Clinical Rheumatology

, Volume 35, Issue 11, pp 2669–2678 | Cite as

Is ankle involvement underestimated in rheumatoid arthritis? Results of a multicenter ultrasound study

  • Marwin Gutierrez
  • Carlos Pineda
  • Fausto Salaffi
  • Bernd Raffeiner
  • Tomas Cazenave
  • Gabriela A. Martinez-Nava
  • Chiara Bertolazzi
  • Florentin Vreju
  • Nevsun Inanc
  • Eduardo Villaman
  • Andrea Delle Sedie
  • Fernando Dal Pra
  • Marcos Rosemffet
Original Article


The aim of this study is to investigate the prevalence of subclinical ankle involvement by ultrasound in patients with rheumatoid arthritis (RA). The study was conducted on 216 patients with RA and 200 healthy sex- and age-matched controls. Patients with no history or clinical evidence of ankle involvement underwent US examination. For each ankle, tibio-talar (TT) joint, tibialis anterior (TA) tendon, extensor halux (EH) and extensor common (EC) tendons, tibialis posterior (TP) tendon, flexor common (FC) tendon and flexor hallux (FH) tendon, peroneous brevis (PB) and longus (PL) tendons, Achilles tendon (AT) and plantar fascia (PF) were assessed. The following abnormalities were recorded: synovitis, tenosynovitis, bursitis, enthesopathy and rupture. BMI, DAS28, RF ESR and CRP were also obtained. A total of 432 ankles of patients with RA and 400 ankles of healthy controls were assessed. In 188 (87%) patients with RA, US showed ankle abnormalities whereas, in control group, US found abnormalities in 57 (28.5 %) subjects (p = 0.01). The most frequent US abnormality in RA patients was TP tenosynovits (69/216) (31.9 %), followed by PL tenosynovitis (58/216) (26.9 %), TT synovitis (54/216) (25 %), PB tenosynovitis (51/216) (23.6 %), AT enthesopathy (41/216) (19 %) and AT bursitis (22/216) (10.2 %). In 118 RA patients out of 216 (54.6%), a positive PD was found. No statistically significant correlation was found between the US findings and age, disease duration, BMI, DAS28, RF, ESR and CRP. The present study provides evidence of the higher prevalence of subclinical ankle involvement in RA patients than in age- and gender-matched healthy controls identified by US.


Ankle Rheumatoid arthritis Subclinical involvement Ultrasound 


Compliance with ethical standards

Authors’ contributions

MG participated in the design of the study and the acquisition and interpretation of data, and performed the drafting of the manuscript. BR, TC, FV, NI, EV, AdS, FDP participated in data acquisition and performed the US examinations. CP, FS made substantial contributions to the conception and design of the study, participated in the acquisition of data and was involved in revising the manuscript for important intellectual content. GMN performed the statistical analysis and was involved in revising the manuscript for intellectual content MR participated in the conception of the study and data interpretation, was involved in drafting the manuscript, and gave final approval of the version of the paper to be published. All authors read and approved the final manuscript.



Supplementary material

10067_2016_3226_MOESM1_ESM.doc (30 kb)
ESM 1 Proportion of patients according the possible combination of treatments. (DOC 30 kb)


