Skip to main content

Assessment of Skeletal Muscle Microperfusion Using MRI

  • Chapter
  • First Online:
Magnetic Resonance Imaging of the Skeletal Musculature

Part of the book series: Medical Radiology ((Med Radiol Diagn Imaging))

  • 2492 Accesses

Abstract

Blood oxygenation level-dependent (BOLD) MRI, arterial spin labeling (ASL) and dynamic contrast enhancement (DCE) are current magnetic resonance imaging (MRI) techniques allowing the non-invasive functional assessment of peripheral microvasculature in healthy and diseased individuals. The functional imaging of skeletal muscle microvasculature helps to understand muscular and vascular physiology and alterations of microcirculation under certain pathological conditions such as peripheral arterial occlusive disease, diabetes mellitus, chronic compartment syndrome and rheumatic disorders. BOLD MRI uses blood as an endogenous contrast agent provided by the different magnetic properties of oxy- and deoxyhemoglobin. The BOLD contrast in skeletal muscle tissue primarily arises from the microcirculation yielding a very sensitive tool for alterations of the physiological oxygen supply and demand. However, the complex nature of the BOLD contrast’s origin also entails a variety of variables complicating the interpretation of BOLD signal changes. ASL’s ability to directly measure muscle perfusion may prove to be a powerful tool for the evaluation of disease progression and the evaluation of therapies aimed at improving muscle perfusion. As is the case with BOLD MRI, this holds particularly true for patients who are unable to receive contrast agents, a collective which is often afflicted with vascular impairments. Dynamic contrast enhanced MRI may contribute considerably to objectively evaluate many musculoskeletal diseases through its ability to measure multiple microvascular properties. The potential of these three MRI methods to non-invasively assess disease severity and the efficacy of new therapeutic strategies, such as stem cell and gene therapy, renders them as very appealing future research targets.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alsop DC, Detre JA (1996) Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J Cereb Blood Flow Metab 16:1236–1249

    CAS  PubMed  Google Scholar 

  • Alsop DC, Detre JA (1998) Multisection cerebral blood flow MR imaging with continuous arterial spin labeling. Radiology 208:410–416

    CAS  PubMed  Google Scholar 

  • Alsop DC, Detre JA, Grossman M (2000) Assessment of cerebral blood flow in Alzheimer’s disease by spin-labeled magnetic resonance imaging. Ann Neurol 47:93–100

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Amarteifio E 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. doi:10.1177/1479164113484165 (Epub ahead of print)

  • Aronen HJ, Cohen MS, Belliveau JW, Fordham JA, Rosen BR (1993) Ultrafast imaging of brain tumors. Top Magn Reson Imaging 5:14–24

    CAS  PubMed  Google Scholar 

  • Aronen HJ et al (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51

    CAS  PubMed  Google Scholar 

  • Baligand C et al (2011) Measuring perfusion and bioenergetics simultaneously in mouse skeletal muscle: a multiparametric functional-NMR approach. NMR Biomed 24:281–290

    CAS  PubMed  Google Scholar 

  • Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25:390–397

    CAS  PubMed  Google Scholar 

  • Barbier EL et al (1999) A model of the dual effect of gadopentetate dimeglumine on dynamic brain MR images. J Magn Reson Imaging 10:242–253

    CAS  PubMed  Google Scholar 

  • Berglund B, Eklund B (1981) Reproducibility of treadmill exercise in patients with intermittent claudication. Clin Physiol (Oxford England) 1:253–256

    CAS  Google Scholar 

  • Bertoldi D et al (2006) New insight into abnormal muscle vasodilatory responses in aged hypertensive rats by in vivo nuclear magnetic resonance imaging of perfusion. J Vasc Res 43:149–156

    PubMed  Google Scholar 

  • Blamire AM, Styles P (2000) Spin echo entrapped perfusion image (SEEPAGE). A nonsubtraction method for direct imaging of perfusion. Magn Reson Med 43:701–704

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Boushel R et al (2000) Blood flow and oxygenation in peritendinous tissue and calf muscle during dynamic exercise in humans. J Physiol 524(Pt 1):305–313

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brix G et al (2004) Microcirculation and microvasculature in breast tumors: pharmacokinetic analysis of dynamic MR image series. Magn Reson Med 52:420–429

    PubMed  Google Scholar 

  • Bulte DP, Alfonsi J, Bells S, Noseworthy MD (2006) Vasomodulation of skeletal muscle BOLD signal. J Magn Reson Imaging 24:886–890

    PubMed  Google Scholar 

  • Bunt TJ, Holloway GA (1996) TcPO2 as an accurate predictor of therapy in limb salvage. Ann Vasc Surg 10:224–227

    CAS  PubMed  Google Scholar 

  • Buxton RB et al (1998) A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 40:383–396

