Tensile properties of the human femuranterior cruciate ligament-tibia complex The effects of SAVIO L-Y.
specimen age and orientation*
WOO,†‡ PhD,
J. MARCUS HOLLIS,† PhD, DOUGLAS J. ADAMS,§ MS, ROGER M. LYON,§ MD, AND SHINRO TAKAI,† MD
From the †Musculoskeletal Research Laboratories,
Department of Orthopaedic Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania, and the §Orthopaedic Bioengineering Laboratory, University of California, San Diego, California Although the
tensile behavior of the human ACL has been studied for many decades, there are only a few published works characterizing its stiffness and strength properties, partly due to the difficulties in procuring young and healthy cadaveric specimens. In addition, its complex anatomy makes the geometric alignment for tensile loading difficult. In 1976, Kennedy et al.19 measured the strength of the isolated ACL in cadavers with a median age of 62 years and reported an ultimate load of 640 N. Trent et al. 34 tested the femur-ACL-tibia complex (FATC) in human knees between 25 and 55 years of age and reported an average stiffness of 141 N/mm and ultimate load of 633 N. In the same year, a landmark article published by Noyes and Grood25 showed the linear stiffness and ultimate load for six FATCs from three young donors between 16 and 26 years of age to be 182 ± 56 N/mm (mean ± SD) and 1730 ± 660 N, respectively. In addition, older specimens from 20 cadaver knees with ages ranging from 48 to 86 years were tested and the corresponding values reduced to 129 ± 39 N/mm and 734 ± 266 N, respectively. The data for the younger knees have since been the basis for matching the tensile properties of autograft and allograft tissues4,24,28 as well as for the design of artificial ligaments for ACL replacement. In a recent consensus workshop on the human ACL, new data on tensile properties of FATC were reported.3o, 37 Rauch et al .21,3’ reported similar data to that of Noyes and Grood,25 while Woo et a1.37 reported higher stiffness and strength values for FATC from younger donors. On the other hand, there exist many published works on the tensile properties of FATC from animals, including rabbits,2,12, 36 dogs, 1,4,6,9,15,16,26,27,31,32.35,39 goats,18 and monkeys.3, 7, 25 In general, the knee flexion angle and the direction of the applied tensile load with respect to the ACL were chosen arbitrarily, in spite of the fact that an early study by
ABSTRACT The structural properties of 27 pairs of human cadaver knees were evaluated. Specimens were equally divided into three groups of nine pairs each based on age: younger (22 to 35 years), middle (40 to 50 years), and older (60 to 97 years). Anterior-posterior displacement tests with the intact knee at 30° and 90° of flexion revealed a significant effect of knee flexion angle, but not of specimen age. Tensile tests of the femur-ACLtibia complex were performed at 30° of knee flexion with the ACL aligned vertically along the direction of applied tensile load. One knee from each pair was oriented anatomically (anatomical orientation), and the contralateral knee was oriented with the tibia aligned vertically (tibial orientation). Structural properties of the femur-ACL-tibia complex, as represented by the linear stiffness, ultimate load, and energy absorbed, were found to decrease significantly with specimen age and were also found to have higher values in specimens tested in the anatomical orientation. In the younger specimens, linear stiffness (242 ± 28 N/mm) and ultimate load (2160 ± 157 N) values found when the femurACL-tibia complex was tested in the anatomical orientation were higher than those reported previously in the literature. These values provide new baseline data for the design and selection of grafts for ACL replacement in an attempt to reproduce normal knee kinematics. *
Presented at the 16th annual meeting of the AOSSM, Sun
Valley, Idaho,
July 1990 $ address correspondence and reprnt requests to: Samo L-Y. Woo, PhD, Department of Orthopaedic Surgery, M-272 Scaife Hall, Urnversity of Pittsburgh,
Pittsburgh,
PA 15261.
