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Quantitative evaluation of muscle perfusion with CEUS and with MR

  • Musculoskeletal
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Abstract

Functional imaging might increase the role of imaging in muscular diseases, since alterations of muscle morphology alone are not specific for a particular disease. Perfusion, i.e., the blood flow per tissue and time unit including capillary flow, is an important functional parameter. Pathological changes of skeletal muscle perfusion can be found in various clinical conditions, such as degenerative or inflammatory myopathies or peripheral arterial occlusive disease. This article reviews the theoretical basics of functional radiological techniques for assessing skeletal muscle perfusion and focuses on contrast-enhanced ultrasound (CEUS) and magnetic resonance imaging (MRI) techniques. Also, the applications of microvascular imaging, such as in detection of myositis and for discriminating myositis from other myopathies or evaluating peripheral arterial occlusive disease, are presented, and possible clinical indications are discussed. In conclusion, dedicated MR and CEUS methods are now available that visualize and quantify (patho-)physiologic information about microcirculation within skeletal muscles in vivo and hence establish a useful diagnostic tool for muscular diseases.

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References

  1. Lovitt S, Marden FA, Gundogdu B, Ostrowski ML (2004) MRI in myopathy. Neurol Clin 22:509–538

    Article  PubMed  Google Scholar 

  2. Scott DL, Kingsley GH (2004) Use of imaging to assess patients with muscle disease. Curr Opin Rheumatol 16:678–683

    Article  PubMed  Google Scholar 

  3. 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 

  4. Joyner MJ, Dietz NM, Shepherd JT (2001) From Belfast to Mayo and beyond: the use and future of plethysmography to study blood flow in human limbs. J Appl Physiol 91:2431–2441

    PubMed  CAS  Google Scholar 

  5. Krix M, Weber MA, Krakowski-Roosen H, Huttner HB, Delorme S, Kauczor HU, Hildebrandt W (2005) Assessment of skeletal muscle perfusion using contrast-enhanced ultrasonography. J Ultrasound Med 24:431–441

    PubMed  Google Scholar 

  6. Nuutila P, Kalliokoski K (2000) Use of positron emission tomography in the assessment of skeletal muscle and tendon metabolism and perfusion. Scand J Med Sci Sports 10:346–350

    Article  PubMed  CAS  Google Scholar 

  7. Forster BB (2006) Is functional MR imaging of skeletal muscle the ultimate tool for assessment of peripheral arterial occlusive disease? Radiology 241:329–330

    Article  PubMed  Google Scholar 

  8. Ament W, Lubbers J, Rakhorst G, Vaalburg W, Verkerke GJ, Paans AM, Willemsen AT (1998) Skeletal muscle perfusion measured by positron emission tomography during exercise. Pflugers Arch 436:653–658

    Article  PubMed  CAS  Google Scholar 

  9. Duet M, Virally M, Bailliart O, Kevorkian JP, Kedra AW, Benelhadj S, Ajzenberg C, Le Dref O, Guillausseau PJ (2001) Whole-body (201)Tl scintigraphy can detect exercise lower limb perfusion abnormalities in asymptomatic diabetic patients with normal Doppler pressure indices. Nucl Med Commun 22:949–954

    Article  PubMed  CAS  Google Scholar 

  10. Ludman PF, Volterrani M, Clark AL, Poole-Wilson PA, Rees S, Coats AJ (1993) Skeletal muscle blood flow in heart failure measured by ultrafast computed tomography: validation by comparison with plethysmography. Cardiovasc Res 27:1109–1115

    PubMed  CAS  Google Scholar 

  11. Goh V, Halligan S, Hugill JA, Bartram CI (2006) Quantitative assessment of tissue perfusion using MDCT: comparison of colorectal cancer and skeletal muscle measurement reproducibility. AJR Am J Roentgenol 187:164–169

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  13. Delorme S, Krix M, Albrecht T (2006) Ultrasound contrast media-Principles and clinical applications. Fortschr Röntgenstr 178:155–164

    Article  CAS  Google Scholar 

  14. Krix M, Kiessling F, Farhan N, Schmidt K, Hoffend J, Delorme S (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 

  15. Delorme S, Krix M (2006) Contrast-enhanced ultrasound for examining tumor biology. Cancer Imaging 6:148–152

    Article  PubMed  Google Scholar 

  16. Calliada F, Campani R, Bottinelli O, Bozzini A, Sommaruga MG (1998) Ultrasound contrast agents: basic principles. Eur J Radiol 27(Suppl 2):S157–S160

