The importance of ultrasound in identifying and differentiating patients with early inflammatory arthritis: a narrative review

Gurjit S Kaeley, Catherine Bakewell, Atul Deodhar, Gurjit S Kaeley, Catherine Bakewell, Atul Deodhar

Abstract

Early differentiation between different types of inflammatory arthritis and subsequent initiation of modern treatments can improve patient outcomes by reducing disease activity and preventing joint damage. Routine clinical evaluation, laboratory testing, and radiographs are typically sufficient for differentiating between inflammatory and predominantly degenerative arthritis (e.g., osteoarthritis). However, in some patients with inflammatory arthritis, these techniques fail to accurately identify the type of early-stage disease. Further evaluation by ultrasound imaging can delineate the inflammatory arthritis phenotype present. Ultrasound is a noninvasive, cost-effective method that enables the evaluation of several joints at the same time, including functional assessments. Further, ultrasound can visualize pathophysiological changes such as synovitis, tenosynovitis, enthesitis, bone erosions, and crystal deposits at a subclinical level, which makes it an effective technique to identify and differentiate most common types of inflammatory arthritis. Limitations associated with ultrasound imaging should be considered for its use in the differentiation and diagnosis of inflammatory arthritides.

Keywords: Bone erosions; Enthesitis; Imaging; Inflammatory arthritis; Synovitis; Ultrasound.

Conflict of interest statement

GSK: Consultant Novartis.

CB: Speaker/consultant for AbbVie, Novartis, Regeneron, Sanofi, and Genzyme.

AD: Received research grants from AbbVie, Eli Lilly, GSK, Janssen, Novartis, Pfizer, and UCB; and has served on the advisory boards of AbbVie, Amgen, BMS, Eli Lilly, Janssen, Novartis, Pfizer, and UCB.

Figures

Fig. 1
Fig. 1
Use of ultrasound in diagnostic decision making. This algorithm was developed by the authors and was not based on a clinical study. Note: *Osteoarthritis can cause synovitis but is excluded from this algorithm. CPPD, calcium pyrophosphate deposition; CTD, connective tissue disorder; MCP, metacarpophalangeal; MTP, metatarsophalangeal, PIP, proximal interphalangeal; PMR, polymyalgia rheumatica; RA, rheumatoid arthritis; SASD, subacromial-subdeltoid; SpA, spondyloarthritis; TFCC, triangular fibrocartilage complex
Fig. 2
Fig. 2
Ultrasound imaging of synovitis and tenosynovitis. a Flexor tenosynovitis in transverse (left) and longitudinal (right) views. b Metacarpophalangeal joint paratenonitis, dorsal aspect of second metacarpophalangeal joint. MC, metacarpal. c Dorsal proximal interphalangeal B-mode (left) and power Doppler (right) images indicating synovitis in the recess (asterisk). PP, proximal phalanx; MP, middle phalanx; ET, extensor digitorum tendon. d Positive power Doppler signal of finger pulp
Fig. 3
Fig. 3
Ultrasound findings for differentiation of psoriatic arthritis from rheumatoid arthritis. a Short-axis view of palmar plate inflammation. FT, flexor tendon; MH, metacarpal head; PP, palmar plate. b Dorsal long view of enthesitis of the extensor tendon from a distal interphalangeal joint in a patient with psoriatic arthritis. DIP, distal interphalangeal; S, DIP synovitis; asterisk (*), enthesophyte; double asterisks (**), extensor tendon demonstrating thickening, hypoechogenicity, and loss of fibrillar architecture; triple asterisks (***), extensor tendon with insertional Doppler
Fig. 4
Fig. 4
Ultrasound imaging of enthesitis. a Achilles enthesophyte in a patient with spondyloarthritis. AT, Achilles tendon; C, calcaneus. b Patellar enthesitis in a patient with psoriatic arthritis. Left, Doppler with abnormal intratendinous signal; right, enthesophyte. P, patella; PT, patellar tendon/ligament; T, tibia
Fig. 5
Fig. 5
Ultrasound imaging of bone erosions and crystal deposits. a Transverse view of second metacarpophalangeal joint in a patient with rheumatoid arthritis; arrowheads denote bone erosion. b Left, chondrosynovial urate deposition at the second metacarpophalangeal joint (arrows); right, at the same joint, intra- and peri-articular tophaceous deposits seen as heterogeneous collections (arrows). c Left, calcium pyrophosphate crystal deposition seen sandwiched within the cartilage; right, magnified view of the white rectangular area on the left

