Abstract
Purpose
The tensiomyography (TMG) technique is increasingly used to determine muscle contractile properties in exercise and injury management. The present study investigated the informative value of TMG parameters in correlation with commonly used (creatine kinase, CK; myoglobin, Mb) and novel candidate biomarkers of muscle damage (heart-type fatty acid-binding protein, h-FABP; high-mobility group box 1, HMGB1).
Methods
Ten untrained men performed 6 × 10 eccentric contractions of the elbow flexors at 110% of the concentric one repetition maximum. CK, Mb, h-FABP, HMGB1, arm circumference, pain and TMG data, including maximal displacement (Dm) and temporal outcomes as the contraction time (Tc), sustained time (Ts), delay time (Td), and relaxation time (Tr), were assessed pre-exercise, post-exercise, 20 min, 2 h and on the consecutive 3 days post-exercise.
Results
CK and h-FABP significantly increased beginning at 24 h, Mb already increased at 2 h (p < 0.05). HMGB1 was only increased immediately post-exercise (p = 0.02). Tc and Td remained unchanged, whereas Ts and Tr were significantly slower beginning at 24 h (p < 0.05). Dm was decreased within the first 24 h and after 72 h (p < 0.01). The % change from pre-exercise correlated for Dm with CK, Mb, and h-FABP the highest at 48 h (r = − 0.95, − 0.87 and − 0.79; p < 0.01) and for h-FABP with CK and Mb the highest at 24 h (r = 0.96 and 0.94, for all p < 0.001).
Conclusion
This study supports the correlation of TMG parameters with muscle damage markers after eccentric exercise. Therefore, TMG could represent a non-invasive and cost effective alternative to quantify the degree of muscle damage after exercise interventions.
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Abbreviations
- ANOVA:
-
Analysis of variance
- ATP:
-
Adenosine triphosphate
- CK:
-
Creatine kinase
- D m :
-
Maximal displacement
- EIMD:
-
Exercise-induced muscle damage
- h-FABP:
-
Heart-type fatty acid binding protein
- HMGB1:
-
High-mobility group box 1
- Mb:
-
Myoglobin
- MVC:
-
Maximal voluntary contraction
- NR:
-
Nonresponders
- POCT:
-
Point-of-care-testing
- TMG:
-
Tensiomyography
- T c :
-
Contraction time
- T d :
-
Delay time
- T r :
-
Relaxation time
- T s :
-
Sustained time
- VAS:
-
Visual analog scale
- 1-RM:
-
One repetition maximum
References
Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue. Cellular mechanisms. Physiol Rev 88(1):287–332. https://doi.org/10.1152/physrev.00015.2007
Behringer M, Kilian Y, Montag J, Geesmann B, Mester J (2016) Plasma concentration of high-mobility group box 1 (HMGB1) after 100 drop to vertical jumps and after a 1200-km bicycle race. Res Sports Med 24(2):119–129. https://doi.org/10.1080/15438627.2015.1126275
Behringer M, Behlau D, Montag JCK, McCourt ML, Mester J (2017a) Low-intensity sprint training with blood flow restriction improves 100-m dash. J Strength Cond Res 31(9):2462–2472. https://doi.org/10.1519/JSC.0000000000001746
Behringer M, Jedlicka D, Mester J (2017b) Effects of lymphatic drainage and cryotherapy on indirect markers of muscle damage. J Sports Med Phys Fit. https://doi.org/10.23736/S0022-4707.17.07261-9
Beiter T, Fragasso A, Hudemann J, Niess AM, Simon P (2011) Short-term treadmill running as a model for studying cell-free DNA kinetics in vivo. Clin Chem 57(4):633–636. https://doi.org/10.1373/clinchem.2010.158030
Chleboun GS, Howell JN, Conatser RR, Giesey JJ (1998) Relationship between muscle swelling and stiffness after eccentric exercise. Med Sci Sports Exerc 30(4):529–535
Clarkson PM, Ebbeling C (1988) Investigation of serum creatine kinase variability after muscle-damaging exercise. Clin Sci (London, England: 1979) 75(3):257–261
Clarkson PM, Nosaka K, Braun B (1992) Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 24(5):512–520
Driessen-Kletter MF, Amelink GJ, Bär PR, van Gijn J (1990) Myoglobin is a sensitive marker of increased muscle membrane vulnerability. J Neurol 237(4):234–238
Fernandez-Gonzalo R, Paz JA de, Rodriguez-Miguelez P, Cuevas MJ, González-Gallego J (2012) Effects of eccentric exercise on toll-like receptor 4 signaling pathway in peripheral blood mononuclear cells. J Appl Physiol (Bethesda Md 1985) 112(12):2011–2018. https://doi.org/10.1152/japplphysiol.01499.2011
