Semin Musculoskelet Radiol 2016; 20(05): 496-506
DOI: 10.1055/s-0036-1593533
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Recommendations of the ESSR Arthritis Subcommittee on Ultrasonography in Inflammatory Joint Disease

Athena Plagou
1   Department of Radiology, Private Institution of Ultrasonography, Athens, Greece
,
James Teh
2   Department of Musculoskeletal Radiology, University of Oxford, Oxford, United Kingdom
,
Andrew J. Grainger
3   Leeds Musculoskeletal Biomedical Research Unit, Leeds Teaching Hospitals, Leeds, United Kingdom
,
Claudia Schueller-Weidekamm
4   Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
,
Iwona Sudoł-Szopińska
5   Department of Radiology, National Institute of Geriatrics, Rheumatology and Rehabilitation, Warsaw, Poland
,
Winston Rennie
6   Department of Musculoskeletal Radiology, University of Loughborough, Leicester Royal Infirmary, Leicester, United Kingdom
,
Gunnar Åström
7   Department of Radiology, University Hospital, Uppsala, Sweden
,
Antoine Feydy
8   Department of Radiology B, Hôpital Cochin, APHP, Paris, France
,
Chiara Giraudo
9   Division of Neuroradiology and Musculoskeletal Radiology, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
,
Henri Guerini
10   Department of Radiology B, Cochin Hospital, Paris, France
,
Giuseppe Guglielmi
11   Department of Radiology, University of Foggia, Foggia, Italy
,
Amanda Isaac
12   Department of Musculoskeletal Radiology, Guys and St Thomas' Hospitals Foundation Trust, Kings College London and GKT, London, United Kingdom
,
Lennart Jans
13   Department of Radiology, Ghent University Hospital, Ghent, Belgium
,
Anne Grethe Jurik
14   Department of Radiology, Aarhus University Hospital, Aarhus, Denmark
,
Franz Kainberger
9   Division of Neuroradiology and Musculoskeletal Radiology, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
,
Mario Maas
15   Department of Radiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
,
Carlo Martinoli
16   Department of Radiology, Università degli Studi di Genova, Genova, Italy
,
Vasco V. Mascarenhas
17   Unidade de Imagem Musculoesquelética (UIME), Hospital da Luz, Lisbon, Portugal
,
Falk Miese
18   Department of Diagnostic and Interventional Radiology, Institute of Radiology, Nuclear Medicine and Radiotherapy, Bottrop, Denmark
,
Philip O'Connor
19   The NIHR Musculoskeletal Biomedical Research Unit, Leeds Teaching Hospital NHS Trust, Leeds, United Kingdom
,
Edwin H. Oei
20   Department of Radiology and Nuclear Medicine, Erasmus MC, University Medical Center, Rotterdam, The Netherlands
,
Mikkel Østergaard
21   Department of Rheumatology, Copenhagen Center for Arthritis Research (COPECARE), Center for Rheumatology and Spine Diseases, Copenhagen University Hospital Rigshospitalet, Glostrup, Denmark
,
Philippe Peetrons
22   Department of Radiology, Hôpitaux Iris Sud, Brussels, Belgium
,
Hannes Platzgummer
9   Division of Neuroradiology and Musculoskeletal Radiology, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
,
Monique Reijnierse
23   Department of Musculoskeletal Radiology, Leiden University Medical Center, Leiden, The Netherlands
,
Philip Robinson
3   Leeds Musculoskeletal Biomedical Research Unit, Leeds Teaching Hospitals, Leeds, United Kingdom
,
Mitja Rupreht
24   Department of Radiology, University Medical Center Maribor, Maribor, Slovenia
,
Paolo Simoni
25   Department of Radiology, Université Libre de Bruxelles (ULB), “Reine Fabiola” Children's University Hospital, Brussels, Belgium
,
Marius C. Wick
26   Functional Unit for Diagnostic and Interventional Musculoskeletal Radiology, Function Imaging and Physiology, Karolinska University Hospital, Stockholm, Sweden
,
Anna Zejden
14   Department of Radiology, Aarhus University Hospital, Aarhus, Denmark
,
Andrea S. Klauser
27   Section Rheumatology and Sports Imaging, Department of Radiology, Medical University Innsbruck, Innsbruck, Austria
› Author Affiliations
Further Information

Publication History

Publication Date:
21 December 2016 (online)

Abstract

This article presents the recommendations of the European Society of Musculoskeletal Radiology Arthritis Subcommittee on the use of ultrasonography (US) in rheumatic disease, focused on the examination of joints in the adult population. The recommended examination technique and protocols used in a radiologic work-up are discussed. The main US features that can lead to a final diagnosis in the most common rheumatic diseases are addressed. The differential diagnosis that should be considered at image interpretation is presented. The role of US in interventional procedures and clinically important recent developments is also discussed.