    CAS  PubMed  Google Scholar 

  • Calcagno C et al (2008) Detection of neovessels in atherosclerotic plaques of rabbits using dynamic contrast enhanced MRI and 18F-FDG PET. Arterioscler Thromb Vasc Biol 28:1311–1317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Calviere L et al (2012) Executive dysfunction in adults with moyamoya disease is associated with increased diffusion in frontal white matter. J Neurol Neurosurg Psychiatry 83:591–593

    PubMed  Google Scholar 

  • Carlier PG, Bertoldi D, Baligand C, Wary C, Fromes Y (2006) Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy. NMR Biomed 19:954–967

    CAS  PubMed  Google Scholar 

  • Chalela JA et al (2000) Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. Stroke 31:680–687

    CAS  PubMed  Google Scholar 

  • Cheng H-LM (2007) T1 measurement of flowing blood and arterial input function determination for quantitative 3D T1-weighted DCE-MRI. J Magn Reson Imaging 25:1073–1078

    PubMed  Google Scholar 

  • Crane DE et al (2012) Evaluating quantitative approaches to dynamic susceptibility contrast MRI among carotid endarterectomy patients. J Magn Reson Imaging 37:936–943

    PubMed  Google Scholar 

  • Dawson JM, Hudlicka O (1990) Changes in the microcirculation in slow and fast skeletal muscles with long term limitations of blood supply. Cardiovasc Res 24:390–395

    CAS  PubMed  Google Scholar 

  • De Lussanet QG et al (2007) Dynamic contrast-enhanced MRI of muscle perfusion combined with MR angiography of collateral artery growth in a femoral artery ligation model. NMR Biomed 20:717–725

    PubMed  Google Scholar 

  • Detre JA, Alsop DC (1999) Perfusion fMRI with arterial spin labeling. In: Bandettini PA, Moonen C (eds) Functional MRI. Springer, Berlin pp 4762

    Google Scholar 

  • Detre JA, Leigh JS, Williams DS, Koretsky AP (1992) Perfusion imaging. Magn Reson Med 23:37–45

    CAS  PubMed  Google Scholar 

  • Detre JA et al (1999) Noninvasive magnetic resonance imaging evaluation of cerebral blood flow with acetazolamide challenge in patients with cerebrovascular stenosis. J Magn Reson Imaging 10:870–875

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Duteil S et al (2004) Metabolic and vascular support for the role of myoglobin in humans: a multiparametric NMR study. Am J Physiol Regul Integr Comp Physiol 287:R1441–R1449

    CAS  PubMed  Google Scholar 

  • Duteil S et al (2006) Influence of vascular filling and perfusion on BOLD contrast during reactive hyperemia in human skeletal muscle. Magn Reson Med 55:450–454

    CAS  PubMed  Google Scholar 

  • Duyn JH, Tan CX, van Gelderen P, Yongbi MN (2001) High-sensitivity single-shot perfusion-weighted fMRI. Magn Reson Med 46:88–94

    CAS  PubMed  Google Scholar 

  • Essig M et al (2002) Dynamic susceptibility contrast-enhanced echo-planar imaging of cerebral gliomas. Effect of contrast medium extravasation. Acta Radiol 43:354–359

    CAS  PubMed  Google Scholar 

  • Fagrell B (1986) Microcirculatory methods for the clinical assessment of hypertension, hypotension, and ischemia. Ann Biomed Eng 14:163–173

    CAS  PubMed  Google Scholar 

  • Faranesh AZ, Kraitchman DL, McVeigh ER (2006) Measurement of kinetic parameters in skeletal muscle by magnetic resonance imaging with an intravascular agent. Magn Reson Med 55:1114–1123

    PubMed Central  PubMed  Google Scholar 

  • Fox PT, Raichle ME (1986) Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci USA 83:1140–1144

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Frouin F et al (2006) An automated image-processing strategy to analyze dynamic arterial spin labeling perfusion studies. Application to human skeletal muscle under stress. Magn Reson Imaging 24:941–951

    PubMed  Google Scholar 

  • Gabrielli A, Avvedimento EV, Krieg T (2009) Mechanisms of disease. Scleroderma. N Engl J Med 19:1989–2003

    Google Scholar 

  • Galbraith SM et al (2002) Reproducibility of dynamic contrast-enhanced MRI in human muscle and tumours: comparison of quantitative and semi-quantitative analysis. NMR Biomed 15:132–142

    PubMed  Google Scholar 

  • Garcia DM, Duhamel G, Alsop DC (2005) Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn Reson Med 54:366–372

    PubMed  Google Scholar 

  • Gati JS, Menon RS, Ugurbil K, Rutt BK (1997) Experimental determination of the BOLD field strength dependence in vessels and tissue. Magn Reson Med 38:296–302

    CAS  PubMed  Google Scholar 

  • Gerontol J et al (2009) Multiparametric NMR-based assessment of skeletal muscle perfusion and metabolism during exercise in elderly persons : preliminary findings. J Gerontol A Biol Sci Med Sci 64:968–974

