Musculoskeletal Ultrasound for Diagnosis and Treatment in Juvenile Idiopathic Arthritis

Pediatric Rheumatology (M Becker and J Harris, Section Editors)
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Opinion statement

Among users of musculoskeletal ultrasound (MSUS), the benefits of real-time imaging of patients with juvenile idiopathic arthritis (JIA) are widely appreciated. Yet to the larger pediatric rheumatology public, these advantages may be easily overlooked. MSUS enhances the routine clinical examination, allowing for detection of subclinical disease and an accurate determination of the location and extent of disease activity. Ultrasound visualizes synovitis and tenosynovitis, enthesitis, erosions, and cartilage changes, enabling one to monitor the response to treatment and assisting in the determination of remission. MSUS is particularly suited for guidance for intraarticular corticosteroid injections. The ability to review images at the bedside with patients and their caregivers can be reassuring, to both the patient and the practitioner. Understanding of the normal, healthy sonoanatomy, however, can be challenging and remains a topic of ongoing research. The significance of subclinical synovitis (US-detected features of synovitis in the context of clinically healthy joint) remains unclear. As a better understanding of normal/physiologic sonographic appearance of the growing joint emerges, in particular, the presence of Doppler signal in the developing articular space, the predictive value and prognostic significance of subclinical synovitis will become more evident. What constitutes subclinical disease, too, is somewhat controversial as many healthy joints can demonstrate physiologic fluid, and it is unknown how long synovial thickening can remain after active inflammation has been treated. In my experience, sonographic evidence of synovial thickening/proliferation with a high degree of Doppler activity (more than a few areas of intermittent pixilations) should be considered an actively diseased joint and be incorporated in therapeutic decisions. This review aims to provide an evidence-based update on recent advances and insights into the healthy sonoanatomy of children and the use of ultrasound in the assessment and treatment of juvenile idiopathic arthritis disease manifestations.

Keywords

Pediatric rheumatology Juvenile idiopathic arthritis (JIA) Musculoskeletal Ultrasonography Power Doppler Imaging 

