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

Journal of Electromyography and Kinesiology 17 (2007) 644–656 www.elsevier.com/locate/jelekin

Myofascial force transmission and tendon transfer for patients suffering from spastic paresis: A review and some new observations Mark J.C. Smeulders *, Michiel Kreulen Department of Plastic, Reconstructive and Hand Surgery, Academic Medical Center, Amsterdam, Suite G4-226, P.O. Box 22700, 1100 DE Amsterdam, The Netherlands

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. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Tendon transfer; Spastic muscle; Force-length characteristics; Myofascial force transmission

1. 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 wellbeing 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 disease cerebral palsy. Patients with cerebral palsy often have deformities and a limited range of motion of the upper extremity due to severe muscle spasms and hypertonia of the flexor-, adductor-, and pronator muscles, in combination with a paresis of the extensor-, abductor-, and supinator muscles (Botte et al., 1988; Hoffer et al., 1987). This typical combination of neurological disorders is caused by ‘‘Spasticity’’, a motor disorder characterized by a velocity-dependent increase in *

Corresponding author. Tel.: +31 20 566 2974; fax: +31 20 691 7549. E-mail address: [email protected] (M.J.C. Smeulders).

1050-6411/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2007.02.002

tonic stretch reflexes with exaggerated tendon jerks resulting from hyper-excitability of the stretch reflex (Lance, 1980). The management of spasticity requires a multi-disciplinary approach, involving physiatrists, surgeons, neurologists, physiotherapists and occupational therapists. Interventions are generally aimed at improving function and cosmesis by maintaining joint motion, muscle strength and stretch or joint support and pharmacotherapy to relieve spasticity. One of the options is surgery. In selected patients, rebalancing of the forces at the involved joints by tenotomy, muscle releases, aponeurectomy (i.e. removal of part of the proximal aponeurosis), and tendon transfer procedures may correct joint deformities and improve the function of both the upper and the lower extremity. Especially in the spastic upper extremity, adequate weakening of the spastic side and concurrent augmentation of the paretic side requires a thorough evaluation of the patient’s functional demands, because a gain in strength and range of motion on one hand is often typically accompanied by a loss on the other (Bunata, 2006; Kreulen et al., 2004; Lieber et al., 2003a; Zancolli, 2003). As such, a variety of procedures is available and during surgery a surgeon is

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

confronted with dilemmas concerning what muscle to transfer, how the muscle should be mobilized, which route it should take, and at what tension it should be inserted, thereby considering the individual needs of the patient. There is presently no evidence based resolution for any of these dilemmas. Generally, surgeons are modest in their expectations of surgical outcome, because experience taught that the result of treatment varies, and the functional outcome for these patients is unpredictable. Often, such disappointing and unexpected results are attributed to the diversity, and severity of the neurological impairment among patients, their motivation, and the post-operative treatment regime. This is obviously true, but to our experience even preoperatively comparable patients with similar post-operative treatment may have completely different outcome. We hypothesize that there may be determinants of success that have been overlooked so far. Recent experimental work on muscle morphological characteristics in vivo, mechanical testing in situ and in vitro, as well as biomechanical modeling has led to new insights on the exertion and transmission of force between muscle and its surroundings. The aim of this review is to discuss implications of such new insights for the surgical treatment of spastic limbs, and to introduce myofascial force transmission as one of the determinants for success. First, the current basis for the clinical practice in tendon transfer is reviewed. Subsequently, some exploratory observations are discussed that illustrate the relevance of myofascial pathways of force transmission in muscle functioning. 2. 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 of function is achieved by improving the balance between the spastic pronator–flexor muscles and the paretic (and not completely paralysed!) supinator–extensor muscles (Zancolli, 2003). Spastic muscles are not considered ideal for tendon transfer, as there is often lack of voluntary control, and the muscles are subject to stretch reflexes, triggered by movement (particularly fast movement) and emotion (Goldner, 1988; Zancolli, 2003). Moreover, the spastic muscles may be subject to structural changes due to the life-long erroneous neural input that further hamper a proper functioning. Although above-mentioned difficulties are well known, the current rationale behind the clinical practice of tendon transfer in cerebral palsy is founded on the same estimates of tendon excursion and force generation capacity of nonspastic muscles (e.g. Brand et al., 1981; Lieber et al., 1992). The possible effects of spasticity on the mechanical behav-

645

ior of the donor muscles has conveniently been disregarded in the clinical management of spasticity, except for the notion that an absence of voluntary control should be considered a contra-indication for surgery (Zancolli, 2003), and that fixed position of joints may lead to muscle fibrosis (Leclercq, 2003). Within the clinical setting, for a large part, the inattentiveness to the mechanical characteristics of spastic muscles could be due to the limited state of knowledge of those characteristics of spastic muscles in the scientific world. At best, spastic muscle’s characteristics may be predicted from histological examination of muscle biopsies (Booth et al., 2001; Botte et al., 1988; Castle et al., 1979; Gracies, 2005; Rose et al., 1994) or from in vivo examination of resistive forces at passive movement of limbs in patients (e.g. Ada et al., 1998; Mirbagheri et al., 2001; O’Dwyer and Ada, 1996; Tardieu et al., 1982, 1988; Vattanasilp and Ada, 1999). Although histological examination is relatively easy to perform, only limited number of muscle cells can be analyzed. Therefore, the observations in samples of the muscle may not be representative for the whole of the muscle. Moreover, while histological analysis may show the presence of morphological changes, it does not inform on the consequences of these changes to functional properties such as the stiffness. Similarly, the application of in vivo measurements of resistive forces is limited because only the net joint moment, rather than the actual force that a muscle exerts at a joint, can be assessed. This moment not only depends on the force exerted, but also on the moment arm. The moment arm varies among subjects and is difficult to assess accurately. In addition, the net moment exerted at a joint represents the net moment of many muscles and passive structures, and it is impossible to accurately distinguish the force of a particular muscle. Therefore, estimating actual muscle force from in vivo resistive moment data has extremely limited accuracy. Likewise, ultrasonography is used to measure muscle fascicle length changes during movement in vivo and for the estimation of volume and moment arm lengths of muscles (e.g. Arampatzis et al., 2006; Kawakami et al., 1998; Maganaris, 2001, 2003). Such measurements are valuable in understanding relative lengths and length changes of muscles and their tendons, and may be a helpful tool for volumetry of muscles, but an erroneous supposition often made in such studies is that fascicle length changes may directly be related to the net measured joint moments for estimation of muscle length–force characteristics. Besides the abovementioned limitations of measuring net joint moments, a direct relation of moment to muscle fascicle length change would imply that muscle fibers are completely free to move with all sarcomeres contracting as one unit. However, adjacent connective tissues may interfere with shortening on contraction (Kozin and Bednar, 2001; Meijer et al., 2007; Smeulders et al., 2005; Yucesoy et al., 2003a; Yucesoy and Huijing, 2007), resulting in a heterogeneous distribution of sarcomere lengths within the muscle fascicles. As a result, within the complex of muscles and connective tissues of the studied limb,