    Google Scholar 

  • Goyault G et al (2012) Diffusion-weighted MRI, dynamic susceptibility contrast MRI and ultrasound perfusion quantification of denervated muscle in rabbits. Skeletal Radiol 41:33–40

    CAS  PubMed  Google Scholar 

  • Green DJ, Spence A, Halliwill JR, Cable NT, Thijssen DHJ (2011) Exercise and vascular adaptation in asymptomatic humans. Exp Physiol 96:57–70

    PubMed  Google Scholar 

  • Green HJ et al (2012) Can increases in capillarization explain the early adaptations in metabolic regulation in human muscle to short-term training? Can J Physiol Pharmacol 90:557–566

    CAS  PubMed  Google Scholar 

  • Gu P, Xu A (2013) Interplay between adipose tissue and blood vessels in obesity and vascular dysfunction. Rev Endoc Metab Disord. doi:10.1007/s11154-012-9230-8

    Google Scholar 

  • Hennig J, Schreiber A, Scheffler K (2000) Time resolved observation of BOLD effect in muscle during isometric exercise. Proc Int Soc Magn Reson Med 8:122

    Google Scholar 

  • Hickey NC, Hudlicka O, Simms MH (1992) Claudication induces systemic capillary endothelial swelling. Eur J Vasc Surg 6:36–40

    CAS  PubMed  Google Scholar 

  • Howseman AM, Bowtell RW (1999) Functional magnetic resonance imaging: imaging techniques and contrast mechanisms. Philos Trans R Soc Lond B Biol Sci 354:1179–1194

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huegli RW et al (2009) Effects of percutaneous transluminal angioplasty on muscle BOLD-MRI in patients with peripheral arterial occlusive disease: preliminary results. Eur Radiol 19:509–515

    PubMed  Google Scholar 

  • Isbell DC et al (2007) Calf muscle perfusion at peak exercise in peripheral arterial disease: measurement by first-pass contrast-enhanced magnetic resonance imaging. J Magn Reson Imaging 25:1013–1020

    PubMed Central  PubMed  Google Scholar 

  • Jackson A (2004) Analysis of dynamic contrast enhanced MRI. Br J Radiol 77:S154–S166

    Google Scholar 

  • Jacobi B et al (2012) Skeletal muscle BOLD MRI: from underlying physiological concepts to its usefulness in clinical conditions. J Magn Reson Imaging 35:1253–1265

    PubMed  Google Scholar 

  • Jacobi B et al (2013) Alterations of skeletal muscle microcirculation detected by blood oxygenation level-dependent MRI in a patient with granulomatosis with polyangiitis. Rheumatology (Oxford, England) 52, 579–581

    Google Scholar 

  • Jaspers K et al (2010) Optimized pharmacokinetic modeling for the detection of perfusion differences in skeletal muscle with DCE-MRI: effect of contrast agent size. Med Phys 37:5746

    CAS  PubMed  Google Scholar 

  • Jiji RS et al (2013) Reproducibility of rest and exercise stress contrast-enhanced calf perfusion magnetic resonance imaging in peripheral arterial disease. J Cardiovasc Magn Reson 15:14

    PubMed Central  PubMed  Google Scholar 

  • Katoh M, Spuentrup E, Barmet C, Stuber M (2008) Local re-inversion coronary MR angiography: arterial spin-labeling without the need for subtraction. J Magn Reson Imaging 27:913–917

    PubMed  Google Scholar 

  • Kerwin W et al (2003) Quantitative magnetic resonance imaging analysis of neovasculature volume in carotid atherosclerotic plaque. Circulation 107:851–856

    PubMed  Google Scholar 

  • Kim SG (1995) Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 34:293–301

    CAS  PubMed  Google Scholar 

  • Konez O et al (1997) Gradient-echo perfusion imaging of musculoskeletal abnormalities with contrast-enhanced two-dimensional fat-saturation FLASH. J Magn Reson Imaging 7:895–902

    Google Scholar 

  • Kober F et al (2004) High-resolution myocardial perfusion mapping in small animals in vivo by spin-labeling gradient-echo imaging. Magn Reson Med 51:62–67

    PubMed  Google Scholar 

  • Kos S et al (2009) Simultaneous dynamic blood oxygen level-dependent magnetic resonance imaging of foot and calf muscles: aging effects at ischemia and postocclusive hyperemia in healthy volunteers. Invest Radiol 44:741–747

    PubMed  Google Scholar 

  • Krix M 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

    PubMed  Google Scholar 

  • Kuperman VY et al (1996) Differentiating between T1 and T2* changes caused by gadopentetate dimeglumine in the kidney by using a double-echo dynamic MR imaging sequence. J Magn Reson Imaging 6:764–768