Foley JM, Jayaraman RC, Prior BM, Pivarnik JM, Meyer RA (1999) MR measurements of muscle damage and adaptation after eccentric exercise. J Appl Physiol (Bethesda Md 1985) 87(6):2311–2318
Franz A, Behringer M, Harmsen J-F, Mayer C, Krauspe R, Zilkens C, Schumann M (2017) Ischemic preconditioning blunts muscle damage responses induced by eccentric exercise. Med Sci Sports Exerc. https://doi.org/10.1249/MSS.0000000000001406
García-Manso JM, Rodríguez-Matoso D, Sarmiento S, Saa Y de, Vaamonde D, Rodríguez-Ruiz D, Da Silva-Grigoletto ME (2012) Effect of high-load and high-volume resistance exercise on the tensiomyographic twitch response of biceps brachii. J Electromyogr Kinesiol 22(4):612–619. https://doi.org/10.1016/j.jelekin.2012.01.005
Hedayatpour N, Izanloo Z, Falla D (2018) The effect of eccentric exercise and delayed onset muscle soreness on the homologous muscle of the contralateral limb. J Electromyogr Kinesiol 41:154–159. https://doi.org/10.1016/j.jelekin.2018.06.003
Herzog W, Schappacher G, DuVall M, Leonard TR, Herzog JA (2016) Residual force enhancement following eccentric contractions. A new mechanism involving titin. Physiology (Bethesda Md) 31(4):300–312. https://doi.org/10.1152/physiol.00049.2014
Hessel AL, Lindstedt SL, Nishikawa KC (2017) Physiological mechanisms of eccentric contraction and its applications: a role for the giant titin protein. Front Physiol 8:70. https://doi.org/10.3389/fphys.2017.00070
Hopkins WG, Marshall SW, Batterham AM, Hanin J (2009) Progressive statistics for studies in sports medicine and exercise science. Med Sci Sports Exerc 41(1):3–13. https://doi.org/10.1249/MSS.0b013e31818cb278
Hubal MJ, Rubinstein SR, Clarkson PM (2007) Mechanisms of variability in strength loss after muscle-lengthening actions. Med Sci Sports Exerc 39(3):461–468. https://doi.org/10.1249/01.mss.0000247007.19127.da
Hunter AM, Galloway SDR, Smith IJ, Tallent J, Ditroilo M, Fairweather MM, Howatson G (2012) Assessment of eccentric exercise-induced muscle damage of the elbow flexors by tensiomyography. J Electromyogr Kinesiol 22(3):334–341. https://doi.org/10.1016/j.jelekin.2012.01.009
Hyldahl RD, Hubal MJ (2014) Lengthening our perspective: morphological, cellular, and molecular responses to eccentric exercise. Muscle Nerve 49(2):155–170. https://doi.org/10.1002/mus.24077
Kim J, Lee J (2015) The relationship of creatine kinase variability with body composition and muscle damage markers following eccentric muscle contractions. J Exerc Nutr Biochem 19(2):123–129. https://doi.org/10.5717/jenb.2015.15061910
Koch AJ, Pereira R, Machado M (2014) The creatine kinase response to resistance exercise. J Musculoskelet Neuronal Interact 14(1):68–77
Krizaj D, Simunic B, Zagar T (2008) Short-term repeatability of parameters extracted from radial displacement of muscle belly. J Electromyogr Kinesiol 18(4):645–651. https://doi.org/10.1016/j.jelekin.2007.01.008
Li C-j, Li J-q, Liang X-f, Li X-x, Cui J-g, Yang Z-j, Guo Q, Cao K-j, Huang J (2010) Point-of-care test of heart-type fatty acid-binding protein for the diagnosis of early acute myocardial infarction. Acta Pharmacol Sin 31(3):307–312. https://doi.org/10.1038/aps.2010.2
Macgregor LJ, Hunter AM, Orizio C, Fairweather MM, Ditroilo M (2018) Assessment of skeletal muscle contractile properties by radial displacement. The case for tensiomyography. Sports Med (Auckland, NZ). https://doi.org/10.1007/s40279-018-0912-6
Newton MJ, Morgan GT, Sacco P, Chapman DW, Nosaka K (2008) Comparison of responses to strenuous eccentric exercise of the elbow flexors between resistance-trained and untrained men. J Strength Cond Res 22(2):597–607. https://doi.org/10.1519/JSC.0b013e3181660003
Nishikawa KC, Monroy JA, Uyeno TE, Yeo SH, Pai DK, Lindstedt SL (2012) Is titin a ‘winding filament’? A new twist on muscle contraction. Proc Biol Sci 279(1730):981–990. https://doi.org/10.1098/rspb.2011.1304
Nosaka K, Chapman D, Newton M, Sacco P (2006) Is isometric strength loss immediately after eccentric exercise related to changes in indirect markers of muscle damage? Appl Physiol Nutr Metab 31(3):313–319. https://doi.org/10.1139/h06-005