  1. 1.
    Vainio K (1956) The rheumatoid foot: a clinical study with pathological and roentgenological comments. Ann Chir Gynaecol Fenn Suppl 45:1–107PubMedGoogle Scholar
  2. 2.
    Brenton-Rule A, Dalbeth N, Menz HB, Bassett S, Rome K (2016) Foot and ankle characteristics associated with falls in adults with established rheumatoid arthritis: a cross-sectional study. BMC Musculoskelet Disord 13:17–22Google Scholar
  3. 3.
    Baan H, Drossaers-Bakker W, Dubbeldam R, van de Laar M (2011) We should not forget the foot: relations between signs and symptoms, damage, and function in rheumatoid arthritis. Clin Rheumatol 30:1475–9CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    van Dijk CN, Lim LS, Bossuyt PM, Marti RK (1996) Physical examination is sufficient for the diagnosis of sprained ankles. J Bone Joint Surg Br 78:958–62CrossRefPubMedGoogle Scholar
  5. 5.
    Coady D, Walker D, Kay L (2004) Regional Examination of the Musculoskeletal System (REMS): a core set of clinical skills for medical students. Rheumatology 43:633–9CrossRefPubMedGoogle Scholar
  6. 6.
    Calin A, Mackay K, Santos H, Brophy S (1999) A new dimension to outcome: application of the Bath Ankylosing Spondylitis Radiology Index. J Rheumatol 26:988–92PubMedGoogle Scholar
  7. 7.
    Resnick D, Niwayama G (1999) Entheses and enthesopathy Anatomical, pathological, and radiological correlation. Radiology 1983 146:1–9Google Scholar
  8. 8.
    Baker JF, Conaghan PG, Emery P, Baker DG, Østergaard M 2015 Validity of early MRI structural damage end points and potential impact on clinical trial design in rheumatoid arthritis. Ann Rheum Dis pii: annrheumdis-2014-206934.Google Scholar
  9. 9.
    Emery P, van der Heijde D, Ostergaard M, Conaghan PG, Genovese MC, Keystone EC, Fleischmann R, Hsia EC, Xu W, Xu S, Rahman MU (2011) Exploratory analyses of the association of MRI with clinical, laboratory and radiographic findings in patients with rheumatoid arthritis. Ann Rheum Dis 70:2126–30CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    D’Agostino MA, Said-Nahal R, Hacquard-Bouder C, Brasseur JL, Dougados M, Breban M (2003) Assessment of peripheral enthesitis in the spondylarthropathies by ultrasonography combined with power Doppler: a cross-sectional study. Arthritis Rheum 48:523–33CrossRefPubMedGoogle Scholar
  11. 11.
    Alarcon GS, Lopez-Ben R, Moreland LW (2002) High-resolution ultrasound for the study of target joints in rheumatoid arthritis. Arthritis Rheum 46:1969–70CrossRefPubMedGoogle Scholar
  12. 12.
    Salaffi F, Ciapetti A, Gasparini S, Carotti M, Filippucci E, Grassi W (2010) A clinical prediction rule combining routine assessment and power Doppler ultrasonography for predicting progression to rheumatoid arthritis from early-onset undifferentiated arthritis. Clin Exp Rheumatol 28:686–94PubMedGoogle Scholar
  13. 13.
    Dougados M, Jousse-Joulin S, Mistretta F (2010) Evaluation of several ultrasonography scoring systems for synovitis and comparison to clinical examination: results from a prospective multicentre study of rheumatoid arthritis. Ann Rheum Dis 69:828–33CrossRefPubMedGoogle Scholar
  14. 14.
    Naredo E, Collado P, Cruz A, Palop MJ, Cabero F, Richi P, Carmona L, Crespo M (2007) Longitudinal power Doppler ultrasonographic assessment of joint inflammatory activity in early rheumatoid arthritis: predictive value in disease activity and radiologic progression. Arthritis Rheum 57:116–24CrossRefPubMedGoogle Scholar
  15. 15.
    Wakefield RJ, Gibbon WW, Conaghan PG, O’Connor P, McGonagle D, Pease C, Green MJ, Veale DJ, Isaacs JD, Emery P et al (2000) The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiography. Arthritis Rheum 43:2762–70CrossRefPubMedGoogle Scholar
  16. 16.
    Gutierrez M, Filippucci E, De Angelis R, Salaffi F, Filosa G, Ruta S, Grassi W (2011) Subclinical entheseal involvement in patients with psoriasis: an ultrasound study. Semin Arthritis Rheum 40:407–12CrossRefPubMedGoogle Scholar
  17. 17.
