Restricted accessResearch articleFirst published online 2021-8
Chronic Sequelae After Muscle Strain Injuries: Influence of Heavy Resistance Training on Functional and Structural Characteristics in a Randomized Controlled Trial
Muscle strain injury leads to a high risk of recurrent injury in sports and can cause long-term symptoms such as weakness and pain. Scar tissue formation after strain injuries has been described, yet what ultrastructural changes might occur in the chronic phase of this injury have not. It is also unknown if persistent symptoms and morphological abnormalities of the tissue can be mitigated by strength training.
Purpose:
To investigate if heavy resistance training improves symptoms and structural abnormalities after strain injuries.
Study Design:
Randomized controlled trial; Level of evidence, 1.
Methods:
A total of 30 participants with long-term weakness and/or pain after a strain injury of the thigh or calf muscles were randomized to eccentric heavy resistance training of the injured region or control exercises of the back and abdominal muscle. Isokinetic (hamstring) or isometric (calf) muscle strength was determined, muscle cross-sectional area measured, and pain and function evaluated. Scar tissue ultrastructure was determined from biopsy specimens taken from the injured area before and after the training intervention.
Results:
Heavy resistance training over 3 months improved pain and function, normalized muscle strength deficits, and increased muscle cross-sectional area in the previously injured region. No systematic effect of training was found upon pathologic infiltration of fat and blood vessels into the previously injured area. Control exercises had no effect on strength, cross-sectional area, or scar tissue but a positive effect on patient-related outcome measures, such as pain and functional scores.
Conclusion:
Short-term strength training can improve sequelae symptoms and optimize muscle function even many years after a strain injury, but it does not seem to influence the overall structural abnormalities of the area with scar tissue.
Arentson-LantzEJEnglishKLPaddon-JonesDFryCS. Fourteen days of bed rest induces a decline in satellite cell content and robust atrophy of skeletal muscle fibers in middle-aged adults. J Appl Physiol. 2016;120(8):965-975. doi:10.1152/japplphysiol.00799.2015
2.
ArrighiNMoratalCClémentN, et al. Characterization of adipocytes derived from fibro/adipogenic progenitors resident in human skeletal muscle. Cell Death Dis. 2015;6:e1733. doi:10.1038/cddis.2015.79
3.
BayerMLBangLHoegberget-KaliszM, et al. Muscle-strain injury exudate favors acute tissue healing and prolonged connective tissue formation in humans. FASEB J. Published online June18, 2019. doi:10.1096/fj.201900542r
4.
BayerMLHoegberget-KaliszMJensenMH, et al. Role of tissue perfusion, muscle strength recovery and pain in rehabilitation after acute muscle strain injury: a randomized controlled trial comparing early and delayed rehabilitation. Scand J Med Sci Sports. 2018;28(12):2579-2591. doi:10.1111/sms.13269
5.
BayerMLMagnussonSPPKjaerM. Early versus delayed rehabilitation after acute muscle injury. N Engl J Med. 2017;377(13):1300-1301. doi:10.1056/NEJMc1708134
6.
BayerMLSchjerlingPHerchenhanA, et al. Release of tensile strain on engineered human tendon tissue disturbs cell adhesions, changes matrix architecture, and induces an inflammatory phenotype. PLoS One. 2014;9(1):e86078. doi:10.1371/journal.pone.0086078
7.
BielerTMagnussonSPKjaerMBeyerN. Intra-rater reliability and agreement of muscle strength, power and functional performance measures in patients with hip osteoarthritis. J Rehabil Med. 2014;46(10):997-1005. doi:10.2340/16501977-1864
8.
BoesenAPDideriksenKCouppéC, et al. Tendon and skeletal muscle matrix gene expression and functional responses to immobilisation and rehabilitation in young males: effect of growth hormone administration. J Physiol. 2013;5912323(591):6039-6052. doi:10.1113/jphysiol .2013.261263
9.
BrughelliMCroninJMendiguchiaJKinsellaDNosakaK. Contralateral leg deficits in kinetic and kinematic variables during running in Australian rules football players with previous hamstring injuries. J Strength Cond Res. 2010;24(9):2539-2544. doi:10.1519/JSC.0b013e3181b603ef
10.
CharltonPCRaysmithBWollinM, et al. Knee flexion not hip extension strength is persistently reduced following hamstring strain injury in Australian football athletes: implications for periodic health examinations. J Sci Med Sport. 2018;21(10):999-1003. doi:10.1016/j.jsams.2018.03.014
11.
ClarksonPMHubalMJ. Exercise-induced muscle damage in humans. Am J Phys Med Rehabil. 2002;81(11):S52-S69. doi:10.1097/00002060-200211001-00007
12.
CorrDTGallant-BehmCLShriveNGHartDA. Biomechanical behavior of scar tissue and uninjured skin in a porcine model. Wound Repair Regen. 2009;17(2):250-259. doi:10.1111/j.1524-475X.2009.00463.x
13.
CorrDTHartDA. Biomechanics of scar tissue and uninjured skin. Adv Wound Care. 2013;2(2):37-43. doi:10.1089/wound.2011.0321
14.
CrameriRMAagaardPQvortrupKLangbergHOlesenJKjaerM. Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol. 2007;583(pt 1):365-380. doi:10.1113/jphysiol.2007.128827
15.
DammoneGKarazSLukjanenkoL, et al. PPARγ controls ectopic adipogenesis and cross-talks with myogenesis during skeletal muscle regeneration. Int J Mol Sci. 2018;19(7):2044. doi:10.3390/ijms19072044
16.
EkstrandJWaldénMHägglundM. Hamstring injuries have increased by 4% annually in men’s professional football, since 2001: a 13-year longitudinal analysis of the UEFA Elite Club injury study. Br J Sports Med. 2016;50(12):731-737. doi:10.1136/bjsports-2015-095359
17.
EliassonPCouppéCLonsdaleM, et al. Ruptured human Achilles tendon has elevated metabolic activity up to 1 year after repair. Eur J Nucl Med Mol Imaging. 2016;43(10):1868-1877. doi:10.1007/s00259-016-3379-4
18.
EngebretsenAHMyklebustGHolmeIEngebretsenLBahrR. Intrinsic risk factors for hamstring injuries among male soccer players: a prospective cohort study. Am J Sports Med. 2010;38(6): 1147-1153. doi:10.1177/0363546509358381
19.
FeeleyBTLiuMMaCB, et al. Human rotator cuff tears have an endogenous, inducible stem cell source capable of improving muscle quality and function after rotator cuff repair. Am J Sports Med. 2020;48(11):2660-2668. doi:10.1177/0363546520935855
20.
FloresDVGómezCMEstrada-CastrillónMSmitamanEPathriaMN. MR imaging of muscle trauma: anatomy, biomechanics, pathophysiology, and imaging appearance. Radiographics. 2018;38(1): 124-148. doi:10.1148/rg.2018170072
21.
FryCSJohnsonDLIrelandMLNoehrenB. ACL injury reduces satellite cell abundance and promotes fibrogenic cell expansion within skeletal muscle. J Orthop Res. 2017;35(9):1876-1885. doi:10.1002/jor.23502
22.
GarciaANCostaLDCMHancockMJ, et al. McKenzie method of mechanical diagnosis and therapy was slightly more effective than placebo for pain, but not for disability, in patients with chronic non-specific low back pain: a randomised placebo controlled trial with short and longer term follow-up. Br J Sports Med. 2018;52(9):594-598. doi:10.1136/bjsports-2016-097327
23.
GardnerKArnoczkySPCaballeroOLavagninoM. The effect of stress-deprivation and cyclic loading on the TIMP/MMP ratio in tendon cells: an in vitro experimental study. Disabil Rehabil. 2008;30(20-22):1523-1529. doi:10.1080/09638280701785395
24.
GerberCSchneebergerAGHoppelerHMeyerDC. Correlation of atrophy and fatty infiltration on strength and integrity of rotator cuff repairs: a study in thirteen patients. J Shoulder Elbow Surg. 2007;16(6):691-696. doi:10.1016/j.jse.2007.02.122
25.
GladstoneJNBishopJYLoIKYFlatowEL. Fatty infiltration and atrophy of the rotator cuff do not improve after rotator cuff repair and correlate with poor functional outcome. Am J Sports Med. 2007;35(5):719-728. doi:10.1177/0363546506297539
26.
GoodeAPReimanMPHarrisL, et al. Eccentric training for prevention of hamstring injuries may depend on intervention compliance: a systematic review and meta-analysis. Br J Sports Med. 2015;49(6):349-356. doi:10.1136/bjsports-2014-093466
27.
GoutallierDPostelJMBernageauJLavauLVoisinMC. Fatty muscle degeneration in cuff ruptures: pre- and postoperative evaluation by CT scan. Clin Orthop Relat Res. 1994;304:78-83.
28.
GreenBPizzariT. Calf muscle strain injuries in sport: a systematic review of risk factors for injury. Br J Sports Med. 2017;51(16):1189-1194. doi:10.1136/bjsports-2016-097177
29.
GumucioJPKornMASaripalliAL, et al. Aging-associated exacerbation in fatty degeneration and infiltration after rotator cuff tear. J Shoulder Elbow Surg. 2014;23(1):99-108. doi:10.1016/j.jse.2013.04.011
30.
GumucioJPQasawaAHFerraraPJ, et al. Reduced mitochondrial lipid oxidation leads to fat accumulation in myosteatosis. FASEB J. 2019;33(7):7863-7881. doi:10.1096/fj.201802457RR
31.
HägglundMWaldénMEkstrandJ. Injury recurrence is lower at the highest professional football level than at national and amateur levels: does sports medicine and sports physiotherapy deliver?Br J Sports Med. 2016;50(12):751-758. doi:10.1136/bjsports-2015-095951
32.
HortobágyiTDempseyLFraserD, et al. Changes in muscle strength, muscle fibre size and myofibrillar gene expression after immobilization and retraining in humans. J Physiol. 2000;524(1): 293-304. doi:10.1111/j.1469-7793.2000.00293.x
33.
JoeAWBYiLNatarajanA, et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol. 2010;12(2):153-163. doi:10.1038/ncb2015
34.
KjærMLangbergHHeinemeierK, et al. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports. 2009;19(4):500-510. doi:10.1111/j.1600-0838.2009.00986.x
35.
LauritzenFPaulsenGRaastadTBergersenLHOweSG. Gross ultrastructural changes and necrotic fiber segments in elbow flexor muscles after maximal voluntary eccentric action in humans. J Appl Physiol. 2009;107(6):1923-1934. doi:10.1152/japplphysiol.001 48.2009
36.
LemosDRBabaeijandaghiFLowM, et al. Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nat Med. 2015;21(7):786-794. doi:10.1038/nm.3869
37.
LiRNariciMVErskineRM, et al. Costamere remodeling with muscle loading and unloading in healthy young men. J Anat. 2013; 223(5):525-536. doi:10.1111/joa.12101
38.
LordCBlazevichAJDrinkwaterEJMa’ayahF. Greater loss of horizontal force after a repeated-sprint test in footballers with a previous hamstring injury. J Sci Med Sport. 2019;22(1):16-21. doi:10.1016/j.jsams.2018.06.008
39.
MackeyALBrandstetterSSchjerlingP, et al. Sequenced response of extracellular matrix deadhesion and fibrotic regulators after muscle damage is involved in protection against future injury in human skeletal muscle. FASEB J. 2011;25(6):1943-1959. doi:10.1096/fj.10-176487
40.
MackeyALKjaerM. The breaking and making of healthy adult human skeletal muscle in vivo. Skelet Muscle. 2017;7(1):1-18. doi:10.1186/s13395-017-0142-x
41.
MagnussonSPKjaerM. The impact of loading, unloading, ageing and injury on the human tendon. J Physiol. 2019;597(5):1283-1298. doi:10.1113/JP275450
42.
MatthewsTJW. Pathology of the torn rotator cuff tendon: reduction in potential for repair as tear size increases. J Bone Joint Surg Br. 2006;88(4):489-495. doi:10.1302/0301-620X.88B4.16845
43.
MelisBDefrancoMJChuinardCWalchG. Natural history of fatty infiltration and atrophy of the supraspinatus muscle in rotator cuff tears. Clin Orthop Relat Res. 2010;468(6):1498-1505. doi:10.1007/s11999-009-1207-x
44.
MeyerDCHoppelerHvon RechenbergBGerberC. A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthop Res. 2004;22(5):1004-1007. doi:10.1016/j.orthres.2004.02.009
NatarajanALemosDRRossiFMV. Fibro/adipogenic progenitors: a double-edged sword in skeletal muscle regeneration. Cell Cycle. 2010;9(11):2045-2046. doi:10.4161/cc.9.11.11854
47.
PaulsenGLauritzenFBayerML, et al. Subcellular movement and expression of HSP27, αB-crystallin, and HSP70 after two bouts of eccentric exercise in humans. J Appl Physiol (1985). 2009;107(2): 570-582. doi:10.1152/japplphysiol.00209.2009
48.
PetersenJThorborgKNielsenMBBudtz-JørgensenEHölmichP. Preventive effect of eccentric training on acute hamstring injuries in men’s soccer: a cluster-randomized controlled trial. Am J Sports Med. 2011;39(11):2296-2303. doi:10.1177/0363546511419277
49.
PizzariTGreenBvan DykN. Extrinsic and intrinsic risk factors associated with hamstring injury. In: ThorborgKOparDAShieldAJ, eds. Prevention and Rehabilitation of Hamstring Injuries. Springer; 2020:83-115. doi:10.1007/978-3-030-31638-9
50.
ReurinkGAlmusaEGoudswaardGJ, et al. No association between fibrosis on magnetic resonance imaging at return to play and hamstring reinjury risk. Am J Sports Med. 2015;43(5):1228-1234. doi:10.1177/0363546515572603
51.
ReurinkGGoudswaardGJATolJL, et al. MRI observations at return to play of clinically recovered hamstring injuries. Br J Sports Med. 2014;48(18):1370-1376. doi:10.1136/bjsports-2013-092450
52.
Ribeiro-AlvaresJBOliveiraGDSDe Lima-E-SilvaFXBaroniBM. Eccentric knee flexor strength of professional football players with and without hamstring injury in the prior season. Eur J Sport Sci. Published online March26, 2020. doi:10.1080/17461391.2020.1743766
53.
RiceDNijsJKosekE, et al. Exercise-induced hypoalgesia in pain-free and chronic pain populations: state of the art and future directions. J Pain. 2019;20(11):1249-1266. doi:10.1016/j.jpain.2019.03.005
54.
SanfilippoJLSilderASherryMATuiteMJHeiderscheitBC. Hamstring strength and morphology progression after return to sport from injury. Med Sci Sports Exerc. 2013;45(3):448-454. doi:10.1249/MSS.0b013e3182776eff
55.
SilderAHeiderscheitBCThelenDGEnrightTTuiteMJ. MR observations of long-term musculotendon remodeling following a hamstring strain injury. Skeletal Radiol. 2008;37(12):1101-1109. doi:10.1007/s00256-008-0546-0
56.
SilderAReederSBThelenDG. The influence of prior hamstring injury on lengthening muscle tissue mechanics. J Biomech. 2010;43(12):2254-2260. doi:10.1016/j.jbiomech.2010.02.038
57.
SullivanGMFeinnR. Using effect size—or why the P value is not enough. J Grad Med Educ. 2012;4(3):279-282. doi:10.4300/JGME-D-12-00156.1
58.
TidballJGChanM. Adhesive strength of single muscle cells to basement membrane at myotendinous junctions. J Appl Physiol. 1989;67(3):1063-1069. doi:10.1152/jappl.1989.67.3.1063
59.
TidballJGDanielTL. Myotendinous junctions of tonic muscle cells: structure and loading. Cell Tissue Res. 1986;245(2):315-322. doi:10.1007/BF00213937
60.
TidballJGSalemGZernickeR. Site and mechanical conditions for failure of skeletal muscle in experimental strain injuries. J Appl Physiol. 1993;74(3):1280-1286. doi:10.1152/jappl.1993.74.3.1280
61.
UezumiAItoTMorikawaD, et al. Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J Cell Sci. 2011;124(pt 21):3654-3664. doi:10.1242/jcs.086629
62.
WieserKJoshyJFilliL, et al. Changes of supraspinatus muscle volume and fat fraction after successful or failed arthroscopic rotator cuff repair. Am J Sports Med. 2019;47(13):3080-3088. doi:10.1177/0363546519876289
63.
WynnTARamalingamTR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med. 2012;18(7):1028-1040. doi:10.1038/nm.2807
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