646

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

sarcomeres may be short where they are expected to be stretched, and vice versa, invalidating fascicle length for the estimation of sarcomere length (Yucesoy et al., 2003b). It may, therefore, not be surprising that results from in vivo measurements are contradictory and do not provide for a clear manifest for the clinical practice. Only recently, renewed interest in possible changes in muscle mechanics due to spasticity has led to the start of actual measurement of spastic muscle mechanics in humans (Friden and Lieber, 2003; Smeulders et al., 2004b). Initially, single muscle fiber segments from muscle biopsies harvested from patients with cerebral palsy who underwent tendon transposition and from controls with healthy muscles of whom biopsies could incidentally be accessed (tendon injuries, forearm trauma) were connected to a force transducer to measure force and allow construction of passive stress–length curves (Friden and Lieber, 2003). The elastic modulus of the spastic fiber segments was found to be over twice that of the healthy muscle fiber segments, indicating that the passive stiffness of the individual spastic muscle fibers was increased. In the process of isolating the muscle fiber the endomysium of the target fiber, may or may not, have remained intact. Altered mechanical properties may have been a result of differences in the endomysium, or its interaction with the sarcomeres, between healthy and spastic muscles. Subsequently, the same authors studied the passive stress–length curves of small bundles of fiber segments, rather than single fibers. Then, they reported that small bundles of spastic muscle fibers including their complete collagen reinforced extracellular matrix, constituting intramuscular connective tissues, were actually less stiff compared to non-spastic muscle fiber bundles. Finding a way of reconciling these two findings is very difficult. Those authors concluded this being a result of poor quality connective tissues in the spastic muscles (Lieber et al., 2003b). Thus, spastic muscle may have markedly altered material properties, but because muscle consists of fibers and intramuscular connective tissues it is not clear what the clinical and functional consequences of these altered properties may be. In any case, they do not explain the apparent stiffness of the spastic muscles and the existence of contractures in the spastic limbs. Obviously, above-mentioned studies only reported differences muscular characteristics under passive loading, and results may be different during activity. For instance, direct measurement of passive and active length–force characteristics of the partially dissected human spastic flexor carpi ulnaris muscle in situ during transfer surgery to correct for wrist flexion deformity revealed that the passive force at the maximal (limited) extension of the wrist was 8.5 N (S.D. 6.0 N), corresponding to between only 0.7% and 18% of the maximum active force (Smeulders et al., 2004b). The active force at maximum wrist extension was above 70% of its maximum in all patients, indicating that the majority of the sarcomeres were not maximally stretched in any of the FCU muscles, but were around optimum length and should still be able

to lengthen against little resistance. We therefore concluded that the FCU itself is not the limiting factor for wrist extension in spastic patients. Unfortunately, the study design does not allow for comparison of the characteristics of the spastic FCU to those of non-spastic ones. However, the passive and active length–force properties of the partially isolated spastic FCU were similar to those predicted for healthy muscle (Burkholder and Lieber, 2001; Lieber and Friden, 1997), indicating that length–force characteristics of spastic muscles may not be dramatically different from non-spastic ones. It may be clear that we only started to fill the gap in the knowledge of spastic muscle characteristics and its adaptive responses, and this may be one of the fields of research that, in the future, may significantly contribute to the clinical practice of treatment of spasticity. 3. 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 excursion, while the cross-sectional area of the muscle determines the maximally available generation of force (Brand et al., 1981). To date, length–force characteristics of human muscles have been mainly estimated from models of muscle function. Mechanical experiments on isolated, dissected frog muscle fibers showed the length dependence of sarcomeres, typically referred to as the length–force relationship (Gordon et al., 1966). Generally, the force and excursion of all sarcomeres in series and parallel are pooled to form one ‘super-sarcomere’, and muscle function is modeled as the functioning of this super-sarcomere. This modeled relationship is still considered to be the most important feature to describe muscle functioning (e.g. Jones and Round, 1992; Lieber and Friden, 2001; Rassier et al., 1999). Such models have been used to predict the outcome of tendon transfers (Herrmann and Delp, 1999; Murray et al., 2002). However, models that predict muscle length–force characteristics based on the assumption that the characteristics of single sarcomeres may simply be summated and extrapolated to whole muscle (Brand, 1993; Lieber and Friden, 2001) are too much of a simplification of the in vivo situation because the shape of the length–force relationship has shown to depend on the time of activation of the sarcomeres (Zuurbier et al., 1995), the geometry of muscle that changes upon its isometric activity (Huijing, 1985; Kawakami et al., 1998), the effects of elasticity of the tendon and aponeurosis and the intra-and extracellular matrix of connective tissues (Heslinga and Huijing, 1993; Huijing, 1998), and because some of the generated force may be

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

transmitted by the curvature in active muscle fibers to the peripheral surface of muscle and beyond (Muramatsu et al., 2002; Sejersted et al., 1984) and myofascially onto the inter- and extramuscular connective tissue (Huijing, 1999b). In other words, muscle activation does not necessarily lead to a homogeneous shortening of muscle fibers within a muscle (Finni et al., 2003; Pappas et al., 2002; Yucesoy et al., 2002; Yucesoy and Huijing, 2007). Yet, these considerations have not led to an altered approach in tendon transfer surgery. The currently advocated surgical prerequisites to preserve the functional properties of a muscle after transfer have been (1) to choose the right donor muscle, (2) not to violate the architecture of the muscle belly, its vascularization or innervation, (3) to transfer the muscle and tendon along an unimpeded and fluent line directed towards its new target and (4) to fix the tendon such that the optimal muscle length corresponds to the optimal joint angle (Brand et al., 1981; Brand, 1993; Lieber et al., 1992). Using these principles, muscles that have an available excursion and force similar to the needed function in the transferred role are considered ideal donor muscles (Brand et al., 1981). Therefore, in addition to the availability of the donor muscle and the functioning with respect to tasks that are aimed for, the estimation of the capacity for excursion and force of both donor and receptor muscles form the basis for selection of the right donor muscle (Lieber and Friden, 2000). A large part of the research in the field of tendon transfer focuses on the clinical problem of optimal tensioning of the tendon (Friden and Lieber, 1998; Lieber et al., 1994,

