Advances in Delayed-Onset Muscle Soreness (DOMS): Part I: Pathogenesis and Diagnostics

Abstract

Delayed-onset muscle soreness (DOMS) is a type of ultrastructural muscle injury. The manifestation of DOMS is caused by eccentric or unfamiliar forms of exercise. Clinical signs include reduced force capacities, increased painful restriction of movement, stiffness, swelling, and dysfunction of adjacent joints. Although DOMS is considered a mild type of injury, it is one of the most common reasons for compromised sportive performance. In the past few decades, many hypotheses have been developed to explain the aetiology of DOMS. Although the exact pathophysiological pathway remains unknown, the primary mechanism is currently considered to be the ultrastructural damage of muscle cells due to unfamiliar sporting activities or eccentric exercise, which leads to further protein degradation, apoptosis and local inflammatory response. The development of clinical symptoms is typically delayed (peak soreness at 48 – 72 h post-exercise) as a result of complex sequences of local and systemic physiological responses. The following narrative review was conducted to present an overview of the current findings regarding the damaging mechanisms as well as the pathophysiology of DOMS and its diagnostic evaluation.

Zusammenfassung

Die Delayed Onset Muscle Soreness (DOMS) oder auch „verzögert einsetzender Muskelkater" wird zu den ultrastrukturellen Muskelschädigungen gezählt. Ursächlich werden vorausgegangene exzentrische Kontraktionsformen oder ungewohnte Muskelbelastungen angesehen. Klinische Symptome imponieren in Form einer reduzierten Kraftentfaltung, schmerzhafter Bewegungseinschränkungen, einer Erhöhung des Muskeltonus, Schwellungen sowie Funktionseinschränkungen angrenzender Gelenke. Obwohl die DOMS den milden Schädigungsformen zugeordnet wird, hat sie aufgrund der leistungseinschränkenden Auswirkungen eine große Bedeutung – insbesondere für den Leistungssport. In den letzten Jahrzehnten sind viele Hypothesen zur Ursache und Pathophysiologie beschrieben worden. Auch, wenn der genaue pathophysiologische Signalweg bis heute nicht vollständig geklärt ist, gilt als primärer Schädigungsmechanismus eine mechanische, ultrastrukturelle Schädigung des Muskelparenchyms, die zu einer weiteren Proteindegradation, Autophagie und einer lokalen Entzündungsantwort führt. Klinische Symptome manifestieren sich typischerweise verzögert (Hauptmanifestation zwischen 24 und 72 h nach der Belastung), als Folge einer komplexen lokalen und systemischen Inflammationsphase. Die vorliegende Arbeit hat das Ziel, eine Übersicht über diese Schädigungsentität zu liefern und dabei Grundlagen der schädigenden Mechanismen, der Pathophysiologie und der Diagnostik aufzuzeigen.

Key word

muscle damage - muscle injury - muscle strain - exercise-induced muscle damage - EIMD - eccentric training - MRI

Schlüsselwörter

Muskelschädigung - Muskelverletzung - Muskelzerrung - Muskelkater - Krafttraining - exzentrisches Training - MRT