    Google Scholar 

  • Kwong KK et al (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 89:5675–5679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kwong KK et al (1995) MR perfusion studies with T1-weighted echo planar imaging. Magn Reson Med 34:878–887

    CAS  PubMed  Google Scholar 

  • Larsson HB, Stubgaard M, Søndergaard L, Henriksen O (1994) In vivo quantification of the unidirectional influx constant for Gd-DTPA diffusion across the myocardial capillaries with MR imaging. J Magn Reson Imaging 4:433–440

    CAS  PubMed  Google Scholar 

  • Lavini C et al (2007) Pixel-by-pixel analysis of DCE MRI curve patterns and an illustration of its application to the imaging of the musculoskeletal system. Magn Reson Imaging 25:604–612

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lebon V, Bloch G, Leroy-Willig A, Carlier PG, Brillault-Salvat C (1998b) Evidence of muscle BOLD effect revealed by simultaneous interleaved gradient-echo NMRI and myoglobin NMRS during leg ischemia. Magn Reson Med 40:551–558

    CAS  PubMed  Google Scholar 

  • Lebon VPG, Brillault-Salvat C, Bloch G, Leroy-Willig AC (1998c) Anisotropy of the BOLD effect in the skeletal muscle. In: Proceedings ISMRM Sydney 1424

    Google Scholar 

  • Ledermann HP et al (2006a) Calf muscles imaged at BOLD MR: correlation with TcPO2 and flowmetry measurements during ischemia and reactive hyperemia–initial experience. Radiology 241:477–484

    PubMed  Google Scholar 

  • Ledermann HP et al (2006b) Blood oxygenation level-dependent magnetic resonance imaging of the skeletal muscle in patients with peripheral arterial occlusive disease. Circulation 113:2929–2935

    PubMed  Google Scholar 

  • Leng GC, Fowkes FG, Allan PL, Ruckley CV (1991) Doppler colour flow imaging in peripheral arterial disease. Br J Hosp Med 45:200, 202, 204–207

    Google Scholar 

  • Leppek R et al (2004) MR-Imaging of lower leg muscle perfusion. Herz 29:32–46

    PubMed  Google Scholar 

  • Loerakker S et al (2011) Ischemia-reperfusion injury in rat skeletal muscle assessed with T2-weighted and dynamic contrast-enhanced MRI. Magn Reson Med 66:528–537

    CAS  PubMed  Google Scholar 

  • Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Luo Y et al (2002) Evaluation of tissue perfusion in a rat model of hind-limb muscle ischemia using dynamic contrast-enhanced magnetic resonance imaging. J Magn Reson Imaging 16:277–283

    PubMed  Google Scholar 

  • Lutz AM et al (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

    PubMed  Google Scholar 

  • MacDonald ME, Smith MR, Frayne R (2011) Deconvolution with simple extrapolation for improved cerebral blood flow measurement in dynamic susceptibility contrast magnetic resonance imaging during acute ischemic stroke. Magn Reson Imaging 29:620–629

    PubMed  Google Scholar 

  • Mai VM, Berr SS (1999) MR perfusion imaging of pulmonary parenchyma using pulsed arterial spin labeling techniques: FAIRER and FAIR. J Magn Reson Imaging 9:483–487

    CAS  PubMed  Google Scholar 

  • Marcovecchio ML, Chiarelli F (2011) Microvascular disease in children and adolescents with type 1 diabetes and obesity. Pediatr Nephrol (Berlin, Germany) 26:365–375

    Google Scholar 

  • Marro K (1997) FAWSETS: flow-driven arterial water stimulation with elimination of tissue signal. J Magn Reson (San Diego, CA: 1997) 124:240–244

    Google Scholar 

  • Marro KI, Hyyti OM, Vincent MA, Kushmerick MJ (2005a) Validation and advantages of FAWSETS perfusion measurements in skeletal muscle. NMR Biomed 18:226–234

    PubMed  Google Scholar 

  • Marro KI, Hyyti OM, Kushmerick MJ (2005b) FAWSETS perfusion measurements in exercising skeletal muscle. NMR Biomed 18:322–330

    PubMed  Google Scholar 

  • Mattila KT, Komu ME, Koskinen SK, Niemi PT (1993) Exercise-induced changes in magnetization transfer contrast of muscles. Acta Radiol (Stockholm, Sweden: 1987) 34:559–562

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Mayr NA et al (1996) Tumor perfusion studies using fast magnetic resonance imaging technique in advanced cervical cancer: a new noninvasive predictive assay. Int J Radiat Oncol Biol Phys 36:623–633

    CAS  PubMed  Google Scholar 

  • Mayr NA et al (2000) Pixel analysis of MR perfusion imaging in predicting radiation therapy outcome in cervical cancer. J Magn Reson Imaging 12:1027–1033

