization of freshly isolated and culture expanded human synovial cell populations in patients with chronic arthritis [Journal Article]. Arthritis Res Ther. 2010;12(1):1–14.
  • Spitzer MH, Nolan GP. Mass cytometry: single cells, many features. Cell. 2016;165(4):780–791.
  • Galli E, Hartmann FJ, Schreiner B, et al. GM-CSF and CXCR4 define a T helper cell signature in multiple sclerosis. Nat Med. 2019;25(8):1290–1300.
  • Zhang F, Wei K, Slowikowski K, et al. Defining inflammatory cell states in rheumatoid arthritis joint synovial tissues by integrating single-cell transcriptomics and mass cytometry. Nat Immunol. 2019 Jul;20(7):928–942. .
  • Rakhmanov M, Keller B, Gutenberger S, et al. Circulating CD21low B cells in common variable immunodeficiency resemble tissue homing, innate-like B cells. Proc Nat Acad Sci. 2009;106(32):13451.
  • Isnardi I, Ng Y-S, Menard L, et al. Complement receptor 2/CD21− human naive B cells contain mostly autoreactive unresponsive clones. Blood. 2010;115(24):5026.
  • You S, Koh JH, Leng L, et al. The tumor-like phenotype of rheumatoid synovium: molecular profiling and prospects for precision medicine. Arthritis Rheumatol (Hoboken). 2018;70(5):637–652.
  • Bottini N, Firestein GS. Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors. Nat Rev Rheumatol. 2013 Jan;9(1):24–33.
  • Spreafico R, Rossetti M, Whitaker JW, et al. Epipolymorphisms associated with the clinical outcome of autoimmune arthritis affect CD4+ T cell activation pathways. Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):13845–13850.
  • Doody KM, Bottini N, Firestein GS. Epigenetic alterations in rheumatoid arthritis fibroblast-like synoviocytes. Epigenomics. 2017 Apr;9(4):479–492.
  • Ai R, Laragione T, Hammaker D, et al. Comprehensive epigenetic landscape of rheumatoid arthritis fibroblast-like synoviocytes. Nat Commun. 2018;9(1):1921.
  • Mandelin AM 2nd, Homan PJ, Shaffer AM, et al. Transcriptional profiling of synovial macrophages using minimally invasive ultrasound-guided synovial biopsies in rheumatoid arthritis. Arthritis Rheumatol (Hoboken). 2018 Jun;70(6):841–854.
  • Udalova IA, Mantovani A, Feldmann M. Macrophage heterogeneity in the context of rheumatoid arthritis. Nat Rev Rheumatol. 2016 Aug;12(8):472–485.
  • Kurowska-Stolarska M, Alivernini S. Synovial tissue macrophages: friend or foe? RMD Open. 2017;3(2):e000527–e000527.
  • Tu J, Hong W, Guo Y, et al. Ontogeny of synovial macrophages and the roles of synovial macrophages from different origins in arthritis [Original Research]. Front Immunol. 2019 May 24;10(1146).DOI: 10.3389/fimmu.2019.01146
  • Culemann S, Grüneboom A, Nicolás-Ávila JÁ, et al. Locally renewing resident synovial macrophages provide a protective barrier for the joint. Nature. 2019;572(7771):670–675.
  • Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012 Mar;122(3):787–795.
  • Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13.
  • Mantovani A. Macrophage diversity and polarization: in vivo veritas. Blood. 2006;108(2):408.
  • Degboé Y, Rauwel B, Baron M, et al. Polarization of rheumatoid macrophages by TNF targeting through an IL-10/STAT3 Mechanism [Original Research]. Front Immunol. 2019;10(3).DOI: 10.3389/fimmu.2019.00003
  • Tak PP, Zvaifler NJ, Green DR, et al. Rheumatoid arthritis and p53: how oxidative stress might alter the course of inflammatory diseases. Immunol Today. 2000 Feb;21(2):78–82.
  • Fearon U, Canavan M, Biniecka M, et al. Hypoxia, mitochondrial dysfunction and synovial invasiveness in rheumatoid arthritis. Nat Rev Rheumatol. 2016 Jul;12(7):385–397.
