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Int J Sports Med 2017; 38(11): 833-841
DOI: 10.1055/s-0043-112501
Orthopedics & Biomechanics
© Georg Thieme Verlag KG Stuttgart · New York

Intramuscular Perfusion Response in Delayed Onset Muscle Soreness (DOMS): A Quantitative Analysis with Contrast-Enhanced Ultrasound (CEUS)

Marion Kellermann
1   Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Division of Orthopedic Rheumatology, Department of Orthopedic Surgery, Erlangen, Germany
,
Rafael Heiss
2   University Hospital Erlangen, Department of Radiology, Erlangen, Germany
,
Bernd Swoboda
1   Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Division of Orthopedic Rheumatology, Department of Orthopedic Surgery, Erlangen, Germany
,
Kolja Gelse
3   University Hospital Erlangen, Department of Orthopedic Trauma Surgery, Erlangen, Germany
,
Jürgen Freiwald
4   University of Wuppertal, Movement Science, Wuppertal, Germany
,
Casper Grim
5   Klinikum Osnabruck GmbH, Department of Trauma and Orthopedic Surgery, Osnabrück, Germany
,
Armin Nagel
2   University Hospital Erlangen, Department of Radiology, Erlangen, Germany
,
Michael Uder
2   University Hospital Erlangen, Department of Radiology, Erlangen, Germany
,
Dane Wildner
6   Friedrich-Alexander-University Erlangen-Nürnberg, Department of Internal Medicine 1, Erlangen, Germany
,
Thilo Hotfiel
1   Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Division of Orthopedic Rheumatology, Department of Orthopedic Surgery, Erlangen, Germany
› Author Affiliations
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Publication History



accepted after revision 19 May 2017

Publication Date:
10 August 2017 (online)

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Abstract

The purpose of this study was to analyse intramuscular perfusion response in ultrastructural muscle lesions, by applying contrast-enhanced ultrasound (CEUS) to a delayed onset muscle soreness (DOMS) model. Results of this analysis were compared to high-resolution 3 Tesla MRI T2-weighted sequences. 14 healthy participants were recruited. Average perfusion parameters, represented as Peak enhancement (contrast agent inflow) and wash-in area under curve (WiAUC) of the gastrocnemius (GM) and soleus muscle (SM) were assessed before (baseline) and 60 h after inducing DOMS by eccentric exercise. Additionally, conventional ultrasound, high-resolution 3T MRI, creatine kinase level, range of motion (ROM) of the ankle joint, calf circumference and muscle soreness data were collected. Perfusion quantification revealed a statistically significant increase of intramuscular perfusion, corresponding to an increase in peak enhancement of 129.6% (p=0.0031) and in WiAUC of 115.2% (p=0.0107) in the gastrocnemius muscle at post-intervention. At follow-up, the MRI investigations showed intramuscular oedema for GM in all participants corresponding to a significant rise in T2 signal intensity (p=0.001) and in T2 time value (p=0.005). CEUS seems to be able to detect intramuscular perfusion changes and therefore may contribute to gaining deeper insight into the histopathology, inflammatory reactions and regeneration processes of ultrastructural muscle lesions.

