mechanical considerations in the design of surgical reconstructive procedures

Journal of Biomechanics 35 (2002) 1039–1045

Keynote lecture from the American Society of Biomechanics Conference 2001

Mechanical considerations in the design of surgical reconstructiveprocedures

Jan Frid!ena,*, Richard L. Lieberb

aDepartment of Hand Surgery, Sahlgrenska University Hospital, SE-413 45 G .oteborg, SwedenbDepartments of Orthopaedics and Bioengineering, University of California and Veterans Administration Medical Centers, San Diego, USA

Accepted 8 March 2002

Abstract

Tendon transfers are used to restore arm and hand function after injury to the peripheral nerves or after spinal cord injury.

Traditional guidelines to choose the length at which the transferred muscle should be attached have a poor scientific foundation. We

postulate that passive tension only becomes significant at relatively long lengths and that passive tension as the major factor in intra-

operative decision making may result in overstretch of the muscle-tendon unit (MTU) and accompanying low-active force

generation. It appears unwise to rely on unknown factors, such as slippage or stress relaxation, to correct an overstretched transfer.

Instead, we suggest the use of intra-operative sarcomere length measurements to predict and set the optimal MTU length during

reconstructive upper limb surgery. r 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Tendon transfer; Muscle architecture; Muscle mechanics; Sarcomeres; Length–tension relationship

1. Introduction

Tendon transfer reconstructive procedures are used toreplace lost function in tetraplegia, peripheral nerve andbrachial plexus injuries, spasticity, and after directinjury to the muscle-tendon unit (MTU). The trans-ferred MTUs provide a functional substitute forparalyzed or ruptured muscles and may also be usedto restore joint balance in spasticity. Tendons of donormuscles are transected distally, rerouted to a newposition and reinserted into a tendon graft or directlyreattached to bone or tendon stump. The motor nerveand blood supply of the transferred MTU remain intact.The donor muscle should be expendable such that thefunction lost by its sacrifice is relatively small comparedto the function being restored. Donor muscles must beinnervated and should not have been previously injured.

The ultimate outcome is a transfer generating max-imal strength at a desired joint angle. However, toachieve that goal, several important pre-, peri- andpostoperative decisions have to be made. Many of these

decisions relate to normal surgical procedures and theremainder of this review will focus on the considerationsessential for the success of tendon transfers based on anunderstanding of muscle physiology and biomechanicsof upper extremity muscles.

2. Muscle architecture and length–tension relationship in

tendon transfer surgery

There is no doubt that muscle architecture influencesthe performance of a donor in muscle-tendon transfersurgery. The properties that most influence musclefunction are physiologic cross-sectional area (PCSA)and fiber length (Lieber, 1993). At the macroscopic level,force generation is directly proportional to PCSA(Brand and Hollister, 1993; Lieber, 1993). Muscleexcursion and contraction velocity are directly propor-tional to muscle fiber length (Lieber, 1992). A well-established principle of tendon transfer reconstruction isto use donor muscles with similar ‘‘strength’’ andexcursion as the muscles being replaced.

The potential muscle excursion is the distance amuscle contracts from its slack length plus the distance amuscle can be stretched from its slack length (Brand and

*Corresponding author. Tel.: +46-31-3423039; fax: +46-31-

820589.

E-mail address: [email protected] (J. Frid!en).

0021-9290/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved.

PII: S 0 0 2 1 - 9 2 9 0 ( 0 2 ) 0 0 0 4 5 - 3

Hollister, 1993). It has been estimated that thesedistances are approximately equal and that contractionfrom slack length is about 40 percent of muscle fiberlength (Smith and Hastings, 1980). Since sarcomeres arethe fundamental units of muscles, it seems intuitive thatthere would be a simple relationship between musclefiber length and excursion. This has been found to betrue in mechanical studies of intact frog single-musclefibers (Gordon et al., 1966)

The potential amplitude of a muscle is directlyproportional to the resting length of its fibers (Brandand Hollister, 1993). Muscle excursion may be estimatedduring surgery, but the selection of donor muscles canbe better planned by using the available data on forearmmuscle architecture. In addition, the effective excursionof a MTU can be increased by intercalary joints overwhich the tendon travels (Smith and Hastings, 1980).One important example of this phenomenon used inreconstructive hand surgery is the fact that the wristmuscles have shorter fibers than the digital extensors.Providing the wrist can operate through its full range ofmotion, a wrist flexor transferred into the extensordigitorum communis (EDC) can produce full metacar-pophalangeal (MCP) joint extension when the transfermuscle functions simultaneously with wrist flexion.

