The Relationship Between Acute Exercise-Induced Changes in Extramuscular Connective Tissue Thickness and Delayed Onset Muscle Soreness in Healthy Participants: A Randomized Controlled Crossover Trial
Tóm tắt
The extramuscular connective tissue (ECT) has been shown to play a significant role in mechanical force transmission between musculoskeletal structures. Due to this and owing to its tight connection with the underlying muscle, the ECT may be vulnerable to excessive loading. The present study aimed to investigate the effect of eccentric elbow flexor exercise on the morphology of the biceps brachii ECT. In view of the high nociceptive capacity of the ECT, an additional objective was to elucidate the potential relationship between ECT damage and the occurrence of delayed onset muscle soreness (DOMS). Eleven healthy participants (♂ = 7; 24 ± 2 years) performed fatiguing dumbbell elbow flexor eccentric exercise (EE) for one arm and concentric exercise (CE) for the other arm in random order and with random arm allocation. Before, immediately after and 24–96 h post-exercise, maximal voluntary isometric contraction torque of the elbow flexors (dynamometer), pressure pain (algometer), palpation pain (100 mm visual analog scale), biceps brachii ECT thickness and ECT/muscle mobility during passive movement (both high-resolution ultrasound) were examined. Palpation pain, suggestive of DOMS, was greater after EE than CE, and maximal voluntary isometric contraction torque decreased greater after EE than CE (p < .05). Relative to CE, EE increased ECT thickness at 48 (+ 17%), 72 (+ 14%) and 96 (+ 15%) hours post-exercise (p < .05). At 96 h post-EE, the increase in ECT thickness correlated with palpation pain (r = .68; p < .05). ECT mobility was not different between conditions, but compared to CE, muscle displacement increased at 24 (+ 31%), 72 (+ 31%) and 96 (+ 41%) hours post-EE (p < .05). Collectively, these results suggest an involvement of the ECT changes in delayed onset muscle soreness.
Tài liệu tham khảo
Wilke J, Schleip R, Yucesoy CA, Banzer W. Not merely a protective packing organ? A review of fascia and its force transmission capacity. J Appl Physiol. 2018;124(1):234–44.
Yucesoy CA, Baan GC, Koopman BH, Grootenboer HJ, Huijing PA. Pre-strained epimuscular connections cause muscular myofascial force transmission to affect properties of synergistic EHL and EDL muscles of the rat. J Biomech Eng. 2005;127(5):819–28.
Krause F, Wilke J, Vogt L, Banzer W. Intermuscular force transmission along myofascial chains: a systematic review. J Anat. 2016;228(6):910–8.
Huijing PA, Baan GC. Myofascial force transmission via extramuscular pathways occurs between antagonistic muscles. Cells Tissues Organs. 2008;188(4):400–14.
Hijikata T, Ishikawa H. Functional morphology of serially linked skeletal muscle fibers. Acta Anat (Basel). 1997;159(2–3):99–107.
Purslow PP, Trotter JA. The morphology and mechanical properties of endomysium in series-fibred muscles: variations with muscle length. J Muscle Res Cell Motil. 1994;15(3):299–308.
Passerieux E, Rossignol R, Letellier T, Delage JP. Physical continuity of the perimysium from myofibers to tendons: involvement in lateral force transmission in skeletal muscle. J Struct Biol. 2007;159(1):19–28.
Stecco A, Masiero S, Macchi V, Stecco C, Porzionato A, De Caro R. The pectoral fascia: anatomical and histological study. J Bodyw Mov Ther. 2009;13(3):255–61.
Stecco C, Macchi V, Porzionato A, Duparc F, De Caro R. The fascia: the forgotten structure. Ital J Anat Embryol = Arch Ital di Anat ed Embriol. 2011;116(3):127–38.
Stecco C, Gagey O, Macchi V, Porzionato A, De Caro R, Aldegheri R, et al. Tendinous muscular insertions onto the deep fascia of the upper limb. First part: anatomical study. Morphologie. 2007;91(292):29–37.
Schleip R, Gabbiani G, Wilke J, Naylor I, Hinz B, Zorn A, et al. Fascia is able to actively contract and may thereby influence musculoskeletal dynamics: a histochemical and mechanographic investigation. Front Physiol. 2019;10:336.
