Myofascial force transmission and tendon transfer for patients suffering from spastic paresis: A review and some new observations

doi:10.1016/j.jelekin.2007.02.002

Journal of Electromyography and Kinesiology

Volume 17, Issue 6, December 2007, Pages 644-656

https://doi.org/10.1016/j.jelekin.2007.02.002 Get rights and content

Abstract

The current rationale of clinical practice in spastic tendon transfer surgery is based on four assumptions: (1) changes in muscle fiber length (serial number of sarcomeres) determine the available length range and joint excursion, (2) muscle cross-sectional area determines the maximal force output, (3) fiber length and muscle force are invariable functions of muscle length, (4) there is an invariable relation between the elastic force and the active force exerted by the sarcomeres. The validity of these assumptions is discussed. Additionally, some new perspectives in muscle research are discussed and myofascial force transmission is introduced as a co-determinant for the outcome of tendon transfer by presenting some exploratory observations.

Section snippets

Tendon transfer surgery in cerebral palsy

Medicine has progressed to a discipline for which survival of patients is no longer the sole criteria for success. Instead, demands are higher and treatments are being optimized for conservation and restoration of maximal well-being of the patient. To accomplish this goal, current clinical medicine demands a scientific rationale for therapy, and such therapy to be dosed optimally for the individual patient. This certainly applies to the treatment of patients suffering from the neurological

Spastic muscles

Tendon transfer is not limited to the treatment of effects of spastic paresis. On the contrary, it has been used for long to restore lost functions after for instance plexus brachialis injuries, tendon ruptures, and tetraplegia. The important differences between the treatment for these indications and that of spastic paresis is that in principle healthy muscles are used to restore a completely lost function, whereas the main concept of tendon transfer of a spastic muscle is that an improvement

Current rationale of clinical practice

Muscle architecture is classically conceptualized as a typical assembly of muscle fibers converging onto a tendon. Each isolated muscle is considered to have a unique capacity to exert a pulling force produced by shortening of the muscle belly and transmitted through its tendon to a target outside the muscle. This unique capacity is a reflection of the specific architecture of the muscle. The length change of the muscle fibers is considered a parameter that determines the available muscle

Myofascial force transmission as a co-determinant of muscle function

Our hypothesis is that also in vivo, a muscle’s capacity to exert force at a particular tendon is determined by more than the length-, and cross-sectional area of the muscle belly. As such, the relation between force at the tendon and muscle–tendon complex length is not an invariable characteristic of a muscle, but is co-determined by the fraction of force transmitted to the myofascial pathway. See also Yucesoy and Huijing in the present issue (Yucesoy and Huijing, 2007).

This fraction is

Concluding remarks

Despite many years of research, the understanding of in vivo functioning of skeletal muscle is still limited. It is, however, obvious that many factors co-determine a muscle’s functioning and that these factors cannot be derived from the muscle architectural characteristics alone. Recent work, see elsewhere within this journal issue, indicates that such factors may be located even within antagonistic muscle groups and their compartments, adjacent to the target muscle or even located further

Mark JC Smeulders was granted the degree of Doctorandus in Human Movement Sciences (i.e. Drs, which is equivalent to having passed the preliminary oral examinations of a Ph.D. program). at the Vrije Universiteit in Amsterdam (1998), and a Ph.D. degree at the University of Amsterdam (2004). He is presently working as director of research at the Department of Plastic, Reconstructive and Hand Surgery of the Academic Medical Center in Amsterdam. In addition, he is studying for his M.D. His main

References (91)

A. Arampatzis et al.
Effect of different ankle- and knee-joint positions on gastrocnemius medialis fascicle length and EMG activity during isometric plantar flexion
J Biomech
(2006)
D.S. Asakawa et al.
In vivo motion of the rectus femoris muscle after tendon transfer surgery
J Biomech
(2002)
P.W. Brand et al.
Relative tension and potential excursion of muscles in the forearm and hand
J Hand Surgery [Am]
(1981)
G.J. Ettema et al.
Properties of the tendinous structures and series elastic component of EDL muscle–tendon complex of the rat
J Biomech
(1989)
A.A. Freehafer et al.
Determination of muscle–tendon unit properties during tendon transfer
J Hand Surgery [Am]
(1979)
J. Friden et al.
Evidence for muscle attachment at relatively long lengths in tendon transfer surgery
J Hand Surgery [Am]
(1998)
J. Friden et al.
Mechanical considerations in the design of surgical reconstructive procedures
J Biomech
(2002)
J. Friden et al.
Effect of muscle tension during tendon transfer on sarcomerogenesis in a rabbit model
J Hand Surgery [Am]
(2000)
J.L. Goldner
Surgical reconstruction of the upper extremity in cerebral palsy
Hand Clin
(1988)
A.M. Herrmann et al.
Moment arm and force-generating capacity of the extensor carpi ulnaris after transfer to the extensor carpi radialis brevis
J Hand Surgery [Am]
(1999)

P.A. Huijing

Muscle, the motor of movement: properties in function, experiment and modelling

J Electromyogr Kinesiol

(1998)

P.A. Huijing

Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb

J Biomech

(1999)

P.A. Huijing

Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis

J Electromyogr Kinesiol

(2007)

P.A. Huijing et al.

Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles

J Electromyogr Kinesiol

(2007)

S.H. Kozin et al.

In vivo determination of available brachioradialis excursion during tetraplegia reconstruction

J Hand Surgery [Am]

(2001)

M. Kreulen et al.

Three-dimensional video analysis of forearm rotation before and after combined pronator teres rerouting and flexor carpi ulnaris tendon transfer surgery in patients with cerebral palsy

J Hand Surgery [Br]

(2004)

C. Leclercq

General assessment of the upper limb

Hand Clin

(2003)

R.L. Lieber et al.

Architecture of selected muscles of the arm and forearm: anatomy and implications for tendon transfer

J Hand Surgery [Am]

(1992)

R.L. Lieber et al.

Sarcomere length changes after flexor carpi ulnaris to extensor digitorum communis tendon transfer

J Hand Surgery [Am]

(1996)

R.L. Lieber et al.

Analysis of posterior deltoid function one year after surgical restoration of elbow extension

J Hand Surgery [Am]

(2003)

R.L. Lieber et al.

Biomechanical properties of the brachioradialis muscle: implications for surgical tendon transfer

J Hand Surgery [Am]

(2005)

G.J. Loren et al.

Tendon biomechanical properties enhance human wrist muscle specialization

J Biomech

(1995)

G.J. Loren et al.

Human wrist motors: biomechanical design and application to tendon transfers

J Biomech

(1996)

R. Malaiya et al.

The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy

J Electromyogr Kinesiol

(2007)

H.J.M. Meijer et al.

Myofascial force transmission between antagonistic rat lower limb muscles: effects of single muscle or muscle group lengthening

J Electromyogr Kinesiol

(2007)

J.M. Rijkelijkhuizen et al.

Myofascial force transmission between antagonistic muscles located in opposite compartments of the rat hindlimb

J Electromyogr Kinesiol

(2007)

M.J. Smeulders et al.

Overstretching of sarcomeres may not cause cerebral palsy muscle contracture

J Orthoped Res

(2004)

W. Vattanasilp et al.

The relationship between clinical and laboratory measures of spasticity

Austr J Physiotherapy

(1999)

C.A. Yucesoy et al.

Substantial effects of epimuscular myofascial force transmission on muscular mechanics have major implications on spastic muscle and remedial surgery

J Electromyogr Kinesiol

(2007)

C.A. Yucesoy et al.

Three-dimensional finite element modeling of skeletal muscle using a two-domain approach: linked fiber-matrix mesh model

J Biomech

(2002)

C.A. Yucesoy et al.

Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling

J Biomech

(2003)

E.A. Zancolli

Surgical management of the hand in infantile spastic hemiplegia

Hand Clin

(2003)

C.J. Zuurbier et al.

Mean sarcomere length–force relationship of rat muscle fibre bundles

J Biomech

(1995)

L. Ada et al.

Does spasticity contribute to walking dysfunction after stroke?

J Neurol Neurosurgery Psychiatry

(1998)

D.S. Asakawa et al.

Three-dimensional muscle–tendon geometry after rectus femoris tendon transfer

J Bone Joint Surgery [Am]

(2004)

C.M. Booth et al.

Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity

Develop Med Child Neurol

(2001)

M.J. Botte et al.

Spasticity and contracture. Physiologic aspects of formation

Clin Orthopaed

(1988)

P.W. Brand

Mechanics of individual muscles at individual joints

R.E. Bunata

Pronator teres rerouting in children with cerebral palsy

J Hand Surgery [Am]

(2006)

T.J. Burkholder et al.

sarcomere length operating range of vertebrate muscles during movement

J Exp Biol

(2001)

M.E. Castle et al.