217
218
Alm et al/ reported that the strength of the canine FATC at 90° of flexion was affected by the axial rotation of the tibia. Gupta et ail. 16 chose to test the canine FATC with the tibia rotated 90° in order to untwist the ACL. Recently, the ultimate load for the canine FATC was demonstrated to decrease significantly with increasing angle of knee flexion.&dquo; Our laboratory confirmed these findings in rabbits and further demonstrated that the direction of tensile load also played an important role on the structural properties of the rabbit FA TC. 38 To alleviate the geometric complexity of the et al.,5 as well as our laboratory,23 have separated the ACL into individual portions for tensile testing. In this way, the tensile stresses in the ligament would be more uniform, and the mechanical (material) properties of the ligament as represented by the stress-strain curve obtained are more reliable. Our laboratory has recently developed an experimental device whereby the FATC can be oriented and tested at any desired loading direction as well as knee flexion angle.23 Paired porcine knee specimens were tested, and the linear stiffness, ultimate load, and energy absorbed at failure for the FATC in both orientations were determined. These parameters were found to be significantly higher in specimens with the tensile load applied along the anatomical axis of the ACL than in those with the tensile load applied along the long axis of the tibia. The objectives of this study were to examine the effects of 1) donor age and 2) direction of the applied load with respect to specimen orientation on the structural properties of the human FATC. It is hypothesized that if the direction of loading was along the normal anatomical orientation of the ACL, the resulting stiffness and strength values would be higher. In that case, the new data obtained from younger, healthy donors could be used as a basis for selection and design of ACL replacements.
ACL, Butler
MATERIALS AND METHODS
Experimental apparatus An apparatus incorporating multiplanar adjustments for testing human knee specimens was used. The device allows the knee to be oriented in a variety of positions, thus permitting the tensile properties of the FATC to be measured at a preselected orientation and knee flexion angle (Fig. 1). Adjustments can be made such that the direction of applied tensile load can be aligned with the ACL without changing the normal anatomical angles of ACL insertion into the femur and the tibia (Fig. 2a). The apparatus consists of two major components to accommodate the femur and tibia. The femoral component permits the femur to be rotated in the frontal and sagittal planes.21 The entire fem-
also be moved in the transverse (horizontal) plane by adjustments of two sets of linear bearings. The tibial component allows rotational adjustments of the tibia in the frontal and sagittal planes similar to those used for the femoral component. A shaft on rotary bearings, to which the tibia and its mounting cylinder are attached, oral component
provides unrestrained axial tibial rotation. Transverse motion of the tibial component is eliminated by rigidly fixing it to the base of an Instron testing machine (Instron Corp., Canton, MA). The linear bearings of the femoral component and changes in the crosshead position permit alterations of the mediallateral, anterior-posterior (AP), and proximal-distal translations of the femur with respect to the tibia. The frontal and sagittal adjustments and the cylindrical clamps for both the femur and tibia permit alteration of knee flexion angle and internal-external and varus-valgus rotations. This device is also adjustable so that the intact knee specimen can be mounted for AP displacement testing at any desired angle of knee flexion
(Fig. 3).
The stiffness of the apparatus was first determined by securing a 15 cm long section of human femur into the two thick-walled cylinders with three 6 mm diameter transfixing bolts through each end of the bone. The cylinders were made of solid aluminum, with an outside diameter of 82 mm and an ovoid-shaped hole to accommodate the shaft of the bone. The setup was tensile loaded up to 3000 N, and its stiffness was found to be 508 N/mm and linear up to 3000 N.
Specimen preparation of cadaveric human knees were equally divided into three age groups, representing younger, middle, and older aged donors. The younger group consisted of knees from donors aged 22 to 35, with a mean age of 29 years. Seven pairs were from donors who had died following acute trauma (Table 1). The middle-aged group was from donors aged 40 to 50, with a mean age of 45 years. The cause of death for these donors was primarily acute trauma. The older age group was from donors aged 60 to 97, with a mean age of 75 years. The cause of death for this age group was largely due to chronic illness, such as cancer. The paired knee specimens were obtained after routine autopsy, freezing, and storage at -20°C. Prior to testing, each knee was thawed at room temperature for 24 hours, and was then dissected free of all skin and subcutaneous and muscle tissues, leaving the joint capsule and knee ligaments intact. The patella and patellar ligament were removed. The femur and tibia were cut to a length of approximately 15 cm from the joint line, and each was secured into a thick-walled aluminum cylinder using three 6 mm diameter transfixing bolts. The knee specimen, with its mounting cylinders, was then secured within the femoral and tibial components of the testing apparatus (Fig. 1). The soft tissues of all specimens were kept moist throughout the specimen preparation and testing with physiologic saline.