Few measurements of muscle passive tension inhuman upper extremity muscles have been performed.Typically, passive properties are extrapolated fromanalogous studies in amphibian or rodent skeletalmuscle. In a case report, Freehafer and colleaguesexplicitly measured passive and active tension in variousmuscles used for tendon transfer (Freehafer et al., 1979).They generated the active length–tension relationshipvia electrical stimulation of the peripheral nerve andfound that slack length roughly corresponded tooptimal length across the five muscles reported. Un-fortunately, simple predictions of the relationshipbetween passive tension and muscle length are notpossible due to variation in fiber length within upperextremity muscles (Brand et al., 1981; Lieber et al., 1990,1992). Also, the possibility that resting sarcomere lengthvaries between muscles cannot be ruled out.

Theoretically, the surgeon can choose the jointposition at which maximal muscle force is generated

after a tendon transfer, given the knowledge of themuscle length corresponding to optimal sarcomerelength. The tactile ‘‘feel’’ of muscle-tendon unit passivetension is, however, not a reliable guideline forestimating optimal sarcomere length due to muscle-specific passive elements of tension (Labeit and Kol-merer, 1995). Because of the passive elements of muscletension, ‘‘slack length’’ (muscle length when insertion isdetached) is not necessarily synonymous to ‘‘optimalmuscle length’’ (defined as the muscle length at whichsarcomere length is optimal for force generation). As aresult, there is much confusion in the literatureregarding the terms optimal length, slack length, restinglength, in situ length and in vivo length, all of which areoften incorrectly interchanged (Table 1). Consequently,slack length is not a good reference for selecting optimalsarcomere length for force generation, and experiencedhand surgeons do not select the optimal tension forgenerating force during tendon transfers (Frid!en andLieber, 1998). Recently, intra-operative sarcomerelength measurements using laser diffraction have beenshown to be a valuable tool for setting correct tensionfor tendon transfers (Fig. 1, Frid!en and Lieber, 1998;Lieber et al., 1994, 1996). Thus, while it is commonlybelieved that inserting a muscle in the stretched positionmay be beneficial since the repair site may slip or stress-relax, it would be unwise to rely on this unknown factorto optimize an overstretched transfer.

3. Limitation of excursion due to connective tissue factors

Due to muscle architectural differences, differentmuscles have variable and not easily predictableexcursions. In addition, a number of ‘‘other’’ factorsinfluence muscle excursion. This is clearly illustrated bythe brachioradialis (BR) muscle, which is reported tohave a fiber length (12 cm) that would predict afunctional range of about 6 cm (Lieber et al., 1994).Intraoperative experience with this muscle indicates thatthis is not the case. BR excursion rarely exceeds 1 cmeven after release of the distal insertion or 4 cm afterrelease along the entire forearm. Still, the BR is anattractive donor muscle used to replace lost hand

Table 1

Definition of muscle length terms

Optimal length: Length at which myofilament overlap is optimal and force is maximal (2.6–2.8mm in human muscle, Walker and Schrodt,

1973, 2.0–2.2mm in frog muscle, Gordon et al., 1966)

Slack length: Length at which muscle force equals zero. This length is unknown for most human muscles but is the retracted length that

a muscle becomes after severing the tendinous insertion

Resting length: A clear definition of this length is not possible since passive tension is variable between muscles and the resting condition is

not well defined. Should not be used to describe an absolute length

In situ length: Muscle length under a specified joint angle configuration. Should not be used to describe an absolute length

In vivo length: Muscle length under a specified joint angle configuration. Should not be used to describe an absolute length

