Rheumatoid arthritis overview

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1] Associate Editor(s)-in-Chief: Ayesha A. Khan, MD, Manpreet Kaur, MD [2]

Overview

Rheumatoid arthritis is a chronic inflammatory systemic disease which is found commonly in women and starts in mid 30's to 40's. Cause of rheumatoid arthritis is idiopathic but there are genetic factors such as HLA-DR4 cluster, environmental factors like smoking, hormonal factors like hyperprolactinemia, infectious factors like mycoplasma, epstein-Barr virus (EBV), rubella virus, porphyromonas gingivalis, socioeconomic, psychological, and lifestyle factors such as obesity play important role in the development of rheumatoid arthritis. There is no established system for the classification of rheumatoid arthritis. Depending on the presentation of rheumatoid arthritis, it is classified into typical classic rheumatoid arthritis and palindromic rheumatism. Common symptoms of rheumatoid arthritis are joint pain of small joints of the hands, wrist, and forefoot, joint swelling, morning joint stiffness classically lasting for more than an hour, decreased grip strength, generalized aching, and fatigue, weight loss, depression. Less common symptoms are tingling and numbness in the arm and weakness in the arm. Anti-CCP antibodies testing is the gold standard test for the diagnosis of rheumatoid arthritis.It has the specificity of about 81-100%, with the sensitivity of 39–94%. Hallmark of rheumatoid arthritis Xray findings are soft tissue swelling, joint space narrowing, and erosions but it involves small joints with multiple deformities. Findings on an ultrasound suggestive of rheumatoid arthritis are tenosynovitis, bursitis, baker's cyst and inflammation of synovium. Therapeutic use of ultrasound is the guidance of corticosteroid injection in the joint and fluid aspiration from the joint effusion. MRI is helpful in the diagnosis of early and subacute rheumatoid arthritis. Findings on MRI diagnostic of rheumatoid arthritis are synovial hyperemia, synovial hyperplasia, pannus, subchondral cysts, erosions, effusion of joints and bone marrow edema. The mainstay of treatment of rheumatoid arthritis is pharmacotherapy. There are two types of therapies- non-pharmacological therapy and pharmacological therapy. There are different drug regimen depending upon the stage of the disease. In active stage, combined therapy include disease-modifying antirheumatic drugs (DMARDs) are used along with the anti-inflammatory drugs. Therapy for resistant disease and flares is the addition of oral glucocorticoids. In case of the flare, add another DMARDs with methotrexate or replace with another DMARDs. Surgery is usually reserved for patients with debilitating disease, failure of medical therapy and radiographic findings of end-stage arthritis. Various surgical options used for the treatment of RA are tenosynovectomy, arthroscopic or open synovectomy, joint fusion, small joint implant arthroplasty, total joint replacement of deformed joint. Effective measures for the primary prevention of rheumatoid arthritis are patient education, exercise, physical and occupational therapy and cognitive behavioral therapies. Effective measures for the secondary prevention of rheumatoid arthritis are calcium and vitamin D supplementation to prevent osteoporosis. To prevent cardiovascular complications and recurrent attacks of RA, effective methods are exercise, smoking cessation, and dietary control.

Historical Perspective

Rheumatoid arthritis signs and symptoms were first noticed by Augustin Jacob Landre-Beauvais, a resident physician at the Saltpetriere asylum in France, in 1800, He named it as Goutte Asthenique Primitive or Primary Asthenic Gout. The name Rheumatoid arthritis coined by Archibald Garrod in 1890. In 1970, human leukocyte antigen (HLA) was first implicated in the pathogenesis of rheumatoid arthritis.

Classification

There is no established system for the classification of rheumatoid arthritis. Depending on the presentation of rheumatoid arthritis, it is classified into typical classic rheumatoid arthritis and palindromic rheumatism. Rheumatoid arthritis is seropositive when ACPAs (anti-CCP) and/or rheumatoid factor are present. Seronegative disease is a distinct polyarthritis with less well-defined pathogenesis and typically less joint destruction, but the treatment approach is similar. The classification criterion for the diagnosis of rheumatoid arthritis according to American College of Rheumatology, uses 4 parameters including joint involvement, serology, duration of symptoms, and acute phase reactants. If the score is more than 6 according to this criteria, the disease is classified as definite rheumatoid arthritis.[1]