647

1996; Loren and Lieber, 1995; Loren et al., 1996). Several attempts have been made to estimate the optimal range of excursion of the muscle, such that maximal force is established in the functionally optimal joint angle (Fig. 1). Apparently, however, in practice surgeons tend to stretch the muscles more than they aim for at insertion (Friden and Lieber, 1998; Lieber et al., 2005). The concept of a unique capacity for each separate muscle to pull and shorten, implies that the relationship between muscle length and force is an invariable characterization of its functional capacity. If a transferred muscle is shown to be able to adapt its fiber length by adding or removing sarcomeres in-series, its tendon length, or the length of its muscle belly by hypertrophy or atrophy, such optimalization of the range of excursion during surgery would not be crucial. Excellent reviews exist that discuss the adaptability of muscle properties (Friden and Lieber, 2002; Huijing and Jaspers, 2005; Lieber et al., 2004). Therefore after emphasizing some points no further treatment is provided here. There seems to be adequate consensus that the cross-sectional area of the muscle fibers adapts to immobilization, disuse, load training, growth, and to surgical interventions. However, the consensus on the adaptation of muscle fiber length, or more specifically, adaptation of the amount of sarcomeres in-series is lacking, although there are clear signs that normal growth and some other physiological conditions are able to trigger an adaptive response of the muscle fibers (e.g. Friden et al., 2000; Heslinga and Huijing, 1992; Williams and Goldspink, 1978). Some of the contradicting results from the literature

Fig. 1. Schematic representation of the tuning of tension in case of a fixed active and passive length–force curve. The operating length range, defined as the range of muscle lengths that is attained by moving the joint through the whole range of motion, is indicated by the grey area. A surgeon’s goal is to manipulate the muscle’s length at insertion such that this operating range is positioned over the active force curve of the muscle, and the optimum active force corresponds to the joint position that is most functional (e.g. often a neutral joint position). The only tool available for that is the subjective feeling of the tension of the muscle when pulling, indicated by the grey ‘F’. The grey dot and line marks the point of fixation of the tendon at passive tension ‘F’. However, even when a surgeon is able to correctly feel the right tension, the relation between the active and passive length–force curve is not known, and is not a constant factor. Such estimations of tensioning of the tendon for optimizing the muscle operating range are very inaccurate.

648

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

on adaptation may be explained by differences in conditions to which the muscle fibers were exposed. Such differences may not always be obvious, because the experimental condition of the sarcomeres of muscle fibers within a muscle–tendon complex may vary depending on the tendon properties, the effects of pennation (Huijing and Jaspers, 2005), and of adjacent connective tissues that may interfere with shortening on contraction (Kozin and Bednar, 2001; Smeulders et al., 2005; Yucesoy et al., 2003a). Such parameters are difficult to control during in vivo, or in situ studies on muscles. Nonetheless, the adaptive response of a muscle fiber length to spasticity seems to be limited. Measurement of length–force characteristics during surgery (Smeulders et al., 2004b), and sarcomere length range (Lieber and Friden, 2002) of spastic muscles showed that the limitation in the wrist range of motion in patients with cerebral palsy is not caused by structural shortening of the fibers. Similarly, ultrasound images of patients with limited ankle dorsiflexion due to spasticity showed that the gastrocnemius muscle

fibers were not shorter than those of healthy controls, although the muscle–tendon complex did seem to have shortened (Malaiya et al., 2007; Shortland et al., 2002). Such shortening of the very pennate muscle belly (Heslinga et al., 1995) was attributed to be due to atrophy of the muscle fibers (Shortland et al., 2002). Similar muscle shortening was also proposed to explain differences in a longitudinal study of passive and active length–force characteristics of the FCU in a patient with wrist extension deformity developed secondary to transposition of the FCU to the extensor carpi radialis brevis (Smeulders and Kreulen, 2006). The FCU did not visually appear to have marked increase of intramuscular connective tissues, nor did it appear markedly atrophied. Nonetheless, the passive length–force curve was steeper at the second operation, indicating an increased stiffness of the muscle fibers, or of the intra-, inter-, or extramuscular connective tissues over time. Additionally, the optimum of the active length–force curve had moved approximately 2 cm to shorter muscle length. This

Fig. 2. Schematic representation of the flexor carpi ulnaris (FCU) length changes before and after tenotomy The mean passive excursion of the FCU during movement from maximal flexion of the wrist to maximal extension before tenotomy, after tenotomy and after muscle dissection in 10 patients with cerebral palsy (upper graph), and mean shortening of the muscle belly of the FCU after tenotomy and after dissection, before and after tetanic contraction in these patients (lower graph).

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

indicated the FCU to have structurally shortened. The excursion potential of the FCU, however, was not changed, indicating the shortening to be a result of muscle atrophy, rather than of loss of sarcomeres in-series (Heslinga and Huijing, 1993). From these studies it is concluded that spastic muscle is to be capable of some adaptability after tendon transfer, but mostly limited to adaptation of its cross-sectional area, rather than of its muscle fiber length. Nonetheless, this would mean that at least in part, spastic muscles may be able to adjust the length of their muscle bellies to conditions that are imposed on them. It may be questioned, however, whether this adjustment actually takes place in such a pathological condition. An area of research in tendon transfer surgery that recently has drawn the attention is the route of the donor muscle. Two studies showed that transfer of the rectus femoris muscle of cerebral palsy patients from its extension insertion to a flexion insertion at the knee did not convert the rectus femoris to a knee flexor (Asakawa et al., 2002; Riewald and Delp, 1997). Subsequent to transfer Riewald and Delp showed that selective stimulation of the rectus femoris muscle did not generate a knee flexion moment, but instead still generated a knee extension moment (Riewald and Delp, 1997). Asakawa measured the rectus femoris motion after surgery using dynamic MRI. They found that during knee motion, the rectus femoris displaced in the direction of the knee extensors instead of in the direction of the knee flexors to which it had been transferred. These observations suggest that the transferred rectus femoris is connected to adjacent structures at the extension side and exerts at least part of it force as an extension force via myofascial force transmission. This may be a result of post-operative scarring, as was suggested later (Asakawa et al., 2004) or the physiological connections that remain after the partial dissection of the muscle as was also suggested (Huijing, 1999a). The prerequisite of a transfer in a fluent line necessitates a partial dissection of the distal part of the muscle belly from its surrounding connective tissues. Such connective tissues may limit the total available excursion of a muscle as was shown for the brachioradialis muscle (Friden et al., 2001; Kozin and Bednar, 2001), and may be responsible for the abrupt angulation in the route of the rectus femoris muscle after transfer to the semitendinosus (Asakawa et al., 2004). In addition, such connections form potential pathways of force transmission (Huijing, 1999a) that may affect the homogeneity of the sarcomere lengths (Yucesoy et al., 2003a; Yucesoy and Huijing, 2007) and, as such, the length–force curves of the muscles. We noticed during surgery that tenotomy of the FCU did not result in a major retraction of the muscle to slack length but, instead, FCU remained more or less near its former insertion. Therefore, we per-operatively (i.e. under conditions of general anesthesia abolishing the spastic responses) measured the length of the muscle belly before, and after complete tenotomy in 10 patients with cerebral palsy under several conditions (Kreulen et al., 2003): First,