Key words

muscle injury - CEUS - DOMS - ultrasound - MRI - eccentric exercise
 

  • References

  • 1 Amarteifio E, Wormsbecher S, Krix M, Demirel S, Braun S, Delorme S, Bockler D, Kauczor HU, Weber MA. Dynamic contrast-enhanced ultrasound and transient arterial occlusion for quantification of arterial perfusion reserve in peripheral arterial disease. Eur J Radiol 2012; 81: 3332-3338
    CrossrefPubMedGoogle Scholar
  • 2 Armstrong RB. Initial events in exercise-induced muscular injury. Med Sci Sports Exerc 1990; 22: 429-435
    PubMedGoogle Scholar
  • 3 Balius R, Rodas G, Pedret C, Capdevila L, Alomar X, Bong DA. Soleus muscle injury: sensitivity of ultrasound patterns. Skeletal Radiol 2014; 43: 805-812
    CrossrefPubMedGoogle Scholar
  • 4 Chung YE, Kim KW. Contrast-enhanced ultrasonography: advance and current status in abdominal imaging. Ultrasonography 2015; 34: 3-18
    PubMedGoogle Scholar
  • 5 Damas F, Nosaka K, Libardi CA, Chen TC, Ugrinowitsch C. Susceptibility to exercise-induced muscle damage: A cluster analysis with a large sample. Int J Sports Med 2016; 37: 633-640
    Article in Thieme ConnectPubMedGoogle Scholar
  • 6 Davidson BP, Belcik JT, Mott BH, Landry G, Lindner JR. Quantification of residual limb skeletal muscle perfusion with contrast-enhanced ultrasound during application of a focal junctional tourniquet. J Vasc Surg 2016; 63: 148-153
    CrossrefPubMedGoogle Scholar
  • 7 Drew RC, Bell MP, White MJ. Modulation of spontaneous baroreflex control of heart rate and indexes of vagal tone by passive calf muscle stretch during graded metaboreflex activation in humans. J Appl Physiol (1985) 2008; 104: 716-723
    CrossrefPubMedGoogle Scholar
  • 8 Drobnic F, Riera J, Appendino G, Togni S, Franceschi F, Valle X, Pons A, Tur J. Reduction of delayed onset muscle soreness by a novel curcumin delivery system (Meriva(R)): A randomised, placebo-controlled trial. J Int Soc Sports Nutr 2014; 11: 31
    CrossrefPubMedGoogle Scholar
  • 9 Ekstrand J, Lee JC, Healy JC. MRI findings and return to play in football: a prospective analysis of 255 hamstring injuries in the UEFA Elite Club Injury Study. Br J Sports Med 2016; 50: 738-743
    CrossrefPubMedGoogle Scholar
  • 10 Fischer C, Frank M, Kunz P, Tanner M, Weber MA, Moghaddam A, Schmidmaier G, Hug A. Dynamic contrast-enhanced ultrasound (CEUS) after open and minimally invasive locked plating of proximal humerus fractures. Injury 2016; 47: 1725-1731
    CrossrefPubMedGoogle Scholar
  • 11 Fischer C, Krammer D, Hug A, Weber MA, Kauczor HU, Krix M, Bruckner T, Kunz P, Schmidmaier G, Zeifang F. Dynamic contrast-enhanced ultrasound and elastography assess deltoid muscle integrity after reverse shoulder arthroplasty. J Shoulder Elbow Surg 2017; 26: 108-117
    CrossrefPubMedGoogle Scholar
  • 12 Foure A, Le Troter A, Guye M, Mattei JP, Bendahan D, Gondin J. Localization and quantification of intramuscular damage using statistical parametric mapping and skeletal muscle parcellation. Sci Rep 2015; 5: 18580
    CrossrefPubMedGoogle Scholar
  • 13 Friden J, Sjostrom M, Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 1983; 4: 170-176
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Frohlich E, Muller R, Cui XW, Schreiber-Dietrich D, Dietrich CF. Dynamic contrast-enhanced ultrasound for quantification of tissue perfusion. J Ultrasound Med 2015; 34: 179-196
    CrossrefPubMedGoogle Scholar