    CAS  PubMed  Google Scholar 

  • Ménard JC, Giacomini E, Baligand C, Fromes Y, Carlier PG (2010) Non-invasive and quantitative evaluation of peripheral vascular resistances in rats by combined NMR measurements of perfusion and blood pressure using ASL and dynamic angiography. NMR Biomed 23:188–195

    PubMed  Google Scholar 

  • Meyer RA et al (2004) BOLD MRI mapping of transient hyperemia in skeletal muscle after single contractions. NMR Biomed 17:392–398

    PubMed  Google Scholar 

  • Muller-Delp JM (2006) Aging-induced adaptations of microvascular reactivity. Microcirculation 13:301–314

    CAS  PubMed  Google Scholar 

  • Niemi PT, Komu ME, Koskinen SK (1992) Tissue specificity of low-field-strength magnetization transfer contrast imaging. J Magn Reson Imaging 2:197–201

    CAS  PubMed  Google Scholar 

  • Norris DG, Schwarzbauer C (1999) Velocity selective radiofrequency pulse trains. J Magn Reson (San Diego, CA: 1997) 137:231–236

    Google Scholar 

  • Noseworthy MD, Kim JK, Stainsby JA, Stanisz GJ, Wright GA (1999) Tracking oxygen effects on MR signal in blood and skeletal muscle during hyperoxia exposure. J Magn Reson Imaging 9:814–820

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Noseworthy MD, Davis AD, Elzibak AH (2010) Advanced MR imaging techniques for skeletal muscle evaluation. Semin Musculoskelet Radiol 14:257–268

    PubMed  Google Scholar 

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

    Google Scholar 

  • O’Connor JPB et al (2011) Dynamic contrast-enhanced imaging techniques: CT and MRI. Br J Radiol 84:S112–S120

    Google Scholar 

  • Ogawa S, Lee TM, Nayak AS, Glynn P (1990a) Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn Reson Med 14:68–78

    CAS  PubMed  Google Scholar 

  • Ogawa S, Lee TM, Kay AR, Tank DW (1990b) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ogawa S et al (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951–5955

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pack NA, DiBella EVR (2010) Comparison of myocardial perfusion estimates from dynamic contrast-enhanced magnetic resonance imaging with four quantitative analysis methods. Magn Reson Med 64:125–137

    PubMed Central  PubMed  Google Scholar 

  • Panting JR et al (2002) Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance imaging. N Engl J Med 346:1948–1953

    PubMed  Google Scholar 

  • Partovi S et al (2012a) Effects of covert and overt paradigms in clinical language fMRI. Acad Radiol 19:518–525

    PubMed  Google Scholar 

  • Partovi S et al (2012b) Clinical implications of skeletal muscle blood-oxygenation-level-dependent (BOLD) MRI. Magma New York NY. doi:10.1007/s10334-012-0306-y

    Google Scholar 

  • Partovi S et al (2012c) Blood oxygenation level-dependent (BOLD) MRI of human skeletal muscle at 1.5 and 3 T. J Magn Reson Imaging 35:1227–1232

    PubMed  Google Scholar 

  • Partovi S et al (2012d) Impaired skeletal muscle microcirculation in systemic sclerosis. Arthritis Res Ther 14:R209

    PubMed Central  PubMed  Google Scholar 

  • Partovi S et al (2012e) Clinical standardized fMRI reveals altered language lateralization in brain tumor patients. Am J Neuroradiol 1–7. doi:10.3174/ajnr.A3137

  • Partovi S et al (2013) Correlation of muscle BOLD MRI with transcutaneous oxygen pressure for assessing microcirculation in patients with systemic sclerosis. J Magn Reson Imaging. doi:10.1002/jmri.24046. (Epub ahead of print)

  • Pedersen BK, Akerstrom TC, Nielsen AR, Fischer CP (2007) Role of myokines in exercise and metabolism. J Appl Physiol 103:1093–1098

    CAS  PubMed  Google Scholar 

  • Picchi A et al (2010) Coronary microvascular dysfunction in diabetes mellitus: a review. World J Cardiol 2:377–390

    PubMed Central  PubMed  Google Scholar 

  • Pollak AW et al (2012) Arterial spin labeling MR imaging reproducibly measures peak-exercise calf muscle perfusion: a study in patients with peripheral arterial disease and healthy volunteers. JACC Cardiovasc Imaging 5:1224–1230

    PubMed  Google Scholar 

  • Potthast S, Schulte A, Kos S, Aschwanden M, Bilecen D (2009) Blood oxygenation level-dependent MRI of the skeletal muscle during ischemia in patients with peripheral arterial occlusive disease. Rofo 181:1157–1161

    CAS  PubMed  Google Scholar 

  • Prince MR (1998) Peripheral vascular MR angiography: the time has come. Radiology 206:592–593

