Extramuscular myofascial force transmission alters substantially the acute effects of surgical aponeurotomy: assessment by finite element modeling

  • Can A. YucesoyEmail author
  • Bart H. F. J. M. Koopman
  • Henk J. Grootenboer
  • Peter A. Huijing
Original Paper


Effects of extramuscular myofascial force transmission on the acute effects of aponeurotomy were studied using finite element modeling and implications of such effects on surgery were discussed. Aponeurotomized EDL muscle of the rat was modeled in two conditions: (1) fully isolated (2) with intact extramuscular connections. The specific goal was to assess the alterations in muscle length-force characteristics in relation to sarcomere length distributions and to investigate how the mechanical mechanism of the intervention is affected if the muscle is not isolated. Major effects of extramuscular myofascial force transmission were shown on muscle length-force characteristics. In contrast to the identical proximal and distal forces of the aponeurotomized isolated muscle, substantial proximo-distal force differences were shown for aponeurotomized muscle with extramuscular connections (for all muscle lengths F dist > F prox after distal muscle lengthening). Proximal optimal length did not change whereas distal optimal length was lower (by 0.5 mm). The optimal forces of the aponeurotomized muscle with extramuscular connections exerted at both proximal and distal tendons were lower than that of isolated muscle (by 15 and 7%, respectively). The length of the gap separating the two cut ends of the intervened aponeurosis decreases substantially due to extramuscular myofascial force transmission. The amplitude of the difference in gap length was muscle length dependent (maximally 11.6% of the gap length of the extramuscularly connected muscle). Extramuscular myofascial force transmission has substantial effects on distributions of lengths of sarcomeres within the muscle fiber populations distal and proximal to the location of intervention: (a) Within the distal population, the substantial sarcomere shortening at the proximal ends of muscle fibers due to the intervention remained unaffected however, extramuscular myofascial force transmission caused a more pronounced serial distribution towards the distal ends of muscle fibers. (b) In contrast, extramuscular myofascial force transmission limits the serial distribution of sarcomere lengths shown for the aponeurotomized isolated muscle in the proximal population. Fiber stress distributions showed that extramuscular myofascial force transmission causes most sarcomeres within the aponeurotomized muscle to attain lengths favorable for higher force exertion. It is concluded that acute effects of aponeurotomy on muscular mechanics are affected greatly by extramuscular myofascial force transmission. Such effects have important implications for the outcome of surgery performed to improve impeded function since muscle in vivo is not isolated both anatomically and mechanically.


Aponeurotomy Extramuscular myofascial force transmission Muscle length-force characteristics Sarcomere length distributions Finite element method Rat extensor digitorum longus (EDL) muscle 