References

    1. Mc Ardle A, Flatley B, Pennington SR, FitzGerald O. Early biomarkers of joint damage in rheumatoid and psoriatic arthritis. Arthritis Res Ther. 2015;17:141. doi: 10.1186/s13075-015-0652-z.
    1. Hazes JM, Luime JJ. The epidemiology of early inflammatory arthritis. Nat Rev Rheumatol. 2011;7:381–390. doi: 10.1038/nrrheum.2011.78.
    1. Merola JF, Espinoza LR, Fleischmann R. Distinguishing rheumatoid arthritis from psoriatic arthritis. RMD Open. 2018;4:e000656. doi: 10.1136/rmdopen-2018-000656.
    1. Epis O, Paoletti F, d'Errico T, Favalli E, Garau P, Mancarella L, et al. Ultrasonography in the diagnosis and management of patients with inflammatory arthritides. Eur J Intern Med. 2014;25:103–111. doi: 10.1016/j.ejim.2013.08.700.
    1. Finckh A, Liang MH, van Herckenrode CM, de Pablo P. Long-term impact of early treatment on radiographic progression in rheumatoid arthritis: a meta-analysis. Arthritis Rheum. 2006;55:864–872. doi: 10.1002/art.22353.
    1. Gladman DD, Thavaneswaran A, Chandran V, Cook RJ. Do patients with psoriatic arthritis who present early fare better than those presenting later in the disease? Ann Rheum Dis. 2011;70:2152–2154. doi: 10.1136/ard.2011.150938.
    1. Codreanu C, Enache L. Is ultrasound changing the way we understand rheumatology? Including ultrasound examination in the classification criteria of polymyalgia rheumatica and gout. Med Ultrason. 2015;17:97–103. doi: 10.11152/mu.2013.2066.171.ccle.
    1. Richette P, Bardin T, Doherty M. An update on the epidemiology of calcium pyrophosphate dihydrate crystal deposition disease. Rheumatology (Oxford) 2009;48:711–715. doi: 10.1093/rheumatology/kep081.
    1. Zhu Y, Pandya BJ, Choi HK. Prevalence of gout and hyperuricemia in the US general population: the National Health and nutrition examination survey 2007-2008. Arthritis Rheum. 2011;63:3136–3141. doi: 10.1002/art.30520.
    1. Mease PJ, Garg A, Helliwell PS, Park JJ, Gladman DD. Development of criteria to distinguish inflammatory from noninflammatory arthritis, enthesitis, dactylitis, and spondylitis: a report from the GRAPPA 2013 annual meeting. J Rheumatol. 2014;41:1249–1251. doi: 10.3899/jrheum.140182.
    1. Cohen JM, Husni ME, Qureshi AA, Merola JF. Psoriatic arthritis: it's as easy as “PSA”. J Am Acad Dermatol. 2015;72:905–906. doi: 10.1016/j.jaad.2014.12.008.
    1. Helliwell PS, Porter G, Taylor WJ, CASPAR Study Group Polyarticular psoriatic arthritis is more like oligoarticular psoriatic arthritis, than rheumatoid arthritis. Ann Rheum Dis. 2007;66:113–117. doi: 10.1136/ard.2006.054288.
    1. Veale DJ, Fearon U. What makes psoriatic and rheumatoid arthritis so different? RMD Open. 2015;1:e000025. doi: 10.1136/rmdopen-2014-000025.
    1. Gladman DD. Clinical features and diagnostic considerations in psoriatic arthritis. Rheum Dis Clin N Am. 2015;41:569–579. doi: 10.1016/j.rdc.2015.07.003.
    1. Eder L, Jayakar J, Thavaneswaran A, Haddad A, Chandran V, Salonen D, et al. Is the MAdrid Sonographic Enthesitis Index useful for differentiating psoriatic arthritis from psoriasis alone and healthy controls? J Rheumatol. 2014;41:466–472. doi: 10.3899/jrheum.130949.
    1. Punzi L, Podswiadek M, Oliviero F, Lonigro A, Modesti V, Ramonda R, et al. Laboratory findings in psoriatic arthritis. Reumatismo. 2007;59(Suppl 1):52–55.