Wilke J, Debelle H, Tenberg S, Dilley A, Maganaris C. Ankle motion is associated with soft tissue displacement in the dorsal thigh: an in vivo investigation suggesting myofascial force transmission across the knee joint. Front Physiol. 2020;11:180.
Wilke J, Hespanhol L, Behrens M. Is it all about the fascia? A systematic review and meta-analysis of the prevalence of extramuscular connective tissue lesions in muscle strain injury. Orthop J Sport Med. 2019;7(12):2325967119888500.
Stecco C, Gagey O, Belloni A, Pozzuoli A, Porzionato A, Macchi V, et al. Anatomy of the deep fascia of the upper limb. Second part: study of innervation. Morphologie. 2007;91(292):38–43. https://doi.org/10.1016/j.morpho.2007.05.002.
Mense S. Innervation of the thoracolumbar fascia. Eur J Transl Myol. 2020;29(3):151–8. https://doi.org/10.4081/ejtm.2019.8297.
Langevin HM, Fox JR, Koptiuch C, Badger GJ, Greenan-Naumann AC, Bouffard NA, et al. Reduced thoracolumbar fascia shear strain in human chronic low back pain. BMC Musculoskelet Disord. 2011;12(1):203. https://doi.org/10.1186/1471-2474-12-203.
Gibson W, Arendt-Nielsen L, Mizumura TTK, Graven-Nielsen T. Increased pain from muscle fascia following eccentric exercise: animal and human findings. Exp Brain Res. 2009;194(2):299–308. https://doi.org/10.1186/1471-2474-12-203.
Lau WY, Blazevich AJ, Newton MJ, Wu SSX, Nosaka K. Changes in electrical pain threshold of fascia and muscle after initial and secondary bouts of elbow flexor eccentric exercise. Eur J Appl Physiol. 2015;115(5):959–68.
Klingler W, Jäger H, Pedro MT, Schleip R. Faszien als Ursache von Schmerzsyndromen. In: Herbert M, Meißner W, editors. Aktuelle Schmerzmedizin. Ecomed Medizin. Heidelberg: Verlagsgruppe HÜThig Jehle Rehm Gmbh; 2014.
Schilder A, Hoheisel U, Magerl W, Benrath J, Klein T, Treede R-D. Sensory findings after stimulation of the thoracolumbar fascia with hypertonic saline suggest its contribution to low back pain. Pain. 2014;155(2):222–31.
Stecco C, Stern R, Porzionato A, Macchi V, Masiero S, Stecco A, et al. Hyaluronan within fascia in the etiology of myofascial pain. Surg Radiol Anat. 2011;33(10):891–6.
Nosaka K, Newton M, Sacco P. Delayed-onset muscle soreness does not reflect the magnitude of eccentric exercise-induced muscle damage. Scand J Med Sci Sport. 2002;12(6):337–46. https://doi.org/10.1034/j.1600-0838.2002.10178.x.
Nurenberg P, Giddings CJ, Stray-Gundersen J, Fleckenstein JL, Gonyea WJ, Peshock RM. MR imaging-guided muscle biopsy for correlation of increased signal intensity with ultrastructural change and delayed-onset muscle soreness after exercise. Radiology. 1992;184(3):865–9. https://doi.org/10.1148/radiology.184.3.1509081.
Hotfiel T, Freiwald J, Hoppe MW, Lutter C, Forst R, Grim C, Bloch W, Hüttel M, Hiess R. Advances in delayed-onset muscle soreness (DOMS): part I: pathogenesis and diagnostics. Sportverletz Sportschaden. 2018;32(4):243–50. https://doi.org/10.1055/A-0753-1884.
Veale JF. Edinburgh Handedness Inventory—short form: a revised version based on confirmatory factor analysis. Laterality. 2014;19(2):164–77. https://doi.org/10.1080/1357650X.2013.783045.
Chen TC, Yang TJ, Huang MJ, Wang HS, Tseng KW, Chen HL, et al. Damage and the repeated bout effect of arm, leg, and trunk muscles induced by eccentric resistance exercises. Scand J Med Sci Sport. 2019;29(5):725–35. https://doi.org/10.1111/sms.13388.
Lau WY, Muthalib M, Nosaka K. Visual analog scale and pressure pain threshold for delayed onset muscle soreness assessment. J Musculoskelet Pain. 2013;21(4):320–6.
Lau WY, Blazevich AJ, Newton MJ, Wu SSX, Nosaka K. Reduced muscle lengthening during eccentric contractions as a mechanism underpinning the repeated-bout effect. Am J Physiol. 2015;308(10):879–86.