Pathophysiology

Rheumatoid arthritis is mediated by the combination of a predisposing genotype upon which genetic factors, environmental and microorganism also contribute resulting in the inflammation and destruction of the synovial membrane. All the factors lead to citrullination or post-translational modifications, the altered peptides bind to MHC protein with shared epitopes which further lead to antigen presentation to T-cells. T-cells further stimulate B-cells and cytokines which leads to cartilage damage. Mutation of human leukocyte antigen (HLA) genes on chromosome 6 is involved in pathogenesis of rheumatoid arthritis. Conditions associated with RA are vasculitis, uveitis, scleritis, peripheral ulcerative keratitis, interstitial fibrosis, pulmonary nodules, bronchiolitis obliterans, organizing pneumonia, venous thromboembolism, pericarditis, myocarditis, congestive heart failure, atrial fibrillation, sjogren's syndrome, felty's syndrome.

Rheumatoid arthritis follows a continuum from healthy to a preclinical at-risk stage, transition, early synovitis, and ultimately established destructive disease. This progression is not always unidirectional. ACPA positivity can revert to negative, and some ACPA-positive individuals never develop RA, creating opportunities for prevention and reflecting multiple possible pathogenic pathways in different patients. [1]

Causes

Rheumatoid arthritis occurs when your immune system attacks the synovium — the lining of the membranes that surround your joints.The resulting inflammation thickens the synovium, which can eventually destroy the cartilage and bone within the joint.The tendons and ligaments that hold the joint together weaken and stretch. Gradually, the joint loses its shape and alignment.Cause of rheumatoid arthritis is idiopathic but genetic like HLA-DR4 cluster, environmental like smoking, hormonal like hyperprolactinemia, immunologic, infectious factors like mycoplasma, epstein-Barr virus (EBV), rubella virus, porphyromonas gingivalis, socioeconomic, psychological, and lifestyle factors such as obesity play important role in the development of rheumatoid arthritis.

Only about 15% of identical twins both develop rheumatoid arthritis, so genes alone do not explain the disease. Epigenetic changes such as DNA methylation may increase risk, as shown in RA-discordant twins.[2] In at-risk people with high RF or ACPA levels, abnormal DNA methylation in immune genes can appear years before symptoms.[3] Later, T cells with these abnormal epigenetic marks build up in inflamed synovium, unlike in osteoarthritis.[4]

Differentiating Rheumatoid Arthritis from other Diseases

Rheumatoid arthritis must be differentiated from osteoarthritis , septic arthritis, reactive arthritis, behcet's disease and psoriatic arthritis.

Epidemiology and Demographics

The incidence of rheumatoid arthritis is approximately 40 per 100,000 individuals worldwide. The prevalence of rheumatoid arthritis is approximately 1 percent in Caucasians per 100,000 individuals worldwide.The peak onset of the disease is between the age of  50 and 75 years. Women are three times more commonly affected by rheumatoid arthritis than men. The mortality rate of rheumatoid arthritis is approximately 10%.

Risk Factors

Environmental and behavioral exposures are major determinants of rheumatoid arthritis susceptibility and disease severity. Common risk factors in the development of rheumatoid arthritis are the family history of RA, cigarette smoking, race like more prevalent in Native Americans, strongly associated with major histocompatibility complex (MHC) class II antigen HLA-DR4 and patient with silica and asbestos exposure. Less common risk factors are obesity and high consumption of red meat.

Cigarette smoking and genetic risk can sometimes act together: in ACPA-positive smokers with two shared-epitope copies, RA risk is ~20 times higher than in nonsmokers.[5]After quitting, the risk slowly falls and can approach that of nonsmokers within 2–3 decades.[6]

Screening

According to the American College of Rheumatology Guideline, screening for rheumatoid arthritis is not recommended.

Natural History, Complications and Prognosis

The symptoms of rheumatoid arthritis usually develop in the third to fourth decade of life and start with symptoms such as fatigue, small joints pain and morning stiffness which lasts more than 1 hour. Complication of rheumatoid arthritis involve all the systems. Cardiac complications are pericarditis, congestive heart failure, endocarditis and myocardial infarction. Pulmonary complications are pleurisy, alveolitis, pleural effusion and pulmonary fibrosis. Rheumatological complications are joint deformities, felty's syndrome, sjögren's syndrome, osteoporosis and atlantoaxial subluxation. Eye complications such as scleritis and keratitis. Renal complications are chronic renal failure from amyloidosis. Nervous system complications like peripheral neuropathy and mononeuritis multiplex. Prognosis is generally good with early diagnosis and treatment, and 10-year disability rate of patients with rheumatoid arthritis is approximately 40%.