Notes

Compliance with Ethical Standards

Conflict of Interest

Edward Oberle declares that he has no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    McAlindon T, Kissin E, Nazarian L, Ranganath V, Prakash S, Taylor M, et al. American College of Rheumatology report on reasonable use of musculoskeletal ultrasonography in rheumatology clinical practice. Arthritis Care Res. 2012;64(11):1625–40. doi: 10.1002/acr.21836.CrossRefGoogle Scholar
  2. 2.
    Bruyn GA, Naredo E, Iagnocco A, Balint PV, Backhaus M, Gandjbakhch F, et al. The OMERACT ultrasound working group 10 years on: update at OMERACT 12. J Rheumatol. 2015;42(11):2172–6. doi: 10.3899/jrheum.141462.CrossRefPubMedGoogle Scholar
  3. 3.
    Naredo E, Wakefield RJ, Iagnocco A, Terslev L, Filippucci E, Gandjbakhch F, et al. The OMERACT ultrasound task force—status and perspectives. J Rheumatol. 2011;38(9):2063–7. doi: 10.3899/jrheum.110425.CrossRefPubMedGoogle Scholar
  4. 4.
    • Colebatch-Bourn AN, Edwards CJ, Collado P, D’Agostino MA, Hemke R, Jousse-Joulin S, et al. EULAR-PReS points to consider for the use of imaging in the diagnosis and management of juvenile idiopathic arthritis in clinical practice. Ann Rheum Dis. 2015;74(11):1946–57. doi: 10.1136/annrheumdis-2015-207892. Recent recommendations on use of imaging in JIA, highlighting the importance and benefits of ultrasonography.CrossRefPubMedGoogle Scholar
  5. 5.
    Magni-Manzoni S, Collado P, Jousse-Joulin S, Naredo E, D’Agostino MA, Muratore V, et al. Current state of musculoskeletal ultrasound in paediatric rheumatology: results of an international survey. Rheumatology (Oxford). 2014;53(3):491–6. doi: 10.1093/rheumatology/ket368.CrossRefGoogle Scholar
  6. 6.
    Lanni S, De Lucia O, Possemato N, Malattia C, Ravagnani V, Magni-Manzoni S. Musculoskeletal ultrasound in paediatric rheumatology: the Italian perspective. Clin Exp Rheumatol. 2016;34(5):957–8.PubMedGoogle Scholar
  7. 7.
    Hernández-Díaz V-R, Gutiérrez M, Roth J. Ultrasonography in pediatric rheumatology in Latin America. Expanding front Clin Rheum. 2016;35(4):1077–80.CrossRefGoogle Scholar
  8. 8.
    • Collado P, Vojinovic J, Nieto JC, Windschall D, Magni-Manzoni S, Bruyn GA, et al. Toward standardized musculoskeletal ultrasound in pediatric rheumatology: normal age-related ultrasound findings. Arthritis Care Res. 2016;68(3):348–56. doi: 10.1002/acr.22670.OMERACT workgroup reports on a systematic approach to an ultrasound assessment in children of different age groups and comments on observations made of vascularization of healthy pediatric joints.CrossRefGoogle Scholar
  9. 9.
    Windschall D, Trauzeddel R, Haller M, Krumrey-Langkammerer M, Nimtz-Talaska A, Berendes R, et al. Pediatric musculoskeletal ultrasound: age- and sex-related normal B-mode findings of the knee. Rheumatol Int. 2016;36(11):1569–77. doi: 10.1007/s00296-016-3528-x.CrossRefPubMedGoogle Scholar
  10. 10.
    Spannow AH, Pfeiffer-Jensen M, Andersen NT, Stenbog E, Herlin T. Inter -and intraobserver variation of ultrasonographic cartilage thickness assessments in small and large joints in healthy children. Pediatr Rheumatol. 2009;7:12. doi: 10.1186/1546-0096-7-12.CrossRefGoogle Scholar
  11. 11.
    Laurell L, Court-Payen M, Nielsen S, Zak M, Boesen M, Fasth A. Comparison of ultrasonography with Doppler and MRI for assessment of disease activity in juvenile idiopathic arthritis: a pilot study. Pediatr Rheumatol. 2012;10(1):23. doi: 10.1186/1546-0096-10-23.CrossRefGoogle Scholar
  12. 12.
    • Roth J, Jousse-Joulin S, Magni-Manzoni S, Rodriguez A, Tzaribachev N, Iagnocco A, et al. Definitions for the sonographic features of joints in healthy children. Arthritis Care Res. 2015;67(1):136–42. doi: 10.1002/acr.22410. In order to ultimately detect ultrasonographic abnormalities and therefore confirm disease states, there has been a need to first define the appearance of healthy joints in children. The OMERACT work group reports on their process and final definitions.CrossRefGoogle Scholar
  13. 13.
    Jousse-Joulin S, Cangemi C, Gerard S, Gestin S, Bressollette L, de Parscau L, et al. Normal sonoanatomy of the paediatric entheses including echostructure and vascularisation changes during growth. Eur Radiol. 2015;25(7):2143–52. doi: 10.1007/s00330-014-3586-y.CrossRefPubMedGoogle Scholar
  14. 14.