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  1. Asakawa DS, Blemker SS, Gold GE, Delp SL (2002) In vivo motion of the rectus femoris muscle after tendon transfer surgery. J Biomech 35:1029–1037CrossRefGoogle Scholar
  2. Baumann JU, Koch HG (1989) Ventrale aponeurotische Verlängerung des Musculus Gastrocnemius. Oper Orthopaedie Traumatol 1:254–258CrossRefGoogle Scholar
  3. Berthier C, Blaineau S (1997) Supramolecular organization of the subsarcolemmal cytoskeleton of adult skeletal muscle fibers. A review. Biol Cell 89:413–434CrossRefGoogle Scholar
  4. Brunner R, Jaspers RT, Pel JJ, Huijing PA (2000) Acute and long-term effects on muscle force after intramuscular aponeurotic lengthening. Clin Orthopaed Relat Res 378:264–273CrossRefGoogle Scholar
  5. Delp SL, Ringwelski DA, Carroll NC (1994) Transfer of the rectus femoris: effects of transfer site on moment arms about the knee and hip. J Biomech 27:1201–1211CrossRefGoogle Scholar
  6. Dhawlikar SH, Root L, Mann RL (1992) Distal lengthening of the hamstrings in patients who have cerebral palsy. Long-term retrospective analysis. J Bone Joint Surg 74:1385–1391Google Scholar
  7. Friden J, Lieber RL (2003) Spastic muscle cells are shorter and stiffer than normal cells. Muscle Nerve 27:157–164CrossRefGoogle Scholar
  8. Gielen S (1998) A continuum approach to the mechanics of contracting skeletal muscle. PhD Thesis in Eindhoven University of Technology, Eindhoven, The NetherlandsGoogle Scholar
  9. Huijing PA (1999) Muscular force transmission: a unified, dual or multiple sytem? A review and some explorative experimental results. Arch Physiol Biochem 170:292–311CrossRefGoogle Scholar
  10. Huijing PA, Baan GC (2001) Extramuscular myofascial force transmission within the rat anterior tibial compartment: Proximo-distal differences in muscle force. Acta Physiol Scand 173:1–15CrossRefGoogle Scholar
  11. Huijing PA, Baan GC, Rebel G (1998) Non myo-tendinous force transmission in rat extensor digitorum longus muscle. J Exp Biol 201:682–691Google Scholar
  12. Huijing PA, Maas H, Baan GC (2003) Compartmental fasciotomy and isolating a muscle from neighboring muscles interfere with extramuscular myofascial force transmission within the rat anterior crural compartment. J Morphol 256:306–321CrossRefGoogle Scholar
  13. 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 24:841–849CrossRefGoogle Scholar
  14. 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 266:123–135CrossRefGoogle Scholar
  15. 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 32:71–79CrossRefGoogle Scholar
  16. 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 23:266–273CrossRefGoogle Scholar
  17. Johansson T, Meier P, Blickhan R (2000) A finite-element model for the mechanical analysis of skeletal muscles. J Theor Biol 206:131–149CrossRefGoogle Scholar
  18. Kreulen M, Smeulders MJ, Hage JJ, Huijing PA (2003) Biomechanical effects of dissecting flexor carpi ulnaris. J Bone Joint Surg Br 85:856–859Google Scholar
  19. Lieber RL, Runesson E, Einarsson F, Friden J (2003) Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material. Muscle Nerve 28:464–471CrossRefGoogle Scholar
  20. Maas H, Baan GC, Huijing PA (2001) Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle. J Biomech 34:927–940CrossRefGoogle Scholar
  21. Maas H, Baan GC, Huijing PA (2004) Muscle force is determined also by muscle relative position: isolated effects. J Biomech 37:99–110CrossRefGoogle Scholar
  22. Maas H, Baan GC, Huijing PA, Yucesoy CA, Koopman B HFJM, Grootenboer HJ (2003) The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finite element modeling. J Biomech Eng 125:745–753CrossRefGoogle Scholar
  23. Meijer K, Grootenboer HJ, Koopman HFJM, Huijing PA (1996) Isometric length-force curves during and after concentric contractions differ from the initial isometric length-force curve in rat muscle. J Appl Biomech 16:164–181Google Scholar
  24. 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 Physiol 522(Pt 3):503–513CrossRefGoogle Scholar
  25. 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 358:1453–1460CrossRefGoogle Scholar
  26. Reimers J (1990) Functional changes in the antagonists after lengthening the agonists in cerebral palsy. II. Quadriceps strength before and after distal hamstring lengthening. Clin Orthopaed Relat Res 253:35–37Google Scholar