  • 15 Fulford J, Eston RG, Rowlands AV, Davies RC. Assessment of magnetic resonance techniques to measure muscle damage 24h after eccentric exercise. Scand J Med Sci Sports 2015; 25: e28-e39
    CrossrefPubMedGoogle Scholar
  • 16 Genovese EA, Callegari L, Combi F, Leonardi A, Angeretti MG, Benazzo F, D’Angelo F, Fugazzola C. Contrast-enhanced ultrasound with second generation contrast agent for the follow-up of lower-extremity muscle-strain-repairing processes in professional athletes. Radiol Med 2007; 112: 740-750
    CrossrefPubMedGoogle Scholar
  • 17 Gulati M, King KG, Gill IS, Pham V, Grant E, Duddalwar VA. Contrast-enhanced ultrasound (CEUS) of cystic and solid renal lesions: A review. Abdom Imaging 2015; 40: 1982-1996
    CrossrefPubMedGoogle Scholar
  • 18 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2016 update. Int J Sports Med 2015; 36: 1121-1124
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Hotfiel T, Carl HD, Swoboda B, Engelhardt M, Heinrich M, Strobel D, Wildner D. Contrast-enhanced ultrasound in diagnostic imaging of muscle injuries: perfusion imaging in the early arterial phase. Sportverletz Sportschaden 2016; 30: 54-57
    Article in Thieme ConnectPubMedGoogle Scholar
  • 20 Hu CF, Chen CP, Tsai WC, Hu LL, Hsu CC, Tseng ST, Shau YW. Quantification of skeletal muscle fibrosis at different healing stages using sonography: A morphologic and histologic study in an animal model. J Ultrasound Med 2012; 31: 43-48
    CrossrefPubMedGoogle Scholar
  • 21 Jansson E, Sylven C. Myoglobin concentration in single type I and type II muscle fibres in man. Histochemistry 1983; 78: 121-124
    CrossrefPubMedGoogle Scholar
  • 22 Jarvinen TA, Jarvinen M, Kalimo H. Regeneration of injured skeletal muscle after the injury. Muscles Ligaments Tendons J 2013; 3: 337-345
    PubMedGoogle Scholar
  • 23 Kim SK, Kim MC. The affect on delayed onset muscle soreness recovery for ultrasound with bee venom. J Phys Ther Sci 2014; 26: 1419-1421
    CrossrefPubMedGoogle Scholar
  • 24 Koch AJ, Pereira R, Machado M. The creatine kinase response to resistance exercise. J Musculoskelet Neuronal Interact 2014; 14: 68-77
    PubMedGoogle Scholar
  • 25 Lacourpaille L, Nordez A, Hug F, Couturier A, Dibie C, Guilhem G. Time-course effect of exercise-induced muscle damage on localized muscle mechanical properties assessed using elastography. Acta Physiol (Oxf) 2014; 211: 135-146
    CrossrefPubMedGoogle Scholar
  • 26 Lewis PB, Ruby D, Bush-Joseph CA. Muscle soreness and delayed-onset muscle soreness. Clin Sports Med 2012; 31: 255-262
    CrossrefPubMedGoogle Scholar
  • 27 Lieber RL, Friden J. Morphologic and mechanical basis of delayed-onset muscle soreness. J Am Acad Orthop Surg 2002; 10: 67-73
    CrossrefPubMedGoogle Scholar
  • 28 Lohman 3rd EB, Bains GS, Lohman T, DeLeon M, Petrofsky JS. A comparison of the effect of a variety of thermal and vibratory modalities on skin temperature and blood flow in healthy volunteers. Med Sci Monit 2011; 17: Mt72-Mt81
    PubMedGoogle Scholar
  • 29 Mueller-Wohlfahrt HW, Haensel L, Mithoefer K, Ekstrand J, English B, McNally S, Orchard J, van Dijk CN, Kerkhoffs GM, Schamasch P, Blottner D, Swaerd L, Goedhart E, Ueblacker P. Terminology and classification of muscle injuries in sport: The Munich consensus statement. Br J Sports Med 2013; 47: 342-350
    CrossrefPubMedGoogle Scholar
  • 30 Oh J, Jeon S, Choi J. Contrast-enhanced ultrasonography to assess blood perfusion of skeletal muscles in normal dogs. J Vet Med Sci 2015; 77: 783-788