    CAS  PubMed  Google Scholar 

  • Proctor DN, Koch DW, Newcomer SC, Le KU, Leuenberger UA (2003) Impaired leg vasodilation during dynamic exercise in healthy older women. J Appl Physiol 95:1963–1970

    PubMed  Google Scholar 

  • Quarles CC, Gore JC, Xu L, Yankeelov TE (2012) Comparison of dual-echo DSC-MRI- and DCE-MRI-derived contrast agent kinetic parameters. Magn Reson Imaging 30:944–953

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ranft J, Heidrich H, Peters A, Trampisch H (1986) Laser-Doppler examinations in persons with healthy vasculature and in patients with peripheral arterial occlusive disease. Angiology 37:818–827

    CAS  PubMed  Google Scholar 

  • Raynaud JS et al (2001) Determination of skeletal muscle perfusion using arterial spin labeling NMRI: validation by comparison with venous occlusion plethysmography. Magn Reson Med 46:305–311

    CAS  PubMed  Google Scholar 

  • Rehwald WG, Chen E-L, Kim RJ, Judd RM (2004) Noninvasive cineangiography by magnetic resonance global coherent free precession. Nat Med 10:545–549

    CAS  PubMed  Google Scholar 

  • Richardson RS, Haseler LJ, Nygren AT, Bluml S, Frank LR (2001) Local perfusion and metabolic demand during exercise: a noninvasive MRI method of assessment. J Appl Physiol (Bethesda, MD: 1985) 91:1845–1853

    Google Scholar 

  • Rieber A et al (2002) Breast MRI for monitoring response of primary breast cancer to neo-adjuvant chemotherapy. Eur Radiol 12:1711–1719

    CAS  PubMed  Google Scholar 

  • Rissanen TT et al (2005) Blood flow remodels growing vasculature during vascular endothelial growth factor gene therapy and determines between capillary arterialization and sprouting angiogenesis. Circulation 112:3937–3946

    CAS  PubMed  Google Scholar 

  • Robson PM et al (2012) Imaging of renal masses: correlation with Histopathologic. 265:799–808

    Google Scholar 

  • Rofsky NM, Adelman MA (2000) MR angiography in the evaluation of atherosclerotic peripheral vascular disease. Radiology 214:325–338

    CAS  PubMed  Google Scholar 

  • Saeed M (2001) New concepts in characterization of ischemically injured myocardium by MRI. Exp Biol Med (Maywood, NJ) 226:367–376

    Google Scholar 

  • Sanchez OA, Copenhaver EA, Elder CP, Damon BM (2010) Absence of a significant extravascular contribution to the skeletal muscle BOLD effect at 3 T. Magn Reson Med 64:527–535

    PubMed Central  PubMed  Google Scholar 

  • Sanchez OA et al (2011) Postmaximal contraction blood volume responses are blunted in obese and type 2 diabetic subjects in a muscle-specific manner. Am J Physiol 301:H418–H427

    CAS  Google Scholar 

  • Sarelius I, Pohl U (2010) Control of muscle blood flow during exercise: local factors and integrative mechanisms. Acta Physiol (Oxf) 199:349–365

    CAS  Google Scholar 

  • Schraml C, Schwenzer NF, Martirosian P, Claussen CD, Schick F (2011) Temporal course of perfusion in human masseter muscle during isometric contraction assessed by arterial spin labeling at 3T. Magma (New York, NY) 24:201–209

    Google Scholar 

  • Schulte AC, Speck O, Oesterle C, Hennig J (2001) Separation and quantification of perfusion and BOLD effects by simultaneous acquisition of functional I(0)- and T2(*)-parameter maps. Magn Reson Med 45:811–816

    CAS  PubMed  Google Scholar 

  • Schulte AC, Aschwanden M, Bilecen D (2008) Calf muscles at blood oxygen level-dependent MR imaging: aging effects at postocclusive reactive hyperemia. Radiology 247:482–489

    PubMed  Google Scholar 

  • Schwarzbauer C, Morrissey SP, Haase A (1996) Quantitative magnetic resonance imaging of perfusion using magnetic labeling of water proton spins within the detection slice. Magn Reson Med 35:540–546

    CAS  PubMed  Google Scholar 

  • Silva AC, Kim SG (1999) Pseudo-continuous arterial spin labeling technique for measuring CBF dynamics with high temporal resolution. Magn Reson Med 42:425–429

    CAS  PubMed  Google Scholar 

  • Slade JM, Towse TF, Gossain VV, Meyer RA (2011) Peripheral microvascular response to muscle contraction is unaltered by early diabetes but decreases with age. J Appl Physiol (Bethesda, MD: 1985) 111, 1361–1371

    Google Scholar 

  • Slagsvold C-E, Stranden E, Rosen L, Kroese AJ (1992) The role of blood perfusion and tissue oxygenation in the postischemic transcutaneous pO2 response. Angiology 43:155–162