    1. Landry A, Docherty P, Ouellette S, Cartier LJ. Causes and outcomes of markedly elevated C-reactive protein levels. Can Fam Physician. 2017;63:e316–e323.
    1. Suresh E. Diagnosis and management of gout: a rational approach. Postgrad Med J. 2005;81:572–579. doi: 10.1136/pgmj.2004.030692.
    1. Caylor TL, Perkins A. Recognition and management of polymyalgia rheumatica and giant cell arteritis. Am Fam Physician. 2013;88:676–684.
    1. Combe B, Landewe R, Daien CI, Hua C, Aletaha D, Álvaro-Gracia JM, et al. 2016 update of the EULAR recommendations for the management of early arthritis. Ann Rheum Dis. 2017;76:948–959. doi: 10.1136/annrheumdis-2016-210602.
    1. Forney MC, Winalski CS, Schils JP. Magnetic resonance imaging of inflammatory arthropathies of peripheral joints. Top Magn Reson Imaging. 2011;22:45–59. doi: 10.1097/RMR.0b013e31825c008d.
    1. Freeston JE, Coates LC, Nam JL, Moverley AR, Hensor EM, Wakefield RJ, et al. Is there subclinical synovitis in early psoriatic arthritis? A clinical comparison with gray-scale and power Doppler ultrasound. Arthritis Care Res (Hoboken) 2014;66:432–439. doi: 10.1002/acr.22158.
    1. Wakefield RJ, Green MJ, Marzo-Ortega H, Conaghan PG, Gibbon WW, McGonagle D, et al. Should oligoarthritis be reclassified? Ultrasound reveals a high prevalence of subclinical disease. Ann Rheum Dis. 2004;63:382–385. doi: 10.1136/ard.2003.007062.
    1. Anandarajah A. Imaging in psoriatic arthritis. Clin Rev Allergy Immunol. 2013;44:157–165. doi: 10.1007/s12016-012-8304-4.
    1. Eder L, Barzilai M, Peled N, Gladman DD, Zisman D. The use of ultrasound for the assessment of enthesitis in patients with spondyloarthritis. Clin Radiol. 2013;68:219–223. doi: 10.1016/j.crad.2012.07.018.
    1. Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D'Agostino MA, et al. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol. 2005;32:2485–2487.
    1. Fodor D, Nestorova R, Vlad V, Micu M. The place of musculoskeletal ultrasonography in gout diagnosis. Med Ultrason. 2014;16:336–344.
    1. Patil P, Dasgupta B. Role of diagnostic ultrasound in the assessment of musculoskeletal diseases. Ther Adv Musculoskelet Dis. 2012;4:341–355. doi: 10.1177/1759720X12442112.
    1. Dasgupta B, Cimmino MA, Kremers HM, Schmidt WA, Schirmer M, Salvarani C, et al. 2012 Provisional classification criteria for polymyalgia rheumatica: a European League Against Rheumatism/American College of Rheumatology collaborative initiative. Arthritis Rheum. 2012;64:943–954. doi: 10.1002/art.34356.
    1. Neogi T, Jansen TL, Dalbeth N, Fransen J, Schumacher HR, Berendsen D, et al. 2015 gout classification criteria: an American College of Rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheumatol. 2015;67:2557–2568. doi: 10.1002/art.39254.
    1. Brown AK. Using ultrasonography to facilitate best practice in diagnosis and management of RA. Nat Rev Rheumatol. 2009;5:698–706. doi: 10.1038/nrrheum.2009.227.
    1. Terslev L, Naredo E, Iagnocco A, Balint PV, Wakefield RJ, Aegerter P, et al. Defining enthesitis in spondyloarthritis by ultrasound: results of a Delphi process and of a reliability reading exercise. Arthritis Care Res (Hoboken). 2014;66:741–748. doi: 10.1002/acr.22191.