 
  • References

  • 1 Watt I. Basic differential diagnosis of arthritis. Eur Radiol 1997; 7 (3) 344-351
  • 2 Wakefield RJ, Green MJ, Marzo-Ortega H , et al. Should oligoarthritis be reclassified? Ultrasound reveals a high prevalence of subclinical disease. Ann Rheum Dis 2004; 63 (4) 382-385
  • 3 Naredo E, Bonilla G, Gamero F, Uson J, Carmona L, Laffon A. Assessment of inflammatory activity in rheumatoid arthritis: a comparative study of clinical evaluation with grey scale and power Doppler ultrasonography. Ann Rheum Dis 2005; 64 (3) 375-381
  • 4 Taljanovic MS, Melville DMH, Gimber LH , et al. High-resolution US of rheumatologic diseases. Radiographics 2015; 35 (7) 2026-2048
  • 5 McNally EG. Ultrasound of the small joints of the hands and feet: current status. Skeletal Radiol 2008; 37 (2) 99-113
  • 6 Martinoli C. Musculoskeletal ultrasound: technical guidelines. Insights Imaging 2010; 1 (3) 99-141
  • 7 Wakefield RJ, Balint PV, Szkudlarek M , et al; OMERACT 7 Special Interest Group. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 2005; 32 (12) 2485-2487
  • 8 van der Heijde DM, van Leeuwen MA, van Riel PL, van de Putte LB. Radiographic progression on radiographs of hands and feet during the first 3 years of rheumatoid arthritis measured according to Sharp's method (van der Heijde modification). J Rheumatol 1995; 22 (9) 1792-1796
  • 9 Lopez-Ben R, Bernreuter WK, Moreland LW, Alarcon GS. Ultrasound detection of bone erosions in rheumatoid arthritis: a comparison to routine radiographs of the hands and feet. Skeletal Radiol 2004; 33 (2) 80-84
  • 10 Colebatch AN, Edwards CJ, Østergaard M , et al. EULAR recommendations for the use of imaging of the joints in the clinical management of rheumatoid arthritis. Ann Rheum Dis 2013; 72 (6) 804-814
  • 11 Harris Jr ED. Recent insights into the pathogenesis of the proliferative lesion in rheumatoid arthritis. Arthritis Rheum 1976; 19 (1) 68-72
  • 12 Wakefield RJ, Brown AK, O'Connor PJ, Emery P. Power Doppler sonography: improving disease activity assessment in inflammatory musculoskeletal disease. Arthritis Rheum 2003; 48 (2) 285-288
  • 13 Naredo E, Collado P, Cruz A , et al. Longitudinal power Doppler ultrasonographic assessment of joint inflammatory activity in early rheumatoid arthritis: predictive value in disease activity and radiologic progression. Arthritis Rheum 2007; 57 (1) 116-124
  • 14 Ohrndorf S, Backhaus M. Advances in sonographic scoring of rheumatoid arthritis. Ann Rheum Dis 2013; 72 (2) (Suppl. 02) ii69-ii75
  • 15 Szkudlarek M, Court-Payen M, Jacobsen S, Klarlund M, Thomsen HS, Østergaard M. Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum 2003; 48 (4) 955-962
  • 16 Szkudlarek M, Klarlund M, Narvestad E , et al. Ultrasonography of the metacarpophalangeal and proximal interphalangeal joints in rheumatoid arthritis: a comparison with magnetic resonance imaging, conventional radiography and clinical examination. Arthritis Res Ther 2006; 8 (2) R52
  • 17 Szkudlarek M, Narvestad E, Klarlund M, Court-Payen M, Thomsen HS, Østergaard M. Ultrasonography of the metatarsophalangeal joints in rheumatoid arthritis: comparison with magnetic resonance imaging, conventional radiography, and clinical examination. Arthritis Rheum 2004; 50 (7) 2103-2112
  • 18 Naredo E, D'Agostino MA, Wakefield RJ , et al; OMERACT Ultrasound Task Force*. Reliability of a consensus-based ultrasound score for tenosynovitis in rheumatoid arthritis. Ann Rheum Dis 2013; 72 (8) 1328-1334
  • 19 Wakefield RJ, Gibbon WW, Conaghan PG , et al. The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiography. Arthritis Rheum 2000; 43 (12) 2762-2770