Twenty-seven pairs
Experimental procedure
can
were performed. First, the intact knee specimen was subjected to AP displacement tests to quantify the ACL’s contribution to the stability of each knee. Second,
Two different tests
tensile
testing of the FATC structural properties
was
performed to
examine its
219
1. Schematic diagram of the experimental apparatus used to evaluate the structural properties of the human FATC. Shown is the preparation of a specimen tested in the anatomical orientation. The clamps are oriented so that the tensile load is applied with the FATC specimen remaining in its anatomical position. A, anterior-posterior view; B, medial-lateral view.
Figure
displacement testing. AP displacement tests were peron each knee specimen (with all ligaments and joint capsule intact). The knee was oriented with the tibia aligned perpendicular to the applied load (i.e., horizontally) and the femur positioned with the knee at 30° of flexion (Fig. 3). The axial tibial rotation and medial-lateral and proximaldistal translations were unrestrained. We performed cyclic AP drawer tests using a 100 N force applied to the femur at a displacement rate of 20 mm/min. The AP load displacement curves were recorded, and the total AP displacement for the 10th cycle was used. The knee was then flexed to 90°, and the test was repeated. Tensile testing. One knee from each pair was randomly assigned to be tested with the tensile load applied along the axis of the ACL while preserving the normal anatomical angles of ACL insertion into the femur and tibia (anatomical AP
formed
orientation). The contralateral knee was tested with the applied along the long axis of the tibia (tibial orientation) without preserving the anatomical orientation
tensile load
of the ACL. All FATCs were tested at 30° of knee flexion. For specimens tested in the anatomical orientation, the fat pad was removed to allow visualization of the ACL. The femoral and tibial components of the clamps were rotated in the medial-lateral plane and then in the AP plane so as to align the long axis of the ACL with the direction of tensile load (Figs. 2a and 3) while the knee angle was maintained at 30° of flexion. The FATC was then secured in this position. The joint capsule, meniscus, and other soft tissues were then removed, leaving only the ACL. The orientation of the ACL with respect to the line of applied tensile load
checked by means of a plumb line, and minor rotational alignment was done prior to tensile testing. Thus, the direction of tensile loading for this test was aligned with the anatomical axis of the ACL. For the contralateral specimen, which was tested in the tibial orientation, the tibia was secured vertically along the loading axis in both the frontal and sagittal planes (Fig. 2b). The remaining soft tissues around the knee were removed, leaving only the ACL. The femur was translated medially and anteriorly so that the femoral insertion of the ACL was directly above its tibial insertion and the ACL was aligned along the line of tensile load. The FATC was then secured in this position and only vertical elongation along the tibial axis was permitted. The reason for aligning the ligament in this manner was to examine the effects of nonanatomical angles of ACL insertions on the load-elongation properties of the FATC. In other words, although the ACL was aligned in the line of tensile load application, its natural anatomical orientation with respect to the femur and tibia was not maintained. This procedure was different from many previous studies in the literature in which the ACL was often oriented at an angle with respect to the direction of applied tensile load. A small preload of 2.5 N was applied to the FATC after which it was cyclically preconditioned between 0 and 2 mm of deformation at a rate of 20 mm/min. After 10 cycles, the FATC was loaded to failure at a rate of 200 mm/min. The load and elongation were recorded continuously using a strip chart recorder. The resulting load-elongation curve, corrected for the stiffness of the testing apparatus, represented was
220
Figure 3. Schematic diagram demonstrating that the experimental apparatus as described in Figure 1 can be adapted for AP displacement testing of an intact knee at preselected angles of knee flexion. properties of FATC were analyzed using a two-way ANOVA. Significance was set at P < 0.05. RESULTS
Figure 2. Schematic of specimen orientation for tensile testing. a, for the anatomical orientation, the tensile load is applied along the axis of the ACL while the normal anatomical angles of ACL insertion to bone are preserved. b, for the tibial orientation, the femur is moved anteriorly and medially so that the tensile load can be applied in line with the femoral and tibial insertion sites. Note that in this case, the anatomical angles of ACL insertion to bone are distorted. the structural properties of the FATC, and parameters such as the linear stiffness, ultimate load, energy absorbed at failure, and failure mode were documented. Linear stiffness was defined as the linear slope of the load-elongation curve between 3 and 7 mm of elongation. Statistical analysis. The effects of specimen age and knee flexion angle on AP displacement were analyzed statistically using a two-way analysis of variance (ANOVA). Likewise, the effects of specimen age and orientation on the tensile