Diagnostic study of choice

Anti-CCP antibodies testing is the gold standard test for the diagnosis of rheumatoid arthritis.It has the specificity of about 81-100%, with the sensitivity of 39–94%.

History and Symptoms

Patients with rheumatoid arthritis may have a positive history of the family history of RA, history of smoking and other autoimmune disease. Common symptoms of rheumatoid arthritis are joint pain of small joints of the hands, wrist, and forefoot, joint swelling, morning joint stiffness classically lasting for more than an hour, decreased grip strength, generalized aching, and fatigue, weight loss, depression. Less common symptoms are tingling and numbness in the arm and weakness in the arm.

Physical Examination

Patients with rheumatoid arthritis usually appear fatigued. On skin examination, rheumatoid nodules, erythema nodosum, atrophy of the digital skin, palmar erythema and diffuse thinning of the skin are found. If there is involvement of eyes, Scleritis and Scleromalacia are seen. On auscultation of lungs, there are decreased breath sounds on both sides and crackles may be present. On palpation of the abdomen, hepatomegaly and splenomegaly is usually found when it is associated with Felty's syndrome. On examination of extremities, redness, and swelling of the affected joints, tenderness, pain on movement and decreased the range of movement is usually found.

Laboratory findings

Laboratory tests used to diagnose rheumatoid arthritis are complete blood count with differentials, erythrocyte sedimentation rate, CRP, Renal function test, LFT and antibodies such as rheumatoid factor, anti-CCP and anti MCV.

X-ray

Hallmark of rheumatoid arthritis are soft tissue swelling, joint space narrowing and erosions. Hand and wrist findings on xray are subchondral cysts, ulnar deviation of the MCP joints, boutonniere and swan neck deformities, hitchhiker’s thumb deformity, scapholunate dissociation, ulnar translocation and ankylosis. Feet findings on xray are Subtalar joint involvement, posterior calcaneal tubercle erosion, hammer toe deformity and hallux valgus. Findings of shoulder such as distal clavicle erosions, erosions of the superolateral aspect of the head of the humerus, high riding shoulder due to subacromial-subdeltoid bursitis. Knee findigs are joint effusions, loss of joint space and prepatellar bursitis. Hip findings are concentric loss of joint space and acetabular protrusio. Spine findings are atlantoaxial subluxation, atlantoaxial impaction: cephalad migration of C2,osteoporosis and osteoporotic fractures and erosion of spinous processes.

ECG

There are no ECG findings associated with rheumatoid arthritis. An ECG may be helpful in the diagnosis of pericarditis associated with rheumatoid arthritis. Findings of pericarditis are diffuse ST-segment elevation and PR segment depression.

Ultrasound

Ultrasound is helpful in the diagnosis of rheumatoid arthritis. Findings on an ultrasound suggestive of rheumatoid arthritis are tenosynovitis, bursitis, baker's cyst and inflammation of synovium. Therapeutic use of ultrasound are guidance of corticosteroid injection in the joint and fluid aspiration from the joint effusion.

CT

CT scan is a useful non-invasive test used to diagnose the complications of rheumatoid arthritis such as subluxation of the alanto-axial joint. It is also used in the presurgical assessment of neurological symptoms.

MRI

MRI is helpful in the diagnosis of early and subacute rheumatoid arthritis. Findings on MRI diagnostic of rheumatoid arthritis are synovial hyperemia, synovial hyperplasia, pannus, subchondral cysts, erosions, effusion of joints and bone marrow edema.

Other imaging studies

DEXA Scan is helpful in the diagnosis of the complication of rheumatoid arthritis such as osteoporosis and osteopenia.

Other diagnostic studies

There are no other diagnostic studies associated with rheumatoid arthritis.

Treatment

Medical Therapy

The mainstay of treatment of rheumatoid arthritis is pharmacotherapy. Early diagnosis of rheumatoid arthritis is helpful in treatment. Choice of treatment depends on various factors such as stage of disease, comorbid conditions, stage of therapy and presence of severe prognostic signs. There are two types of therapies- non-pharmacological therapy and pharmacological therapy. There are different drug regimen depending upon the stage of the disease. In active stage, combined therapy include disease-modifying antirheumatic drugs (DMARDs) are used along with the anti-inflammatory drugs. Therapy for resistant disease and flares is the addition of oral glucocorticoids. In case of the flare, add another DMARDs with methotrexate or replace with another DMARDs.