    •• Roth J, Ravagnani V, Backhaus M, Balint P, Bruns A, Bruyn GA et al. Preliminary definitions for the sonographic features of synovitis in children. Arthritis care & research. 2016. doi: 10.1002/acr.23130. First report on pediatrics-specific definitions for the sonographic appearance of synovitis—composed of definitions of synovial proliferation and fluid collection. Future definitions will be based on the work outlined in this manuscript.
  15. 15.
    Breton S, Jousse-Joulin S, Cangemi C, de Parscau L, Colin D, Bressolette L, et al. Comparison of clinical and ultrasonographic evaluations for peripheral synovitis in juvenile idiopathic arthritis. Semin Arthritis Rheum. 2011;41(2):272–8. doi: 10.1016/j.semarthrit.2010.12.005.CrossRefPubMedGoogle Scholar
  16. 16.
    Chauvin NA, Ho-Fung V, Jaramillo D, Edgar JC, Weiss PF. Ultrasound of the joints and entheses in healthy children. Pediatr Radiol. 2015;45(9):1344–54. doi: 10.1007/s00247-015-3313-0.CrossRefPubMedGoogle Scholar
  17. 17.
    Lin C, Diab M, Milojevic D. Grey-scale ultrasound findings of lower extremity entheses in healthy children. Pediatr Rheumatol. 2015;13:14. doi: 10.1186/s12969-015-0012-1.CrossRefGoogle Scholar
  18. 18.
    Collado P, Naredo E, Calvo C, Crespo M. Assessment of the joint recesses and tendon sheaths in healthy children by high-resolution B-mode and power Doppler sonography. Clin Exp Rheumatol. 2007;25(6):915–21.PubMedGoogle Scholar
  19. 19.
    Collado P, Jousse-Joulin S, Alcalde M, Naredo E, D’Agostino MA. Is ultrasound a validated imaging tool for the diagnosis and management of synovitis in juvenile idiopathic arthritis? A systematic literature review. Arthritis Care Res. 2012;64(7):1011–9. doi: 10.1002/acr.21644.Google Scholar
  20. 20.
    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(12):2485–7.PubMedGoogle Scholar
  21. 21.
    Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, et al. International league of associations for rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol. 2004;31(2):390–2.PubMedGoogle Scholar
  22. 22.
    Hendry GJ, Gardner-Medwin J, Steultjens MP, Woodburn J, Sturrock RD, Turner DE. Frequent discordance between clinical and musculoskeletal ultrasound examinations of foot disease in juvenile idiopathic arthritis. Arthritis Care Res. 2012;64(3):441–7. doi: 10.1002/acr.20655.CrossRefGoogle Scholar
  23. 23.
    Magni-Manzoni S, Epis O, Ravelli A, Klersy C, Veisconti C, Lanni S, et al. Comparison of clinical versus ultrasound-determined synovitis in juvenile idiopathic arthritis. Arthritis Rheum. 2009;61(11):1497–504. doi: 10.1002/art.24823.CrossRefPubMedGoogle Scholar
  24. 24.
    Haslam KE, McCann LJ, Wyatt S, Wakefield RJ. The detection of subclinical synovitis by ultrasound in oligoarticular juvenile idiopathic arthritis: a pilot study. Rheumatology (Oxford). 2010;49(1):123–7. doi: 10.1093/rheumatology/kep339.CrossRefGoogle Scholar
  25. 25.
    Karmazyn B, Bowyer SL, Schmidt KM, Ballinger SH, Buckwalter K, Beam TT, et al. US findings of metacarpophalangeal joints in children with idiopathic juvenile arthritis. Pediatr Radiol. 2007;37(5):475–82. doi: 10.1007/s00247-007-0438-9.CrossRefPubMedGoogle Scholar
  26. 26.
    Pascoli L, Wright S, McAllister C, Rooney M. Prospective evaluation of clinical and ultrasound findings in ankle disease in juvenile idiopathic arthritis: importance of ankle ultrasound. J Rheumatol. 2010;37(11):2409–14. doi: 10.3899/jrheum.091262.CrossRefPubMedGoogle Scholar
  27. 27.
    Lanni S, Bovis F, Ravelli A, Viola S, Magnaguagno F, Pistorio A, et al. Delineating the application of ultrasound in detecting synovial abnormalities of the subtalar joint in juvenile idiopathic arthritis. Arthritis Care Res. 2016;68(9):1346–53. doi: 10.1002/acr.22846.CrossRefGoogle Scholar
  28. 28.
    Rooney ME, McAllister C, Burns JF. Ankle disease in juvenile idiopathic arthritis: ultrasound findings in clinically swollen ankles. J Rheumatol. 2009;36(8):1725–9. doi: 10.3899/jrheum.080508.CrossRefPubMedGoogle Scholar
  29. 29.
    Janow GL, Panghaal V, Trinh A, Badger D, Levin TL, Ilowite NT. Detection of active disease in juvenile idiopathic arthritis: sensitivity and specificity of the physical examination vs ultrasound. J Rheumatol. 2011;38(12):2671–4. doi: 10.3899/jrheum.110360.CrossRefPubMedGoogle Scholar
  30. 30.