J. Frid!en, R.L. Lieber / Journal of Biomechanics 35 (2002) 1039–10451040

function after nerve or spinal cord injury. It is widelyused because it does not cross the finger or wrist jointsand is therefore expendable. In light of the importanceof BR as a donor muscle and the discrepancy betweenanatomical values reported in the literature and mostsurgeon’s practical experience, we suspected that, eitherprevious architectural studies were oversimplified in

terms of BR fiber length or other nonmuscle tissues werepresent in vivo that restricted BR excursion. Wedetermined the detailed architectural properties of theBR muscle along with its mechanical attachment tosurrounding tissues in an effort to understand itsminimal excursion even after relatively complete release(Frid!en et al., 2001). Our study demonstrated that a

Fig. 1. Laser diffraction device used to measure sarcomere length in a patient undergoing surgical tendon transfer. The laser beam is directed toward

the prism tip, is reflected up through the muscle and creates a diffraction pattern that is imaged onto a photodiode (PDA). The PDA is interfaced via

a custom circuit board to a controller board and analog-to-digital converter within the computer. This apparatus permits real-time, high-resolution

muscle sarcomere length values displayed in a graphical form for use by the surgeon.

3.2 mm

1.7 mm3.4 mm

5.0 mm

9.2 mm

7.5 mm

1 min

10 m

m

Fig. 2. Length–time records measured during progressive release of BR muscle from the radius and surrounding tissues. The time intervals

(horizontal axis) correspond to the time it took to release the muscle tendon from its surrounding. For each of the first three releases, 30 s of

dissection was allowed while loading (simulating an assistant pulling the tendon while released). These releases are technically simple because it is

only the distal tendon that is detached. For the ensuing more complicated releases, 1.5min was allowed for dissection on each segment free from

neighboring muscle and fascial tissue. A constant load of 4.9 N was applied to the distal tendon while released. The magnitude of each release length

is given in the panel to the right. Each color represents a 3 cm release with the overall release length obtained for each segment shown to the right-

hand side of the panel. Vertical lines separating colors represent the excursion magnitude after each release. Friden, J., Albrecht, D., Lieber, R., 2001,

reproduced by permission of Lippincott Williams & Wilkins r 2001.

J. Frid!en, R.L. Lieber / Journal of Biomechanics 35 (2002) 1039–1045 1041

release of B3 cm was necessary simply to linearly loadthe MTU, providing enough free tissue on which toalign the tendon clamp. Subsequent release, up to 9 cmproximal from the insertion, provided minimal addi-tional mobility (Fig. 2). Finally, as the release pro-gressed toward the elbow, large increases in mobilitywere measured. These large increases were typicallyobtained at the point of muscle–muscle contactcompared to the more distal connections which weretendon-bone and tendon-surrounding connective tissuecontacts. Anatomically, the first muscle–muscle connec-tion to be severed was that between the BR and theextensor carpi radialis longus (ECRL) muscle followedby release of the BR-pronator teres (PT) and BR-flexorcarpi radialis (FCR) connections which also providedincreased excursions. Based on a combined under-standing of our mechanical and architectural data, wethus believe that BR excursion is limited by connectivetissue constraints. There is a prominent internal tendonon the deep aspect of the muscle as well as a significanttendinous inscription along the deep border of themuscle. Should this limit excursion, one could argue forthe division of this inscription as a method to increaseBR functional range.

4. Consequences of overstretch in tendon transfer surgery

To be able to select a donor muscle with properstrength potential in a tendon transfer, the surgeon hasto consider (1) the function of the transfer to be made,(2) the composite strength of the antagonists, and (3)joint mobility. There are multiple factors that affect thetransfer strength and its origin is multiple and complex,and therefore there is a strong need for surgicalguidelines to match the physiological cross-sectionalarea of the donor muscle (PSCA) to that of the recipientmuscle. Critical factors that influence active jointmotion are muscle excursion, muscle force generatingcapability and joint moment arm. Traditional principlesused to choose the length at which the transferredmuscle should be attached are relatively vague and havenot been thoroughly examined (Frid!en and Lieber,1998). The biomechanical determinant of active muscleforce after transfer is the classic Blix curve that depictsthe relationship between active force, passive force andmuscle length (Gordon et al., 1966). The sarcomerelength–tension relationship illustrates that active muscleforce increases as myofilament overlap increases andpassive muscle force increases as sarcomere lengthincreases (Fig. 3). Optimal length is not uniquely relatedto length at which passive tension is zero. This wasillustrated by our previous study of the flexor carpiulnaris (FCU) muscle length–tension properties usinglaser diffraction when transferred to wrist or fingerextensor recipient tendons (Lieber and Frid!en, 1997;