Surgical Therapy

The mainstay of treatment for rheumatoid arthritis is medical therapy. Surgery is usually reserved for patients with debilitating disease, failure of medical therapy and radiographic findings of end-stage arthritis. Various surgical options used for the treatment of RA are tenosynovectomy, arthroscopic or open synovectomy, joint fusion, small joint implant arthroplasty, total joint replacement of deformed joint.

Primary prevention

Effective measures for the primary prevention of rheumatoid arthritis are patient education, exercise, physical and occupational therapy and cognitive behavioral therapies.

Secondary prevention

Effective measures for the secondary prevention of rheumatoid arthritis are calcium and vitamin D supplementation to prevent osteoporosis. To prevent cardiovascular complications and recurrent attacks of RA, effective methods are exercise, smoking cessation, and dietary control.

Recent advances

Recently Identified Cell Lineages and Cell Phenotypes Contributing to Rheumatoid Arthritis (RA).[1]

Cell class Cell lineage / phenotype Comments Study
T cells CD4+ PD1+ CXCR5− (Tph) Located in lymphoid aggregates adjacent to B cells; produce interleukin-21, which supports B-cell proliferation and differentiation into plasma cells Rao et al.[7]
T cells CD8+ GZMK+ Located in RA synovial sublining; source of interferon-γ Jonsson et al.[8]
B cells Mucosal, circulating, and synovial B cells Oligoclonal expansion with evidence of recirculation and ACPA affinity maturation due to somatic mutation Kongpachith et al.[9]
B cells NR4A+ Produces lymphotoxins and interleukin-6, which promote lymphoid aggregate formation Meednu et al.[10]
Macrophages MerTK− Proinflammatory; found in active RA synovium; associated with interleukin-6 and TNF production Alivernini et al.[11]
Macrophages MerTK+ Antiinflammatory; associated with lipoxin and resolvin production Cai et al.[12]
Macrophages CX3CR1+ Resident cells in RA synovial lining with tight junctions that serve as immunologic barrier; disrupted in RA synovium Culemann et al.[13]
Macrophages Alternatively activated Interleukin-33 reprogrammed with metabolic rewiring that uncouples respiratory chain and enhances inflammation resolution Faas et al.[14]
Macrophages HBEGF+ Promotes fibroblast aggressiveness and invasion Kuo et al.[15]
Fibroblasts FAP+ CD90+ Proinflammatory phenotype located in sublining; regulated by NOTCH3 Wei et al.[16]
Fibroblasts FAP+ CD90− Located in intimal lining; produce interleukin-6, metalloproteinases, and prostanoids in RA Mizoguchi et al.[17]
Fibroblasts ETS1 Regulates bone damage through production of RANKL by fibroblasts in synovium Yan et al.[18]
Fibroblasts PRIME cells Present in circulation of patients with RA (transcriptome profile); increase in peripheral-blood PRIME cells precedes RA flares, possibly associated with B-cell activation Orange et al.[19]
Neutrophils (synovium and lung mucosa) - Produce NETs, which bind citrullinated peptides to enhance ACPA production Corsiero et al.[20]