• References

• 1 Jarvinen TA, Jarvinen TL, Kaariainen M. et al. Muscle injuries: biology and treatment. The American journal of sports medicine 2005; 33: 745-764
• 2 Huard J, Li Y, Fu FH. Muscle injuries and repair: current trends in research. The Journal of bone and joint surgery American volume 2002; 84-A: 822-832
• 3 Best TM, Hunter KD. Muscle injury and repair. Phys Med Rehabil Clin N Am 2000; 11: 251-266
• 4 Hotfiel T, Seil R, Bily W. et al. Nonoperative treatment of muscle injuries – recommendations from the GOTS expert meeting. Journal of Experimental Orthopaedics 2018; 5: 24
• 5 Mueller-Wohlfahrt HW, Haensel L, Mithoefer K. et al. Terminology and classification of muscle injuries in sport: the Munich consensus statement. Br J Sports Med 2013; 47: 342-350
• 6 Armstrong RB. Initial events in exercise-induced muscular injury. Medicine and science in sports and exercise 1990; 22: 429-435
• 7 Friden J, Sjostrom M, Ekblom B. Myofibrillar damage following intense eccentric exercise in man. International journal of sports medicine 1983; 4: 170-176
• 8 Ulbricht A, Gehlert S, Leciejewski B. et al. Induction and adaptation of chaperone-assisted selective autophagy CASA in response to resistance exercise in human skeletal muscle. Autophagy 2015; 11: 538-546
• 9 Paulsen G, Mikkelsen UR, Raastad T. et al. 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
• 10 Hotfiel T, Bily W, Bloch W. et al. Konservative Therapie von Muskelverletzungen. In: Engelhardt M, Mauch F. Hrsg. Muskel- und Sehnenverletzungen. Rolle-Verlag; 2017: 145-153
• 11 Kim SK, Kim MC. The affect on delayed onset muscle soreness recovery for ultrasound with bee venom. Journal of physical therapy science 2014; 26: 1419-1421
• 12 Mizuno S, Morii I, Tsuchiya Y. et al. Wearing Compression Garment after Endurance Exercise Promotes Recovery of Exercise Performance. Int J Sports Med 2016; 37: 870-877
• 13 Pearcey GE, Bradbury-Squires DJ, Kawamoto JE. et al. Foam rolling for delayed-onset muscle soreness and recovery of dynamic performance measures. Journal of athletic training 2015; 50: 5-13
• 14 Valle X, Til L, Drobnic F. et al. Compression garments to prevent delayed onset muscle soreness in soccer players. Muscles, ligaments and tendons journal 2013; 3: 295-302
• 15 Hoppeler H. Eccentric Exercise. Physiology and Application in Sport and Rehabilitation. Vol. 8). London: Routledge; 2015
• 16 Böning D. Muskelkater. Dtsch Z Sportmed 2000; 51 (02) 63-64
• 17 Kim J, Lee J. A review of nutritional intervention on delayed onset muscle soreness. Part I. J Exerc Rehabil 2014; 10: 349-356
• 18 Peake J, Nosaka K, Suzuki K. Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev 2005; 11: 64-85
• 19 Lewis PB, Ruby D, Bush-Joseph CA. Muscle soreness and delayed-onset muscle soreness. Clinics in sports medicine 2012; 31: 255-262
• 20 Beaton LJ, Tarnopolsky MA, Phillips SM. Contraction-induced muscle damage in humans following calcium channel blocker administration. The Journal of physiology 2002; 544: 849-859
• 21 Douglas J, Pearson S, Ross A. et al. Eccentric Exercise: Physiological Characteristics and Acute Responses. Sports medicine (Auckland, NZ) 2017; 47: 663-675
• 22 Hoppeler H. Moderate Load Eccentric Exercise; A Distinct Novel Training Modality. Front Physiol 2016; 7: 483
• 23 Linari M, Lucii L, Reconditi M. et al. A combined mechanical and X-ray diffraction study of stretch potentiation in single frog muscle fibres. The Journal of physiology 2000; 526 Pt 3: 589-596
