0363-5465/99/2727-0533$02.00/0 THE AMERICAN JOURNAL OF SPORTS MEDICINE, Vol. 27, No.

4 1999 American Orthopaedic Society for Sports Medicine

Current Concepts
Biomechanics of Knee Ligaments
Savio L-Y. Woo,* PhD, Richard E. Debski, PhD, John D. Withrow, and Marsie A. Janaushek

From the University of Pittsburgh Medical Center, Musculoskeletal Research Center, Department of Orthopaedic Surgery, Pittsburgh, Pennsylvania
Biomechanics is the application of engineering principles to the study of forces and motions of biologic systems. As they relate to sports medicine, biomechanical studies are designed to determine the magnitude and direction of forces and moments of various tissues in and around a diarthrodial joint, as well as to measure the corresponding joint kinematics. This information can then be used by clinicians for the assessment of function of a normal or an injured joint and for planning the appropriate course of treatment. This article will first address the functional aspect of the knee joint, specifically the joint kinematics in multiple degrees of freedom, and it will describe the function of the individual components within the knee joint that enable its motion. Finally, the basic mechanical properties of these components, especially those of the tendons and ligaments, will also be described. Various soft tissue structures in and around the knee joint have been studied extensively; therefore, we will use these findings to illustrate a number of biomechanical principles and concepts. Much of the knowledge gained through the study of the knee joint can also be applied to other synovial joints of the body, such as the shoulder, ankle, or wrist. A glossary of the frequently used technical terms to describe the biomechanical properties of tissues, adapted from the AAOS Orthopaedic Basic Science book,53 is provided in Appendix 1 at the end of this paper. The determination of mechanical properties of ligaments and tendons has been challenging because of the many biologic and experimental testing factors; these factors contribute to the wide spectrum of published tensile property data. In recent years, advanced technology has become available that allows for more refined experimental procedures, enabling more accurate and reliable data collection. Specifically, the use of robotic technology has afforded us the opportunity to examine joint kinematics and the contribution of ligaments without artificial constraints.

JOINT KINEMATICS
Kinematics, as it relates to the human body, describes the motion of diarthrodial joints as well as locomotion and gait. An understanding of normal joint kinematics is important for comparison purposes during diagnosis of injury and for evaluating the success of treatment protocols. Clinical examination of an injured knee joint is performed by examining the motion of the knee and comparing this motion with that of the noninjured, contralateral knee. Excessive knee motion in a certain direction during examination may be an indication that a specific structure within the knee has been damaged. However, it is important to recognize that the knee does not move only in the direction of the applied load; motion also occurs naturally in other translational and rotational directions. Multiple Degrees of Freedom of Joint Motion The movement of the knee joint is governed by its ligaments, other supporting soft tissue structures, and the geometric constraints of the articular surfaces. The knee is capable of movement in six degrees of freedom: three rotations and three translations. The description of knee motion can be accomplished by relating movement to three principle axes: the tibial shaft axis, the epicondylar axis, and the anteroposterior axis, which is perpendicular to the other axes (Fig. 1).30 Translations along these axes are referred to as proximal-distal, medial-lateral, and anterior-posterior translation, respectively. Rotations about these axes are referred to as internal-external rotation, flexion-extension, and varus-valgus rotation, respectively. Early laboratory studies on knee motion frequently limited joint motion to a single degree of freedom. The results of these studies were reported as changes in knee kinematics, in one degree of freedom, in response to an applied load. For example, anterior tibial translation in response
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* Address correspondence and reprint requests to Savio L-Y. Woo, PhD, Musculoskeletal Research Center, Department of Orthopaedic Surgery, University of Pittsburgh, POB 71199, Pittsburgh, PA 15213. No author or affiliated institution has received financial benefit from research in this study.

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Figure 2. Schematic diagram of the robotic/UFS testing system with a knee specimen in place. Figure 1. Schematic diagram illustrating the six degrees of motion of the human knee joint. (Reproduced with permission from Woo SL-Y, Livesay GA, Smith: Kinematics, in Fu FH, Harner CD, Vince KG (eds): Knee Surgery. Baltimore, Williams & Wilkins, 1994, pp 155173.) to an anterior tibial load was measured while constraining other degrees of freedom (such as medial-lateral translation and internal-external rotation). Tests conducted in this manner yield knee kinematic data under artificially constrained conditions that do not necessarily represent the in vivo kinematics of the knee. One example of limitations imposed by constraining degrees of freedom is varus-valgus stress testing of the knee at various flexion angles. When knee motion is limited to three degrees of freedom (varus-valgus rotation, proximal-distal and medial-lateral translation), varus-valgus stability is increased and the medial collateral ligament is the primary restraint for resisting valgus moments applied to the tibia.38 However, when the knee is less constrained (allowing anteroposterior translation and internal-external tibial rotation), knee stability is reduced and the ACL becomes the dominant ligament for resisting valgus knee motion. This result is observed because the ACL controls coupled anteroposterior translations and axial tibial rotations to a greater degree than does the medial collateral ligament. Therefore, if one is interested in studying normal knee kinematics, a five degrees of freedom valgus stress test should be performed. In contrast, if one is interested in studying the function of the medial collateral ligament, a three degrees of freedom valgus test would be appropriate. Multiple degrees of freedom experiments have been performed by our research group using a robotic/universal force-moment sensor (UFS) testing system (Fig. 2). This system can operate in both force and position control. While operating in force control, the robot applies a predetermined external load to the specimen and the corresponding five degrees of freedom kinematics of the specimen are recorded. Alternatively, the robotic/UFS testing