Lieber et al., 1996). In general, the short FCU fiberswere stretched to sarcomere lengths exceeding 3.5 mmi.e., well beyond optimal filament overlap. We foundthat the transferred FCU muscles that were placed at arelatively high passive tension generated only about25% of maximum active force (Fig. 4, Frid!en andLieber, 1998). This could provide an explanation for thecommon statement among hand surgeons that atransferred muscle loses at least one strength grade.Clearly, the active tension corresponding to a particularpassive tension depends on the resting sarcomere lengthof the muscle studied. If resting sarcomere length is

4.54.03.53.02.52.01.51.00

20

40

60

80

100

120

Sarcomere Length (µm)

1.6 µm

1.3 µm

Fig. 3. Length–tension curve obtained using human filament lengths

and assuming the sliding filament mechanism proposed by Gordon

et al. (1966). Top: schematic of filament lengths. Schematic myofi-

brillar filament overlaps at three different sarcomere lengths are

illustrated along the length–tension curve.

4.54.03.53.02.52.01.51.00

20

40

60

80

100

120

Sarcomere Length (µm)

2.8 3.8 4.8

#1 #2

Fig. 4. Schematic examples of two different relationships between

passive tension and sarcomere length. If resting sarcomere length is

short (#1), at a given tension, sarcomere length will be near optimal. If

resting sarcomere length is long (#2), at a given tension, sarcomere

length will be far beyond optimal and the resulting transfer will have

no power.


short (#1 in Fig. 4), at a given passive tension, sarcomerelength will be close to optimal. If resting sarcomerelength is long (#2 in Fig. 4), at a given passive tension,sarcomere length will be beyond optimal and theresulting transfer will have little or no power. Usingthe data obtained in many of our studies, we believe thatthe upper extremity muscles have a resting sarcomerelength between 2.5 and 3.5 mm, but the factors thatgovern an individual muscle’s resting sarcomere lengthremain to be determined. Until such factors are clarified,we suggest that the use of passive tension as the majorfactor in intra-operative decision making may result inoverstretch of the MTU and a corresponding low-activeforce generation.

We have had good reasons to believe that overstretchwas an important factor to the substantial slippageobserved in the muscle tendon attachments afterreconstruction of elbow extension in tetraplegic patients(Frid!en et al., 2000). In a recent investigation, wetherefore measured the detailed architectural propertiesof the posterior deltoid (PD) and triceps muscles incadaveric specimens as well as mathematically modeledthe posterior deltoid-to-triceps tendon transfer. Itwas done to determine whether this is an architecturallyappropriate transfer and whether the transfer isvulnerable to tendon slippage as we observed earlier(Frid!en et al., 2000). Based on the observation thatposterior deltoid fiber length is very long (12378mm)and would be predicted to have a large excursion, wesuggest that this transfer is an excellent choice to restorelost elbow extension function. Because the elbow jointmoment arm is onlyB12mm and thus muscle excursiononly B25mm, it would be difficult to imagine surgicallyplacing the muscle in a position where it would result inan insufficient active range of motion. A possiblelimitation of the transfer is that the transferred portionof the deltoid would only generate about 20% of theforce of the normal triceps (Fig. 5). Thus, while thetransfer might be adequate to power antigravity move-ments and placing of the hand in space, it may notsuffice for high force elbow extension maneuvers such astransfer to and from a wheelchair or to bear full bodyweight as in push-ups.

In principle, the PD-to-Triceps transfer represents theopposite extreme of architectural matching betweendonor and recipient muscle properties compared to thetendon transfer we recently studied, the FCU-to-EDCtransfer. In that transfer, the short fibers of the singlejoint FCU (42mm) could not provide adequate excur-sion to provide adequate wrist, metacarpophalangeal,and digital extension. Conversely, based on the longposterior deltoid fiber length measured in the PD-Triceps architecture study, we conclude that the slippagethat can occur after PD-Triceps transfer would havelittle functional effect. It is impossible to predict theprecise effect of this degree of slippage without knowl-

edge of the actual sarcomere length of the transferredmuscle. In fact, slippage could result in force increase,force decrease or no change whatsoever depending onthe sarcomere length at the time of transfer.