649

on moving the wrist passively from flexion to extension, the tenotomized FCU (not spanning the wrist anymore) was lengthened by almost equal distance as the intact FCU (Fig. 2). Apparently, the FCU is connected to structures that span the wrist via epimuscular of epitendinous connective tissues. Even after tenotomy, such connections pull the FCU along on passive wrist extension. This lengthening diminished greatly, but did not fully disappear after partial dissection from distally to approximately halfway the muscle belly from its adjacent connective tissues. Second, supra-maximal stimulation of the ulnar nerve after tenotomy provoked a maximal tetanic contraction of the FCU, but the FCU did not shorten to slack length as would be expected if the FCU was free to move. Apparently, the connective tissues were so stiff that they could resist the full FCU force and strong enough so that they did not break on such force exertion. Again after dissection, the FCU retracted significantly more. In order to study the implications of such connections on FCU characteristics we developed and applied a method to directly measure human forearm muscle force during tendon transfer surgery, using relative simple equipment (Smeulders et al., 2004a). Using this method, we showed that both the active and passive length–force curve of the

Fig. 3. (A) Images of human flexor carpi ulnaris muscle (FCU) and its adjacent tissues. Image taken during surgery for tendon transfer, after tenotomy and prior to, further dissection for transfer. Note the extramuscular connective tissues adjacent to the FCU and its tendon. (B) Image taken of a cadaver arm projected on top of image A showing the relation of FCU to adjacent muscle and the neurovascular tract (indicated by n.ulnaris). The connective tissues connect FCU to the underlying flexor digitorum superficialis (FDS), and – profundus (FDP), as well as to the ulnar nerve and artery.

650

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

90 80 70 60 50 40 30 20

Force (N)

10 0 16

17

18

19

20

80 70 60 50 40 30 20 10 0 20

21

22

23

Muscle length (cm) Fig. 4. Active and passive length–force profile of a spastic flexor carpi ulnaris muscle (FCU) in two positions of the wrist from two patients with cerebral palsy representative to show the variability of the effects of wrist movement. After tenotomy of the distal tendon length–force data were collected twice, once with the wrist held in flexion (solid lines), and once with the wrist held in extension (dashed lines). By varying the position of the wrist while keeping the FCU at a constant length, the stretch of the connective tissues between the FCU and its adjacent structures is changed, resulting in changed stiffness of the structures, a variation of the fraction of myofascial force transmission, and a different length–force curve. Note that measurements were done for a range of FCU lengths to construct a length–force curve, while in vivo only one FCU length would correspond to the length at extended wrist, and one length corresponds to that in flexion of the wrist. Remarkably, the effects of wrist movement on the length– force curves varied among patients, as some showed significant effects between flexed and extended wrist mainly at short FCU length, and passive force was highest in flexion (upper graph), while others showed effects mainly at high FCU length, and passive force was highest in extension (lower graph). This may be explained as the change of stretch of the connective tissues may vary among patients depending on the initial length and orientation of the myofascial structures (see text).

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

tenotomized FCU significantly varied when the structures adjacent to the FCU (Fig. 3) were kept short, compared to when they were held at lengthened position, proving that the relative length and position of adjacent structures co-determine the function of the FCU (Smeulders et al.,

A

B

C

D

651

2005). Interestingly, some patients showed differences in the length–force characteristics at flexion and extension of the wrist mainly at low FCU lengths, and the passive force was highest in flexed position of the wrist, while others showed differences at high FCU length, and the passive force was highest in the extended position of the wrist (Fig. 4). The differences between the patients were not related to the clinical presentation and severity of the spasticity and are difficult to interpret, but could be a factor that explains part of the unpredictability of the outcome of tendon transfer in spastic patients (see below, and Fig. 5). Our observations cannot be explained if the myotendinous pathway the sole pathway of force transmission. The fact that wrist movement affects the length–force characteristics of the tenotomized FCU may be a result of variations in the amount of force that is transmitted to the second pathways of force transmission via intra-, inter-, and extramuscular connective tissues (i.e. myofascial force transmission) (Maas et al., 2003b) when, due to the wrist movement, stiffness of these structures varies. In rat muscle, direct evidence for such connections has been reported as the force exerted at the proximal tendon differed from the force exerted at the distal tendon when surrounding fascial connections to the muscle and/or tendon (Rijkelijkhuizen et al., 2005) were intact (Huijing and Baan, 2001a,b; Huijing, 2007; Huijing et al., 2007). This proximo-distal force difference proves that part of the muscle force is transmitted to the muscle’s surroundings somewhere along the surface of the muscle belly or its tendon. Similar principles also apply for human spastic muscle, conceivably even in an enhanced fashion. 4. Myofascial force transmission as a co-determinant of muscle function

Fig. 5. Schematic representation of human flexor carpi ulnaris muscle (FCU) that is attached to its environment and to a distal load cell (LC). Such simplified view of muscle force transmission may help to explain the role of myofascial force transmission. Attachments to the environment are represented by the lines arranged in parallel. The adjacent structures are not shown, but are represented by the thick black line. The numbers are fictive and are only added for clarity. (A) The condition is shown that indicates the role of myofascial force transmission that leads to a lower force measured at the load cell. As may be clear, the force measured in the load cell depends on both the force exerted by the FCU and the net amount, and orientation of force that is transmitted by the myofascial pathway. (B) Increased stiffness of the myofascial pathways (represented by increased number of parallel lines) may lead to a larger portion of the force that is transmitted by the myofascial pathway, and in a further lowered force measured by the load cell. (C) Condition is shown of the FCU attached to its environment that changes its position relative to the FCU in figure (A) such, that the connective tissues are stretched. Such stretch leads to greater stiffness of the myofascial pathway and, therefore, to increased myofascial force, resulting in lower force exerted at the load cell. (D) Condition is shown of the FCU attached to its environment that changes its position relative to the FCU such, that the orientation of the connective tissues changes compared to condition (A). Such a change of orientation leads to addition of force from the adjacent structures onto the load cell, resulting in a higher force measured than exerted by the FCU itself.