system can operate under position control by moving the specimen along a previously recorded motion path and the UFS records a new set of force and moment data. This allows measurement of the in situ forces in various soft tissue structures using the principle of superposition (the vector difference in forces measured before and after the sectioning of a ligament can be attributed to the ligament because identical knee motions are repeated).25, 52

Normal Versus Injured Knee Joint The overall motion of the knee is controlled by interactions between its many supporting structures. If any one structure is damaged, the overall motion of the knee will likely be altered. Complete disruption of a ligament may lead to symptoms of knee instability. The resulting, altered motion of the knee may injure other structures, especially the menisci and the articular cartilage. Specific clinical examinations such as the anterior drawer test, Lachman test, and pivot-shift test are performed to assess ligament integrity. These tests are performed at given knee flexion angles and allow the tibia to displace anteriorly and also to rotate internally, producing five degrees of freedom motion.28 In the intact knee, anterior tibial translation of 3 to 5 mm is considered normal during an anterior drawer or Lachman test. In an ACL-deficient knee, anterior translation and internal rotation of the tibia are increased to varying degrees. In this scenario, other structures are recruited to resist the abnormal joint motion that is present in the ACL-deficient knee. From this information, one can see that normal function of the knee involves many soft tissue structures, and when a single ligament is disrupted, the remaining structures compensate by carrying increased loads. The increased demand placed on the structures may render them more susceptible to injury.

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CONTRIBUTION OF INDIVIDUAL STRUCTURES

The primary role of the ligaments surrounding the knee is to provide stability to the joint throughout its range of motion. Each ligament plays a role in providing stability in more than one degree of freedom as well as restraining knee motion in response to externally applied loads. Overall joint stability depends on the contributions of the individual ligaments as well as the interaction between ligaments. Knowledge of the in situ forces in the ligaments during normal knee function contributes to our understanding of injury mechanisms and aids in the development of rehabilitation protocols after knee injury. Determination of In Situ Forces in the Ligaments Recently, many devices have been used to measure the force in ligaments, including both contact and noncontact methods. Contact methods include devices that are attached to the ligament (for example, the buckle transducer),3, 4, 6, 10, 40, 41 implantable force transducer, modified pressure probe, and various strain gauges. With buckle transducers, the ligament is passed through a buckle, which deflects when the tension in the ligament increases. The deflected beam transducer (or implantable force transducer) and the implantable pressure transducer (or modified pressure probe) are similar to the buckle transducer, but must be implanted in the ligamentous tissue.29, 34 These devices work on the concept that increases in ligament tension will increase the transverse force on the implanted device. The force in the ligament is then determined during posttest calibration in which a relation between the deflection of the device and the force in the ligament is established. Devices attached to the subchondral bone beneath the ACL for direct measurement of in situ forces have also been used.20, 33 One study used a load cell attached to the tibial insertion of the ACL for measurement of the resultant forces in the ligament during testing.42, 43 The ACL was found to be loaded under both internal and external tibial rotation between full extension and 45 of flexion. An internal tibial torque of 10 N m produced a force on the order of 100 N in the ACL at 20 of flexion, while an external tibial torque of 10 N m produced a smaller force on the order of 50 N. Changes in ligament forces were also determined after the sectioning of the posterolateral structures. The force in the PCL increased after posterolateral-structure sectioning under an applied external torque, whereas the force in the ACL decreased. As will be illustrated later, the resultant measurement of ligament in situ force for constrained (limiting the degrees of freedom) versus unconstrained motion (where multiple degrees of freedom motion is allowed) is significantly different. Thus, it is difficult to compare results between different studies because the number of degrees of freedom used during testing has a significant effect on the resultant kinematics. When using noncontact methods for determining the in situ forces in a ligament, a device is used that avoids the potential alteration of the ligament response induced by