• 24 Nishikawa KC, Monroy JA, Uyeno TE. et al. Is titin a “winding filament”? A new twist on muscle contraction. Proceedings Biological sciences 2012; 279: 981-990
• 25 Herzog W. Mechanisms of enhanced force production in lengthening (eccentric) muscle contractions. Journal of applied physiology (Bethesda, Md: 1985) 2014; 116: 1407-1417
• 26 Duchateau J, Baudry S. Insights into the neural control of eccentric contractions. Journal of applied physiology (Bethesda, Md: 1985) 2014; 116: 1418-1425
• 27 Kellis E, Baltzopoulos V. Muscle activation differences between eccentric and concentric isokinetic exercise. Medicine and science in sports and exercise 1998; 30: 1616-1623
• 28 Hedayatpour N, Falla D. Physiological and Neural Adaptations to Eccentric Exercise: Mechanisms and Considerations for Training. Biomed Res Int 2015; 2015: 193741
• 29 Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. The Journal of physiology 2001; 537: 333-345
• 30 Nicol C, Avela J, Komi PV. The stretch-shortening cycle: a model to study naturally occurring neuromuscular fatigue. Sports medicine (Auckland, NZ) 2006; 36: 977-999
• 31 Tesch PA, Fernandez-Gonzalo R, Lundberg TR. Clinical Applications of Iso-Inertial, Eccentric-Overload (YoYo) Resistance Exercise. Front Physiol 2017; 8: 241
• 32 Verrall GM, Slavotinek JP, Barnes PG. et al. Clinical risk factors for hamstring muscle strain injury: a prospective study with correlation of injury by magnetic resonance imaging. Br J Sports Med 2001; 35: 435-439 ; discussion 440
• 33 Orchard JW, Farhart P, Leopold C. Lumbar spine region pathology and hamstring and calf injuries in athletes: is there a connection?. Br J Sports Med 2004; 38: 502-504 ; discussion 502–504
• 34 Mueller-Wohlfahrt HW, Ueblacker P, Haensel L. Muskelverletzungen im Sprt. Thieme; 2010
• 35 Yanagisawa O, Sakuma J, Kawakami Y. et al. Effect of exercise-induced muscle damage on muscle hardness evaluated by ultrasound real-time tissue elastography. SpringerPlus 2015; 4: 308
• 36 Kellermann MHM, Swoboda B, Gelse K. et al. Intramuscular Perfusion Response in Delayed Onset Muscle Soreness (DOMS): A Quantitative Analysis with Contrast-Enhanced Ultrasound (CEUS). Int J Sports Med 2017 ahead of print
• 37 Armstrong RB. Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Medicine and science in sports and exercise 1984; 16: 529-538
• 38 Aoi W, Naito Y, Takanami Y. et al. Oxidative stress and delayed-onset muscle damage after exercise. Free radical biology & medicine 2004; 37: 480-487
• 39 Drobnic F, Riera J, Appendino G. et al. Reduction of delayed onset muscle soreness by a novel curcumin delivery system (Meriva(R)): a randomised, placebo-controlled trial. Journal of the International Society of Sports Nutrition 2014; 11: 31
• 40 Close GL, Ashton T, McArdle A. et al. The emerging role of free radicals in delayed onset muscle soreness and contraction-induced muscle injury. Comp Biochem Physiol A Mol Integr Physiol 2005; 142: 257-266
• 41 Nie H, Madeleine P, Arendt-Nielsen L. et al. Temporal summation of pressure pain during muscle hyperalgesia evoked by nerve growth factor and eccentric contractions. Eur J Pain 2009; 13: 704-710
• 42 Hurme T, Kalimo H, Lehto M. et al. Healing of skeletal muscle injury: an ultrastructural and immunohistochemical study. Medicine and science in sports and exercise 1991; 23: 801-810
• 43 Sciorati C, Rigamonti E, Manfredi AA. et al. Cell death, clearance and immunity in the skeletal muscle. Cell Death Differ 2016; 23: 927-937