    CAS  PubMed  Google Scholar 

  • Speck O, Hennig J (1998) Functional imaging by I0- and T2*-parameter mapping using multi-image EPI. Magn Reson Med 40:243–248

    CAS  PubMed  Google Scholar 

  • Talagala SL, Barbier EL, Williams DS, Silva AC, Koretsky AP (1998) Multi-slice perfusion MRI using continuous arterial water labeling: controling for MT effects with simultaneous proximal and distal RF irradiation. In: Proceedings of the 6th annual meeting of ISMRM 381. http://cds.ismrm.org/ismrm-1998/PDF2/p0381.pdf

  • Themen F (1997) Methodische Ansätze zur quantitativen Beurteilung der Mikrozirkulation im Gewebe mit der dynamischen. Radiologe 37: 470–480

    Google Scholar 

  • Thompson RB et al (2005) Measurement of skeletal muscle perfusion during postischemic reactive hyperemia using contrast-enhanced MRI with a step-input function. Magn Reson Med 54:289–298

    PubMed Central  PubMed  Google Scholar 

  • Thulborn KR, Waterton JC, Matthews PM, Radda GK (1982) Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field. Biochim Biophys Acta 714:265–270

    CAS  PubMed  Google Scholar 

  • Tofts PS et al (1999) Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 10:223–232

    CAS  PubMed  Google Scholar 

  • Toussaint JF et al (1996) Perfusion changes in human skeletal muscle during reactive hyperemia measured by echo-planar imaging. Magn Reson Med 35:62–69

    CAS  PubMed  Google Scholar 

  • Towse TF, Slade JM, Meyer RA (2005) Effect of physical activity on MRI-measured blood oxygen level-dependent transients in skeletal muscle after brief contractions. J Appl Physiol 99:715–722

    PubMed  Google Scholar 

  • Towse TF, Slade JM, Ambrose JA, Delano MC, Meyer RA (2011) Quantitative analysis of the post-contractile blood-oxygenation-level-dependent (BOLD) effect in skeletal muscle. J Appl Physiol 111:27–39

    PubMed Central  PubMed  Google Scholar 

  • Troalen T, Capron T, Cozzone PJ, Bernard M, Kober F (2013) Cine-ASL: a steady-pulsed arterial spin labeling method for myocardial perfusion mapping in mice. Part I. Experimental study. Magn Reson Med. doi:10.1002/mrm.24565

    Google Scholar 

  • Turner R (1997) Signal sources in bold contrast fMRI. Adv Exp Med Biol 413:19–25

    CAS  PubMed  Google Scholar 

  • Utz W et al (2005) Blood oxygen level-dependent MRI of tissue oxygenation: relation to endothelium-dependent and endothelium-independent blood flow changes. Arterioscler Thromb Vasc Biol 25:1408–1413

    CAS  PubMed  Google Scholar 

  • Van der Leij C, van de Sande MGH, Lavini C, Tak PP, Maas M (2009) Rheumatoid synovial inflammation: pixel-by-pixel dynamic contrast-enhanced MR imaging time-intensity curve shape analysis – a feasibility study. Radiology 253:234–240

    PubMed  Google Scholar 

  • Van der Woude HJ et al (1998) Musculoskeletal tumors: does fast dynamic contrast-enhanced subtraction MR imaging contribute to the characterization? Radiology 208:821–828

    PubMed  Google Scholar 

  • Van der Zwaag W et al (2009) fMRI at 1.5, 3 and 7 T: characterising BOLD signal changes. Neuroimage 47:1425–1434

    PubMed  Google Scholar 

  • Van Rijswijk CS, Hogendoorn PC, Taminiau AH, Bloem JL (2001) Synovial sarcoma: dynamic contrast-enhanced MR imaging features. Skeletal Radiol 30:25–30

    PubMed  Google Scholar 

  • Versluis B et al (2011) Magnetic resonance imaging in peripheral arterial disease: reproducibility of the assessment of morphological and functional vascular status. Invest Radiol 46:11–24

    PubMed  Google Scholar 

  • Versluis B et al (2012) Dynamic contrast-enhanced MRI assessment of hyperemic fractional microvascular blood plasma volume in peripheral arterial disease: initial findings. PLoS ONE 7:e37756

    CAS  PubMed Central  PubMed  Google Scholar 

  • Verstraete KL et al (1994) Benign and malignant musculoskeletal lesions: dynamic contrast-enhanced MR imaging–parametric “first-pass” images depict tissue vascularization and perfusion. Radiology 192:835–843

    CAS  PubMed  Google Scholar 

  • Vonken EP, van Osch MJ, Bakker CJ, Viergever MA (2000) Simultaneous quantitative cerebral perfusion and Gd-DTPA extravasation measurement with dual-echo dynamic susceptibility contrast MRI. Magn Reson Med 43:820–827