mechanical contact between the device and the ligament.27, 35, 36, 56 In our research center, in situ forces in the ACL were determined by combining ligament length data obtained from a six degrees of freedom kinematic linkage system with its load-elongation data. Under the application of a 100 N external anteroposterior load, the length of the entire ACL, as well as the anterior portion of the ACL, were determined. Subsequently, the load-length curve for the same portions of the ACL during tensile tests were determined.55 With these two sets of data, the in situ forces in the ACL in response to the anteroposterior load were determined. It should be noted that this is an indirect approach and requires an assumption of the direction of force in the ACL. Another noncontact method involves the use of the UFS, which measures three forces and three moments along and about a Cartesian coordinate system fixed with respect to the sensor.26 For a rigid body attached to the UFS, the three forces collected by the sensor can be used to determine the magnitude and direction of an external force applied to the body. The point of application of the force can also be determined based on evaluation of the three moments recorded. Recently, we have used a UFS in combination with a robotic manipulator to develop a testing system that can directly determine the in situ forces in ligaments without contact with the tissue or dissection of the joint. This technology has led to accurate simulation of multiple degrees of freedom joint motion and enables the determination of the in situ forces in individual soft tissue structures in and around the joint in response to external loading conditions. Additionally, the robotic/UFS testing system allows researchers to apply multiple and combined loading conditions to the same knee specimen, thus eliminating interspecimen variability. Furthermore, the robotic/ UFS testing system can provide a quantitative comparison of in situ forces in intact ligaments with those in replacement grafts. This enables investigators to determine the efficacy of reconstruction in reproducing normal force transmission through the replacement graft. The next section will illustrate the potential of this testing system. Individual Ligament Function: Effect of Constraints Using the robotic/UFS testing system, it is possible to assess the five degrees of freedom joint kinematics and determine the in situ forces in the knee ligaments.24, 52 The robotic/UFS testing system is advantageous because it has a high degree of repeatability for position, orientation, and load application. Additionally, it is capable of producing loads similar to those used during clinical examinations.17 The robotic manipulator can learn the complex motion of a knee specimen in response to external loads and reproduce these motions after the specimen has been modified (that is, after transecting a ligament or reconstructing an injured ligament). The UFS simultaneously records the forces and moments acting on the knee while the knee is being moved by the robot. This testing system has been used to study the effect of constraint conditions on knee kinematics and the in situ

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force in the ACL in response to an externally applied load. Anteroposterior tibial loads were applied to the same knee when it was in an unconstrained (five degrees of freedom) and a constrained (one degree of freedom, anteroposterior translation only) condition (Fig. 3). For the unconstrained case, the anterior tibial load resulted in anterior tibial translation that was 1.3 to 1.4 times greater than the translation observed in the constrained knee from 30 to 90. Although the magnitude of the in situ force did not differ significantly between the constrained and unconstrained cases (Fig. 4), the direction of the in situ force did differ significantly (Fig. 5). In the unconstrained case, the force was directed more parallel to the tibial plateau. Constrained knee motion also caused a shift in the force sharing between the anteromedial and posterolateral bundles of the ACL. Thus, constraints placed on the motion of the knee will yield very different results. The direction of the force vector and distribution of in situ forces within the ACL provide important functional information. Therefore, it is clear that, during experiments, the knee joint must be allowed multiple degrees of freedom motion to accommodate the complexity of the knee.

Figure 4. Graph depicting the percent of the in situ force in the ACL supported by the anteromedial bundle under 100 N anterior tibial loading (N 8; mean plus or minus SD).

TENSILE PROPERTIES OF LIGAMENTS

Knowing that the ligaments are essential elements for proper knee function, it is necessary to characterize their biomechanical properties, that is, the relation between length and tension. A uniaxial tensile test is generally employed to obtain fundamental ligament properties.

Figure 5. Schematic diagrams showing the direction of the in situ forces the ACL for a right knee at 30 of knee flexion, under a 100-N anterior tibial load.

These properties are valuable for our understanding ligament function and for evaluating which types of graft material would be best suited for their replacement. Because ligaments are usually short, the bone-ligament-bone complex is normally tested as a functional unit. However, testing the entire complex makes it difficult to distinguish between elongations of the midsubstance and those of the bony insertions. With the advent of video systems, a method has been developed for tensile testing whereby both the structural properties of the bone-ligament-bone complex and the mechanical properties of the ligament substance are obtained simultaneously.60 Basic Anatomy Ligaments are composed of water and densely packed collagen fibers that run in the longitudinal direction, parallel to the axis of loading. The collagen is primarily type I (approximately 70% fat-free dry weight), with a small amount of type III (3% to 10% fat-free dry weight) and trace amounts of types V, X, XII, and XIV collagen. Noncollagenous proteins such as elastin, a fibrillar protein (less than 1%), and proteoglycans are also present. Water and proteoglycans provide lubrication and spacing, which are critical to the gliding function of a joint.

Figure 3. Schematic diagrams detailing the joint motions allowed during unconstrained and constrained test conditions. V-V, varus-valgus; A-P, anterior-posterior; M-L, medial-lateral; I-E, internal-external; P-D, proximal-distal.