Reference

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  2. Svendsen AJ, Gervin K, Lyle R, Christiansen L, Kyvik K, Junker P, Nielsen C, Houen G, Tan Q. Differentially Methylated DNA Regions in Monozygotic Twin Pairs Discordant for Rheumatoid Arthritis: An Epigenome-Wide Study. Front Immunol. 2016 Nov 17;7:510. doi: 10.3389/fimmu.2016.00510. PMID: 27909437; PMCID: PMC5112246.
  3. Shao X, Hudson M, Colmegna I, Greenwood CMT, Fritzler MJ, Awadalla P, Pastinen T, Bernatsky S. Rheumatoid arthritis-relevant DNA methylation changes identified in ACPA-positive asymptomatic individuals using methylome capture sequencing. Clin Epigenetics. 2019 Jul 31;11(1):110. doi: 10.1186/s13148-019-0699-9. PMID: 31366403; PMCID: PMC6668183.
  4. Ai R, Boyle DL, Wang W, Firestein GS. Distinct DNA Methylation Patterns of Rheumatoid Arthritis Peripheral Blood and Synovial Tissue T Cells. ACR Open Rheumatol. 2021 Mar;3(3):127-132. doi: 10.1002/acr2.11231. Epub 2021 Feb 5. PMID: 33544432; PMCID: PMC7966880.
  5. Klareskog L, Malmström V, Lundberg K, Padyukov L, Alfredsson L. Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis. Semin Immunol. 2011 Apr;23(2):92-8. doi: 10.1016/j.smim.2011.01.014. Epub 2011 Mar 3. PMID: 21376627.
  6. Liu X, Tedeschi SK, Barbhaiya M, Leatherwood CL, Speyer CB, Lu B, Costenbader KH, Karlson EW, Sparks JA. Impact and Timing of Smoking Cessation on Reducing Risk of Rheumatoid Arthritis Among Women in the Nurses' Health Studies. Arthritis Care Res (Hoboken). 2019 Jul;71(7):914-924. doi: 10.1002/acr.23837. PMID: 30790475; PMCID: PMC6597309.
  7. Rao DA, Gurish MF, Marshall JL, Slowikowski K, Fonseka CY, Liu Y, Donlin LT, Henderson LA, Wei K, Mizoguchi F, Teslovich NC, Weinblatt ME, Massarotti EM, Coblyn JS, Helfgott SM, Lee YC, Todd DJ, Bykerk VP, Goodman SM, Pernis AB, Ivashkiv LB, Karlson EW, Nigrovic PA, Filer A, Buckley CD, Lederer JA, Raychaudhuri S, Brenner MB. Pathologically expanded peripheral T helper cell subset drives B cells in rheumatoid arthritis. Nature. 2017 Feb 1;542(7639):110-114. doi: 10.1038/nature20810. PMID: 28150777; PMCID: PMC5349321.
  8. Jonsson AH, Zhang F, Dunlap G, Gomez-Rivas E, Watts GFM, Faust HJ, Rupani KV, Mears JR, Meednu N, Wang R, Keras G, Coblyn JS, Massarotti EM, Todd DJ, Anolik JH, McDavid A; Accelerating Medicines Partnership RA/SLE Network; Wei K, Rao DA, Raychaudhuri S, Brenner MB. Granzyme K+ CD8 T cells form a core population in inflamed human tissue. Sci Transl Med. 2022 Jun 15;14(649):eabo0686. doi: 10.1126/scitranslmed.abo0686. Epub 2022 Jun 15. PMID: 35704599; PMCID: PMC9972878.
  9. Kongpachith S, Lingampalli N, Ju CH, Blum LK, Lu DR, Elliott SE, Mao R, Robinson WH. Affinity Maturation of the Anti-Citrullinated Protein Antibody Paratope Drives Epitope Spreading and Polyreactivity in Rheumatoid Arthritis. Arthritis Rheumatol. 2019 Apr;71(4):507-517. doi: 10.1002/art.40760. Epub 2019 Feb 27. PMID: 30811898; PMCID: PMC6519961.
  10. Meednu N, Rangel-Moreno J, Zhang F, Escalera-Rivera K, Corsiero E, Prediletto E, DiCarlo E, Goodman S, Donlin LT, Raychauduri S, Bombardieri M, Pitzalis C, Orange DE; Accelerating Medicines Partnership Rheumatoid Arthritis and Systemic Lupus Erythematosus (AMP RA/SLE) Consortium; McDavid A, Anolik JH. Dynamic spectrum of ectopic lymphoid B cell activation and hypermutation in the RA synovium characterized by NR4A nuclear receptor expression. Cell Rep. 2022 May 3;39(5):110766. doi: 10.1016/j.celrep.2022.110766. PMID: 35508128; PMCID: PMC9234997.
  11. Alivernini S, MacDonald L, Elmesmari A, Finlay S, Tolusso B, Gigante MR, Petricca L, Di Mario C, Bui L, Perniola S, Attar M, Gessi M, Fedele AL, Chilaka S, Somma D, Sansom SN, Filer A, McSharry C, Millar NL, Kirschner K, Nerviani A, Lewis MJ, Pitzalis C, Clark AR, Ferraccioli G, Udalova I, Buckley CD, Gremese E, McInnes IB, Otto TD, Kurowska-Stolarska M. Distinct synovial tissue macrophage subsets regulate inflammation and remission in rheumatoid arthritis. Nat Med. 2020 Aug;26(8):1295-1306. doi: 10.1038/s41591-020-0939-8. Epub 2020 Jun 29. PMID: 32601335.