AP displacement tests. Typical load-displacement curves obtained from AP displacement testing of the intact human knees are shown in Figure 4. The AP displacement, defined as the total displacement between 100 N of anterior and 100 N of posterior load, was 45% and 34% higher at 30° of flexion than at 90° for the younger-aged and middle-aged specimens, respectively, but only 12% higher for the older group (Table 2). Two-way ANOVA revealed a significant effect of flexion angle on the AP displacement (P < 0.001) but not of specimen age (P > 0.10). There was no significant interaction between age and flexion angle (P > 0.10), indicating no interdependence between specimen age and knee flexion angle. Tensile testing. Typical load-elongation curves for the paired FATC from the younger age group tested in the anatomical and tibial orientations are shown in Figure 5. The two curves show that the structural properties of the
221 TABLE 1
History of cadaver donors
Figure 5. Typical load-elongation curves for paired FATC from a younger donor demonstrating the differences in results between the anatomical and tibial orientations. different modes of failure of the FATC were observed: 1) avulsion of bone at the insertion site, 2) insertion site failure but without bony fragment, and 3) ligament substance failure of collagen fibers. The modes of failure were found to be different between specimen orientations. The tensile load-elongation curves for all FATC specitested are plotted in Figure 6. Both donor age and the specimen orientation had a significant effect on the resulting structural properties of the FATC (Table 3). For specimens tested in the anatomical orientation, the values of stiffness were 242 ± 28 N/mm, 220 ± 24 N/mm, and 180 ± 25 N/ mm for the younger, middle, and older aged specimens, respectively. For specimens tested in the tibial orientation these values reduced to 218 ± 27 N/mm, 192 ± 17 N/mm, and 124 ± 16 N/mm. A two-way ANOVA showed a significant effect of age on the linear stiffness (P < 0.001), with the younger specimens having a higher linear stiffness than the older specimens (Table 3). The linear stiffness for the FATCs tested in the anatomical orientation was 11%, 15%, and 45% higher than those tested in the tibial orientation for the younger, middle, and older aged specimens, respectively, although statistical significance was not shown (P 0.07) for the effect of specimen orientation. There was not a significant correlation between age and orientation (P > 0.50), indicating that the differences documented between age groups were independent of the specimen orientation. The ultimate load for the younger specimens tested in the anatomical orientation (2160 ± 157 N) was found to be 44% higher than that of the middle-aged group (1503 ± 83 N), and 328% higher than that of the older group (658 ± 129 mens
Figure 4. Typical load-displacement curves for a young knee during AP displacement testing at 30° and 90° of flexion. TABLE 2 Effects of specimen age and knee flexion angle on the AP displacement of intact knees (mean ± SEM) -
=
FATC were affected by the specimen orientation. The FATCs tested in the anatomical orientation resulted in a higher linear stiffness, ultimate load, and energy absorbed at failure than those tested in the tibial orientation. Three
222 TABLE 3 Effects of specimen age and orientation on the structural properties of the FATC (mean ± SEM)
Figure 7. The effect of specimen age on FATC ultimate load. Data on ultimate load as a function of specimen age and orientation using a least squares curve fit demonstrated that the strength of FATC decreases in an exponential manner. The values of energy absorbed at failure followed the same trend as for the linear stiffness. The younger specimens absorbed more energy at failure than did the older specimens, while the specimens tested in the anatomical orientation absorbed only slightly more energy at failure than those tested in the tibial orientation (Table 3). Statistical analysis revealed that energy absorbed was significantly affected by age (P < 0.001), and although energy absorbed was similarly affected by specimen orientation, statistical significance was not shown (P 0.06). Again no significant interaction was found between age and orientation (P > =
Figure 6. The load-elongation curves for FATC tested at 30° of flexion in the (a) anatomical orientation and (b) tibial orientation for younger, middle, and older human donors.