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The insertions of tendons and ligaments into bone are functionally adapted to dissipate forces through the transition from soft tissues to bone70; insertions are classified as either direct or indirect. Direct insertions consist of four morphologic zones: tendon, fibrocartilage, mineralized fibrocartilage, and bone (Fig. 6). Indirect insertions consist of a superficial layer, which connects directly with the periosteum, with deeper layers that anchor to the bone via Sharpeys fibers. A ligament that exhibits both types of insertions is the medial collateral ligament; it has a direct femoral insertion and an indirect tibial insertion. Collagen fibrils in ligaments are arranged in varying degrees of crimp such that an increase in tensile force results in the recruitment of more fibrils to help resist the increased load. The crimped nature of the fibrils serves to guide joint motion and provide restraint at extremes of joint motion. When a ligament is loaded in tension, it responds by elongating. During normal activity, ligaments are easily elongated to maintain normal kinematics and allow the joint to move easily and smoothly. With higher externally applied loads, such as during exercise, the stiff-

ness of the ligament increases to restrict any excessive motion in the joint. However, if the applied load exceeds the maximum limits of the ligament, as may occur during athletic events, the risk of ligament damage increases. Structural Properties of Bone-Ligament-Bone Complex Load-Elongation Curve. The structural properties that characterize the behavior of the bone-ligament-bone complex are represented by a load-elongation curve obtained from a uniaxial tensile test. These properties depend on the geometry of the ligament in addition to the properties of the bony insertion sites. During tensile testing of the bone-ligament-bone complex, load is measured simultaneously with the corresponding elongation. By plotting elongation as the independent variable, and load as the dependent variable, a load-elongation curve is obtained (Fig. 7). This curve can be divided into several regions. The first region, or the toe region, has a low initial stiffness and is nonlinear. During activity, the crimped collagen fibers are easily extended and small initial forces produce large elongations. Next, there is a linear region with a higher stiffness (the slope of the curve), which results from the fibers being stretched. Finally, the curve reaches the ultimate load that the structure can withstand. On additional loading, failure of the bone-ligamentbone complex occurs. The selected parameters used to represent the structural properties of the bone-ligamentbone complex are the linear stiffness (measured in newtons per millimeter), ultimate load (measured in newtons), ultimate elongation (measured in millimeters), and energy absorbed at failure (measured in newton-millimeters, and calculated by determining the area under the entire load-elongation curve) (Fig. 7). Mechanical Properties of the Ligament Substance Mechanical properties characterize the behavior of the ligament substance and are represented by a stress-strain curve. These properties depend on the collagen composition, fiber orientation, and the interaction between collagen and the ground substance. Determination of Strain. Strain ( ) is defined as the

Figure 6. Top, a direct insertion with its four morphologic zones: tendon (T), uncalcified fibrocartilage (UF), calcified cartilage (CF), and bone (B). Bottom, an indirect insertion where the deep fibers of the ligament (L) pass into bone through a well-defined zone of fibrocartilage (F). The arrow represents the line of calcification.

Figure 7. A schematic load-elongation curve for ligament.

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deformation per unit length of a ligament and can be found by placing markers on the soft tissue in the region to be studied (such as midsubstance). Strain is calculated by the formula (l lo)/lo; where lo represents the initial distance between the markers and l is the length after a load is applied. Strain has no units but is usually expressed as a percent. Strain in ligaments has been measured by a wide variety of devices including liquid mercury strain gauges,2, 11, 19, 39, 45 Hall-effect strain transducers (Microstrain, Inc., Burlington, Vermont),8, 9, 12, 22, 23, 50 and the differential-variable-reluctance-transducer (Microstrain). These devices are attached to the tendon or ligament along the direction of the soft tissue. Noncontact methods have also been developed to measure strains. The video dimension analyzer system60, 68 and the Motion Analysis System (Motion Analysis Corporation, Santa Rosa, California) both use a video camera and an image-processing system. All of these techniques have the advantage of measuring midsubstance strain independently of strain at the insertion sites. In addition, noncontact techniques do not require mechanical or physical attachments onto the soft tissue substance when the strains are measured. Determination of Stress. Stress (measured in newtons per square millimeter) is defined as the load per unit cross-sectional area of a ligament. It can be calculated by the formula: F / A where is stress, F is the externally applied load, and A is the cross-sectional area of the ligament. Because stress is defined as the tensile load per cross-sectional area, an accurate measure of cross-sectional area is necessary. The earliest biomechanical studies used gravimetric methods in which the volume of water displaced by a specimen could be related to cross-sectional area by assuming a simple crosssectional shape.1, 44 Mechanical devices like calipers have also been used to measure the width and thickness of a specimen, with the cross-sectional area obtained by assuming a rectangular or elliptical shape.58 These methods are adequate for simple geometric structures, but may introduce large errors for ligaments that have more complex geometries. Noncontact methods have been developed that have the advantages of avoiding tissue deformation and providing more accurate cross-sectional area measurements for more complex geometries. These methods involve an optical system (either visible or laser light) for measurement, or an image-reconstruction technique to determine the cross-sectional area or shape, or both.37 Examples of noncontact approaches include the shadow amplitude method21 and the profile method.31 Another method uses a laser micrometer system that casts a band of laser light across a ligament that is rotating, allowing diameter readings from all directions.58 Recently, a laser reflectance system that can account for concavities in the tissue has been developed.14 These laser methods perform much better than contact methods for measurement of complex geometries. In addition to accurate cross-sectional area readings, they allow for graphic representation of the ligaments profile. Stress-Strain Curve. During a uniaxial tensile test, the