    1. Poggenborg RP, Terslev L, Pedersen SJ, Østergaard M. Recent advances in imaging in psoriatic arthritis. Ther Adv Musculoskelet Dis. 2011;3:43–53. doi: 10.1177/1759720X10394031.
    1. Schirmer M, Duftner C, Schmidt WA, Dejaco C. Ultrasonography in inflammatory rheumatic disease: an overview. Nat Rev Rheumatol. 2011;7:479–488. doi: 10.1038/nrrheum.2011.95.
    1. van der Ven M, van der Veer-Meerkerk M, Ten Cate DF, Rasappu N, Kok MR, Csakvari D, et al. Absence of ultrasound inflammation in patients presenting with arthralgia rules out the development of arthritis. Arthritis Res Ther. 2017;19:202. doi: 10.1186/s13075-017-1405-y.
    1. Ekiz T, Ozturk GT, Yalcin S, Kinikli G, Ozcakar L. Ultrasonographic diagnosis of posterior interosseous nerve entrapment due to ganglion cyst in a patient with rheumatoid arthritis. Rheumatology (Oxford) 2014;53:2208. doi: 10.1093/rheumatology/keu342.
    1. Kaeley GS, Nishio MJ, Goyal JR, MacCarter DK, Wells AF, Chen S, et al. Changes in ultrasonographic vascularity upon initiation of adalimumab combination therapy in rheumatoid arthritis patients with an inadequate response to methotrexate. Arthritis Rheumatol. 2016;68:2584–2592. doi: 10.1002/art.39751.
    1. Kaeley GS, Eder L, Aydin SZ, Gutierrez M, Bakewell C. Dactylitis: a hallmark of psoriatic arthritis. Semin Arthritis Rheum. 2018;48:263–273. doi: 10.1016/j.semarthrit.2018.02.002.
    1. Zabotti A, Salvin S, Quartuccio L, De Vita S. Differentiation between early rheumatoid and early psoriatic arthritis by the ultrasonographic study of the synovio-entheseal complex of the small joints of the hands. Clin Exp Rheumatol. 2016;34:459–465.
    1. Ramrattan LA, Kaeley GS. Sonographic characteristics of extensor tendon abnormalities and relationship with joint disease activity in rheumatoid arthritis: a pilot study. J Ultrasound Med. 2017;36:985–992. doi: 10.7863/ultra.16.05024.
    1. Liu JT, Yeh HM, Liu SY, Chen KT. Psoriatic arthritis: epidemiology, diagnosis, and treatment. World J Orthop. 2014;5:537–543. doi: 10.5312/wjo.v5.i4.537.
    1. Bakewell CJ, Olivieri I, Aydin SZ, Dejaco C, Ikeda K, Gutierrez M, et al. Ultrasound and magnetic resonance imaging in the evaluation of psoriatic dactylitis: status and perspectives. J Rheumatol. 2013;40:1951–1957. doi: 10.3899/jrheum.130643.
    1. Huh YH, Lee G, Song WH, Koh JT, Ryu JH. Crosstalk between FLS and chondrocytes is regulated by HIF-2α-mediated cytokines in arthritis. Exp Mol Med. 2015;47:e197. doi: 10.1038/emm.2015.88.
    1. Suzuki T. Power Doppler ultrasonographic assessment of the ankle in patients with inflammatory rheumatic diseases. World J Orthop. 2014;5:574–584. doi: 10.5312/wjo.v5.i5.574.
    1. Tang CY, Fung B. The last defence? Surgical aspects of gouty arthritis of hand and wrist. Hong Kong Med J. 2011;17:480–486.
    1. Padovano I, Costantino F, Breban M, D'Agostino MA. Prevalence of ultrasound synovial inflammatory findings in healthy subjects. Ann Rheum Dis. 2016;75:1819–1823. doi: 10.1136/annrheumdis-2015-208103.
    1. Balint PV, Kane D, Wilson H, McInnes IB, Sturrock RD. Ultrasonography of entheseal insertions in the lower limb in spondyloarthropathy. Ann Rheum Dis. 2002;61:905–910. doi: 10.1136/ard.61.10.905.