    Nieto-Gonzalez JC, Monteagudo I, Vargas-Henny L, Janta I, Naredo E, Carreno L. Impact of musculoskeletal ultrasound on clinical practice in paediatric rheumatology. Clin Exp Rheumatol. 2015;33(4):583–7.PubMedGoogle Scholar
  31. 31.
    Walther M, Harms H, Krenn V, Radke S, Faehndrich TP, Gohlke F. Correlation of power Doppler sonography with vascularity of the synovial tissue of the knee joint in patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum. 2001;44(2):331–8. doi: 10.1002/1529-0131(200102)44:2<331::AID-ANR50>3.0.CO;2-0.CrossRefPubMedGoogle Scholar
  32. 32.
    Swidrowska J, Smolewski P, Stanczyk J, Smolewska E. Serum angiogenesis markers and their correlation with ultrasound-detected synovitis in juvenile idiopathic arthritis. Int J Immunol Res. 2015;2015:741457. doi: 10.1155/2015/741457.Google Scholar
  33. 33.
    Ranjan S, Jahan A, Yadav TP, Sachdev N, Dewan V, Singh S. Evaluation of synovial inflammation in juvenile idiopathic arthritis by power color Doppler and spectral Doppler ultrasonography. Indian J Pediatr. 2014;81(1):29–35. doi: 10.1007/s12098-013-1085-9.CrossRefPubMedGoogle Scholar
  34. 34.
    Sparchez M, Fodor D, Miu N. The role of power Doppler ultrasonography in comparison with biological markers in the evaluation of disease activity in juvenile idiopathic arthritis. Med Ultrason. 2010;12(2):97–103.PubMedGoogle Scholar
  35. 35.
    Bugni Miotto e Silva V, de Freitas Tavares da Silva C, de Aguiar Vilela Mitraud S, Nely Vilar Furtado R, Esteves Hilario MO, Natour J et al. Do patients with juvenile idiopathic arthritis in remission exhibit active synovitis on joint ultrasound? Rheumatology international. 2014; 34(7):937–45. doi: 10.1007/s00296-013-2909-7
  36. 36.
    Collado P, Gamir ML, Lopez-Robledillo JC, Merino R, Modesto C, Monteagudo I. Detection of synovitis by ultrasonography in clinically inactive juvenile idiopathic arthritis on and off medication. Clin Exp Rheumatol. 2014;32(4):597–603.PubMedGoogle Scholar
  37. 37.
    Rebollo-Polo M, Koujok K, Weisser C, Jurencak R, Bruns A, Roth J. Ultrasound findings on patients with juvenile idiopathic arthritis in clinical remission. Arthritis Care Res. 2011;63(7):1013–9. doi: 10.1002/acr.20478.CrossRefGoogle Scholar
  38. 38.
    Scire CA, Montecucco C, Codullo V, Epis O, Todoerti M, Caporali R. Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse. Rheumatology (Oxford). 2009;48(9):1092–7. doi: 10.1093/rheumatology/kep171.CrossRefGoogle Scholar
  39. 39.
    •• Magni-Manzoni S, Scire CA, Ravelli A, Klersy C, Rossi S, Muratore V, et al. Ultrasound-detected synovial abnormalities are frequent in clinically inactive juvenile idiopathic arthritis, but do not predict a flare of synovitis. Ann Rheum Dis. 2013;72(2):223–8. doi: 10.1136/annrheumdis-2011-201264. Only prospective longitudinal study to date following long-term outcomes of subclinical synovitis in patients with clinical remission.CrossRefPubMedGoogle Scholar
  40. 40.
    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. 2014;66(5):741–8. doi: 10.1002/acr.22191.CrossRefGoogle Scholar
  41. 41.
    Jousse-Joulin S, Breton S, Cangemi C, Fenoll B, Bressolette L, de Parscau L, et al. Ultrasonography for detecting enthesitis in juvenile idiopathic arthritis. Arthritis Care Res. 2011;63(6):849–55. doi: 10.1002/acr.20444.CrossRefGoogle Scholar
  42. 42.
    Weiss PF, Chauvin NA, Klink AJ, Localio R, Feudtner C, Jaramillo D, et al. Detection of enthesitis in children with enthesitis-related arthritis: dolorimetry compared to ultrasonography. Arthritis Rheum. 2014;66(1):218–27. doi: 10.1002/art.38197.CrossRefGoogle Scholar
  43. 43.
    Shenoy S, Aggarwal A. Sonologic enthesitis in children with enthesitis-related arthritis. Clin Exp Rheumatol. 2016;34(1):143–7.PubMedGoogle Scholar
  44. 44.
    Spannow AH, Stenboeg E, Pfeiffer-Jensen M, Fiirgaard B, Haislund M, Ostergaard M, et al. Ultrasound and MRI measurements of joint cartilage in healthy children: a validation study. Ultraschall in der Medizin (Stuttgart, Germany : 1980). 2011;32 Suppl 1:S110–6. doi: 10.1055/s-0029-1245374.CrossRefGoogle Scholar
  45. 45.
    Spannow AH, Stenboeg E, Pfeiffer-Jensen M, Herlin T. Ultrasound measurement of joint cartilage thickness in large and small joints in healthy children: a clinical pilot study assessing observer variability. Pediatr Rheumatol. 2007;5:3. doi: 10.1186/1546-0096-5-3.CrossRefGoogle Scholar