Nosaka K, Newton M. Concentric or eccentric training effect on eccentric exercise-induced muscle damage. Med Sci Sports Exerc. 2002;34(1):63–9.
Seo DI, Kim E, Fahs CA, Rossow L, Young K, Ferguson SL, et al. Reliability of the one-repetition maximum test based on muscle group and gender. J Sports Sci Med. 2012;11(2):221–5.
Nguyen D, Brown LE, Coburn JW, Judelson DA, Eurich AD, Khamoui AV, et al. Effect of delayed-onset muscle soreness on elbow flexion strength and rate of velocity development. J Strength Cond Res. 2009;23(4):1282–6.
Chen TC, Nosaka K. Responses of elbow flexors to two strenuous eccentric exercise bouts separated by three days. J Strength Cond Res. 2006;20(1):108–16.
Morishita S, Yamauchi S, Fujisawa C, Domen K. Rating of perceived exertion for quantification of the intensity of resistance exercise. Int J Phys Med Rehabil. 2013;1(9):172.
Prieske O, Wick D, Granacher U. Intrasession and intersession reliability in maximal and explosive isometric torque production of the elbow flexors. J Strength Cond Res. 2014;28(6):1771–7.
Haefeli M, Elfering A. Pain assessment. Eur Spine J. 2006;15:S17–24. https://doi.org/10.1007/s00586-005-1044-x.
Turk DC, Melzack R. The measurement of pain and the assessment of people experiencing pain. In: Turk DC, Melzack R, editors. Handbook of pain assessment. 3rd ed. New York, NY: The Guilford Press; 2011. p. 3–16.
Lau WY, Blazevich AJ, Newton MJ, Wu SSX, Nosaka K. Assessment of muscle pain induced by elbow-flexor eccentric exercise. J Athl Train. 2015;50(11):1140–8.
Cheng JW, Tsai WC, Yu TY, Huang KY. Reproducibility of sonographic measurement of thickness and echogenicity of the plantar fascia. J Clin Ultrasound. 2012;40(1):14–9.
Bisi-Balogun A, Cassel M, Mayer F. Reliability of various measurement stations for determining plantar fascia thickness and echogenicity. Diagnostics. 2016;6(2):15.
Cruz-Montecinos C, González Blanche A, López Sánchez D, Cerda M, Sanzana-Cuche R, Cuesta-Vargas A. In vivo relationship between pelvis motion and deep fascia displacement of the medial gastrocnemius: anatomical and functional implications. J Anat. 2015;227(5):665–72. https://doi.org/10.1111/joa.12370.
Gajdosik RL. Influence of age on calf muscle length and passive stiffness variables at different stretch velocities. Isokinet Exerc Sci. 1997;6(3):163–74.
Lamontagne A, Malouin F, Richards CL. Viscoelastic behavior of plantar flexor muscle-tendon unit at rest. J Orthop Sports Phys Ther. 1997;26(5):244–52. https://doi.org/10.2519/jospt.1997.26.5.244.
Krause F, Wilke J, Niederer D, Vogt L, Banzer W. Acute effects of foam rolling on passive stiffness, stretch sensation and fascial sliding: a randomized controlled trial. Hum Mov Sci. 2019;67:102514. https://doi.org/10.1016/j.humov.2019.102514.
Dilley A, Greening J, Lynn B, Leary R, Morris V. The use of cross-correlation analysis between high-frequency ultrasound images to measure longitudinal median nerve movement. Ultrasound Med Biol. 2001;27(9):1211–8. https://doi.org/10.1016/S0301-5629(01)00413-6.
Cohen J. Statistical power analysis for the behavioral sciences. Hoboken: Taylor and Francis; 1988.
Cohen L, Manion L. Research methods in education. London: Croom Helm; 1980.
Friden J, Kjorell U, Thornell LE. Delayed muscle soreness and cytoskeletal alterations: an immunocytological study in man. Int J Sports Med. 1984;5(1):15–8. https://doi.org/10.1055/s-2008-1025873.
Friden J, Sjostrom M, Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med. 1983;4(3):170–6. https://doi.org/10.1055/s-2008-1026030.
Fridén J, Lieber RL. Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand. 2001;171:321–6. https://doi.org/10.1046/j.1365-201X.2001.00834.x.
