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CEUS – Einsatzmöglichkeiten am Bewegungsapparat

CEUS—application possibilities in the musculoskeletal system

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Zusammenfassung

Methodische Grundlagen

Der konstrastmittelverstärkte Ultraschall („contrast-enhanced ultrasound“, CEUS) ermöglicht die Visualisierung und Quantifizierung der Mikroperfusion der Skelettmuskulatur und anderer Gewebe in vivo und in Echtzeit. Er ist eine schnell verfügbare Untersuchungsmodalität, die sehr nebenwirkungsarm und für nahezu jeden Patienten geeignet ist.

Ziel

Ziel dieses Übersichtsbeitrags ist es, die vielfältigen und zunehmenden CEUS-Anwendungsoptionen am Bewegungsapparat vorzustellen.

Leistungsfähigkeit/Methodische Innovationen

Die Einsatzmöglichkeiten des CEUS am Bewegungsapparat reichen weit über die Darstellung der rein muskulären Mikroperfusion hinaus und erstrecken sich ebenfalls auf Anwendungen am Knochen und an Gelenken. Neben grundlegenden muskelphysiologischen Fragestellungen waren die eingeschränkte Mikrozirkulation bei Patienten mit peripherer arterieller Verschlusskrankheit oder Diabetes mellitus sowie die Diagnostik entzündlicher Myopathien Schwerpunkt verschiedener CEUS-Studien. Neuere Arbeiten fokussieren auf orthopädisch-unfallchirurgische Fragestellungen, wie die Differenzierung von infizierten und aseptischen Pseudarthrosen oder die Auswirkungen verschiedener Osteosynthesematerialien und Prothesen auf die muskuläre Mikroperfusion als Surrogatparameter für den klinischen Erfolg.

Empfehlung für Praxis

Die Anwendung des CEUS bei muskuloskeletalen Fragestellungen erfolgt im Rahmen klinischer Studien oder „off-label“ und ist dementsprechend im klinischen Alltag bisher kaum etabliert. In Anbetracht der zunehmenden Anwendungsgebiete könnte sich dies künftig ändern.

Abstract

Methodical issue

Contrast-enhanced ultrasound (CEUS) offers easily accessible visualization and quantification of the skeletal muscle microcirculation and other tissues in vivo and in real-time with almost no side effects.

Aim

The aim of this review is to present the increasing number of musculoskeletal CEUS applications.

Methodical innovations/performance

CEUS applications regarding the musculoskeletal system include applications at bone and joints extending beyond the visualization of only the muscular microcirculation. Besides basic muscle physiology, impaired microcirculation in patients with peripheral artery disease or diabetes mellitus and the diagnosis of inflammatory myopathies have been the subject of previous CEUS studies. More recent studies in orthopedics and traumatology have focused on osseous and muscular perfusion characteristics, e. g., in differentiating infected and aseptic non-unions or the impact of different types of implants and prostheses on muscular microcirculation as a surrogate marker of clinical success.

Practical recommendations

CEUS of the musculoskeletal system is used in clinical trials or off-label. Therefore, it is not well established in clinical routine. However, considering the increasing number of musculoskeletal CEUS applications, this could change in the future.

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Literatur

  1. Aboyans V, Criqui MH, Denenberg JO et al (2006) Risk factors for progression of peripheral arterial disease in large and small vessels. Circulation 113:2623–2629

    Article  PubMed  Google Scholar 

  2. Aboyans V, Ricco JB, Bartelink MEL et al (2017) 2017 ESC Guidelines on the diagnosis and treatment of peripheral arterial diseases, in collaboration with the European Society for Vascular Surgery (ESVS): document covering atherosclerotic disease of extracranial carotid and vertebral, mesenteric, renal, upper and lower extremity arteries. Endorsed by: the European Stroke Organization (ESO), the Task Force for the Diagnosis and Treatment of Peripheral Arterial Diseases of the European Society of Cardiology (ESC) and of the European Society for Vascular Surgery (ESVS). Eur Heart J. https://doi.org/10.1093/eurheartj/ehx095