  27. Riewald SA, Delp SL (1997) The action of the rectus femoris muscle following distal tendon transfer: does it generate knee flexion moment? Dev Med Child Neurol 39:99–105CrossRefGoogle Scholar
  28. Sinkjaer T, Magnussen I (1994) Passive, intrinsic and reflex-mediated stiffness in the ankle extensors of hemiparetic patients. Brain 117:355–363CrossRefGoogle Scholar
  29. Smeulders MJ (2004) Introducing intraoperative direct measurement of muscle force and myofascial force transmission in tendon transfer for cerebral palsy. PhD Thesis in Academic Medical Centre, Amsterdam University, AmsterdamGoogle Scholar
  30. Strumpf RK, Humphrey JD, Yin FC (1993) Biaxial mechanical properties of passive and tetanized canine diaphragm. J Biomech 265:469–475Google Scholar
  31. Suso S, Vicente P, Angles F (1985) Surgical treatment of the non-functional spastic hand. J Hand Surg 10:54–56Google Scholar
  32. 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 Rehabilit 63:97–102Google Scholar
  33. Trombitas K, Jin JP, Granzier H (1995) The mechanically active domain of titin in cardiac muscle. Circ Res 77:856–861Google Scholar
  34. van der Linden BJJJ (1998) Mechanical modeling of muscle functioning. PhD Thesis in Faculty of Mechanical Engineering, University of Twente, Enschede, The NetherlandsGoogle Scholar
  35. Willems ME, Huijing PA (1994) Heterogeneity of mean sarcomere length in different fibres: effects on length range of active force production in rat muscle. Euro J Appl Physiol Occup Physiol 68:489–496CrossRefGoogle Scholar
  36. Wohlfart B, Grimm AF, Edman KA (1977) Relationship between sarcomere length and active force in rabbit papillary muscle. Acta Physiol Scand 101:155–164CrossRefGoogle Scholar
  37. 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. Journal of Biomechanics 35:1253–1262CrossRefGoogle Scholar
  38. Yucesoy CA, Koopman HJFM, Baan GC, Grootenboer HJ, Huijing PA (2003) Extramuscular myofascial force transmission: experiments and finite element modeling. Arch Physiol Biochem 111:377–388CrossRefGoogle Scholar
  39. Yucesoy CA, Baan GC, Koopman HJFM, Grootenboer HJ, Huijing PA (2005) Pre-strained epimuscular connections cause muscular myofascial force transmission to affect properties of synergistic EHL and EDL muscles of the rat. J Biomech Eng 127:819–828CrossRefGoogle Scholar
  40. Yucesoy CA, Koopman HJFM, Grootenboer HJ, Huijing PA (2006a) Finite element modeling of aponeurotomy: altered intramuscular myofascial force transmission yields complex sarcomere length distributions determining acute effects. Biomech Model Mechanobiol (in press)Google Scholar
  41. Yucesoy CA, Maas H, Koopman HJFM, Grootenboer HJ, Huijing PA (2006b) Finite element modeling of relative position of a muscle: effects of extramuscular myofascial force transmission. Med Eng Phys 28:214–226CrossRefGoogle Scholar
  42. Yucesoy CA, Maas H, Koopman HJFM, Grootenboer HJ, Huijing PA (2006c) Mechanisms causing effects of muscle position on proximo-distal muscle force differences in extra-muscular myofascial force transmission. Medical Engineering and Physics 28:214–226CrossRefGoogle Scholar
  43. 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 27:445–453CrossRefGoogle Scholar
  44. 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 28:83–87CrossRefGoogle Scholar
  45. Zwick EB, Saraph V, Zwick G, Steinwender C, Linhart W E, Steinwender G (2002) Medial hamstring lengthening in the presence of hip flexor tightness in spastic diplegia. Gait Posture 16:288–296CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Can A. Yucesoy
    • 1
    • 2
    • 3
    Email author
  • Bart H. F. J. M. Koopman
    • 3
  • Henk J. Grootenboer
    • 3
  • Peter A. Huijing
    • 2
    • 3
  1. 1.Biomedical Engineering InstituteBoğaziçi UniversityBebek – IstanbulTurkey
  2. 2.Instituut voor Fundamentele en Klinische Bewegingswetenschappen, Faculteit BewegingswetenschappenVrije UniversiteitAmsterdamThe Netherlands
  3. 3.Integrated Biomedical Engineering for Restoration of Human Function, Faculteit Constructieve Technische WetenschappenUniversiteit TwenteEnschedeThe Netherlands

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