    CrossrefPubMedGoogle Scholar
  • 31 Paulsen G, Mikkelsen UR, Raastad T, Peake JM. Leucocytes, cytokines and satellite cells: What role do they play in muscle damage and regeneration following eccentric exercise?. Exerc Immunol Rev 2012; 18: 42-97
    PubMedGoogle Scholar
  • 32 Peake J, Nosaka K, Suzuki K. Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev 2005; 11: 64-85
    PubMedGoogle Scholar
  • 33 Pearcey GE, Bradbury-Squires DJ, Kawamoto JE, Drinkwater EJ, Behm DG, Button DC. Foam rolling for delayed-onset muscle soreness and recovery of dynamic performance measures. J Athl Train 2015; 50: 5-13
    CrossrefPubMedGoogle Scholar
  • 34 Peetrons P. Ultrasound of muscles. Eur Radiol 2002; 12: 35-43
    CrossrefPubMedGoogle Scholar
  • 35 Piscaglia F, Bolondi L. The safety of Sonovue in abdominal applications: retrospective analysis of 23188 investigations. Ultrasound Med Biol 2006; 32: 1369-1375
    CrossrefPubMedGoogle Scholar
  • 36 Pringle JS, Doust JH, Carter H, Tolfrey K, Campbell IT, Sakkas GK, Jones AM. Oxygen uptake kinetics during moderate, heavy and severe intensity “submaximal” exercise in humans: The influence of muscle fibre type and capillarisation. Eur J Appl Physiol 2003; 89: 289-300
    CrossrefPubMedGoogle Scholar
  • 37 Rijkelijkhuizen JM, de Ruiter CJ, Huijing PA, de Haan A. Low-frequency fatigue is fibre type related and most pronounced after eccentric activity in rat medial gastrocnemius muscle. Pflugers Arch 2003; 447: 239-246
    CrossrefPubMedGoogle Scholar
  • 38 Serafin-Krol M, Krol R, Jedrzejczyk M, Ziolkowski M, Mlosek R, Jakubowski W, Deszczynski J. Potential value of contrast-enhanced gray-scale ultrasonography in diagnosis of acute muscle injury–preliminary results. Ortop Traumatol Rehabil 2008; 10: 131-136
    PubMedGoogle Scholar
  • 39 Song Y, Li Y, Wang PJ, Gao Y. Contrast-enhanced ultrasonography of skeletal muscles for type 2 diabetes mellitus patients with microvascular complications. Int J. Clin Exp Med 2014; 7: 573-579
    PubMedGoogle Scholar
  • 40 Sugawara J, Maeda S, Otsuki T, Tanabe T, Ajisaka R, Matsuda M. Effects of nitric oxide synthase inhibitor on decrease in peripheral arterial stiffness with acute low-intensity aerobic exercise. Am J Physiol Heart Circ Physiol 2004; 287: H2666-H2669
    CrossrefPubMedGoogle Scholar
  • 41 Ulbricht A, Gehlert S, Leciejewski B, Schiffer T, Bloch W, Hohfeld J. Induction and adaptation of chaperone-assisted selective autophagy CASA in response to resistance exercise in human skeletal muscle. Autophagy 2015; 11: 538-546
    CrossrefPubMedGoogle Scholar
  • 42 Valderrabano V, Pagenstert G, Horisberger M, Knupp M, Hintermann B. Sports and recreation activity of ankle arthritis patients before and after total ankle replacement. Am J Sports Med 2006; 34: 993-999
    CrossrefPubMedGoogle Scholar
  • 43 Yanagisawa O, Kurihara T, Kobayashi N, Fukubayashi T. Strenuous resistance exercise effects on magnetic resonance diffusion parameters and muscle-tendon function in human skeletal muscle. J Magn Reson Imaging 2011; 34: 887-894
    CrossrefPubMedGoogle Scholar
  • 44 Yanagisawa O, Sakuma J, Kawakami Y, Suzuki K, Fukubayashi T. Effect of exercise-induced muscle damage on muscle hardness evaluated by ultrasound real-time tissue elastography. Springerplus 2015; 4: 308
    CrossrefPubMedGoogle Scholar
  • 45 Yu JY, Jeong JG, Lee BH. Evaluation of muscle damage using ultrasound imaging. J Phys Ther Sci 2015; 27: 531-534
    CrossrefPubMedGoogle Scholar