Pathology of spastic muscle in cerebral palsy

Clin Orthopaed

(1979)

T. Finni et al.

Nonuniform strain of human soleus aponeurosis–tendon complex during submaximal voluntary contractions in vivo

J Appl Physiol

(2003)

J. Friden et al.

Spastic muscle cells are shorter and stiffer than normal cells

Muscle Nerve

(2003)

J. Friden et al.

Biomechanical analysis of the brachioradialis as a donor in tendon transfer

Clin Orthopaed

(2001)

A.M. Gordon et al.

The variation in isometric tension with sarcomere length in vertebrate muscle fibres

J Physiol

(1966)

Cited by (45)

Force transmission and interactions between synergistic muscles
2023, Journal of Biomechanics
The classical view of muscles as independent motors has been challenged over the past decades. An alternative view has emerged in which muscles are not isolated but embedded in a three-dimensional connective tissue network that links them to adjacent muscles and other non-muscular structures in the body. Animal studies showing that the forces measured at the distal and proximal ends of a muscle are not equal have provided undisputable evidence that these connective tissue linkages are strong enough to serve as an extra pathway for muscular force transmission. In this historical review, we first introduce the terminology and anatomy related to these pathways of muscle force transmission and provide a definition for the term epimuscular force transmission. We then focus on important experimental evidence indicating mechanical interactions between synergistic muscles that may affect force transmission and/or influence the muscles’ force generating capacity. We illustrate that there may exist different expressions of the highly relevant force–length properties depending on whether the force is measured at the proximal or distal tendon and depending on the dynamics of surrounding structures. Changes in length, activation level or disruption of the connective tissue of neighboring muscles, can affect how muscles interact and produce force on the skeleton. While most direct evidence is from animal experiments, studies on humans also suggest functional implications of the connective tissues surrounding muscles. These implications may explain how distant segments, which are not part of the same joint system, affect force generation at a given joint, and, in clinical conditions, explain observations from tendon transfer surgeries, where a muscle transferred to act as an antagonist continues to produce agonistic moments.
Effects of inter-synergistic mechanical interactions on the mechanical behaviour of activated spastic semitendinosus muscle of patients with cerebral palsy
2018, Journal of the Mechanical Behavior of Biomedical Materials
Previous physiological experiments and finite element modelling indicate that inter-synergistic epimuscular myofascial force transmission (EMFT) between co-activated muscles has a potential to affect healthy muscle's contribution to joint moment and joint range of movement. This is quite relevant for patients with cerebral palsy (CP) since, amplitude of spastic muscle's force and the joint range of force exertion are central to the joint movement limitation. Stiffness of activated spastic muscle is also a determinant for pathological joint movement. However, assessments of effects of inter-synergistic EMFT on the mechanical behaviour of spastic muscle are lacking. Those assessments require measurement during surgery of activated spastic muscle's forces directly at its tendon and as a function of joint angle. Employing this methodology, the aim was to test the following study hypotheses: added activation of semimembranosus (SM) and gracilis (GRA) muscles of patients with CP changes (1) force, (2) stiffness and (3) joint range of force exertion of activated spastic semitendinosus (ST) due to inter-synergistic EMFT. Isometric spastic ST forces were measured intraoperatively (12 limbs of 7 patients (mean age 8 years 9 months) for knee angles from flexion (120°) to full extension (0°). Conditions I and II: spastic ST was activated alone, and simultaneously with its synergists SM and GRA muscles, respectively. Condition II did increase activated spastic ST's forces significantly (by 33.3%), but did not change its stiffness and joint range of force exertion, confirming only study hypothesis 1. Therefore, we conclude that inter-synergistic EMFT affects forces exerted at spastic ST tendon, but not other characteristics of its angle-force relationship.
The mechanics of activated semitendinosus are not representative of the pathological knee joint condition of children with cerebral palsy
2016, Journal of Electromyography and Kinesiology
Citation Excerpt :
This is ascribable to difficulties in accessing human muscles for direct force measurements. Smeulders and Kreulen (2007), Smeulders et al. (2004) overcame such difficulty in a series of studies conducted during remedial surgery, but in the upper extremity only. Recently, we developed an intra-operative experimental method to study lower extremity muscles, particularly the knee flexors (Yucesoy et al., 2010a).