    Article  PubMed  Google Scholar 

  3. Adler RS, Johnson KM, Fealy S et al (2011) Contrast-enhanced sonographic characterization of the vascularity of the repaired rotator cuff: utility of maximum intensity projection imaging. J Ultrasound Med 30:1103–1109

    Article  PubMed  Google Scholar 

  4. Amarteifio E, Krix M, Wormsbecher S et al (2013) Dynamic contrast-enhanced ultrasound for assessment of therapy effects on skeletal muscle microcirculation in peripheral arterial disease: pilot study. Eur J Radiol 82:640–646

    Article  PubMed  CAS  Google Scholar 

  5. Amarteifio E, Nagel AM, Kauczor HU et al (2011) Functional imaging in muscular diseases. Insights Imaging 2:609–619

    Article  PubMed  PubMed Central  Google Scholar 

  6. Amarteifio E, Weber MA, Wormsbecher S et al (2011) Dynamic contrast-enhanced ultrasound for assessment of skeletal muscle microcirculation in peripheral arterial disease. Invest Radiol 46:504–508

    Article  PubMed  Google Scholar 

  7. Amarteifio E, Wormsbecher S, Demirel S et al (2013) Assessment of skeletal muscle microcirculation in type 2 diabetes mellitus using dynamic contrast-enhanced ultrasound: a pilot study. Diab Vasc Dis Res 10:468–470

    Article  PubMed  Google Scholar 

  8. Amarteifio E, Wormsbecher S, Krix M et al (2012) Dynamic contrast-enhanced ultrasound and transient arterial occlusion for quantification of arterial perfusion reserve in peripheral arterial disease. Eur J Radiol 81:3332–3338

    Article  PubMed  CAS  Google Scholar 

  9. Angst F, Schwyzer HK, Aeschlimann A et al (2011) Measures of adult shoulder function: Disabilities of the Arm, Shoulder, and Hand Questionnaire (DASH) and its short version (QuickDASH), Shoulder Pain And Disability Index (SPADI), American Shoulder and Elbow Surgeons (ASES) Society standardized shoulder assessment form, Constant (Murley) Score (CS), Simple Shoulder Test (SST), Oxford Shoulder Score (OSS), Shoulder Disability Questionnaire (SDQ), and Western Ontario Shoulder Instability Index (WOSI). Arthritis Care Res (Hoboken) 63(Suppl 11):S174–S188

    Article  Google Scholar 

  10. Arditi M, Frinking PJ, Zhou X et al (2006) A new formalism for the quantification of tissue perfusion by the destruction-replenishment method in contrast ultrasound imaging. IEEE Trans Ultrason Ferroelectr Freq Control 53:1118–1129

    Article  PubMed  Google Scholar 

  11. Broholm R, Pingel J, Simonsen L et al (2017) Applicability of contrast-enhanced ultrasound in the diagnosis of plantar fasciitis. Scand J Med Sci Sports 27:2048–2058

    Article  PubMed  CAS  Google Scholar 

  12. Cadet ER, Adler RS, Gallo RA et al (2012) Contrast-enhanced ultrasound characterization of the vascularity of the repaired rotator cuff tendon: short-term and intermediate-term follow-up. J Shoulder Elbow Surg 21:597–603

    Article  PubMed  Google Scholar 

  13. Calori GM, Phillips M, Jeetle S et al (2008) Classification of non-union: need for a new scoring system? Injury 39(Suppl 2):S59–S63

    Article  PubMed  Google Scholar 

  14. Chang KV, Lew HL, Wang TG et al (2012) Use of contrast-enhanced ultrasonography in musculoskeletal medicine. Am J Phys Med Rehabil 91:449–457

    Article  PubMed  Google Scholar 

  15. Clerk LH, Vincent MA, Jahn LA et al (2006) Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 55:1436–1442

    Article  PubMed  CAS  Google Scholar 

  16. Cosgrove D, Lassau N (2010) Imaging of perfusion using ultrasound. Eur J Nucl Med Mol Imaging 37(Suppl 1):S65–S85

    Article  PubMed  Google Scholar 

  17. Delorme S, Krix M, Albrecht T (2006) Ultrasound contrast media—principles and clinical applications. Rofo 178:155–164