Newham DJ, McPhail G, Mills KR, Edwards RHT. Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci. 1983;61(1):109–22. https://doi.org/10.1016/0022-510X(83)90058-8.
Solomonow M. Neuromuscular manifestations of viscoelastic tissue degradation following high and low risk repetitive lumbar flexion. J Electromyogr Kinesiol. 2012;22:155–75. https://doi.org/10.1016/j.jelekin.2011.11.008.
Brown S, Day S, Donnelly A. Indirect evidence of human skeletal muscle damage and collagen breakdown after eccentric muscle actions. J Sports Sci. 1999;17(5):397–402. https://doi.org/10.1080/026404199365911.
Takagi R, Ogasawara R, Tsutaki A, Nakazato K, Ishii N. Regional adaptation of collagen in skeletal muscle to repeated bouts of strenuous eccentric exercise. Pflugers Arch Eur J Physiol. 2016;468(9):1565–72. https://doi.org/10.1007/s00424-016-1860-3.
Koskinen SO, Ahtikoski AM, Komulainen J, Hesselink MK, Drost MR, Takala TE. Short-term effects of forced eccentric contractions on collagen synthesis and degradation in rat skeletal muscle. Pflugers Arch Eur J Physiol. 2002;444(1–2):59–72. https://doi.org/10.1007/s00424-002-0792-2.
Schleip R, Duerselen L, Vleeming A, Naylor IL, Lehmann-Horn F, Zorn A, et al. Strain hardening of fascia: static stretching of dense fibrous connective tissues can induce a temporary stiffness increase accompanied by enhanced matrix hydration. J Bodyw Mov Ther. 2012;16(19):94–100.
Pavan PG, Stecco A, Stern R, Stecco C. Painful connections: densification versus fibrosis of fascia. Curr Pain Headache Repo. 2014;18(8):441.
Konrad A, Tafilidis S, Tilp M, Konrad MA. Effects of acute static, ballistic, and PNF stretching exercise on the muscle and tendon tissue properties. Scand J Med Sci Sports. 2017;27(10):1070–80.
Clifford T, Ventress M, Allerton DM, Stansfield S, Tang JCY, Fraser WD, et al. The effects of collagen peptides on muscle damage, inflammation and bone turnover following exercise: a randomized, controlled trial. Amino Acids. 2019;51(4):691–704. https://doi.org/10.1007/s00726-019-02706-5.
Frey Law LA, Evans S, Knudtson J, Nus S, Scholl K, Sluka KA. Massage reduces pain perception and hyperalgesia in experimental muscle pain: a randomized, controlled trial. J Pain. 2008;9(8):714–21. https://doi.org/10.1016/j.jpain.2008.03.009.
Micklewright D. The effect of soft tissue release on delayed onset muscle soreness: a pilot study. Phys Ther Sport. 2009;10(1):19–24. https://doi.org/10.1016/j.ptsp.2008.09.003.
Zainuddin Z, Newton M, Sacco P, Nosaka K. Effects of massage on delayed-onset muscle soreness, swelling, and recovery of muscle function. J Athl Train. 2005;40(3):174–80.
Jay K, Sundstrup E, Søndergaard SD, Behm D, Brandt M, Særvoll CA, et al. Specific and cross over effects of massage for muscle soreness: randomized controlled trial. Int J Sports Phys Ther. 2014;9(1):82–91.
Macdonald GZ, Button DC, Drinkwater EJ, Behm DG. Foam rolling as a recovery tool after an intense bout of physical activity. Med Sci Sports Exerc. 2014;46(1):131–42. https://doi.org/10.1249/MSS.0b013e3182a123db.
Pearcey GEP, 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(1):5–13. https://doi.org/10.4085/1062-6050-50.1.01.
Romero-Moraleda B, La TR, Lerma-Lara S, Ferrer-Peña R, Paredes V, Peinado AB, et al. Neurodynamic mobilization and foam rolling improved delayed-onset muscle soreness in a healthy adult population: a randomized controlled clinical trial. PeerJ. 2017;2017(10):e3908. https://doi.org/10.7717/peerj.3908.
Zügel M, Maganaris CN, Wilke J, Jurkat-Rott K, Klingler W, Wearing SC, et al. Fascial tissue research in sports medicine: from molecules to tissue adaptation, injury and diagnostics: consensus statement. Br J Sport Med. 2018;52:1497. https://doi.org/10.1136/bjsports-2018-099308.