midsubstance strain is measured while simultaneous load-elongation behavior is recorded. Using the load data, along with the cross-sectional area measurement of the ligament, stress can be calculated. The stress-strain curve for a ligament is nonlinear (Fig. 8) and can be divided into several regions. The first region is the nonlinear toe region. The second region is linear; the stress is linearly proportional to the strain and the slope of this region is called the Youngs (or tangent) modulus (E, measured in megapascals). Physically, a higher modulus can have several different meanings: the ligament is made of a stiffer material, there is more collagen per unit area, or its collagen fibrils have larger diameters. Other important parameters obtained from this curve are the ultimate stress (or sometimes called the tensile strength, measured in megapascals), ultimate strain, and the strain energy density (measured in megapascals). The ultimate stress, ultimate strain, and strain energy density are properties of the ligamentous tissue and therefore can only be determined if failure occurs within the substance of the tissue. For this reason, it is also important to know the mode of failure of the specimen. Time- and History-Dependent Behavior: Viscoelasticity Ligaments also display time- and history-dependent viscoelastic properties.15 These properties include creep (an increase in the length over time under a constant load), stress-relaxation (a decrease in the load when the ligament is held at a fixed elongation), and hysteresis (energy dissipation with continual loading and unloading) when subjected to a cycle of loading and unloading. Stretching or prolonged activity may cause a gradual creep of the ligaments that results in increasing knee laxity after exercise. However, after a period of rest, the ligaments can recover and return to their original resting length, while the knee also returns to its original stiffness. Conversely, cyclic loading and unloading results in a corresponding cyclic stress relaxation, as the ligament is experiencing a continuous decrease in stress with increasing cycles. This behavior may serve as a mechanism for pro-

Figure 8. A schematic stress-strain curve resulting from tensile testing of a ligament.

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tecting the ligament from fatigue failure. The unloading path of the load-elongation curve does not follow the same path as the loading portion, known as the hysteresis effect, indicating energy dissipation (Fig. 9). The peak load decreases with an increasing number of cycles (that is, stress relaxation); however, after a number of cycles the loading and unloading curves become repeatable, indicating the importance of preconditioning before experimental testing. Examples demonstrating the importance of viscoelastic properties of ligaments are numerous. During ACL reconstruction, the initial force applied to tension the graft decreases over time as a result of stress relaxation. This effect has also been demonstrated in the primate patellar tendon where the stress in the tendon was reduced to 69.8% of the initial stress within 30 minutes.13 However, preconditioning the graft can reduce the amount of stress relaxation by approximately 50% when compared with nonpreconditioning. These viscoelastic properties can also be used to the surgeons advantage during intraoperative spinal distraction. By applying the distraction in small steps separated by a few minutes, the peak forces applied to the instrumentation and its insertions on the vertebra can be reduced over 50% because of vertebral soft tissue creep.47

with another difficult. Some of these factors are identified and are discussed in the next section to help the readers identify the effects of these factors on the mechanical properties of ligaments. Biologic Factors The biomechanical properties of ligaments and tendons depend on several biologic factors. For example, differences in specimen age, species, skeletal maturation, anatomic location, as well as exercise or immobilization can affect the properties of these tissues. Effects of Maturation and Age. Skeletal maturation has significant effects on the biomechanical properties of ligaments and tendons. In general, these properties seem to improve once skeletal maturity is reached. Several studies performed on the rat tail tendon have shown an increase in collagen fibril size, ultimate load, and ultimate tensile strength as the animal ages from puberty to adulthood32, 46, 48 with no further changes observed until senescence. Similarly, rapid increases in the cross-sectional area, stiffness, and ultimate load of the rabbit medial collateral ligament were found with maturation.66, 68 In addition to changing mechanical properties during maturation, the mode of failure of the femur-medial collateral ligament-tibia complex (FMTC) also changes. In younger animals, where the epiphyses are not yet closed, the mechanism of failure is most often tibial avulsion. However, in skeletally mature animals in which the epiphyses are closed, ligaments are more likely to fail at the midsubstance.66 In recent studies on the human femur-ACL-tibia complex (FATC), values of structural properties from young human donors have been significantly higher than those from older donors. The stiffness and ultimate load for the young ACL specimens (from donors aged 22 to 35 years) were upwards of three times as high as those for older specimens, and reported to be 242 28 N/mm and 2160 157 N, respectively.49, 62 The properties obtained for femur-ACL-tibia complexes from young donors should be used as the strength requirements for ACL grafts used for reconstructions. Effect of Exercise. Recent research has suggested that an increase in physical activity could improve the biomechanical properties of the medial collateral ligament. Short-term exercise regimens, ranging from treadmill walking to running and swimming, have been studied using various animal models. The tensile properties of swine femur-medial collateral ligament-tibia complexes were assessed after 12 months of exercise59; some increases in the structural properties of these complexes were observed. When normalized to body weight, the ultimate load and linear stiffness increased 38% and 14%, respectively, compared with the complexes of the sedentary controls. The mechanical properties also showed a minimal change with an increase in tensile strength and ultimate strain of 20% and 10%, respectively. Effect of Immobilization/Remobilization. After musculoskeletal injuries, immobilization is often used to protect damaged tissue from further harm during the early stages