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 determined by the ratio of stiffness of the complete myofascial pathway and the complete myotendinous pathway (Fig. 5A). The stiffness of the pathways depends on the elastic modulus and quantity of the materials involved and on the length of the tissues, with stretched tissues being stiffer than short tissues (Ettema and Huijing, 1989). The stiffer pathways transmits most of the force (Huijing, 1999a; Maas et al., 2003a) because they are the most efficient route. The concept of myofascial force transmission may help to explain (1) the differences in the length–force characteristics of the tenotomized FCU between a flexed position

652

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

and an extended position of the wrist as well as (2) the variability among patients in our previous study (Smeulders et al., 2005): (1) Changing wrist position from flexion to extension lengthens the flexor digitorum superficialis and – profundus, as well as the extramuscular tissues that connect the forearm to the hand relative to the tenotomized FCU (see also Yucesoy and Huijing, 2007). As a consequence, connective tissues between the FCU and these adjacent structures (Fig. 3) will either lengthen, or shorten, depending on their orientation. Moreover, the initial length and stiffness of these connective tissues determine the fraction of force that is transmitted myofascially (Fig. 5A and B), lengthening or shortening of the connective tissues at varied wrist positions changes this fraction (Fig. 5C), whereas the (initial) orientation of the connective tissues determine whether the force is ‘‘added’’ or ‘‘subtracted’’ to the force exerted at the force transducer (Fig. 5D). Hence, the varied position of the wrist, and concomitant variable stiffness of the myofascial structures may as such cause variation of the fraction of force transmitted to the myofascial pathway and, using such a concept of muscle with both a myotendinous and myofascial pathway of force transmission would explain different force measured at its distal tendon for identical FCU lengths as the wrist angle is varied. (2) The fraction of the force transmitted to the myofascial pathway may vary among patients due to differences in the stiffness, the initial length and the orientation of the connective tissues. Both an increased stiffness and a greater initial length of the connective tissues would lead to higher fraction of myofascial force, and lengthening of such stiffer or stretched tissues would lead to greater increase of the fraction (Fig. 6). Hence, apparently random variability of the fraction of myofascial force among patients may be explained by variability of three initial conditions. Unfortunately, we lack any knowledge on (variability in) stiffness, length, and orientation of the connective tissues for the quantification of such variability, and this should be an emphasis for future work. The myofascial force that is exerted by FCU is transmitted to the extramuscular connective tissues, and onto the adjacent flexor digitorum profundus muscle (FDP) or – superficialis muscle (FDS) (Fig. 3). After tenotomy of the FCU, this myofascial pathway may form an alternative pathway through which force that is exerted by the FCU remains to cause a flexion moment at the wrist. For transposition purposes, the FCU is only dissected distally to about half way its muscle belly until a transposition in a fluent line is possible (Green, 1942). Consequently, the epimuscular connections at the proximal half of the muscle remain intact, and continue forming a pathway for force transmission. It is difficult to predict what the contribution of this pathway is for the clinical outcome of the surgery but, theoretically, part of the FCU may remain to be a flexor of the wrist; see also discussion of this point by Yucesoy and Huijing (2007), similar to the rectus femoris remaining an extensor of the knee (Riewald and Delp, 1997).

Fig. 6. Schematical drawing of the human flexor carpi ulnaris muscle (FCU) that is attached to its environment and to a distal load cell (LC), at two different lengths. Two situations are shown indicating (1) the effect of stretch of the connective tissues resulting in higher myofascial force transmission and lower force measured at the LC, similar to Fig. 5C (light grey arrows), and (2) the effect of the length of the FCU (dashed lines) may differ depending on the initial stretch of the connective tissues. Further stretching of already stretched connective tissues (lower graph) may lead to a greater increase of the stiffness, and concomitant greater increase of the myofascial force transmission (dark grey arrows). (The numbers are fictive and are only added for clarity.)

Accepting that myofascial pathways are involved in the transmission of muscle force would imply that the force exerted at the FCU tendon changes when the muscle is dissected from its surroundings and the myofascial pathway is disrupted. The first indication that dissection of muscles would influence muscle active function was shown by Freehafer et al. (1979). For force measurement during electri-

Fig. 7. Passive and active length–tension characteristics of brachioradialis muscle. Results are shown before and after soft tissue dissection. After dissection, the available muscle excursion increased, and the active force increased at all lengths studied. Note that the passive force at the reference length in the undissected condition is not zero. The authors did not explain these phenomena, but the findings could be explained when myofascial force transmission is considered (see text) (Redrawn from Freehafer et al., 1979).

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

cally induced maximal muscle activation at different muscle lengths before and after dissection, they showed that dissection of the non-spastic brachioradialis muscle affected both its active and passive length–force characteristics. Force increased after dissection at all lengths, resulting in a shift of optimum length to higher length (Fig. 7). After dissection, passive force decreased at all lengths studied. Muscle length was related to the length at standard anatomical position of the arm as a reference. Although the authors refer to this length as ‘‘resting length’’, this reference length does not correspond to muscle slack length, because the passive force at the reference length before dissection was greater than zero and does yield a potential for further shortening. We recently studied the effect of dissection of the FCU from its soft tissue surroundings on the length–force characteristics at the distal tendon in six patients with cerebral palsy. The active length–force characteristics of the nondissected muscle differed from those after dissection in all patients. Similarly as in the study where wrist position was varied in the non-dissected FCU, the effects varied

653

considerably among patients. Dissection caused an increase in FCU active force in one patient similarly to Freehafer et al., but the others showed a decrease of active force after dissection (Fig. 8). Optimum length shifted by up to approximately 5% to higher length in four, and to lower length the two other patients. Passive force decreased in all patients after dissection, although the magnitude of the decrease varied. In three patients, muscle resting length, defined as the maximum muscle length at which there is no passive force measured at the tendon, had shifted to higher length, while the other three patients did not have a changed resting length. Variability of the effects of dissection may, again, be explained by variability in the stiffness, stretch and orientation of the structures of the myofascial pathway. Stiffer or stretched connective tissues that bear higher myofascial force may, when dissected, result in greater shift of the fraction of force that is transmitted to the tendon, and the orientation of the connective tissues determines whether this shift of the fraction of force results in an ‘‘adding’’ or ‘‘subtracting’’ of this force to the force exerted at the tendon.