    Article  PubMed  CAS  Google Scholar 

  18. Duerschmied D, Maletzki P, Freund G et al (2010) Success of arterial revascularization determined by contrast ultrasound muscle perfusion imaging. J Vasc Surg 52:1531–1536

    Article  PubMed  Google Scholar 

  19. Duerschmied D, Olson L, Olschewski M et al (2006) Contrast ultrasound perfusion imaging of lower extremities in peripheral arterial disease: a novel diagnostic method. Eur Heart J 27:310–315

    Article  PubMed  Google Scholar 

  20. Duerschmied D, Zhou Q, Rink E et al (2009) Simplified contrast ultrasound accurately reveals muscle perfusion deficits and reflects collateralization in PAD. Atherosclerosis 202:505–512

    Article  PubMed  CAS  Google Scholar 

  21. Fischer C, Frank M, Kunz P et al (2016) Dynamic contrast-enhanced ultrasound (CEUS) after open and minimally invasive locked plating of proximal humerus fractures. Injury 47:1725–1731

    Article  PubMed  Google Scholar 

  22. Fischer C, Krammer D, Hug A et al (2017) Dynamic contrast-enhanced ultrasound and elastography assess deltoid muscle integrity after reverse shoulder arthroplasty. J Shoulder Elbow Surg 26:108–117

    Article  PubMed  Google Scholar 

  23. Fischer C, Preuss EM, Tanner M et al (2016) Dynamic contrast-enhanced sonography and dynamic contrast-enhanced magnetic resonance imaging for preoperative diagnosis of infected nonunions. J Ultrasound Med 35:933–942

    Article  PubMed  Google Scholar 

  24. Gamradt SC, Gallo RA, Adler RS et al (2010) Vascularity of the supraspinatus tendon three months after repair: characterization using contrast-enhanced ultrasound. J Shoulder Elbow Surg 19:73–80

    Article  PubMed  Google Scholar 

  25. Genovese EA, Callegari L, Combi F et al (2007) Contrast enhanced ultrasound with second generation contrast agent for the follow-up of lower-extremity muscle-strain-repairing processes in professional athletes. Radiol Med 112:740–750

    Article  PubMed  CAS  Google Scholar 

  26. Harjacek M (2012) Non-invasive imaging of chronic inflammatory myopathies. Reumatizam 59:39–43

    PubMed  Google Scholar 

  27. Harvey CJ, Sidhu PS, Bachmann Nielsen M (2013) Contrast-enhanced ultrasound in renal transplants: applications and future directions. Ultraschall Med 34:319–321

    Article  PubMed  CAS  Google Scholar 

  28. Hildebrandt W, Schwarzbach H, Pardun A et al (2017) Age-related differences in skeletal muscle microvascular response to exercise as detected by contrast-enhanced ultrasound (CEUS). PLoS ONE 12:e172771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Hotfiel T, Carl HD, Swoboda B et al (2016) Contrast-enhanced ultrasound in diagnostic imaging of muscle injuries: perfusion imaging in the early arterial phase. Sportverletz Sportschaden 30:54–57

    PubMed  CAS  Google Scholar 

  30. Hou XX, Chu GH, Yu Y (2017) Prospects of contrast-enhanced ultrasonography for the diagnosis of peripheral arterial disease: a meta-analysis. J Ultrasound Med. https://doi.org/10.1002/jum.14451

    Article  PubMed  Google Scholar 

  31. Hudson JM, Karshafian R, Burns PN (2009) Quantification of flow using ultrasound and microbubbles: a disruption replenishment model based on physical principles. Ultrasound Med Biol 35:2007–2020

    Article  PubMed  Google Scholar 

  32. Klauser A, Demharter J, De Marchi A et al (2005) Contrast enhanced gray-scale sonography in assessment of joint vascularity in rheumatoid arthritis: results from the IACUS study group. Eur Radiol 15:2404–2410