Characteristic cerebral palsy effects in the knee include a restricted joint range of motion and forcefully kept joint in a flexed position. To show whether the mechanics of activated spastic semitendinosus muscle are contributing to these effects, we tested the hypothesis that the muscle’s joint range of force exertion is narrow and force production capacity in flexed positions is high. The isometric semitendinosus forces of children with cerebral palsy (n = 7, mean (SD) = 7 years (8 months), GMFCS levels III–IV, 12 limbs tested) were measured intra-operatively as a function of knee angle, from flexion (120°) to full extension (0°). Peak force measured in the most flexed position was considered as the benchmark. However, peak force (mean (SD) = 112.4 N (54.3 N)) was measured either at intermediate or even full knee extension (three limbs) indicating no narrow joint range of force exertion. Lack of high force production capacity in flexed knee positions (e.g., at 120° negligible or below 22% of the peak force) was shown except for one limb. Therefore, our hypothesis was rejected for a vast majority of the limbs. These findings and those reported for spastic gracilis agree, indicating that the patients’ pathological joint condition must rely on a more complex mechanism than the mechanics of individual spastic muscles.
Tendon and fascial structure contributions to knee muscle excursions and knee joint displacement
2014, Clinical Biomechanics
Semitendinosus and gracilis muscles whose tendons are used in surgical reconstruction of the anterior cruciate ligament maintain their contractile ability, and a limited decrease of hamstring muscles force is observed postoperatively despite important changes.
The goal was to quantify the influence of the myofascial structures on excursions and moment arms of knee muscles to attempt explaining the above-mentioned post-surgical observations.
Hamstring harvesting procedures were performed by a senior orthopaedic surgeon on seven lower limbs from fresh-frozen specimens.
Femoro-tibial kinematics and tendons excursion were simultaneously recorded at each steps of the surgery.
No significant difference was demonstrated for excursions and moment arms after tenotomies and gracilis tendon harvesting (P ≥ 0.05).
The first significant semitendinosus excursion (P < 1.17 × 10^− 4) and moment arm (P < 6.88 × 10^− 5) decrease was observed after semitendinosus tendon harvesting (46% of the initial excursion).
Gracilis and semitendinosus myofascial pathway is crucial for force transmission towards the knee joint.
Fascia Research Congress Evidence from the 100 year perspective of Andrew Taylor Still
2013, Journal of Bodywork and Movement Therapies
More than 100 years ago AT Still MD founded osteopathic medicine, and specifically described fascia as a covering, with common origins of layers of the fascial system despite diverse names for individual parts. Fascia assists gliding and fluid flow and is highly innervated. Fascia is intimately involved with respiration and with nourishment of all cells of the body, including those of disease and cancer. This paper reviews information presented at the first three International Fascia Research Congresses in 2007, 2009 and 2012 from the perspective of Dr Still, that fascia is vital for organism's growth and support, and it is where disease is sown.
Myofascial force transmission between the latissimus dorsi and gluteus maximus muscles: An in vivo experiment
2013, Journal of Biomechanics
There are extensive connections between the latissimus dorsi (LD) and gluteus maximus (GMax) muscles and the thoracolumbar fascia (TLF), which suggests a possible pathway for myofascial force transmission. The present study was designed to provide empirical evidence of myofascial force transmission from LD to contralateral GMax through TFL in vivo. To accomplish this goal, we evaluated whether active or passive tensioning of the LD results in increased passive tension of the contralateral GMax, indexed by changes in the hip resting position (RP) or passive stiffness. The hip RP was defined as the angular position in which the passive joint torque equals zero, and passive hip stiffness was calculated as the change in passive torque per change in joint angle. Thirty-seven subjects underwent an assessment of their passive hip torque against medial rotation by means of an isokinetic dynamometer. These measures were carried out under three test conditions: (1) control, (2) passive LD tensioning and (3) active LD tensioning. Electromyography was used to monitor the activity of the hip muscles and the LD under all conditions. Repeated measures analyses of variance demonstrated that passive LD tensioning shifted the hip RP towards lateral rotation (p=0.009) but did not change the passive hip stiffness (p>0.05). Active LD tensioning shifted the hip RP towards lateral rotation (p<0.001) and increased the passive hip stiffness (p≤0.004). The results demonstrated that manipulation of the LD tension modified the passive hip variables, providing evidence of myofascial force transmission in vivo.

View all citing articles on Scopus

Michiel Kreulen became an M.D. in 1992 at the Academic Medical Center of the University of Amsterdam. Since January 2000, he is a registered plastic surgeon. He holds a dual appointment at the department of plastic, reconstructive and hand surgery of the Academic Medical Center in Amsterdam and at the Red Cross Hospital at Beverwijk the Netherlands.

His clinical practice is focused predominantly on hand surgery, and more specifically on the surgical treatment of the spastic hand. He was granted the Ph.D. degree at the University of Amsterdam (2004) with a thesis entitled “Tendon transfer surgery of the upper extremity in cerebral palsy”. His main field of interest in research is on tailoring tendon and muscle surgery and three-dimensional upper extremity movement analysis.

View full text