Fig. 8. Graphical display of the active, and passive length–force curves of the spastic FCU of six patients with cerebral palsy, before and after soft tissue dissection. The data are shown as a percentage of maximum active force, and percentage of optimum length before dissection (black dot). The curves before dissection are averaged for clarity (black curve). After dissection, the curves both shifted either to higher length or to lower length, and to higher or lower maximum active force (open dots, grey lines). Passive force decreased in all patients, after dissection, indicating that connective tissues are able to bear resistive forces to stretch. In three of the six patients, muscle resting length, defined as the highest muscle length at no passive force, had shifted to higher length. Note the rather high variety of the effect of dissection for both the active and passive length–force curves among patients.

654

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

In addition, the varied stiffness and direction of pull of the inter-, and extramuscular connective tissues may have contributed to non-uniform lengths of sarcomeres within the fibers of the muscles (Finni et al., 2003; Pappas et al., 2002; Yucesoy and Huijing, 2007). For isolated muscles, a non-uniform shortening of sarcomeres would imply that sarcomeres reach their optimum length at different muscle lengths, resulting in a lower maximum muscle active force, accompanied by length–force curves that comprise increased length range of active force exertion (Huijing, 1998; Willems and Huijing, 1994). However, to what extent this holds up for non-dissected muscle with intact myofascial pathways remains to be studied. In any case, as non-uniformity of sarcomere lengths is very plausible when myofascial force transmission is accounted for (Yucesoy et al., 2006), such transmission may not only affect the fraction of the force that is transmitted to the tendon, but may also affect the actual force that is exerted by the muscle. 5. 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 away (Huijing et al., 2007; Meijer et al., 2007; Rijkelijkhuizen et al., 2007). Specific characteristics of skeletal muscle adapt to specific physiological or pathological conditions and cerebral palsy likely represents a range of conditions. During tendon transfer, both the muscle function and its environment are changed acutely as the muscle is partially dissected and its mechanical effects for the movement of arm and hand changed. Ultimately, the success of the treatment depends on the muscle’s adaptation and its interaction with its old and new environment after transfer. Still, little is known about the physiological demands that cerebral palsy imposes on the muscles involved. The common assumption that spastic muscle adapts to the pathological neurological input still requires proof, and we do not know whether, or to what degree, spasticity affects muscle characteristics. Likewise, we do not know whether, or to what degree, initial scar tissue surrounding the rerouted muscle is replaced by more functional tissue. Now that we established that the inter- and extramuscular connective tissues are important determinants of muscle characteristics, we need to continue exploring in which way this knowledge is to be taken into consideration during the planning and execution of tendon transfer surgery. An important aspect of such considerations is that the surgical muscle transposition itself is merely the starting point from where newly formed connective tissue will develop that will

affect the function of the transposed muscle again (Asakawa et al., 2004). Ideally, we should conduct a more top down approach and evaluate FCU function in its new role after full recovery from the transposition surgery. This could be done by studying the patients during and after rehabilitation by using ultrasonography or magnetic resonance imaging, as well as by histological and or physiological studies of spastic muscle needle biopsies. Important data, however, can also be derived from kinematical data by studying patients using 3-Dimensional video analysis or from mathematical modeling of muscle function and movement. To do so, it will be necessary to adapt the currently available models to incorporate the specific anatomical constraints that the concept of myofascial force transmission dictates. References Ada L, Vattanasilp W, O’Dwyer NJ, Crosbie J. Does spasticity contribute to walking dysfunction after stroke?. J Neurol Neurosurgery Psychiatry 1998;64:628–35. Arampatzis A, Karamanidis K, Stafilidis S, Morey-Klapsing G, DeMonte G, Bruggemann GP. Effect of different ankle- and kneejoint positions on gastrocnemius medialis fascicle length and EMG activity during isometric plantar flexion. J Biomech 2006;39:1891–902. Asakawa DS, Blemker SS, Gold GE, Delp SL. In vivo motion of the rectus femoris muscle after tendon transfer surgery. J Biomech 2002;35:1029–37. Asakawa DS, Blemker SS, Rab GT, Bagley A, Delp SL. Threedimensional muscle–tendon geometry after rectus femoris tendon transfer. J Bone Joint Surgery [Am] 2004;86-A:348–54. Booth CM, Cortina-Borja MJF, Theologis TN. Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Develop Med Child Neurol 2001;43:314–20. Botte MJ, Nickel VL, Akeson WH. Spasticity and contracture. Physiologic aspects of formation. Clin Orthopaed 1988:7–18. Brand PW. Mechanics of individual muscles at individual joints. In: Brand PW, Hollister A, editors. Clinical mechanics of the hand. St. Louis: Mosby Yearbook; 1993. p. 254–352. Brand PW, Beach RB, Thompson DE. Relative tension and potential excursion of muscles in the forearm and hand. J Hand Surgery [Am] 1981;6:209–19. Bunata RE. Pronator teres rerouting in children with cerebral palsy. J Hand Surgery [Am] 2006;31:474–82. Burkholder TJ, Lieber RL. sarcomere length operating range of vertebrate muscles during movement. J Exp Biol 2001;204:1529–36. Castle ME, Reyman TA, Schneider M. Pathology of spastic muscle in cerebral palsy. Clin Orthopaed 1979;142:223–32. Ettema GJ, Huijing PA. Properties of the tendinous structures and series elastic component of EDL muscle–tendon complex of the rat. J Biomech 1989;22:1209–15. Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S. Nonuniform strain of human soleus aponeurosis–tendon complex during submaximal voluntary contractions in vivo. J Appl Physiol 2003;95:829–37. Freehafer AA, Peckham PH, Keith MW. Determination of muscle– tendon unit properties during tendon transfer. J Hand Surgery [Am] 1979;4:331–9. Friden J, Lieber RL. Evidence for muscle attachment at relatively long lengths in tendon transfer surgery. J Hand Surgery [Am] 1998;23:105–10. Friden J, Lieber RL. Mechanical considerations in the design of surgical reconstructive procedures. J Biomech 2002;35:1039–45. Friden J, Lieber RL. Spastic muscle cells are shorter and stiffer than normal cells. Muscle Nerve 2003;27:157–64.