    Gisondi P, Tinazzi I, El-Dalati G, Gallo M, Biasi D, Barbara LM, Girolomoni G (2008) Lower limb enthesopathy in patients with psoriasis without clinical signs of arthropathy: a hospital-based case-control study. Ann Rheum Dis 67:26–30CrossRefPubMedGoogle Scholar
  18. 18.
    Bandinelli F, Denaro V, Prignano F, Collaku L, Ciancio G, Matucci-Cerinic M (2015) Ultrasonographic wrist and hand abnormalities in early psoriatic arthritis patients: correlation with clinical, dermatological, serological and genetic indices. Clin Exp Rheumatol 33:330–5PubMedGoogle Scholar
  19. 19.
    Wakefield RJ, Green MJ, Marzo- Ortega H, Conaghan PG, Gibbon WW, McGonagle D, Proudman S, Emery P et al (2004) Should oligoarthritis be reclassified? Ultrasound reveals a high prevalence of subclinical disease. Ann Rheum Dis 63:382–5CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Kane D, Balint PV, Sturrock RD (2003) Ultrasonography is superior to clinical examination in the detection and localization of knee joint effusion in rheumatoid arthritis. J Rheumatol 30:966–71PubMedGoogle Scholar
  21. 21.
    Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, Birnbaum NS, Burmester GR, Bykerk VP, Cohen MD, Combe B, Costenbader KH, Dougados M, Emery P, Ferraccioli G, Hazes JM, Hobbs K, Huizinga TW, Kavanaugh A, Kay J, Kvien TK, Laing T, Mease P, Ménard HA, Moreland LW, Naden RL, Pincus T, Smolen JS, Stanislawska-Biernat E, Symmons D, Tak PP, Upchurch KS, Vencovský J, Wolfe F, Hawker G (2010) Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62:2569–81CrossRefPubMedGoogle Scholar
  22. 22.
    Backhaus M, Burmester GR, Gerber T, Grassi W, Machold KP, Swen WA, Wakefield RJ, Manger B, Working Group for Musculoskeletal Ultrasound in the EULAR Standing Committee on International Clinical Studies including Therapeutic Trials (2001) Guidelines for musculoskeletal ultrasound in rheumatology. Ann Rheum Dis 60:641–9CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D’Agostino MA Sanchez EN, Iagnocco A, Schmidt WA, Bruyn GA, Kane D, O’Connor PJ, Manger B, Joshua F, Koski J, Grassi W, Lassere MN, Swen N, Kainberger F, Klauser A, Ostergaard M, Brown AK, Machold KP, Conaghan PG; OMERACT 7 Special Interest Group (2005) Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 32:2485–7Google Scholar
  24. 24.
    Bouysset M, Tebib J, Noel E, Tavernier T, Miossec P, Vianey JC (2002) Rheumatoid flat foot and deformity of the first ray. J Rheumatol 29:903–5PubMedGoogle Scholar
  25. 25.
    Turner D, Woodburn J, Helliwell P, Cornwall M, Emery P (2006) Pes planovalgus in RA: a descriptive and analytical study of foot function determined by gait analysis. Musculoskeletal Care 1:21–33CrossRefGoogle Scholar
  26. 26.
    Barn R, Turner DE, Rafferty D, Sturrock RD, Woodburn J (2013) Tibialis posterior tenosynovitis and associated pes plano valgus in rheumatoid arthritis: electromyography, multisegment foot kinematics, and ultrasound features. Arthritis Care Res 65:495–502CrossRefGoogle Scholar
  27. 27.
    Woodburn J, Nelson KM, Siegel KL, Kepple TM, Gerber LH (2004) Multisegment foot motion during gait: proof of concept in rheumatoid arthritis. J Rheumatol 31:1918–27PubMedGoogle Scholar
  28. 28.
    Lehtinen A, Paimela L, Kreula J, Leirisalo-Repo M, Taavitsainen M (1996) Painful ankle region in rheumatoid arthritis. Analysis of soft-tissue changes with ultrasonography and MR imaging. Acta Radiol 37:572–7PubMedGoogle Scholar
  29. 29.
    Wakefield RJ, Freeston JE, O’Connor P, Reay N, Budgen A, Hensor EM, Helliwell PS, Emery P, Woodburn J (2008) The optimal assessment of the rheumatoid arthritis hindfoot: a comparative study of clinical examination, ultrasound and high field MRI. Ann Rheum Dis 67:1678–82CrossRefPubMedGoogle Scholar
  30. 30.
    Filer A, De Pablo P, Allen G, Nightingale P, Jordan A, Jobanputra P (2011) Utility of ultrasound joint counts in the prediction of rheumatoid arthritis in patients with very early synovitis. Ann Rheum Dis 70:500–7CrossRefPubMedGoogle Scholar
  31. 31.
    Micu MC, Serra S, Fodor D, Crespo M, Naredo E (2011) Inter-observer reliability of ultrasound detection of tendon abnormalities at the wrist and ankle in patients with rheumatoid arthritis. Rheumatology 50:1120–4CrossRefPubMedGoogle Scholar