    Article  PubMed  Google Scholar 

  17. Wei K, Jayaweera AR, Firoozan S, Linka A, Skyba DM, Kaul S (1998) Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97:473–483

    PubMed  CAS  Google Scholar 

  18. Porter TR, Xie F (1995) Transient myocardial contrast after initial exposure to diagnostic ultrasound pressures with minute doses of intravenously injected microbubbles. Demonstration and potential mechanisms. Circulation 92:2391–2395

    PubMed  CAS  Google Scholar 

  19. Lencioni R, Cioni D, Bartolozzi C (2002) Tissue harmonic and contrast-specific imaging: back to gray scale in ultrasound. Eur Radiol 12:151–165

    Article  PubMed  Google Scholar 

  20. Bruce M, Averkiou M, Tiemann K, Lohmaier S, Powers J, Beach K (2004) Vascular flow and perfusion imaging with ultrasound contrast agents. Ultrasound Med Biol 30:735–743

    Article  PubMed  Google Scholar 

  21. Leppek R, Hoos O, Sattler A, Kohle S, Azzam S, Al Haffar I, Keil B, Ricken P, Klose KJ, Alfke H (2004) MR-Imaging of lower leg muscle perfusion. Herz 29:32–46

    Article  PubMed  Google Scholar 

  22. Lutz AM, Weishaupt D, Amann-Vesti BR, Pfammatter T, Goepfert K, Marincek B, Nanz D (2004) Assessment of skeletal muscle perfusion by contrast medium first-pass magnetic resonance imaging: technical feasibility and preliminary experience in healthy volunteers. J Magn Reson Imaging 20:111–121

    Article  PubMed  Google Scholar 

  23. Nygren AT, Greitz D, Kaijser L (2000) Skeletal muscle perfusion during exercise using Gd-DTPA bolus detection. J Cardiovasc Magn Reson 2:263–270

    PubMed  CAS  Google Scholar 

  24. Garcia J (2000) MRI in inflammatory myopathies. Skeletal Radiol 29:425–438

    Article  PubMed  CAS  Google Scholar 

  25. Reimers CD, Finkenstaedt M (1997) Muscle imaging in inflammatory myopathies. Curr Opin Rheumatol 9:475–485

    Article  PubMed  CAS  Google Scholar 

  26. Dion E, Cherin P, Payan C, Fournet JC, Papo T, Maisonobe T, Auberton E, Chosidow O, Godeau P, Piette JC, Herson S, Grenier P (2002) Magnetic resonance imaging criteria for distinguishing between inclusion body myositis and polymyositis. J Rheumatol 29:1897–1906

    PubMed  Google Scholar 

  27. Olsen NJ, Qi J, Park JH (2005) Imaging and skeletal muscle disease. Curr Rheumatol Rep 7:106–114

    Article  PubMed  Google Scholar 

  28. Mercuri E, Jungbluth H, Muntoni F (2005) Muscle imaging in clinical practice: diagnostic value of muscle magnetic resonance imaging in inherited neuromuscular disorders. Curr Opin Neurol 18:526–537

    Article  PubMed  Google Scholar 

  29. Weber MA, Krix M, Jappe U, Huttner HB, Hartmann M, Meyding-Lamade U, Essig M, Fiehn C, Kauczor HU, Delorme S (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 

  30. Sam AD 2nd, Morasch MD, Collins J, Song G, Chen R, Pereles FS (2003) Safety of gadolinium contrast angiography in patients with chronic renal insufficiency. J Vasc Surg 38:313–318

    Article  PubMed  Google Scholar 

  31. Akgun H, Gonlusen G, Cartwright J Jr, Suki WN, Truong LD (2006) Are gadolinium-based contrast media nephrotoxic? A renal biopsy study. Arch Pathol Lab Med 130:1354–1357

    PubMed  Google Scholar 

  32. Raynaud JS, Duteil S, Vaughan JT, Hennel F, Wary C, Leroy-Willig A, Carlier PG (2001) Determination of skeletal muscle perfusion using arterial spin labeling NMRI: validation by comparison with venous occlusion plethysmography. Magn Reson Med 46:305–311

    Article  PubMed  CAS  Google Scholar 

  33. Wong EC, Buxton RB, Frank LR (1998) A theoretical and experimental comparison of continuous and pulsed arterial spin labeling techniques for quantitative perfusion imaging. Magn Reson Med 40:348–355

    Article  PubMed  CAS  Google Scholar 

  34. Frank LR, Wong EC, Haseler LJ, Buxton RB (1999) Dynamic imaging of perfusion in human skeletal muscle during exercise with arterial spin labelling. Magn Reson Med 42:258–267