    Article  PubMed  Google Scholar 

  33. Klauser A, Halpern EJ, Frauscher F et al (2005) Inflammatory low back pain: high negative predictive value of contrast-enhanced color Doppler ultrasound in the detection of inflamed sacroiliac joints. Arthritis Rheum 53:440–444

    Article  PubMed  Google Scholar 

  34. Klauser AS, Franz M, Arora R et al (2010) Detection of vascularity in wrist tenosynovitis: power doppler ultrasound compared with contrast-enhanced grey-scale ultrasound. Arthritis Res Ther 12:R209

    Article  PubMed  PubMed Central  Google Scholar 

  35. Krix M, Kauczor HU, Delorme S (2003) Quantification of tissue perfusion with novel ultrasound methods. Radiologe 43:823–830

    Article  PubMed  CAS  Google Scholar 

  36. Krix M, Kiessling F, Farhan N et al (2003) A multivessel model describing replenishment kinetics of ultrasound contrast agent for quantification of tissue perfusion. Ultrasound Med Biol 29:1421–1430

    Article  PubMed  Google Scholar 

  37. Krix M, Kiessling F, Vosseler S et al (2003) Comparison of intermittent-bolus contrast imaging with conventional power Doppler sonography: quantification of tumour perfusion in small animals. Ultrasound Med Biol 29:1093–1103

    Article  PubMed  Google Scholar 

  38. Krix M, Krakowski-Roosen H, Amarteifio E et al (2011) Comparison of transient arterial occlusion and muscle exercise provocation for assessment of perfusion reserve in skeletal muscle with real-time contrast-enhanced ultrasound. Eur J Radiol 78:419–424

    Article  PubMed  Google Scholar 

  39. Krix M, Krakowski-Roosen H, Kauczor HU et al (2009) Real-time contrast-enhanced ultrasound for the assessment of perfusion dynamics in skeletal muscle. Ultrasound Med Biol 35:1587–1595

    Article  PubMed  Google Scholar 

  40. Krix M, Plathow C, Kiessling F et al (2004) Quantification of perfusion of liver tissue and metastases using a multivessel model for replenishment kinetics of ultrasound contrast agents. Ultrasound Med Biol 30:1355–1363

    Article  PubMed  Google Scholar 

  41. Krix M, Weber MA, Kauczor HU et al (2010) Changes in the micro-circulation of skeletal muscle due to varied isometric exercise assessed by contrast-enhanced ultrasound. Eur J Radiol 76:110–116

    Article  PubMed  Google Scholar 

  42. Krix M, Weber MA, Krakowski-Roosen H et al (2005) Assessment of skeletal muscle perfusion using contrast-enhanced ultrasonography. J Ultrasound Med 24:431–441

    Article  PubMed  Google Scholar 

  43. Kundi R, Prior SJ, Addison O et al (2017) Contrast-enhanced ultrasound reveals exercise-induced perfusion deficits in claudicants. Eur J Vasc Endovasc Surg. https://doi.org/10.21767/2573-4482.100041

    Article  Google Scholar 

  44. Mancini M, Di Donato O, Saldalamacchia G et al (2013) Contrast-enhanced ultrasound evaluation of peripheral microcirculation in diabetic patients: effects of cigarette smoking. Radiol Med 118:206–214

    Article  PubMed  CAS  Google Scholar 

  45. Mitchell WK, Phillips BE, Williams JP et al (2013) Development of a new Sonovue contrast-enhanced ultrasound approach reveals temporal and age-related features of muscle microvascular responses to feeding. Physiol Rep 1:e119

    Article  PubMed  PubMed Central  Google Scholar 

  46. Ohrndorf S, Hensch A, Naumann L et al (2011) Contrast-enhanced ultrasonography is more sensitive than grayscale and power Doppler ultrasonography compared to MRI in therapy monitoring of rheumatoid arthritis patients. Ultraschall Med 32(Suppl 2):E38–E44