  • Nayar S, Campos J, Smith CG, et al. Immunofibroblasts are pivotal drivers of tertiary lymphoid structure formation and local pathology. Proc Natl Acad Sci U S A. 2019;116:13490–13497.
  • Huang W, Hennrick K, Drew S. A colorful future of quantitative pathology: validation of Vectra technology using chromogenic multiplexed immunohistochemistry and prostate tissue microarrays. Hum Pathol. 2013;44(1):29–38.
  • Bodenmiller B. Multiplexed epitope-based tissue imaging for discovery and healthcare applications. Cell Syst. 2016;2(4):225–238.
  • Wang YJ, Traum D, Schug J, et al. Multiplexed in situ imaging mass cytometry analysis of the human endocrine pancreas and immune system in type 1 diabetes. Cell Metab. 2019;29(3):769–783.e4.
  • Guo Y, Walsh AM, Fearon U, et al. CD40L-dependent pathway is active at various stages of rheumatoid arthritis disease progression. J Immunol. 2017 Jun 1;198(11):4490–4501.
  • Xie JH, Yamniuk AP, Borowski V, et al. Engineering of a novel anti-CD40L domain antibody for treatment of autoimmune diseases. J Immunol. 2014;192(9):4083.
  • Visvanathan S, Daniluk S, Ptaszyński R, et al. Effects of BI 655064, an antagonistic anti-CD40 antibody, on clinical and biomarker variables in patients with active rheumatoid arthritis: a randomised, double-blind, placebo-controlled, phase IIa study. Ann Rheum Dis. 2019;78(6):754.
  • Guo Y, Walsh AM, Canavan M, et al. Immune checkpoint inhibitor PD-1 pathway is down-regulated in synovium at various stages of rheumatoid arthritis disease progression. PloS One. 2018;13(2):e0192704.
  • Karnell JL, Albulescu M, Drabic S, et al. A CD40L-targeting protein reduces autoantibodies and improves disease activity in patients with autoimmunity. Sci Transl Med. 2019;11(489).DOI: 10.1126/scitranslmed.aar6584
  • Cole S, Walsh A, Yin X, et al. Integrative analysis reveals CD38 as a therapeutic target for plasma cell-rich pre-disease and established rheumatoid arthritis and systemic lupus erythematosus. Arthritis Res Ther. 2018 May 2;20(1):85.
  • Alivernini S, Bruno D, Tolusso B, et al. Differential synovial tissue biomarkers among psoriatic arthritis and rheumatoid factor/anti-citrulline antibody-negative rheumatoid arthritis. Arthritis Res Ther. 2019;21:116.
  • Aungier SR, Cartwright AJ, Schwenzer A, et al. Targeting early changes in the synovial microenvironment: a new class of immunomodulatory therapy? Ann Rheum Dis. 2019;78(2):186.
  • Haringman JJ, Gerlag DM, Zwinderman AH, et al. Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis. 2005 Jun;64(6):834–838.
  • Zimmer L, Goldinger SM, Hofmann L, et al. Neurological, respiratory, musculoskeletal, cardiac and ocular side-effects of anti-PD-1 therapy. Eur J Cancer. 2016;60:210–225.
  • Klarenbeek PL, de Hair MJ, Doorenspleet ME, et al. Inflamed target tissue provides a specific niche for highly expanded T-cell clones in early human autoimmune disease. Ann Rheum Dis. 2012 Jun;71(6):1088–1093.
  • Doorenspleet ME, Klarenbeek PL, de Hair MJ, et al. Rheumatoid arthritis synovial tissue harbours dominant B-cell and plasma-cell clones associated with autoreactivity. Ann Rheum Dis. 2014 Apr;73(4):756–762.
  • Tak PP, Doorenspleet ME, de Hair MJH, et al. Dominant B cell receptor clones in peripheral blood predict onset of arthritis in individuals at risk for rheumatoid arthritis. Ann Rheum Dis. 2017;76(11):1924.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.