  32. 32.
    Suzuki T, Okamoto A (2013) Ultrasound examination of symptomatic ankles in shorter-duration rheumatoid arthritis patients often reveals tenosynovitis. Clin Exp Rheumatol 31:281–4PubMedGoogle Scholar
  33. 33.
    Suzuki T, Tohda E, Ishihara K (2009) Power Doppler ultrasonography of symptomatic rheumatoid arthritis ankles revealed a positive association between tenosynovitis and rheumatoid factor. Mod Rheumatol 19:235–44CrossRefPubMedGoogle Scholar
  34. 34.
    Genc H, Cakit BD, Tuncbilek I, Erdem HR (2005) Ultrasonographic evaluation of tendons and enthesal sites in rheumatoid arthritis: comparison with ankylosing spondylitis and healthy subjects. Clin Rheumatol 24:272–7CrossRefPubMedGoogle Scholar
  35. 35.
    Falsetti P, Frediani B, Fioravanti A, Acciai C, Baldi F, Filippou G, Marcolongo R (2003) Sonographic study of calcaneal entheses in erosive osteoarthritis, nodal osteoarthritis, rheumatoid arthritis and pso-riatic arthritis. Scand J Rheumatol 32:229–34CrossRefPubMedGoogle Scholar
  36. 36.
    Paramarta JE, van der Leij C, Gofita I, Yeremenko N, van de Sande MG, de Hair MJ, Tak PP, Maas M, Baeten D (2014) Peripheral joint inflammation in early onset spondyloarthritis is not specifically related to enthesitis. Ann Rheum Dis 73:735–40CrossRefPubMedGoogle Scholar
  37. 37.
    Naredo E, Batlle-Gualda E, García-Vivar ML, García-Aparicio AM, Fernández-Sueiro JL, Fernández-Prada M, Giner E, Rodriguez-Gomez M, Pina MF, Medina-Luezas JA, Toyos FJ, Campos C, Gutiérrez-Polo R, Ferrer MA, Martínez O, Díaz-Torne C, Gonzalez T, Campos S, Queiro R, Castaño-Sánchez M, Aznar JJ, Bustabad S, Paez-Camino M, Tuneu R, Ruiz T, Mateo L, Pujol M, Ponce A, Ros I, Gallegos A, Moreno J, Gumbau D, Sianes M, Poveda-Elices MJ, Romero-Gómez M, Raya E, Ultrasound Group of the Spanish Society of Rheumatology (2010) Power Doppler ultrasonography assessment of entheses in spondyloarthropathies: response to therapy of entheseal abnormalities. J Rheumatol 37:2110–7CrossRefPubMedGoogle Scholar
  38. 38.
    Suzuki T (2014) Power Doppler ultrasonographic assessment of the ankle in patients with inflammatory rheumatic diseases. World J Orthop 18:574–84CrossRefGoogle Scholar
  39. 39.
    Ozcakar L, Cetin A, Inanici F, Kaymak B, Gurer CK, Kolemen F (2005) Ultrasonographical evaluation of the Achilles’ tendon in psoriasis patients. Int J Dermatol 44:930–2CrossRefPubMedGoogle Scholar
  40. 40.
    De Simone C, Guerriero C, Giampetruzzi AR, Costantini M, Di Gregorio F, Amerio P (2003) Achilles tendinitis in psoriasis: Clinical and sonographic findings. J Am Acad Dermatolm 49:217–22CrossRefGoogle Scholar
  41. 41.
    Bruyn GA, Hanova P, Lagnocco A, D’Agostino MA, Möller I, Terslev L, Backhaus M, Balint PV, Filippucci E, Baudoin P, van Vugt R, Pineda C, Wakefield R, Garrido J, Pecha O, Naredo E, OMERACT Ultrasound Task Force (2014) Ultrasound definition of tendon damage in patients with rheumatoid arthritis. Results of a OMERACT consensus-based ultrasound score focussing on the diagnostic reliability. Ann Rheum Dis 73:1929–34CrossRefPubMedGoogle Scholar
  42. 42.
    Naredo E, D’Agostino MA, Wakefield RJ, Möller I, Balint PV, Filippucci E, Iagnocco A, Karim Z, Terslev L, Bong DA, Garrido J, Martínez-Hernández D, Bruyn GA, OMERACT Ultrasound Task Force (2013) Reliability of a consensus-based ultrasound score for tenosynovitis in rheumatoid arthritis. Ann Rheum Dis 72:1328–34CrossRefPubMedGoogle Scholar
  43. 43.
    Hb H, Kvien T (2011) Ultrasonography shows significant improvement in wrist and ankle tenosynovitis in rheumatoid arthritis patients treated with adalimumab. Scand J Rheumatol 40:178–82CrossRefGoogle Scholar
  44. 44.
    van Tuyl LHD, Britsemmer K, Wells GA, Smolen J, Zhang B, Funovits J, van Schaardenburg D, Felson D, Boers M (2012) Remission in early rheumatoid arthritis defined by 28 joint counts: limited consequences of residual disease activity in the forefeet on outcome. Ann Rheum Dis 71:33–7CrossRefPubMedGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2016