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656 Friden J, Ponten E, Lieber RL. Effect of muscle tension during tendon transfer on sarcomerogenesis in a rabbit model. J Hand Surgery [Am] 2000;25:138–43. Friden J, Albrecht D, Lieber RL. Biomechanical analysis of the brachioradialis as a donor in tendon transfer. Clin Orthopaed 2001;383:152–61. Goldner JL. Surgical reconstruction of the upper extremity in cerebral palsy. Hand Clin 1988;4:223–65. Gordon AM, Huxley AF, Julian FJ. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 1966;184:170–92. Gracies JM. Pathophysiology of spastic paresis. I: Paresis and soft tissue changes. Muscle Nerve 2005;31:535–51. Green WT. Tendon transplantation of the flexor carpi ulnaris for pronation–flexion deformity of the wrist. Surgery Gynecol Obstetrics 1942;75:337–42. Herrmann AM, Delp SL. Moment arm and force-generating capacity of the extensor carpi ulnaris after transfer to the extensor carpi radialis brevis. J Hand Surgery [Am] 1999;24:1083–90. Heslinga JW, Huijing PA. Effects of short length immobilization of medial gastrocnemius muscle of growing young adult rats. Eur J Morphol 1992;30:257–73. Heslinga JW, Huijing PA. Muscle length–force characteristics in relation to muscle architecture: a bilateral study of gastrocnemius medialis muscles of unilaterally immobilized rats. Eur J Appl Physiol Occupat Physiol 1993;66:289–98. Heslinga JW, te KG, Huijing PA. Growth and immobilization effects on sarcomeres: a comparison between gastrocnemius and soleus muscles of the adult rat. Eur J Appl Physiol Occupat Physiol 1995;70:49–57. Hoffer MM, Knoebel RT, Roberts R. Contractures in cerebral palsy. Clin Orthopaed 1987;219:70–7. Huijing PA. Architecture of the human gastrocnemius muscle and some functional consequences. Acta Anatomica 1985;123:101–7. Huijing PA. Muscle, the motor of movement: properties in function, experiment and modelling. J Electromyogr Kinesiol 1998;8:61–77. Huijing PA. Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. J Biomech 1999a;32: 329–45. Huijing PA. Muscular force transmission: a unified, dual, or multiple system? a review and some explorative experimental results. Arch Physiol Biochem 1999b;170:292–311. Huijing PA. Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis. J Electromyogr Kinesiol 2007;17:708–24. Huijing PA, Baan GC. Extramuscular myofascial force transmission within the rat anterior tibial compartment: proximo-distal differences in muscle force. Acta Physiol Scand 2001a;173: 297–311. Huijing PA, Baan GC. Myofascial force transmission causes interaction between adjacent muscles and connective tissue: effects of blunt dissection and compartmental fasciotomy on length force characteristics of rat extensor digitorum longus muscle. Arch Physiol Biochem 2001b;109:97–109. Huijing PA, Jaspers RT. Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand J Med Sci Sports 2005;15:349–80. Huijing PA, van de Langenberg RW, Meesters JJ, Baan GC. Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles. J Electromyogr Kinesiol 2007;17:680–9. Jones DA, Round JM. Histochemistry, contractile properties and motor control. In: Jones DA, Round JM, editors. Skeletal muscle in health and disease. Manchester, UK: Manchester University Press; 1992. p. 55–77. Kawakami Y, Ichinose Y, Fukunaga T. Architectural and functional features of human triceps surae muscles during contraction. J Appl Physiol 1998;85:398–404.

655

Kozin SH, Bednar M. In vivo determination of available brachioradialis excursion during tetraplegia reconstruction. J Hand Surgery [Am] 2001;26:510–4. Kreulen M, Smeulders MJ, Hage JJ, Huijing PA. Biomechanical effects of dissecting flexor carpi ulnaris. J Bone Joint Surgery [Br] 2003;85:856–9. Kreulen M, Smeulders MJ, Veeger HE, Hage JJ, van der Horst CM. 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;29:55–60. Lance JW. Symposium synopsis. In: Feldman RG, Young RR, Koella WP, editors. Miami: Symposium Specialists 1980. p. 485–500. Leclercq C. General assessment of the upper limb. Hand Clin 2003;19:557–64. Lieber RL, Friden J. Intraoperative measurement and biomechanical modeling of the flexor carpi ulnaris-to-extensor carpi radialis longus tendon transfer. J Biomech Eng 1997;119:386–91. Lieber RL, Friden J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 2000;23:1647–66. Lieber RL, Friden J. Clinical significance of skeletal muscle architecture. Clin Orthopaed 2001:140–51. Lieber RL, Friden J. Spasticity causes a fundamental rearrangement of muscle–joint interaction. Muscle Nerve 2002;25:265–70. Lieber RL, Jacobson MD, Fazeli BM, Abrams RA, Botte MJ. Architecture of selected muscles of the arm and forearm: anatomy and implications for tendon transfer. J Hand Surgery [Am] 1992;17:787–98. Lieber RL, Loren GJ, Friden J. In vivo measurement of human wrist extensor muscle sarcomere length changes. J Neurophysiol 1994;71:874–81. Lieber RL, Ponten E, Burkholder TJ, Friden J. Sarcomere length changes after flexor carpi ulnaris to extensor digitorum communis tendon transfer. J Hand Surgery [Am] 1996;21:612–8. Lieber RL, Friden J, Hobbs T, Rothwell AG. Analysis of posterior deltoid function one year after surgical restoration of elbow extension. J Hand Surgery [Am] 2003a;28:288–93. Lieber RL, Runesson E, Einarsson F, Friden J. Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material. Muscle Nerve 2003b;28:464–71. Lieber RL, Steinman S, Barash IA, Chambers H. Structural and functional changes in spastic skeletal muscle. Muscle Nerve 2004;29:615–27. Lieber RL, Murray WM, Clark DL, Hentz VR, Friden J. Biomechanical properties of the brachioradialis muscle: implications for surgical tendon transfer. J Hand Surgery [Am] 2005;30:273–82. Loren GJ, Lieber RL. Tendon biomechanical properties enhance human wrist muscle specialization. J Biomech 1995;28:791–9. Loren GJ, Shoemaker SD, Burkholder TJ, Jacobson MD, Friden J, Lieber RL. Human wrist motors: biomechanical design and application to tendon transfers. J Biomech 1996;29:331–42. Maas H, Baan GC, Huijing PA, Yucesoy CA, Koopman BH, Grootenboer HJ. The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finiteelement modeling. J Biomech Eng 2003a;125:745–53. Maas H, Jaspers RT, Baan GC, Huijing PA. Myofascial force transmission between a single muscle head and adjacent tissues: length effects of head III of rat EDL. J Appl Physiol 2003b;95:2004–13. Maganaris CN. Force–length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 2001;172:279–85. Maganaris CN. Force–length characteristics of the in vivo human gastrocnemius muscle. Clin Anatomy 2003;16:215–23. Malaiya R, McNee AE, Fry EL, Gough M, Shortland AP. The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. J Electromyogr Kinesiol 2007;17:657–63. Meijer HJM, Baan GC, Huijing PA. Myofascial force transmission between antagonistic rat lower limb muscles: effects of single muscle or muscle group lengthening. J Electromyogr Kinesiol 2007;17: 698–707.