FACTORS AFFECTING THE MECHANICAL PROPERTIES OF LIGAMENTS

Although much work has been done to determine the mechanical properties of ligaments, the biologic and experimental testing factors have contributed to differences in reported results, making comparison of one set of data

Figure 9. An example of a hysteresis curve. Typical loading (up arrow) and unloading (down arrow) curves from cyclic loading of soft tissue. The shaded area between the curves, called the area of hysteresis, represents the energy losses within the tissue.

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of healing. However, the effect of joint immobilization can have profound, adverse effects on the joint. Joint stiffness as a result of synovial adhesions and proliferation of fibrofatty connective tissue has been observed both clinically and experimentally after immobilization.5, 65 The effects of joint immobilization and remobilization on ligament properties on the rabbit medial collateral ligament have also been studied in our research center.61 Tensile testing of rabbit femur-medial collateral ligamenttibia complexes was performed after 9 and 12 weeks of immobilization, in addition to 9 weeks of immobilization followed by 9 weeks of remobilization. The 9- and 12-week immobilized groups had ultimate loads (tensile load required for failure) that were 31% and 29% of the contralateral controls, respectively (P 0.01). The elastic modulus of the medial collateral ligament also decreased after immobilization. In the remobilized group, the mechanical properties returned nearly to those levels of the control group; however the structural properties remained inferior to those of the controls. Experimental Testing Factors Several known experimental factors can also affect the determination of biomechanical properties of ligaments and tendons. Some factors such as the direction of the applied external load and temperature of the specimen during testing will have an effect on these properties, while strain rate and proper specimen storage will not. Specimen Orientation. The medial collateral ligament is an extraarticular ligament with a relatively simple geometry and is oriented such that simultaneous loading of all ligament fibers is possible. However, most bone-ligamentbone complexes are nonuniform in geometry and shape; therefore, the direction of applied force and the initial position of the ligament are both important for accurate assessment of load-elongation behavior. This is especially true for the ACL, which has a complex geometry and a nonuniform arrangement of the fiber bundles, making uniform loading of the entire ligament impossible. Thus, the structural properties of the femur-ACL-tibia complex depend largely on the direction of applied load and initial orientation of the ligament during testing. Force application along the anatomic orientation of the ACL allows a greater proportion of the fiber bundles to be loaded than does applying the force in an arbitrary direction. In a study performed on the human femur-ACL-tibia complex, using 27 pairs of cadaveric knees, the structural properties of the ACL were examined by applying a force along the axis of the ACL as well as along the long axis of the tibia in the contralateral specimen.62 The structural properties for the femur-ACL-tibia complexes tested along the anatomic axis were significantly different from those of the complexes tested along the tibial orientation. The linear stiffness for the femur-ACL-tibia complexes tested in the anatomic orientation was 11% to 45% higher than for those tested in the tibial orientation, depending on specimen age. The ultimate load of the femur-ACL-tibia complexes was also 35% higher when tested in the anatomic direction. Additionally, data from tests performed