    Article  PubMed  CAS  Google Scholar 

  35. Boss A, Martirosian P, Claussen CD, Schick F (2006) Quantitative ASL muscle perfusion imaging using a FAIR-TrueFISP technique at 3.0 T. NMR Biomed 19:125–132

    Article  PubMed  Google Scholar 

  36. Toussaint JF, Kwong KK, Mkparu FO, Weisskoff RM, LaRaia PJ, Kantor HL (1996) Perfusion changes in human skeletal muscle during reactive hyperemia measured by echo-planar imaging. Magn Reson Med 35:62–69

    Article  PubMed  CAS  Google Scholar 

  37. Donahue KM, Van Kylen J, Guven S, El-Bershawi A, Luh WM, Bandettini PA, Cox RW, Hyde JS, Kissebah AH (1998) Simultaneous gradient-echo/spin-echo EPI of graded ischemia in human skeletal muscle. J Magn Reson Imaging 8:1106–1113

    Article  PubMed  CAS  Google Scholar 

  38. Lebon V, Carlier PG, Brillault-Salvat C, Leroy-Willig A (1998) Simultaneous measurement of perfusion and oxygenation changes using a multiple gradient-echo sequence: application to human muscle study. Magn Reson Imaging 16:721–729

    Article  PubMed  CAS  Google Scholar 

  39. Meyer RA, Towse TF, Reid RW, Jayaraman RC, Wiseman RW, McCully KK (2004) BOLD MRI mapping of transient hyperemia in skeletal muscle after single contractions. NMR Biomed 17:392–398

    Article  PubMed  Google Scholar 

  40. Ledermann HP, Heidecker HG, Schulte AC, Thalhammer C, Aschwanden M, Jaeger KA, Scheffler K, Bilecen D (2006) Calf muscles imaged at BOLD MR: correlation with TcPO2 and flowmetry measurements during ischemia and reactive hyperemia-initial experience. Radiology 241:477–484

    Article  PubMed  Google Scholar 

  41. Noseworthy MD, Bulte DP, Alfonsi J (2003) BOLD magnetic resonance imaging of skeletal muscle. Semin Musculoskelet Radiol 7:307–315

    Article  PubMed  Google Scholar 

  42. Ledermann HP, Schulte AC, Heidecker HG, Aschwanden M, Jager KA, Scheffler K, Steinbrich W, Bilecen D (2006) Blood oxygenation level-dependent magnetic resonance imaging of the skeletal muscle in patients with peripheral arterial occlusive disease. Circulation 113:2929–2935

    Article  PubMed  Google Scholar 

  43. Leroy-Willig A (2005) BOLD indirect vs. ASL direct measurement of muscle perfusion. J Appl Physiol 99:376–377

    Article  PubMed  CAS  Google Scholar 

  44. Wigmore DM, Damon BM, Pober DM, Kent-Braun JA (2004) MRI measures of perfusion–related changes in human skeletal muscle during progressive contractions. J Appl Physiol 97:2385–2394

    Article  PubMed  CAS  Google Scholar 

  45. Dalakas MC, Hohlfeld R (2003) Polymyositis and dermatomyositis. Lancet 362:971–982

    Article  PubMed  CAS  Google Scholar 

  46. Mastaglia FL, Garlepp MJ, Phillips BA, Zilko PJ (2003) Inflammatory myopathies: clinical, diagnostic and therapeutic aspects. Muscle Nerve 27:407–425

    Article  PubMed  Google Scholar 

  47. Maillard SM, Jones R, Owens C, Pilkington C, Woo P, Wedderburn LR, Murray KJ (2004) Quantitative assessment of MRI T2 relaxation time of thigh muscles in juvenile dermatomyositis. Rheumatology 43:603–608

    Article  PubMed  CAS  Google Scholar 

  48. O’Connell MJ, Powell T, Brennan D, Lynch T, McCarthy CJ, Eustace SJ (2002) Whole-body MR imaging in the diagnosis of polymyositis. AJR Am J Roentgenol 179:967–971

    PubMed  Google Scholar 

  49. Park JH, Olsen NJ (2001) Utility of magnetic resonance imaging in the evaluation of patients with inflammatory myopathies. Curr Rheumatol Rep 3:334–345

    Article  PubMed  CAS  Google Scholar 

  50. Schweitzer ME, Fort J (1995) Cost-effectiveness of MR imaging in evaluating polymyositis. AJR Am J Roentgenol 165:1469–1471

    PubMed  CAS  Google Scholar 

  51. May DA, Disler DG, Jones EA, Balkissoon AA, Manaster BJ (2000) Abnormal signal intensity in skeletal muscle at MR imaging: patterns, pearls, and pitfalls. Radiographics 20:S295–S315, Spec No