  46. 46.
    Spannow AH, Pfeiffer-Jensen M, Andersen NT, Herlin T, Stenbog E. Ultrasonographic measurements of joint cartilage thickness in healthy children: age- and sex-related standard reference values. J Rheumatol. 2010;37(12):2595–601. doi: 10.3899/jrheum.100101.CrossRefPubMedGoogle Scholar
  47. 47.
    Pradsgaard DO, Spannow AH, Heuck C, Herlin T. Decreased cartilage thickness in juvenile idiopathic arthritis assessed by ultrasonography. J Rheumatol. 2013;40(9):1596–603. doi: 10.3899/jrheum.121077.CrossRefPubMedGoogle Scholar
  48. 48.
    Pradsgaard DO, Fiirgaard B, Spannow AH, Heuck C, Herlin T. Cartilage thickness of the knee joint in juvenile idiopathic arthritis: comparative assessment by ultrasonography and magnetic resonance imaging. J Rheumatol. 2015;42(3):534–40. doi: 10.3899/jrheum.140162.CrossRefPubMedGoogle Scholar
  49. 49.
    Panghaal V, Janow G, Trinh A, Ilowite N, Levin TL. Normal epiphyseal cartilage measurements in the knee in children: an alternative sonographic approach. J Ultrasound Med Off J Am Institute of Ultrasound in Med. 2012;31(1):49–53.Google Scholar
  50. 50.
    Wakefield RJ, Gibbon WW, Conaghan PG, O’Connor P, McGonagle D, Pease C, 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):2762–70. doi: 10.1002/1529-0131(200012)43:12<2762::AID-ANR16>3.0.CO;2-#.CrossRefPubMedGoogle Scholar
  51. 51.
    Malattia C, Damasio MB, Magnaguagno F, Pistorio A, Valle M, Martinoli C, et al. Magnetic resonance imaging, ultrasonography, and conventional radiography in the assessment of bone erosions in juvenile idiopathic arthritis. Arthritis Rheum. 2008;59(12):1764–72. doi: 10.1002/art.24313.CrossRefPubMedGoogle Scholar
  52. 52.
    Laurell L, Court-Payen M, Nielsen S, Zak M, Boesen M, Fasth A. Ultrasonography and color Doppler in juvenile idiopathic arthritis: diagnosis and follow-up of ultrasound-guided steroid injection in the ankle region. A descriptive interventional study. Pediatric Rheumatology. 2011;9(1):4. doi: 10.1186/1546-0096-9-4.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Laurell L, Court-Payen M, Nielsen S, Zak M, Fasth A. Ultrasonography and color Doppler in juvenile idiopathic arthritis: diagnosis and follow-up of ultrasound-guided steroid injection in the wrist region. A descriptive interventional study. Pediatric Rheumatology. 2012;10:11. doi: 10.1186/1546-0096-10-11.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    • Young CM, Shiels 2nd WE, Coley BD, Hogan MJ, Murakami JW, Jones K, et al. Ultrasound-guided corticosteroid injection therapy for juvenile idiopathic arthritis: 12-year care experience. Pediatr Radiol. 2012;42(12):1481–9. doi: 10.1007/s00247-012-2487-y. Report on the safety and efficacy of ultrasound-guided joint injections. Provides an age-weight-joint-based corticosteroid dose protocol.CrossRefPubMedGoogle Scholar
  55. 55.
    Parra DA, Chan M, Krishnamurthy G, Spiegel L, Amaral JG, Temple MJ, et al. Use and accuracy of US guidance for image-guided injections of the temporomandibular joints in children with arthritis. Pediatr Radiol. 2010;40(9):1498–504. doi: 10.1007/s00247-010-1581-2.CrossRefPubMedGoogle Scholar
  56. 56.
    Habibi S, Ellis J, Strike H, Ramanan AV. Safety and efficacy of US-guided CS injection into temporomandibular joints in children with active JIA. Rheumatology (Oxford). 2012;51(5):874–7. doi: 10.1093/rheumatology/ker441.CrossRefGoogle Scholar
  57. 57.
    Weiss PF, Arabshahi B, Johnson A, Bilaniuk LT, Zarnow D, Cahill AM, et al. High prevalence of temporomandibular joint arthritis at disease onset in children with juvenile idiopathic arthritis, as detected by magnetic resonance imaging but not by ultrasound. Arthritis Rheum. 2008;58(4):1189–96. doi: 10.1002/art.23401.CrossRefPubMedGoogle Scholar
  58. 58.
    Collado P, Naredo E, Calvo C, Gamir ML, Calvo I, Garcia ML, et al. Reduced joint assessment vs comprehensive assessment for ultrasound detection of synovitis in juvenile idiopathic arthritis. Rheumatology (Oxford). 2013;52(8):1477–84. doi: 10.1093/rheumatology/ket148.CrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Division of Pediatric Rheumatology, Nationwide Children’s HospitalThe Ohio State UniversityColumbusUSA

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