• 44 Ceafalan LC, Popescu BO, Hinescu ME. Cellular players in skeletal muscle regeneration. Biomed Res Int 2014; 2014: 957014
• 45 Jarvinen TA, Jarvinen M, Kalimo H. Regeneration of injured skeletal muscle after the injury. Muscles Ligaments Tendons J 2013; 3: 337-345
• 46 Hotfiel T, Carl HD, Swoboda B. et al. Current Conservative Treatment and Management Strategies of Skeletal Muscle Injuries. Z Orthop Unfall 2016; 154: 245-253
• 47 Pollock N, James SLJ, Lee JC. et al. British athletics muscle injury classification: a new grading system. British journal of sports medicine 2014; 48: 1347
• 48 Yu JY, Jeong JG, Lee BH. Evaluation of muscle damage using ultrasound imaging. J Phys Ther Sci 2015; 27: 531-534
• 49 Kraemer WJ, Bush JA, Wickham RB. et al. Influence of compression therapy on symptoms following soft tissue injury from maximal eccentric exercise. The Journal of orthopaedic and sports physical therapy 2001; 31: 282-290
• 50 Deme D, Telekes A. Prognostic importance of lactate dehydrogenase (LDH) in oncology. Orvosi hetilap 2017; 158: 1977-1988
• 51 Del GiudiceM, Gangestad SW. Rethinking IL-6 and CRP: Why They Are More Than Inflammatory Biomarkers, and Why It Matters. Brain, behavior, and immunity 2018;
• 52 Miyaki A, Maeda S, Choi Y. et al. Habitual aerobic exercise increases plasma pentraxin 3 levels in middle-aged and elderly women. Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme 2012; 37: 907-911
• 53 Tunc-Ata M, Turgut G, Mergen-Dalyanoglu M. et al. Examination of levels pentraxin-3, interleukin-6, and C-reactive protein in rat model acute and chronic exercise. J Exerc Rehabil 2017; 13: 279-283
• 54 Draghi F, Zacchino M, Canepari M. et al. Muscle injuries: ultrasound evaluation in the acute phase. J Ultrasound 2013; 16: 209-214
• 55 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. British journal of sports medicine 2016; 50: 738-743
• 56 Fulford J, Eston RG, Rowlands AV. et al. Assessment of magnetic resonance techniques to measure muscle damage 24h after eccentric exercise. Scand J Med Sci Sports 2015; 25: e28-e39
• 57 Slavotinek JP. Muscle injury: the role of imaging in prognostic assignment and monitoring of muscle repair. Seminars in musculoskeletal radiology 2010; 14: 194-200
• 58 Balius R, Rodas G, Pedret C. et al. Soleus muscle injury: sensitivity of ultrasound patterns. Skeletal radiology 2014; 43: 805-812
• 59 Heiss R, Kellermann M, Swoboda B. et al. Effect of Compression Garments on the Development of Delayed-Onset Muscle Soreness: A Multimodal Approach Using Contrast-Enhanced Ultrasound and Acoustic Radiation Force Impulse Elastography. The Journal of orthopaedic and sports physical therapy 2018;
• 60 Nosaka K, Clarkson PM. Variability in serum creatine kinase response after eccentric exercise of the elbow flexors. International journal of sports medicine 1996; 17: 120-127
• 61 Nurenberg P, Giddings CJ, Stray-Gundersen J. et al. MR imaging-guided muscle biopsy for correlation of increased signal intensity with ultrastructural change and delayed-onset muscle soreness after exercise. Radiology 1992; 184: 865-869
• 62 Hotfiel T, Kellermann M, Swoboda B. et al. Application of Acoustic Radiation Force Impulse (ARFI) Elastography in Imaging of Delayed Onset Muscle Soreness (DOMS): A Comparative Analysis With 3T MRI. Journal of sport rehabilitation 2017;
• 63 Hotfiel T, Heiss R, Swoboda B. et al. Contrast-Enhanced Ultrasound as a New Investigative Tool in Diagnostic Imaging of Muscle Injuries-A Pilot Study Evaluating Conventional Ultrasound, CEUS, and Findings in MRI. Clinical journal of sport medicine: official journal of the Canadian Academy of Sport Medicine 2017;