    PubMed  Google Scholar 

  52. Weber MA, Jappe U, Essig M, Krix M, Ittrich C, Huttner HB, Meyding-Lamadé U, Hartmann M, Kauczor HU, Delorme S (2006) Contrast-enhanced ultrasound in dermatomyositis and polymyositis. J Neurol 253:1625–1632

    Article  PubMed  Google Scholar 

  53. Lane RJM, Emslie-Smith A, Mosquera IE, Hudgson P (1989) Clinical, biochemical and histological responses to treatment in polymyositis: a prospective study. J R Soc Med 82:333–338

    PubMed  CAS  Google Scholar 

  54. Bragadeesh T, Sari I, Pascotto M, Micari A, Kaul S, Lindner JR (2005) Detection of peripheral vascular stenosis by assessing skeletal muscle flow reserve. J Am Coll Cardiol 45:780–785

    Article  PubMed  Google Scholar 

  55. Duerschmied D, Olson L, Olschewski M, Rossknecht A, Freund G, Bode C, Hehrlein C (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 

  56. Nygren AT, Greitz D (2006) Delayed contrast agent kinetics in ischemic skeletal muscle. J Magn Reson Imaging 23:171–176

    Article  PubMed  Google Scholar 

  57. Weber MA, Krakowski-Roosen H, Delorme S, Renk H, Krix M, Millies J, Kinscherf R, Künkele A, Kauczor HU, Hildebrandt W (2006) Relationship of skeletal muscle perfusion measured by contrast-enhanced ultrasonography to histologic microvascular density. J Ultrasound Med 25:583–591

    PubMed  Google Scholar 

  58. Padhani AR, Hayes C, Landau S, Leach MO (2002) Reproducibility of quantitative dynamic MRI of normal human tissues. NMR Biomed 15:143–153

    Article  PubMed  Google Scholar 

  59. Andersen P, Saltin B (1985) Maximal perfusion of skeletal muscle in man. J Physiol 366:233–249

    PubMed  CAS  Google Scholar 

  60. Lin CC, Ding HJ, Chen YW, Huang WT, Kao A (2004) Usefulness of thallium-201 muscle perfusion scan to investigate perfusion reserve in the lower limbs of Type 2 diabetic patients. J Diabetes Complications 18:233–236

    Article  PubMed  Google Scholar 

  61. Banci M, Rinaldi E, Ierardi M, Tiberio NS, Boccabella GL, Barbieri C, Scopinaro F, Morelli S, DeSantis M (1998) 99mTc SESTAMIBI scintigraphic evaluation of skeletal muscle disease in patients with systemic sclerosis: diagnostic reliability and comparison with cardiac function and perfusion. Angiology 49:641–648

    Article  PubMed  CAS  Google Scholar 

  62. Hsu HB, Sun SS, Chen JJ, Tsai JJ, Kao CH, ChangLai SP (2004) Usefulness of thallium-201 muscle scan to investigate perfusion reserve in the lower limbs of patients with systemic lupus erythematusus. Rheumatol Int 24:291–293

    PubMed  CAS  Google Scholar 

  63. Mattila KT, Komu ME, Dahlström S, Koskinen SK, Heikkilä J (1999) Medial tibial pain: a dynamic contrast-enhanced MRI study. Magn Reson Imaging 17:947–954

    Article  PubMed  CAS  Google Scholar 

  64. Luh WM, Wong EC, Bandettini PA, Hyde JS (1999) QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn Reson Med 41:1246–1254

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

The authors thank Wolfgang Wiedemair, Department of Medical Physics in Radiology, German Cancer Research Centre, Heidelberg, Germany, for reviewing this manuscript and for the excellent cooperation concerning ASL MRI of skeletal muscles as well as providing the muscular ASL images.

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Authors and Affiliations

  1. Department of Radiology, German Cancer Research Centre, Im Neuenheimer Feld 280, 69120, Heidelberg, Germany

    Marc-André Weber, Martin Krix & Stefan Delorme

  2. Bracco ALTANA Pharma GmbH, Konstanz, Germany

    Martin Krix

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  1. Marc-André Weber
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  2. Martin Krix
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Correspondence to Marc-André Weber.

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Invited review article to European Radiology.

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Weber, MA., Krix, M. & Delorme, S. Quantitative evaluation of muscle perfusion with CEUS and with MR. Eur Radiol 17, 2663–2674 (2007). https://doi.org/10.1007/s00330-007-0641-y

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