656

M.J.C. Smeulders, M. Kreulen / Journal of Electromyography and Kinesiology 17 (2007) 644–656

Mirbagheri MM, Barbeau H, Ladouceur M, Kearney RE. Intrinsic and reflex stiffness in normal and spastic, spinal cord injured subjects. Exp Brain Res 2001;141:446–59. Muramatsu T, Muraoka T, Kawakami Y, Shibayama A, Fukunaga T. In vivo determination of fascicle curvature in contracting human skeletal muscles. J Appl Physiol 2002;92:129–34. Murray WM, Bryden AM, Kilgore KL, Keith MW. The influence of elbow position on the range of motion of the wrist following transfer of the brachioradialis to the extensor carpi radialis brevis tendon. J Bone Joint Surgery [Am] 2002;84-A:2203–10. O’Dwyer NJ, Ada L. Reflex hyperexcitability and muscle contracture in relation to spastic hypertonia. Curr Opin Neurol 1996;9:451–5. Pappas GP, Asakawa DS, Delp SL, Zajac FE, Drace JE. Nonuniform shortening in the biceps brachii during elbow flexion. J Appl Physiol 2002;92:2381–9. Rassier DE, MacIntosh BR, Herzog W. Length dependence of active force production in skeletal muscle. J Appl Physiol 1999;86:1445–57. Riewald SA, Delp SL. The action of the rectus femoris muscle following distal tendon transfer: does it generate knee flexion moment?. Develop Med Child Neurol 1997;39:99–105. Rijkelijkhuizen JM, Baan GC, de Haan A, de Ruiter CJ, Huijing PA. Extramuscular myofascial force transmission for in situ rat medial gastrocnemius and plantaris muscles in progressive stages of dissection. J Exp Biol 2005;208:129–40. Rijkelijkhuizen JM, Baan GC, Huijing PA. Myofascial force transmission between antagonistic muscles located in opposite compartments of the rat hindlimb. J Electromyogr Kinesiol 2007;17:690–7. Rose J, Haskell WL, Gamble JG, Hamilton RL, Brown DA, Rinsky L. Muscle pathology and clinical measures of disability in children with cerebral palsy. J Orthoped Res 1994;12:758–68. Sejersted OM, Hargens AR, Kardel KR, Blom P, Jensen O, Hermansen L. Intramuscular fluid pressure during isometric contraction of human skeletal muscle. J Appl Physiol 1984;56:287–95. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Develop Med Child Neurol 2002;44:158–63. Smeulders MJ, Kreulen M. Adaptation of the properties of spastic muscle with wrist extension deformity. Muscle Nerve 2006;34:365–8. Smeulders MJ, Kreulen M, Hage JJ, Huijing PA, van der Horst CM. Intraoperative measurement of force–length relationship of human forearm muscle. Clin Orthopaed 2004:237–41. Smeulders MJ, Kreulen M, Hage JJ, Huijing PA, van der Horst CM. Overstretching of sarcomeres may not cause cerebral palsy muscle contracture. J Orthoped Res 2004b;22:1331–5. Smeulders MJ, Kreulen M, Hage JJ, Huijing PA, van der Horst CM. Spastic muscle properties are affected by length changes of adjacent structures. Muscle Nerve 2005:208–15. Tardieu C, Huet dlT, Bret MD, Tardieu G. Muscle hypoextensibility in children with cerebral palsy: I. Clinical and experimental observations. Arch Phys Med Rehabil 1982;63:97–102. Tardieu C, Lespargot A, Tabary C, Bret MD. For how long must the soleus muscle be stretched each day to prevent contracture?. Develop Med Child Neurol 1988;30:3–10. Vattanasilp W, Ada L. The relationship between clinical and laboratory measures of spasticity. Austr J Physiotherapy 1999;45:135–9. Willems ME, Huijing PA. Heterogeneity of mean sarcomere length in different fibres: effects on length range of active force production in rat muscle. Eur J Appl Physiol Occupat Physiol 1994;68:489–96.

Williams PE, Goldspink G. Changes in sarcomere length and physiological properties in immobilized muscle. J Anatomy 1978;127:459–68. Yucesoy CA, Huijing PA. Substantial effects of epimuscular myofascial force transmission on muscular mechanics have major implications on spastic muscle and remedial surgery. J Electromyogr Kinesiol 2007;17:664–79. Yucesoy CA, Koopman BH, Huijing PA, Grootenboer HJ. Threedimensional finite element modeling of skeletal muscle using a twodomain approach: linked fiber-matrix mesh model. J Biomech 2002;35:1253–62. Yucesoy CA, Koopman BH, Baan GC, Grootenboer HJ, Huijing PA. Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finiteelement modeling. J Biomech 2003a;36:1797–811. Yucesoy CA, Koopman BH, Baan GC, Grootenboer HJ, Huijing PA. Extramuscular myofascial force transmission: experiments and finite element modeling. Arch Physiol Biochem 2003b;111:377–88. Yucesoy CA, Koopman BH, Grootenboer HJ, Huijing PA. Finite element modeling of aponeurotomy: altered intramuscular myofascial force transmission yields complex sarcomere length distributions determining acute effects. Biomech Model Mechanobiol 2006 [Epub ahead of print]. Zancolli EA. Surgical management of the hand in infantile spastic hemiplegia. Hand Clin 2003;19:609–29. Zuurbier CJ, Heslinga JW, Lee-de Groot MB, Van der Laarse WJ. Mean sarcomere length–force relationship of rat muscle fibre bundles. J Biomech 1995;28:83–7.

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 areas of interest in research are muscle function, biomechanics and three-dimensional upper extremity movement analysis. 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.