• 64 Lee JC, Healy J. Sonography of lower limb muscle injury. Am J Roentgenol 2004; 182: 341-351
• 65 Peetrons P. Ultrasound of muscles. Eur Radiol 2002; 12: 35-43
• 66 Kellermann M, Lutter C, Hotfiel T. Healing Response of a Structural Hamstring Injury – Perfusion Imaging 8 Weeks Follow-Up. J Sport Rehabil 2017;
• 67 Kim HJ, Ryu KN, Sung DW. et al. Correlation between sonographic and pathologic findings in muscle injury: experimental study in the rabbit. Journal of ultrasound in medicine: official journal of the American Institute of Ultrasound in Medicine 2002; 21: 1113-1119
• 68 Serafin-Krol M, Krol R, Jedrzejczyk M. et al. Potential value of contrast-enhanced gray-scale ultrasonography in diagnosis of acute muscle injury--preliminary results. Ortop Traumatol Rehabil 2008; 10: 131-136
• 69 Chung YE, Kim KW. Contrast-enhanced ultrasonography: advance and current status in abdominal imaging. Ultrasonography 2015; 34: 3-18
• 70 Sporea I, Sirli R. Is Contrast Enhanced Ultrasound (CEUS) ready for use in daily practice for evaluation of focal liver lesions?. Med Ultrason 2014; 16: 37-40
• 71 Frohlich E, Muller R, Cui XW. et al. Dynamic contrast-enhanced ultrasound for quantification of tissue perfusion. Journal of ultrasound in medicine: official journal of the American Institute of Ultrasound in Medicine 2015; 34: 179-196
• 72 Gulati M, King KG, Gill IS. et al. Contrast-enhanced ultrasound (CEUS) of cystic and solid renal lesions: a review. Abdom Imaging 2015; 40: 1982-1996
• 73 Hotfiel T, Carl HD, Swoboda B. et al. Contrast-enhanced Ultrasound in Diagnostic Imaging of Muscle Injuries: Perfusion Imaging in the Early Arterial Phase. Sportverletzung Sportschaden: Organ der Gesellschaft fur Orthopadisch-Traumatologische Sportmedizin 2016; 30: 54-57
• 74 Guo LH, Wang SJ, Xu HX. et al. Differentiation of benign and malignant focal liver lesions: value of virtual touch tissue quantification of acoustic radiation force impulse elastography. Med Oncol 2015; 32: 68
• 75 Li DD, Guo LH, Xu HX. et al. Acoustic radiation force impulse elastography for differentiation of malignant and benign breast lesions: a meta-analysis. Int J Clin Exp Med 2015; 8: 4753-4761
• 76 Pfeifer L, Zopf S, Siebler J. et al. Prospective Evaluation of Acoustic Radiation Force Impulse (ARFI) Elastography and High-Frequency B-Mode Ultrasound in Compensated Patients for the Diagnosis of Liver Fibrosis/Cirrhosis in Comparison to Mini-Laparoscopic Biopsy. Ultraschall in Med 2015; 36: 581-589
• 77 Bota S, Sporea I, Sirli R. et al. How useful are ARFI elastography cut-off values proposed by meta-analysis for predicting the significant fibrosis and compensated liver cirrhosis?. Med Ultrason 2015; 17: 200-205
• 78 Cho KH, Nam JH. Evaluation of Stiffness of the Spastic Lower Extremity Muscles in Early Spinal Cord Injury by Acoustic Radiation Force Impulse Imaging. Annals of rehabilitation medicine 2015; 39: 393-400
• 79 D’Onofrio M, Crosara S, Canestrini S. et al. Virtual analysis of pancreatic cystic lesion fluid content by ultrasound acoustic radiation force impulse quantification. Journal of ultrasound in medicine: official journal of the American Institute of Ultrasound in Medicine 2013; 32: 647-651
• 80 Agten CA, Buck FM, Dyer L. et al. Delayed-Onset Muscle Soreness: Temporal Assessment With Quantitative MRI and Shear-Wave Ultrasound Elastography. Am J Roentgenol 2017; 208: 402-412