    Article  PubMed  Google Scholar 

  47. Peetrons P (2002) Ultrasound of muscles. Eur Radiol 12:35–43

    Article  PubMed  CAS  Google Scholar 

  48. Pingel J, Harrison A, Simonsen L et al (2013) The microvascular volume of the Achilles tendon is increased in patients with tendinopathy at rest and after a 1-hour treadmill run. Am J Sports Med 41:2400–2408

    Article  PubMed  Google Scholar 

  49. Pingel J, Harrison A, Suetta C et al (2013) The acute effects of exercise on the microvascular volume of Achilles tendons in healthy young subjects. Clin Physiol Funct Imaging 33:252–257

    Article  PubMed  Google Scholar 

  50. Piscaglia F, Bolondi L, Italian Society for Ultrasound In M et al (2006) The safety of Sonovue in abdominal applications: retrospective analysis of 23188 investigations. Ultrasound Med Biol 32:1369–1375

    Article  PubMed  Google Scholar 

  51. Piscaglia F, Nolsoe C, Dietrich CF et al (2012) The EFSUMB guidelines and recommendations on the clinical practice of Contrast Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med 33:33–59

    Article  PubMed  CAS  Google Scholar 

  52. Ray CA, Dudley GA (1998) Muscle use during dynamic knee extension: implication for perfusion and metabolism. J Appl Physiol 85:1194–1197

    Article  PubMed  CAS  Google Scholar 

  53. Rees JD, Pilcher J, Heron C et al (2007) A comparison of clinical vs ultrasound determined synovitis in rheumatoid arthritis utilizing gray-scale, power Doppler and the intravenous microbubble contrast agent ‘Sono-Vue’. Rheumatology (Oxford) 46:454–459

    Article  CAS  Google Scholar 

  54. Salaffi F, Carotti M, Manganelli P et al (2004) Contrast-enhanced power Doppler sonography of knee synovitis in rheumatoid arthritis: assessment of therapeutic response. Clin Rheumatol 23:285–290

    Article  PubMed  CAS  Google Scholar 

  55. Schueller-Weidekamm C, Krestan C, Schueller G et al (2007) Power Doppler sonography and pulse-inversion harmonic imaging in evaluation of rheumatoid arthritis synovitis. AJR Am J Roentgenol 188:504–508

    Article  PubMed  Google Scholar 

  56. Slaaf DW, Oude Egbrink MG (2002) Capillaries and flow redistribution play an important role in muscle blood flow reserve capacity. J Mal Vasc 27:63–67

    PubMed  CAS  Google Scholar 

  57. Solivetti FM, Elia F, Teoli M et al (2010) Role of contrast-enhanced ultrasound in early diagnosis of psoriatic arthritis. Dermatology (Basel) 220:25–31

    Article  CAS  Google Scholar 

  58. Song IH, Burmester GR, Backhaus M et al (2008) Knee osteoarthritis. Efficacy of a new method of contrast-enhanced musculoskeletal ultrasonography in detection of synovitis in patients with knee osteoarthritis in comparison with magnetic resonance imaging. Ann Rheum Dis 67:19–25

    Article  PubMed  CAS  Google Scholar 

  59. Song Y, Li Y, Wang PJ et al (2014) Contrast-enhanced ultrasonography of skeletal muscles for type 2 diabetes mellitus patients with microvascular complications. Int J Clin Exp Med 7:573–579

    PubMed  PubMed Central  CAS  Google Scholar 

  60. Szkudlarek M, Court-Payen M, Strandberg C et al (2003) Contrast-enhanced power Doppler ultrasonography of the metacarpophalangeal joints in rheumatoid arthritis. Eur Radiol 13:163–168

    PubMed  Google Scholar 

  61. Thomas KN, Cotter JD, Lucas SJ et al (2015) Reliability of contrast-enhanced ultrasound for the assessment of muscle perfusion in health and peripheral arterial disease. Ultrasound Med Biol 41:26–34