  • 20 Grainger AJ, Rowbotham EL. Rheumatoid arthritis. Semin Musculoskelet Radiol 2013; 17 (1) 69-73
  • 21 Mandl P, Navarro-Compán V, Terslev L , et al; European League Against Rheumatism (EULAR). EULAR recommendations for the use of imaging in the diagnosis and management of spondyloarthritis in clinical practice. Ann Rheum Dis 2015; 74 (7) 1327-1339
  • 22 Schueller-Weidekamm C, Mascarenhas VV, Sudol-Szopinska I , et al. Imaging and interpretation of axial spondylarthritis: the radiologist's perspective—consensus of the Arthritis Subcommittee of the ESSR. Semin Musculoskelet Radiol 2014; 18 (3) 265-279
  • 23 Sudoł-Szopińska I, Jurik AG, Eshed I , et al. Recommendations of the ESSR Arthritis Subcommittee for the use of magnetic resonance imaging in musculoskeletal rheumatic diseases. Semin Musculoskelet Radiol 2015; 19 (4) 396-411
  • 24 Benjamin M, Moriggl B, Brenner E, Emery P, McGonagle D, Redman S. The “enthesis organ” concept: why enthesopathies may not present as focal insertional disorders. Arthritis Rheum 2004; 50 (10) 3306-3313
  • 25 Benjamin M, McGonagle D. The enthesis organ concept and its relevance to the spondyloarthropathies. Adv Exp Med Biol 2009; 649: 57-70
  • 26 Gandjbakhch F, Terslev L, Joshua F, Wakefield RJ, Naredo E, D'Agostino MA ; OMERACT Ultrasound Task Force. Ultrasound in the evaluation of enthesitis: status and perspectives. Arthritis Res Ther 2011; 13 (6) R188
  • 27 Spadaro A, Iagnocco A, Perrotta FM, Modesti M, Scarno A, Valesini G. Clinical and ultrasonography assessment of peripheral enthesitis in ankylosing spondylitis. Rheumatology (Oxford) 2011; 50 (11) 2080-2086
  • 28 Feydy A, Lavie-Brion MC, Gossec L , et al. Comparative study of MRI and power Doppler ultrasonography of the heel in patients with spondyloarthritis with and without heel pain and in controls. Ann Rheum Dis 2012; 71 (4) 498-503
  • 29 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 (10) 905-910
  • 30 Wick MC, Weiss RJ, Arora R , et al. Enthesiopathy of the flexor carpi ulnaris at the pisiform: findings of high-frequency sonography. Eur J Radiol 2011; 77 (2) 240-244
  • 31 Neogi T, Jansen TL, Dalbeth N , et al. 2015 Gout classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis 2015; 74 (10) 1789-1798
  • 32 de Avila Fernandes E, Kubota ES, Sandim GB, Mitraud SA, Ferrari AJ, Fernandes AR. Ultrasound features of tophi in chronic tophaceous gout. Skeletal Radiol 2011; 40 (3) 309-315
  • 33 Chowalloor PV, Keen HI. A systematic review of ultrasonography in gout and asymptomatic hyperuricaemia. Ann Rheum Dis 2013; 72 (5) 638-645
  • 34 Gutierrez M, Schmidt WA, Thiele RG , et al; OMERACT Ultrasound Gout Task Force group. International consensus for ultrasound lesions in gout: results of Delphi process and web-reliability exercise. Rheumatology (Oxford) 2015; 54 (10) 1797-1805
  • 35 Terslev L, Gutierrez M, Schmidt WA , et al; OMERACT Ultrasound Working Group. Ultrasound as an outcome measure in gout. a validation process by the OMERACT Ultrasound Working Group. J Rheumatol 2015; 42 (11) 2177-2181
  • 36 Desai MA, Peterson JJ, Garner HW, Kransdorf MJ. Clinical utility of dual-energy CT for evaluation of tophaceous gout. Radiographics 2011; 31 (5) 1365-1375 ; discussion 1376–1377
  • 37 Gamon E, Combe B, Barnetche T, Mouterde G. Diagnostic value of ultrasound in calcium pyrophosphate deposition disease: a systematic review and meta-analysis. RMD Open 2015; 1 (1) e000118
  • 38 Grassi W, Meenagh G, Pascual E, Filippucci E. “Crystal clear”-sonographic assessment of gout and calcium pyrophosphate deposition disease. Semin Arthritis Rheum 2006; 36 (3) 197-202