  12. Cai B, Kasikara C, Doran AC, Ramakrishnan R, Birge RB, Tabas I. MerTK signaling in macrophages promotes the synthesis of inflammation resolution mediators by suppressing CaMKII activity. Sci Signal. 2018 Sep 25;11(549):eaar3721. doi: 10.1126/scisignal.aar3721. PMID: 30254055; PMCID: PMC6171110.
  13. Culemann S, Grüneboom A, Nicolás-Ávila JÁ, Weidner D, Lämmle KF, Rothe T, Quintana JA, Kirchner P, Krljanac B, Eberhardt M, Ferrazzi F, Kretzschmar E, Schicht M, Fischer K, Gelse K, Faas M, Pfeifle R, Ackermann JA, Pachowsky M, Renner N, Simon D, Haseloff RF, Ekici AB, Bäuerle T, Blasig IE, Vera J, Voehringer D, Kleyer A, Paulsen F, Schett G, Hidalgo A, Krönke G. Locally renewing resident synovial macrophages provide a protective barrier for the joint. Nature. 2019 Aug;572(7771):670-675. doi: 10.1038/s41586-019-1471-1. Epub 2019 Aug 7. PMID: 31391580; PMCID: PMC6805223.
  14. Faas M, Ipseiz N, Ackermann J, Culemann S, Grüneboom A, Schröder F, Rothe T, Scholtysek C, Eberhardt M, Böttcher M, Kirchner P, Stoll C, Ekici A, Fuchs M, Kunz M, Weigmann B, Wirtz S, Lang R, Hofmann J, Vera J, Voehringer D, Michelucci A, Mougiakakos D, Uderhardt S, Schett G, Krönke G. IL-33-induced metabolic reprogramming controls the differentiation of alternatively activated macrophages and the resolution of inflammation. Immunity. 2021 Nov 9;54(11):2531-2546.e5. doi: 10.1016/j.immuni.2021.09.010. Epub 2021 Oct 12. PMID: 34644537; PMCID: PMC7617137.
  15. Kuo D, Ding J, Cohn IS, Zhang F, Wei K, Rao DA, Rozo C, Sokhi UK, Shanaj S, Oliver DJ, Echeverria AP, DiCarlo EF, Brenner MB, Bykerk VP, Goodman SM, Raychaudhuri S, Rätsch G, Ivashkiv LB, Donlin LT. HBEGF+ macrophages in rheumatoid arthritis induce fibroblast invasiveness. Sci Transl Med. 2019 May 8;11(491):eaau8587. doi: 10.1126/scitranslmed.aau8587. PMID: 31068444; PMCID: PMC6726376.
  16. Wei K, Korsunsky I, Marshall JL, Gao A, Watts GFM, Major T, Croft AP, Watts J, Blazar PE, Lange JK, Thornhill TS, Filer A, Raza K, Donlin LT; Accelerating Medicines Partnership Rheumatoid Arthritis & Systemic Lupus Erythematosus (AMP RA/SLE) Consortium; Siebel CW, Buckley CD, Raychaudhuri S, Brenner MB. Notch signalling drives synovial fibroblast identity and arthritis pathology. Nature. 2020 Jun;582(7811):259-264. doi: 10.1038/s41586-020-2222-z. Epub 2020 Apr 22. PMID: 32499639; PMCID: PMC7841716.
  17. Mizoguchi, F., Slowikowski, K., Wei, K. et al. Functionally distinct disease-associated fibroblast subsets in rheumatoid arthritis. Nat Commun 9, 789 (2018). https://doi.org/10.1038/s41467-018-02892-y
  18. Yan M, Komatsu N, Muro R, Huynh NC, Tomofuji Y, Okada Y, Suzuki HI, Takaba H, Kitazawa R, Kitazawa S, Pluemsakunthai W, Mitsui Y, Satoh T, Okamura T, Nitta T, Im SH, Kim CJ, Kollias G, Tanaka S, Okamoto K, Tsukasaki M, Takayanagi H. ETS1 governs pathological tissue-remodeling programs in disease-associated fibroblasts. Nat Immunol. 2022 Sep;23(9):1330-1341. doi: 10.1038/s41590-022-01285-0. Epub 2022 Aug 23. PMID: 35999392.
  19. Orange DE, Yao V, Sawicka K, Fak J, Frank MO, Parveen S, Blachere NE, Hale C, Zhang F, Raychaudhuri S, Troyanskaya OG, Darnell RB. RNA Identification of PRIME Cells Predicting Rheumatoid Arthritis Flares. N Engl J Med. 2020 Jul 16;383(3):218-228. doi: 10.1056/NEJMoa2004114. PMID: 32668112; PMCID: PMC7546156.
  20. Corsiero E, Pratesi F, Prediletto E, Bombardieri M and Migliorini P (2016) NETosis as Source of Autoantigens in Rheumatoid Arthritis. Front. Immunol. 7:485. doi: 10.3389/fimmu.2016.00485

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