    Article  PubMed  Google Scholar 

  62. Timmerman KL, Lee JL, Dreyer HC et al (2010) Insulin stimulates human skeletal muscle protein synthesis via an indirect mechanism involving endothelial-dependent vasodilation and mammalian target of rapamycin complex 1 signaling. J Clin Endocrinol Metab 95:3848–3857

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Van Holsbeeck MT, Introcaso JH (2016) Musculoskeletal ultrasound. Jaypee, New Delhi

    Book  Google Scholar 

  64. Walker UA (2008) Imaging tools for the clinical assessment of idiopathic inflammatory myositis. Curr Opin Rheumatol 20:656–661

    Article  PubMed  Google Scholar 

  65. Weber MA, Hildebrandt W, Schroder L et al (2010) Concentric resistance training increases muscle strength without affecting microcirculation. Eur J Radiol 73:614–621

    Article  PubMed  Google Scholar 

  66. Weber MA, Jappe U, Essig M et al (2006) Contrast-enhanced ultrasound in dermatomyositis- and polymyositis. J Neurol 253:1625–1632

    Article  PubMed  Google Scholar 

  67. Weber MA, Krakowski-Roosen H, Delorme S et al (2006) Relationship of skeletal muscle perfusion measured by contrast-enhanced ultrasonography to histologic microvascular density. J Ultrasound Med 25:583–591

    Article  PubMed  Google Scholar 

  68. Weber MA, Krakowski-Roosen H, Hildebrandt W et al (2007) Assessment of metabolism and microcirculation of healthy skeletal muscles by magnetic resonance and ultrasound techniques. J Neuroimaging 17:323–331

    Article  PubMed  Google Scholar 

  69. Weber MA, Krakowski-Roosen H, Schroder L et al (2009) Morphology, metabolism, microcirculation, and strength of skeletal muscles in cancer-related cachexia. Acta Oncol 48:116–124

    Article  PubMed  Google Scholar 

  70. Weber MA, Krix M, Jappe U et al (2006) Pathologic skeletal muscle perfusion in patients with myositis: detection with quantitative contrast-enhanced US—initial results. Radiology 238:640–649

    Article  PubMed  Google Scholar 

  71. Weber MA, Wormsbecher S, Krix M (2011) Contrast-enhanced ultrasound of skeletal muscle. Radiologe 51:497–505

    Article  PubMed  Google Scholar 

  72. Wei K, Jayaweera AR, Firoozan S et al (1998) Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97:473–483

    Article  PubMed  CAS  Google Scholar 

  73. Womack L, Peters D, Barrett EJ et al (2009) Abnormal skeletal muscle capillary recruitment during exercise in patients with type 2 diabetes mellitus and microvascular complications. J Am Coll Cardiol 53:2175–2183

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Institut für Diagnostische und Interventionelle Radiologie, Universitätsmedizin Rostock, Ernst-Heydemann-Str. 6, 18057, Rostock, Deutschland

    M. Jäschke &  M.-A. Weber

  2. Zentrum für Orthopädie, Unfallchirurgie und Paraplegiologie, Universitätsklinikum Heidelberg, HTRG – Heidelberg Trauma Research Group, Heidelberg, Deutschland

    C. Fischer

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  1. M. Jäschke
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  3. C. Fischer
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Correspondence to M. Jäschke.

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Interessenkonflikt

Projekte zum CEUS von M.-A. Weber und C. Fischer wurden zum Teil finanziell durch Forschungsförderungsprogramme von Bracco sowie der DEGUM unterstützt. M. Jäschke gibt an, dass kein Interessenkonflikt besteht.

Für diesen Beitrag wurden von den Autoren keine Studien an Menschen oder Tieren durchgeführt. Für die im Beitrag zitierten Studien gelten die jeweils dort angegebenen ethischen Richtlinien.

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Jäschke, M., Weber, MA. & Fischer, C. CEUS – Einsatzmöglichkeiten am Bewegungsapparat. Radiologe 58, 579–589 (2018). https://doi.org/10.1007/s00117-018-0404-6

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