  • 39 Buchanan WW. William Hunter (1718–1783). Rheumatology (Oxford) 2003; 42 (10) 1260-1261
  • 40 Poole AR. Osteoarthritis as a whole joint disease. HSS J 2012; 8 (1) 4-6
  • 41 Guermazi A, Roemer FW, Hayashi D. Imaging of osteoarthritis: update from a radiological perspective. Curr Opin Rheumatol 2011; 23 (5) 484-491
  • 42 Eckstein F, Mosher T, Hunter D. Imaging of knee osteoarthritis: data beyond the beauty. Curr Opin Rheumatol 2007; 19 (5) 435-443
  • 43 Eckstein F, Le Graverand MP, Charles HC , et al; A9001140, investigators. Clinical, radiographic, molecular and MRI-based predictors of cartilage loss in knee osteoarthritis. Ann Rheum Dis 2011; 70 (7) 1223-1230
  • 44 Keen HI, Wakefield RJ, Conaghan PG. A systematic review of ultrasonography in osteoarthritis. Ann Rheum Dis 2009; 68 (5) 611-619
  • 45 Keen HI, Wakefield RJ, Grainger AJ, Hensor EMA, Emery P, Conaghan PG. Can ultrasonography improve on radiographic assessment in osteoarthritis of the hands? A comparison between radiographic and ultrasonographic detected pathology. Ann Rheum Dis 2008; 67 (8) 1116-1120
  • 46 Keen HI, Wakefield RJ, Grainger AJ, Hensor EM, Emery P, Conaghan PG. An ultrasonographic study of osteoarthritis of the hand: synovitis and its relationship to structural pathology and symptoms. Arthritis Rheum 2008; 59 (12) 1756-1763
  • 47 Klauser AS, Faschingbauer R, Kupferthaler K , et al. Sonographic criteria for therapy follow-up in the course of ultrasound-guided intra-articular injections of hyaluronic acid in hand osteoarthritis. Eur J Radiol 2012; 81 (7) 1607-1611
  • 48 Zamzam MM. The role of ultrasound in differentiating septic arthritis from transient synovitis of the hip in children. J Pediatr Orthop B 2006; 15 (6) 418-422
  • 49 Balint PV, Kane D, Hunter J, McInnes IB, Field M, Sturrock RD. Ultrasound guided versus conventional joint and soft tissue fluid aspiration in rheumatology practice: a pilot study. J Rheumatol 2002; 29 (10) 2209-2213
  • 50 Koski JM, Helle M. Ultrasound guided synovial biopsy using portal and forceps. Ann Rheum Dis 2005; 64 (6) 926-929
  • 51 Sibbitt Jr WL, Band PA, Chavez-Chiang NR, Delea SL, Norton HE, Bankhurst AD. A randomized controlled trial of the cost-effectiveness of ultrasound-guided intraarticular injection of inflammatory arthritis. J Rheumatol 2011; 38 (2) 252-263
  • 52 Klauser AS, Peetrons P. Developments in musculoskeletal ultrasound and clinical applications. Skeletal Radiol 2010; 39 (11) 1061-1071
  • 53 Klauser A, Frauscher F, Schirmer M , et al. The value of contrast-enhanced color Doppler ultrasound in the detection of vascularization of finger joints in patients with rheumatoid arthritis. Arthritis Rheum 2002; 46 (3) 647-653
  • 54 Klauser A, Demharter J, De Marchi A , et al; IACUS study group. Contrast enhanced gray-scale sonography in assessment of joint vascularity in rheumatoid arthritis: results from the IACUS study group. Eur Radiol 2005; 15 (12) 2404-2410
  • 55 Thiele RG, Schlesinger N. Ultrasonography shows disappearance of monosodium urate crystal deposition on hyaline cartilage after sustained normouricemia is achieved. Rheumatol Int 2010; 30 (4) 495-503
  • 56 Kang T, Lanni S, Nam J, Emery P, Wakefield RJ. The evolution of ultrasound in rheumatology. Ther Adv Musculoskelet Dis 2012; 4 (6) 399-411
  • 57 Lalitha P, Reddy MCh, Reddy KJ. Musculoskeletal applications of elastography: a pictorial essay of our initial experience. Korean J Radiol 2011; 12 (3) 365-375
  • 58 Rudwaleit M, van der Heijde D, Landewé R , et al. The development of Assessment of SpondyloArthritis International Society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis 2009; 68 (6) 777-783