    CAS  PubMed  Google Scholar 

  • Walker UA et al (2007) Clinical risk assessment of organ manifestations in systemic sclerosis: a report from the EULAR Scleroderma trials and research group database. Ann Rheum Dis 66:754–763

    CAS  PubMed Central  PubMed  Google Scholar 

  • Van de Sande MGH et al (2012) Characteristics of synovial inflammation in early arthritis analysed by pixel-by-pixel time-intensity curve shape analysis. Rheumatology (Oxford, England) 51:1240–1245

    Google Scholar 

  • Wang DJJ et al (2012) The value of arterial spin-labeled perfusion imaging in acute ischemic stroke: comparison with dynamic susceptibility contrast-enhanced MRI. Stroke 43:1018–1024

    PubMed Central  PubMed  Google Scholar 

  • Weber M-A, Kroll A, Günther M (2004) Noninvasive measurement of relative cerebral blood flow using arterial spin labeling techniques: physical basics and clinical applications. Radiologe 44:164–173

    PubMed  Google Scholar 

  • Weber MA, Risse F, Giesel FL, Schad LR, Kauczor HU, Essig M (2005) Measurement of perfusion using the first-pass dynamic susceptibility-weight ed contrast-enhanced (DSC) MRI in neurooncology. Physical basics and clinical applications. Radiologe 45:618–632

    PubMed  Google Scholar 

  • Weber MA, Krix M, Delorme S (2007) Quantitative evaluation of muscle perfusion with CEUS and with MR. Eur Radiol 17:2663–2674

    PubMed  Google Scholar 

  • Wheaton AJ, Miyazaki M (2012) Non-contrast enhanced MR angiography: physical principles. J Magn Reson Imaging 36:286–304

    PubMed  Google Scholar 

  • 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 (Bethesda, MD: 1985) 97:2385–2394

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wong EC et al (2006) Velocity-selective arterial spin labeling. Magn Reson Med 55:1334–1341

    PubMed  Google Scholar 

  • Wu W-C, Fernández-Seara M, Detre JA, Wehrli FW, Wang J (2007) A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med 58:1020–1027

    PubMed  Google Scholar 

  • Wu W-C, Wang J, Detre JA, Ratcliffe SJ, Floyd TF (2008) Transit delay and flow quantification in muscle with continuous arterial spin labeling perfusion-MRI. J Magn Reson Imaging 28:445–452

    PubMed Central  PubMed  Google Scholar 

  • Wu W-C et al (2009) Skeletal muscle microvascular flow in progressive peripheral artery disease: assessment with continuous arterial spin-labeling perfusion magnetic resonance imaging. J Am Coll Cardiol 53:2372–2377

    PubMed  Google Scholar 

  • Wu W, Lawrence KSS, Licht DJ, Wang DJJ (2011) Quantification issues in arterial spin labeling perfusion. 21:65–73

    Google Scholar 

  • Yankeelov TE, Gore JC (2009) Dynamic contrast enhanced magnetic resonance imaging in oncology: theory, data acquisition, analysis, and examples. Curr Med Imaging Rev 3:91–107

    PubMed Central  PubMed  Google Scholar 

  • Ye FQ, Frank JA, Weinberger DR, McLaughlin AC (2000) Noise reduction in 3D perfusion imaging by attenuating the static signal in arterial spin tagging (ASSIST). Magn Reson Med 44:92–100

    CAS  PubMed  Google Scholar 

  • Yeung DKW, Griffith JF, Li AFW, Ma HT, Yuan J (2012) Air pressure-induced susceptibility changes in vascular reactivity studies using BOLD MRI. J Magn Reson Imaging. doi:10.1002/jmri.23926

    Google Scholar 

  • Zhang H et al (2005) Accurate myocardial T1 measurements: toward quantification of myocardial blood flow with arterial spin labeling. Magn Reson Med 53:1135–1142

    PubMed  Google Scholar 

  • Zhu XP, Zhao S, Isherwood I (1992) Magnetization transfer contrast (MTC) imaging of skeletal muscle at 0.26 Tesla–changes in signal intensity following exercise. Br J Radiol 65:39–43

    CAS  PubMed  Google Scholar 

  • Zierath JR, Hawley JA (2004) Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol 2:e348

    PubMed Central  PubMed  Google Scholar 

  • Ziv K et al (2004) Longitudinal MRI tracking of the angiogenic response to hind limb ischemic injury in the mouse. Magn Reson Med 51:304–311

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Deniz Bilecen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Partovi, S. et al. (2013). Assessment of Skeletal Muscle Microperfusion Using MRI. In: Weber, MA. (eds) Magnetic Resonance Imaging of the Skeletal Musculature. Medical Radiology(). Springer, Berlin, Heidelberg. https://doi.org/10.1007/174_2013_911

Download citation

  • DOI: https://doi.org/10.1007/174_2013_911

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-37218-6

  • Online ISBN: 978-3-642-37219-3

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics