Skip to main content
Log in

Finite element modeling of aponeurotomy: altered intramuscular myofascial force transmission yields complex sarcomere length distributions determining acute effects

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

Finite element modeling of aponeurotomized rat extensor digitorium longus muscle was performed to investigate the acute effects of proximal aponeurotomy. The specific goal was to assess the changes in lengths of sarcomeres within aponeurotomized muscle and to explain how the intervention leads to alterations in muscle length–force characteristics. Major changes in muscle length–active force characteristics were shown for the aponeurotomized muscle modeled with (1) only a discontinuity in the proximal aponeurosis and (2) with additional discontinuities of the muscles’ extracellular matrix (i.e., when both myotendinous and myofascial force transmission mechanisms are interfered with). After muscle lengthening, two cut ends of the aponeurosis were separated by a gap. After intervention (1), only active slack length increased (by approximately 0.9  mm) and limited reductions in muscle active force were found (e.g., muscle optimum force decreased by only 1%) After intervention (2) active slack increased further (by 1.2 mm) and optimum length as well (by 2.0 mm) shifted and the range between these lengths increased. In addition, muscle active force was reduced substantially (e.g., muscle optimum force decreased by 21%). The modeled tearing of the intramuscular connective tissue divides the muscle into a proximal and a distal population of muscle fibers. The altered force transmission was shown to lead to major sarcomere length distributions [not encountered in the intact muscle and after intervention (1)], with contrasting effects for the two muscle fiber populations: (a) Within the distal population (i.e. fibers with no myotendinous connection to the muscles’ origin), sarcomeres were much shorter than within the proximal population (fibers with intact myotendinous junction at both ends). (b) Within the distal population, from proximal ends of muscle fibers to distal ends, the serial distribution of sarcomere lengths ranged from the lowest length to high lengths. In contrast within the proximal population, the direction of the distribution was reversed. Such differences in distribution of sarcomere lengths between the proximal and distal fiber populations explain the shifts in muscle active slack and optimal lengths. Muscle force reduction after intervention (2) is explained primarily by the short sarcomeres within the distal population. However, fiber stress distributions showed contribution of the majority of the sarcomeres to muscle force: myofascial force transmission prevents the sarcomeres from shortening to nonphysiological lengths. It is concluded that interfering with the intramuscular myofascial force transmission due to rupturing of the intramuscular connective tissue leads to a complex distribution of sarcomere lengths within the aponeurotomized muscle and this determines the acute effects of the intervention on muscle length–force characteristics rather than the intervention with the myotendinous force transmission after which the intervention was named. These results suggest that during surgery, but also postoperatively, major attention should be focused on the length and activity of aponeurotomized muscle, as changes in connective tissue tear depth will affect the acute effects of the intervention.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baumann JU, Koch HG (1989) Ventrale aponeurotische Verlangerung des Musculus Gastrocnemius. Oper Orthop Traumatol 1:254–258

    Article  Google Scholar 

  • Berthier C, Blaineau S (1997) Supramolecular organization of the subsarcolemmal cytoskeleton of adult skeletal muscle fibers. A review. Biol Cell 89:413–434

    Article  Google Scholar 

  • Booth CM, Cortina-Borja MJ, Theologis TN (2001) Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol 43:314–320

    Article  Google Scholar 

  • Brunner R, Jaspers RT, Pel JJ, Huijing PA (2000) Acute and long-term effects on muscle force after intramuscular aponeurotic lengthening. Clin Orthop Relat Res 378:264–273

    Article  Google Scholar 

  • Campbell KP (1995) Three muscular dystrophies: loss of cytoskeleton–extracellular matrix linkage. Cell 80:675–679

    Article  Google Scholar 

  • Ejeskar A (1982) Finger flexion force and hand grip strength after tendon repair. J Hand Surg 7:61–65

    Google Scholar 

  • Friden J, Lieber RL (2003) Spastic muscle cells are shorter and stiffer than normal cells. Muscle Nerve 27:157–164

    Article  Google Scholar 

  • Gielen S (1998) A continuum approach to the mechanics of contracting skeletal muscle. PhD thesis Eindhoven University of Technology, Eindhoven, The Netherlands

  • Hawkins D, Bey M (1997) Muscle and tendon force–length properties and their interactions in vivo. J Biomech 30:63–70

    Article  Google Scholar 

  • Hijikata T, Wakisaka H, Niida S (1993) Functional combination of tapering profiles and overlapping arrangements in nonspanning skeletal muscle fibers terminating intrafascicularly. Anat Rec 236:602–610

    Article  Google Scholar 

  • Huijing PA (1998) Muscle the motor of movement: properties in function, experiment and modeling. J Electromyogr Kinesiol 8:61–77

    Article  Google Scholar 

  • Huijing PA (1999a) Muscle as a collagen fiber reinforced composite material: force transmission in muscle and whole limbs. J Biomech 32:329–345

    Article  Google Scholar 

  • Huijing PA (1999b) Muscular force transmission: a unified, dual or multiple sytem? A review and some explorative experimental results. Arch Physiol Biochem 170:292–311

    Article  Google Scholar 

  • Huijing PA, Baan GC, Rebel G (1998) Non myo-tendinous force transmission in rat extensor digitorum longus muscle. J Exp Biol 201:682–691

    Google Scholar 

  • Huyghe JM, van Campen DH, Arts T, Heethaar RM (1991) The constitutive behaviour of passive heart muscle tissue: a quasi-linear viscoelastic formulation. J Biomech 24:841–849

    Article  Google Scholar 

  • Jaspers RT, Brunner R, Pel JJM, Huijing PA (1999) Acute effects of intramuscular aponeurotomy on rat GM Force transmission, muscle force and sarcomere length. J Biomech 32:71–79

    Article  Google Scholar 

  • Jaspers RT, Brunner R, Baan GC, Huijing PA (2002) Acute effects of intramuscular aponeurotomy and tenotomy on multitendoned rat EDL: indications for local adaptation of intramuscular connective tissue. Anat Rec 266:123–135

    Article  Google Scholar 

  • Jaspers RT, Brunner R, Riede UN, Huijing PA (2005) Healing of the aponeurosis during recovery from aponeurotomy: morphological and histological adaptation and related changes in mechanical properties. J Orthop Res 23:266–273

    Article  Google Scholar 

  • Johansson T, Meier P, Blickhan R (2000) A finite-element model for the mechanical analysis of skeletal muscles. J Theor Biol 206:131–149

    Article  Google Scholar 

  • Jung D, Duclos F, Apostol B, Straub V, Lee JC, Allamand V, Venzke DP, Sunada Y, Moomaw CR, Leveille CJ, Slaughter CA, Crawford TO, McPherson JD, Campbell KP (1996) Characterization of delta-sarcoglycan, a novel component of the oligomeric sarcoglycan complex involved in limb-girdle muscular dystrophy. J Biol Chem 271:32321–32329

    Article  Google Scholar 

  • Lieber RL, Friden J (1997) Intraoperative measurement and biomechanical modeling of the flexor carpi ulnaris-to-extensor carpi radialis longus tendon transfer. J Biomech. Eng 119:386–391

    Google Scholar 

  • Morgan DL, Whitehead NP, Wise AK, Gregory JE, Proske U (2000) Tension changes in the cat soleus muscle following slow stretch or shortening of the contracting muscle. J of Physiol 522(Pt 3):503–513

    Article  Google Scholar 

  • Nather A, Fulford GE, Stewart K (1984) Treatment of valgus hindfoot in cerebral palsy by peroneus brevis lengthening. Dev Med Child Neurol 26:335–340

    Article  Google Scholar 

  • Nene AV, Evans GA, Patrick JH (1993) Simultaneous multiple operations for spastic diplegia. Outcome and functional assessment of walking in 18 patients. J Bone Joint Surg 75B:488–494

    Google Scholar 

  • Ohlendieck K (1996) Towards an understanding of the dystrophin–glycoprotein complex: linkage between the extracellular matrix and the membrane cytoskeleton in muscle fibers. Eur J Cell Biol 69:1–10

    Google Scholar 

  • Olney BW, Williams PF, Menelaus MB (1988) Treatment of spastic equinus by aponeurosis lengthening. J Pediatr Orthop 8:422–425

    Google Scholar 

  • Oomens CW, Maenhout M, van Oijen CH, Drost MR, Baaijens FP (2003) Finite element modelling of contracting skeletal muscle. Philos Trans Roy Soc Lond Ser B Biol Sci 358:1453–1460

    Article  Google Scholar 

  • Ramsey RW, Street SF (1940) The isometric length-tension diagram of isolated skeletal muscle fibers of the frog. J Cell Comp Physiol 15:11–34

    Article  Google Scholar 

  • Reimers J (1990) Functional changes in the antagonists after lengthening the agonists in cerebral palsy. I. Triceps surae lengthening. Clin Orthop Relat Res 253:30–34

    Google Scholar 

  • Rekveldt MGC (1999) Finite element modeling of aponeurotomy. M.Sc. thesis, in Faculty of Mechanical Engineering, University of Twente, Enschede, The Netherlands

  • Sinkjaer T, Magnussen I (1994) Passive, intrinsic and reflex-mediated stiffness in the ankle extensors of hemiparetic patients. Brain 117:355–363

    Article  Google Scholar 

  • Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114:346–364

    Article  Google Scholar 

  • Street SF, Ramsey RW (1965) Sarcolemma: transmitter of active tension in frog skeletal muscle. Science 149:1379–1380

    Article  Google Scholar 

  • Suso S, Vicente P, Angles F (1985) Surgical treatment of the non-functional spastic hand. J Hand Surg 10:54–56

    Google Scholar 

  • Tardieu C, Huet de la Tour E, Bret MD, Tardieu G (1982) Muscle hypoextensibility in children with cerebral palsy: I. Clinical and experimental observations. Arch Phys Med Rehabil 63:97–102

    Google Scholar 

  • Trombitas K, Jin JP, Granzier H (1995) The mechanically active domain of titin in cardiac muscle. Circ Res 77:856–861

    Google Scholar 

  • Trotter JA, Purslow PP (1992) Functional morphology of the endomysium in series fibered muscles. J Morphol 212:109–122

    Article  Google Scholar 

  • Trotter JA, Richmond FJ, Purslow PP (1995) Functional morphology and motor control of series-fibered muscles. Exerc Sport Sci Rev 23:167–213

    Article  Google Scholar 

  • van der Linden BJJJ (1998) Mechanical modeling of muscle functioning. PhD thesis, Faculty of Mechanical Engineering, University of Twente, Enschede, The Netherlands

  • Willems ME, Huijing PA (1994) Heterogeneity of mean sarcomere length in different fibres: effects on length range of active force production in rat muscle. Eur J Appl Physiol Occup Physiol 68:489–496

    Google Scholar 

  • Wohlfart B, Grimm AF, Edman KA (1977) Relationship between sarcomere length and active force in rabbit papillary muscle. Acta Physiol Scand 101:155–164

    Article  Google Scholar 

  • Yucesoy CA, Koopman HJFM, Huijing PA, Grootenboer HJ (2002) Three-dimensional finite element modeling of skeletal muscle using a two-domain approach: linked fiber–matrix mesh model. J Biomech 35:1253–1262

    Article  Google Scholar 

  • Zuurbier CJ, Everard AJ, van der Wees P, Huijing PA (1994) Length–force characteristics of the aponeurosis in the passive and active muscle condition and in the isolated condition. J Biomech 27:445–453

    Article  Google Scholar 

  • Zuurbier CJ, Heslinga JW, Lee-de Groot MB, Van der Laarse WJ (1995) Mean sarcomere length–force relationship of rat muscle fibre bundles. J Biomech 28:83–87

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Can A. Yucesoy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yucesoy, C.A., Koopman, B.H.F.J.M., Grootenboer, H.J. et al. Finite element modeling of aponeurotomy: altered intramuscular myofascial force transmission yields complex sarcomere length distributions determining acute effects. Biomech Model Mechanobiol 6, 227–243 (2007). https://doi.org/10.1007/s10237-006-0051-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-006-0051-0

Keywords

Navigation