    1. Acosta-Felquer ML, Ruta S, Rosa J, Marin J, Ferreyra-Garrot L, Galimberti ML, et al. Ultrasound entheseal abnormalities at the distal interphalangeal joints and clinical nail involvement in patients with psoriasis and psoriatic arthritis, supporting the nail-enthesitis theory. Semin Arthritis Rheum. 2017;47:338–342. doi: 10.1016/j.semarthrit.2017.05.002.
    1. Kristensen S, Christensen JH, Schmidt EB, Olesen JL, Johansen MB, Arvesen KB, et al. Assessment of enthesitis in patients with psoriatic arthritis using clinical examination and ultrasound. Muscles Ligaments Tendons J. 2016;6:241–247. doi: 10.32098/mltj.02.2016.12.
    1. Polachek A, Cook R, Chandran V, Gladman DD, Eder L. The association between sonographic enthesitis and radiographic damage in psoriatic arthritis. Arthritis Res Ther. 2017;19:189. doi: 10.1186/s13075-017-1399-5.
    1. Gutierrez M, Filippucci E, Grassi W, Rosemffet M. Intratendinous power Doppler changes related to patient position in seronegative spondyloarthritis. J Rheumatol. 2010;37:1057–1059. doi: 10.3899/jrheum.090900.
    1. Kaeley GS, D'Agostino MA, Grassi W, Ostergaard M, Olivieri I. GRAPPA 2011: proceedings from the ultrasound imaging module. J Rheumatol. 2012;39:2211–2213. doi: 10.3899/jrheum.120826.
    1. Michelsen B, Diamantopoulos AP, Soldal DM, Hammer HB, Kavanaugh A, Haugeberg G. Achilles enthesitis defined by ultrasound is not associated with clinical enthesitis in patients with psoriatic arthritis. RMD Open. 2017;3:e000486. doi: 10.1136/rmdopen-2017-000486.
    1. Balint PV, Terslev L, Aegerter P, Bruyn GAW, Chary-Valckenaere I, Gandjbakhch F, et al. Reliability of a consensus-based ultrasound definition and scoring for enthesitis in spondyloarthritis and psoriatic arthritis: an OMERACT US initiative. Ann Rheum Dis. 2018;77:1730–1735. doi: 10.1136/annrheumdis-2018-213609.
    1. Tom S, Zhong Y, Cook R, Aydin SZ, Kaeley G, Eder L. Development of a preliminary ultrasonographic enthesitis score in psoriatic arthritis - GRAPPA Ultrasound Working Group. J Rheumatol. 2019;46:384–390. doi: 10.3899/jrheum.171465.
    1. D'Agostino MA, Olivieri I. Enthesitis. Best Pract Res Clin Rheumatol. 2006;20:473–486. doi: 10.1016/j.berh.2006.03.007.
    1. Sakellariou G, Iagnocco A, Delle Sedie A, Riente L, Filippucci E, Montecucco C. Ultrasonographic evaluation of entheses in patients with spondyloarthritis: a systematic literature review. Clin Exp Rheumatol. 2014;32:969–978.
    1. de Miguel E, Cobo T, Muñoz-Fernández S, Naredo E, Usón J, Acebes JC, et al. Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann Rheum Dis. 2009;68:169–174. doi: 10.1136/ard.2007.084251.
    1. de Miguel E, Muñoz-Fernández S, Castillo C, Cobo-Ibáñez T, Martín-Mola E. Diagnostic accuracy of enthesis ultrasound in the diagnosis of early spondyloarthritis. Ann Rheum Dis. 2011;70:434–439. doi: 10.1136/ard.2010.134965.
    1. Gisondi P, Tinazzi I, El-Dalati G, Gallo M, Biasi D, Barbara LM, et al. Lower limb enthesopathy in patients with psoriasis without clinical signs of arthropathy: a hospital-based case-control study. Ann Rheum Dis. 2008;67:26–30. doi: 10.1136/ard.2007.075101.
    1. Yumusakhuylu Y, Kasapoglu-Gunal E, Murat S, Kurum E, Keskin H, Icagasioglu A, et al. A preliminary study showing that ultrasonography cannot differentiate between psoriatic arthritis and nodal osteoarthritis based on enthesopathy scores. Rheumatology (Oxford) 2016;55:1703–1704. doi: 10.1093/rheumatology/kew218.