on rabbit femur-ACL-tibia complexes demonstrated that structural properties obtained from loading along the tibial axis varied with knee flexion angle. However, for specimens loaded along the axis of the ligament, the structural properties were independent of knee flexion.63 Effect of Temperature. Studies have been performed to evaluate the relationship between temperature and tensile properties of ligaments, but these studies have yielded varying results. One study found no significant differences in mechanical properties of ligaments over a temperature range of 0 to 37C,51 while others have reported a decline in elastic modulus and stiffness with increasing temperature.7 Studies in our laboratory on canine femur-medial collateral ligament-tibia complexes have revealed that ligaments do exhibit temperature-dependent viscoelastic properties. Each canine femur-medial collateral ligamenttibia complex was tested by cyclic loading in a saline bath at varying temperatures from 2 to 37C.64 These tests revealed an inverse relationship between stiffness and temperature, and also showed that the ligament relaxed to lower values under cyclic loading performed at higher temperatures. Strain Rate. The influence of strain rate on injury is a debated topic. Sports-related injuries are estimated to occur at strain rates that vary from relatively slow rates to rates as high as 500 percent per second.16 Although injuries to ligaments often result at high strain rates, many experimental studies have examined the ligament properties under low-to-medium rates of strain because of the limitations of testing approaches and data collection systems. However, data from recent studies suggest that the effects of strain rate are overestimated, especially when comparing strain rates such as 1 versus 100 percent per second. In fact, the status of the insertions, not the strain rate, may be the primary factor in determining the type of injury to the bone-ligament-bone complex. The effect of strain rates has been studied in medial collateral ligaments from skeletally mature rabbits using elongation rates over 4.5 decades, ranging from 0.008 to 113 mm/s, corresponding to strain rates of the medial collateral ligament midsubstance of 0.01 to 200 percent per second.69 The structural properties of the femur-medial collateral ligament-tibia complex differed minimally between the lowest and highest rates of elongation. The ultimate load increased from 311.5 12.1 N at 0.008 mm/s to 403.7 7.5 N at 113 mm/s. The mechanical properties of the medial collateral ligament followed similar trends, but the increases were even smaller. The ultimate tensile strength of the medial collateral ligament increased only 40% from the 0.01 to 200 percent per second strain. A similar study was also performed on the rabbit ACL.18 Studies of the ACL at slow (0.003 mm/s), medium (0.3 mm/s), and fast (113 mm/s) rates of elongation showed similar effects. Small differences were observed in the modulus of elasticity between the slow and medium strain rates, but the modulus at the fast extension rate was only 30% higher. Specimen Freezing for Storage. It is often necessary to freeze tissue allografts before reconstruction, or to store a specimen before biomechanical testing. Therefore, the ef-

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fect of freezing and storing on biologic tissue is of great interest. There have been several studies investigating the effects of postmortem storage on tissue properties, but the results are conflicting.54, 57 One study found that the rabbit ACL becomes less extensible 1 hour after death,54 but others found no changes after 96 hours in the rabbit femur-ACL-tibia complex.57 The rabbit femur-medial collateral ligament-tibia complex was studied in our research center to examine the effects of storage at 20C for 1 to 3 months.67 Each specimen was wrapped in saline-soaked gauze, with the muscle and soft tissue left intact, and sealed in an airtight plastic bag to prevent dehydration. Before testing, the specimens were thawed overnight in a refrigerator at 4C. Previously frozen specimens and fresh rabbit knees were subjected to cyclic loading and then tensile tested to failure. No significant differences in cyclic stress relaxation, ligament cross-sectional area, ultimate load, ultimate deformation, or energy absorbed to failure were noted between the two tested groups. Additionally, the mechanism of failure was the same in all specimens, suggesting that freezing has no significant effects on ligament properties or on the insertion sites. The one exception, which occurs during the first few cycles of loading and unloading, is a decrease in the area of hysteresis. This phenomenon becomes insignificant with further cycling. Therefore, if care is taken to store specimens properly, the resultant effects on the biomechanical properties will be minimal.

REFERENCES
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SUMMARY
Significant advances have been made during the past 25 years in characterizing the properties of ligaments as a tissue and as an individual component in the bone-ligament-bone complex. The contribution of ligaments to joint function have also been well characterized. We have presented many studies that sought to characterize the tensile and viscoelastic properties of ligaments. As a result of these investigations, some of the most important experimental and biologic factors affecting the measurements of these properties have been identified and elucidated. The identification of the tensile properties of normal ligaments can serve as the basis for evaluating their success in healing and repair after injury. Furthermore, characterization of normal ligament function is crucial for diagnosing joint injuries as well as for evaluating reconstruction strategies and developing rehabilitation protocols. The recent introduction of robotic technology to the study of joint kinematics has resulted in significant advances in the understanding of the relative importance of ligaments to joint function. With the more accurate simulation of joint kinematics that include multiple degrees of freedom motion, data on the in situ forces in ligaments can be used to improve the treatment of ligament repair and reconstruction. More complex external loading conditions that mimic sports activities and rehabilitation protocols can also be introduced in the future. Furthermore, this technology can be extended to study other frequently injured joints, such as the shoulder.