Paddon-Jones DJ, Quigley BM (1997) Effect of cryotherapy on muscle soreness and strength following eccentric exercise. Int J Sports Med 18(8):588–593. https://doi.org/10.1055/s-2007-972686
Peltz ED, Moore EE, Eckels PC, Damle SS, Tsuruta Y, Johnson JL, Sauaia A, Silliman CC, Banerjee A, Abraham E (2009) HMGB1 is markedly elevated within 6 hours of mechanical trauma in humans. Shock (Augusta Ga) 32(1):17–22
Peñailillo L, Blazevich A, Numazawa H, Nosaka K (2013) Metabolic and muscle damage profiles of concentric versus repeated eccentric cycling. Med Sci Sports Exerc 45(9):1773–1781. https://doi.org/10.1249/MSS.0b013e31828f8a73
Scherr J, Braun S, Schuster T, Hartmann C, Moehlenkamp S, Wolfarth B, Pressler A, Halle M (2011) 72-h kinetics of high-sensitive troponin T and inflammatory markers after marathon. Med Sci Sports Exerc 43(10):1819–1827. https://doi.org/10.1249/MSS.0b013e31821b12eb
Simunič B, Degens H, Rittweger J, Narici M, Mekjavić IB, Pišot R (2011) Noninvasive estimation of myosin heavy chain composition in human skeletal muscle. Med Sci Sports Exerc 43(9):1619–1625. https://doi.org/10.1249/MSS.0b013e31821522d0
Thiebaud RS, Yasuda T, Loenneke JP, Abe T (2013) Effects of low-intensity concentric and eccentric exercise combined with blood flow restriction on indices of exercise-induced muscle damage. Interv Med Appl Sci 5(2):53–59. https://doi.org/10.1556/IMAS.5.2013.2.1
van Nieuwenhoven FA, Kleine AH, Wodzig WH, Hermens WT, Kragten HA, Maessen JG, Punt CD, van Dieijen MP, van der Vusse GJ, Glatz JF (1995) Discrimination between myocardial and skeletal muscle injury by assessment of the plasma ratio of myoglobin over fatty acid-binding protein. Circulation 92(10):2848–2854
Venereau E, Schiraldi M, Uguccioni M, Bianchi ME (2013) HMGB1 and leukocyte migration during trauma and sterile inflammation. Mol Immunol 55(1):76–82. https://doi.org/10.1016/j.molimm.2012.10.037
Xu J, Fu SN, Zhou D, Huang C, Hug F (2018) Relationship between pre-exercise muscle stiffness and muscle damage induced by eccentric exercise. Eur J Sport Sci. https://doi.org/10.1080/17461391.2018.1535625
Yanagisawa O, Sakuma J, Kawakami Y, Suzuki K, Fukubayashi T (2015) Effect of exercise-induced muscle damage on muscle hardness evaluated by ultrasound real-time tissue elastography. SpringerPlus 4:308. https://doi.org/10.1186/s40064-015-1094-4
Ye X-D, He Y, Wang S, Wong GT, Irwin MG, Xia Z (2018) Heart-type fatty acid binding protein (H-FABP) as a biomarker for acute myocardial injury and long-term post-ischemic prognosis. Acta Pharmacol Sin. https://doi.org/10.1038/aps.2018.37
Acknowledgements
The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. We thank TMG-BMC Ltd. (Ljubljana, Slovenia) for providing us a Tensiomyography device for the duration of the study.
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JFH, AF, CM, CZ, RK, and MB contributed to the concept and design of the study; JFH, AF, and CM collected the data; JFH, AF, and CM conducted the experiments; BAB and HS were responsible for the laboratory analysis; JFH, AF, and MB analyzed and interpreted the data; JFH and AF created the figures; JFH, AF, and CM wrote the initial draft of the manuscript; and all authors reviewed the manuscript, commented critically, and approved the final version of the manuscript for submission.
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All authors declare that there are no financial and personal relationships with third parties or organizations that could have inappropriately influenced the present work. The authors further state that no funding was received.
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Communicated by Olivier Seynnes.
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Harmsen, JF., Franz, A., Mayer, C. et al. Tensiomyography parameters and serum biomarkers after eccentric exercise of the elbow flexors. Eur J Appl Physiol 119, 455–464 (2019). https://doi.org/10.1007/s00421-018-4043-4
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DOI: https://doi.org/10.1007/s00421-018-4043-4