    1. Tan AL, Toumi H, Benjamin M, Grainger AJ, Tanner SF, Emery P, et al. Combined high-resolution magnetic resonance imaging and histological examination to explore the role of ligaments and tendons in the phenotypic expression of early hand osteoarthritis. Ann Rheum Dis. 2006;65:1267–1272. doi: 10.1136/ard.2005.050112.
    1. Finzel S, Ohrndorf S, Englbrecht M, Stach C, Messerschmidt J, Schett G, et al. A detailed comparative study of high-resolution ultrasound and micro-computed tomography for detection of arthritic bone erosions. Arthritis Rheum. 2011;63:1231–1236. doi: 10.1002/art.30285.
    1. Zayat AS, Ellegaard K, Conaghan PG, Terslev L, Hensor EM, Freeston JE, et al. The specificity of ultrasound-detected bone erosions for rheumatoid arthritis. Ann Rheum Dis. 2015;74:897–903. doi: 10.1136/annrheumdis-2013-204864.
    1. Kawashiri SY, Fujikawa K, Nishino A, Okada A, Aramaki T, Shimizu T, et al. Ultrasound-detected bone erosion is a relapse risk factor after discontinuation of biologic disease-modifying antirheumatic drugs in patients with rheumatoid arthritis whose ultrasound power Doppler synovitis activity and clinical disease activity are well controlled. Arthritis Res Ther. 2017;19:108. doi: 10.1186/s13075-017-1320-2.
    1. Nalbant S, Corominas H, Hsu B, Chen LX, Schumacher HR, Kitumnuaypong T. Ultrasonography for assessment of subcutaneous nodules. J Rheumatol. 2003;30:1191–1195.
    1. Grassi W, Meenagh G, Pascual E, Filippucci E. “crystal clear”-sonographic assessment of gout and calcium pyrophosphate deposition disease. Semin Arthritis Rheum. 2006;36:197–202. doi: 10.1016/j.semarthrit.2006.08.001.
    1. Filippou G, Scirè CA, Damjanov N, Adinolfi A, Carrara G, Picerno V, et al. Definition and reliability assessment of elementary ultrasonographic findings in calcium pyrophosphate deposition disease: a study by the OMERACT calcium pyrophosphate deposition disease ultrasound subtask force. J Rheumatol. 2017;44:1744–1749. doi: 10.3899/jrheum.161057.
    1. Filippou G, Scirè CA, Adinolfi A, Damjanov NS, Carrara G, Bruyn GAW, et al. Identification of calcium pyrophosphate deposition disease (CPPD) by ultrasound: reliability of the OMERACT definitions in an extended set of joints-an international multiobserver study by the OMERACT calcium pyrophosphate deposition disease ultrasound subtask force. Ann Rheum Dis. 2018;77:1194–1199. doi: 10.1136/annrheumdis-2018-213217.
    1. Grassi W, Gutierrez M. Psoriatic arthritis: need for ultrasound in everyday clinical practice. J Rheumatol Suppl. 2012;89:39–43. doi: 10.3899/jrheum.120241.
    1. Peiteado D, Villalba A, Martin-Mola E, Balsa A, De Miguel E. Ultrasound sensitivity to changes in gout: a longitudinal study after two years of treatment. Clin Exp Rheumatol. 2017;35:746–751.
    1. Rutigliano IM, Scirocco C, Ceccarelli F, Finucci A, Iagnocco A. Musculoskeletal ultrasound in the evaluation of polymyalgia Rheumatica. Med Ultrason. 2015;17:361–366. doi: 10.11152/mu.2013.2066.173.aig.
    1. Sakellariou G, Iagnocco A, Riente L, Ceccarelli F, Carli L, Di Geso L, et al. Ultrasound imaging for the rheumatologist XLIII. Ultrasonographic evaluation of shoulders and hips in patients with polymyalgia rheumatica: a systematic literature review. Clin Exp Rheumatol. 2013;31:1–7.

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する