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30. Grood ES, Suntay WJ: A joint coordinate system for the clinical description of three-dimensional motions: Applications to the knee. J Biomech Eng 105: 136 144, 1983 31. Gupta BN, Subramanian KN, Brinker WO, et al: Tensile strength of canine cranial cruciate ligaments. Am J Vet Res 32: 183190, 1971 32. Haut RC: Age-dependent influence of strain rate on the tensile failure of rat-tail tendon. J Biomech Eng 105: 296 299, 1983 33. Henning CE, Lynch MA, Glick KR Jr: An in vivo strain gage study of elongation of the anterior cruciate ligament. Am J Sports Med 13: 2226, 1985 34. Holden JP, Grood ES, Korvick DL, et al: In vivo forces in the anterior cruciate ligament: Direct measurements during walking and trotting in a quadruped. J Biomech 27: 517526, 1994 35. Hollis JM: Development and application of a method for determining the in-situ forces in anterior cruciate ligament bundles. Doctoral thesis, University of California, San Diego (UCSD), 1988 36. 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Simon SR: Orthopaedic Basic Science. Rosemont, IL, American Academy of Orthopaedic Surgeons, 1994 54. Smith JW: The elastic properties of the anterior cruciate ligament of the rabbit. J Anat 88: 369 380, 1954 55. Takai S, Woo SL-Y, Livesay GA, et al: Determination of the in situ loads on the human anterior cruciate ligament. J Orthop Res 11: 686 695, 1993 56. Vahey JW, Draganich LF: Tensions in the anterior and posterior cruciate ligaments of the knee during passive loading: Predicting ligament loads from in situ measurements. J Orthop Res 9: 529 538, 1991 57. Viidik A, Sandqvist L, Magi M: Influence of postmortal storage on tensile strength characteristics and histology of rabbit ligaments. Acta Orthop Scand (Suppl 79): 138, 1965 58. Woo SL-Y, Danto MI, Ohland KJ, et al: The use of a laser micrometer system to determine the cross-sectional shape and area of ligaments: A comparative study with two existing methods. J Biomech Eng 112: 426 431, 1990 59. 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APPENDIX 1 - GLOSSARY
Biomechanics. The application of engineering principles to the study of the forces and motions of biological systems. Center of rotation. A point around which circular motion is described. Component of a force. The magnitude of a force in a specific direction; in three dimensions, a force has three components. Coupling. Motion in which a rotation or translation of a rigid body about one axis is associated with a rotation or translation of that same rigid body about another axis. Creep. A viscoelastic property of materials whereby the deformation continues to increase, without the loss of material, when subjected to a constant force. Degree of freedom. The number of independent quantities needed to describe the position of an object; for example six degrees of freedom describe the position of any segment of the body in three dimensions (three angles and three coordinates on the body). Dynamics. Study of relationships between forces, moments, and motions of objects. Elastic (Youngs) modulus. Measure of material stiffness defined by dividing stress by strain; for linear materials, it is the slope of the stress-strain curve. Elasticity. Property of a material that allows the material to return to its original shape and size after being deformed. Force. A vector that describes the magnitude of a push or pull on an object in a specific direction; a physical quantity that can accelerate or deform, or both, a body. Hysteresis. Conversion of strain energy to heat during cyclic loading; physically, the mechanical energy that is

Adapted with permission from Simon.53

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lost during each cycle of loading such that the unloading path is offset from the loading path. In situ. Latin: at a point; that is, in situ forces, which are measured experimentally, represent the forces present in a particular structure in its natural environment at a given position. In vitro. Latin: in nonliving; that is, in vitro testing is performed on a nonliving subject or nonliving specimen structures removed from their natural environments. In vivo. Latin: in living; that is, in vivo testing is performed on a living subject. Kinematics. Description of motion made up of translations and rotations about an axis, regardless of how the motion came about. Linear strain ( ). Change of length ( l) divided by original length (lo), such that l/lo. Material properties. Any physical characteristic of an objects substance that is independent of the objects structure and geometry. Mechanical properties. A subset of material properties that relates stresses to strains. Normal stress. A force acting perpendicular to the area of interest divided by that area. Range of motion. The range of translation and rotation of a joint for each of its six degrees of freedom. Rotation. Revolving motion of an object about a point or an axis. Stiffness. Resistance of a structure to a deformation.

Strain. See linear strain. Strain rate. Speed at which a material is deformed. Stress. See linear stress. Stress relaxation. Decrease in stress at constant strain by internal molecular rearrangement. Stress-strain plot. The experimental data relating stress (F/A) to strain ( l/lo). Tension. A force tending to elongate an object. Torque. See moment. Translation. Linear motion of an object without regard to rotation. Ultimate strain. Maximum strain sustained by the specimen before failure of the material. Ultimate stress. Maximum stress sustained by the specimen before failure of the material. Uniaxial loading. A loading condition in which the force is applied along a single axis (that is, in one direction). Vector. A quantity that has a magnitude, a line of application, and point of application, commonly represented by a directed line segment. Viscoelastic. In biology, a property of a tissue that exhibits both viscous and elastic behavior (creep and stress relaxation). The materials stress-strain behavior depends on strain rate. Youngs modulus (E). The intrinsic stiffness of a linear material in tension or compression expressed as the ratio of stress to strain: E stress/strain.