Authors and Affiliations

  • Marwin Gutierrez
    • 1
    • 2
  • Carlos Pineda
    • 1
  • Fausto Salaffi
    • 2
  • Bernd Raffeiner
    • 3
  • Tomas Cazenave
    • 4
  • Gabriela A. Martinez-Nava
    • 1
  • Chiara Bertolazzi
    • 1
  • Florentin Vreju
    • 5
  • Nevsun Inanc
    • 6
  • Eduardo Villaman
    • 7
  • Andrea Delle Sedie
    • 8
  • Fernando Dal Pra
    • 4
  • Marcos Rosemffet
    • 4
  1. 1.Division of Musculoskeletal and Rheumatic DiseasesInstituto Nacional de RehabilitaciónMexico CityMexico
  2. 2.Clinica ReumatologicaUniversita Politecnica delle MarcheAnconaItaly
  3. 3.Department of MedicineRheumatology UnitOspedale di BolzanoItaly
  4. 4.Instituto de Rehabilitación PsicofísicaBuenos AiresArgentina
  5. 5.Rheumatology DepartmentUniversity of Medicine and Pharmacy CraiovaCraiovaRomania
  6. 6.Rheumatology DepartmentMarmara UniversityIstanbulTurkey
  7. 7.Research DepartmentUniversidad Autónoma de Baja CaliforniaMexicaliMexico
  8. 8.Rheumatology DepartmentUniversity of PisaPisaItaly

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