5. Synergism

Synergism occurs when muscles contract simulta-neously to augment the effectiveness of each muscle.An example of synergistic muscles are the digitalextensors and the wrist flexors. Both muscle groupsoften function simultaneously during digital extension.Many surgeons believe that using synergistic groupsof muscles as donors facilitates transfer retraining,e.g., synergistic FCR or FCU muscles to extend thefingers usually function better than the nonsynergisticflexor digitorum superficialis (FDS) muscle (Greenet al., 1999). Another example of synergism is themanner in which the digital flexors and wrist extensorsfunction together. Transferring the extensor carpiradialis longus (ECRL) to the deep digital flexors ofthe index and the long fingers for tetraplegia or highmedian nerve palsy are examples of a commonsynergistic transfer.

6. Joint moment arm changes in tendon transfer surgery

Many joints are multiaxial and, as a consequence,moment arms change during joint rotation. Loren et al.(1996) demonstrated that wrist extensor momentsincrease with increasing extension and the flexormoments increase with increasing flexion. Thus, wristflexor–extension torque depends on both flexor and

300250200150100500

200

400

600

800 DeltoidTriceps

Muscle Length (mm)

Mus

cle

For

ce (

N)

Fig. 5. Predicted muscle length-tension properties of posterior deltoid

(dashed line) and combined triceps muscle (solid line) based on

architectural properties measured. Operating range is shown for the

transferred deltoid as the elbow is flexed from full extension to 1501 of

flexion (black bar over dashed curve). Fried!en, J., Lieber, R.L., 2001,

reproduced by permission of W.B. Saunders r 2001.


extensor muscle length and instantaneous moment arm.This phenomenon of varying moment arms is probablycommon in the musculoskeletal system. In this context,it is important to remember that, when planning thereconstruction, it is crucial to avoid overcorrection. Anovercorrection could undo the attempted balance of thetransfer because of hypermobility due to laxity fromprolonged paralysis. A hypermobile joint powered by astrong transferred muscle may sublux the joint, and this,in turn, could restrict the antagonistic force to theparticular joint. For example, replacement of abductionof a thumb with a hypermobile CMC joint couldeliminate the flexor pollicis longus action to flex the IPjoint.

The three elements, which influence torques arecontrolled by the tendon transfer surgeon. PCSA iscontrolled by donor muscle selection and sarcomerelength and moment arm are influenced by position andtechnique for donor tendon insertion. It is intuitive thatin tendon transfers, the larger the moment arm, thehigher the torque, at the expense of lower availablemuscle excursion and joint motion, and conversely,the shorter the moment arm the lower the torque but themore muscle excursion and joint motion is achieved.Since moment arms can change with joint motion andmuscle force changes with joint position due to varyingsarcomere length, joint torque will be influenced by theinteraction of these factors (Loren et al., 1996). Momentarm and muscle force may not always influence jointtorque to the same extent and their relative magnitudesare not necessarily in phase during joint motion. Forexample, during wrist extension, extensor moment armsinfluence the torque profiles more than extensor muscleforces, whereas, during wrist flexion, the wrist flexorforces are more influential than the flexor moment arms(Loren et al., 1996). The maximal torque will occur atthe joint position where the product between muscleforce and moment arm is maximal. Thus, the surgeonmust not only have a good estimate of optimal musclelength but also understand the magnitude of themoment arms. Ideally, measuring intraoperative sarco-mere length during surgery and knowing the momentarms of joints at various degrees of rotation wouldguarantee the best outcome (Lieber et al., 1996). Despiteall the complicated factors involved in the decision-making in muscle tendon transfers, these procedures arehighly successful.

7. Conclusion

Muscle architecture knowledge, basic knowledge ofmuscle physiology and joint mechanics together withintra-operative measurements of sarcomere length,provide the transfer surgeon with the necessary toolsto even more accurately select desired joint torque

profiles and thereby optimize the outcome of muscle-tendon transfer surgery.

Acknowledgements

This work was supported by the Swedish ResearchCouncil (Grant 11200), Departments of Veteran Affairs,NIH Grant AR35192, and The Inga–Britt and ArneLundberg Foundation.

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