N). A decrease related to increasing age was also seen for those tested in the tibial orientation. For the younger FATCs tested in the anatomical orientation, the value was 35% higher than that for the tibial orientation (1602 ± 167 N), but the difference diminished with increasing age (Fig. 7). Statistically, both specimen age and orientation had a significant effect on the ultimate load (P < 0.001 and P < 0.05, respectively; Table 3). There was no significant correlation between age and specimen orientation (P > 0.10), indicating that the differences due to age and specimen orientation were
independent.
0.10). The older specimens had a higher incidence of substance failure (12/18, or 67%) than the younger (5/18, or 28%) or middle (8/18, or 44%) aged specimens regardless of the specimen orientation (Fig. 8). Several of the specimens from younger donors (9/18, or 50%) failed by avulsion of a piece of bone directly under the tibial insertion. FATCs tested in the anatomical orientation failed predominantly by midsubstance tear for older specimens (7/9, or 78%) or bony avulsion for younger specimens (6/9, or 67%). The FATCs tested in the tibial orientation had a higher incidence of insertion failure by sequentially &dquo;peeling off’ individual fiber bundles (13/27, or 48%) than those tested in the anatomical orientation (1/27, or 4%).
223
elongation behavior of the ligament would prevent a direct correlation between the results of tensile testing and the AP
displacement test. The study of tensile testing
of the FATC has identified
two important factors that influence the structural properties of the human FATC-specimen age and orientation. The large decreases in linear stiffness and ultimate load, as well as energy absorbed at failure, of the FATC with increasing age are similar to the previous findings by others.25, 30 These large reductions are due to many factors. The decrease
in types and levels of physical activity with age, the physical condition of older donors, and the changes in joint geometry
Figure 8. Histograms of modes of failure of human FATC tested in the (a) anatomical and (b) tibial orientations from the younger, middle, and older human donors studied. DISCUSSION The AP displacement of intact human knees under ±100 N drawer force in all three age groups studied was greater at 30° than at 90° of knee flexion. This finding correlates with data from previous in vitro and in vivo studies.’,&dquo;,&dquo;, 14,22,33 Fukubayashi et al.ll and Gollehon et a1.13 reported maximum total AP displacement (approximately 13 mm) at 30° for knees subjected to specimen orientation and loading similar to those used in this study. Our data further suggest that the intact knee stability in the AP direction does not change significantly with age. On the other hand, tensile testing of the FATC revealed significant effects of specimen age. The apparent difference between the two tests is presumably due to the fact that the AP displacement test assesses the behavior of the intact knee, which includes the contribution of all periarticular soft tissue structures of the knee such as the menisci, joint capsule, collateral and cruciate ligaments, etc. Also, the level of load experienced by the ACL during this test is small, and only a portion of the ACL may be loaded.&dquo; During the tensile test, only the ACL is loaded, and a larger portion of it would be under load. In addition, comparable load levels between these two tests are unknown. These differences, together with the nonlinear tensile load-
and knee kinematics with aging are some of the causes. The higher incidence of substance failures in the older specimens suggests a more rapid deterioration of the ligament substance than of the insertion sites with increasing age. Preliminary biochemical analysis of the ACL substance revealed significant decreases in collagen synthesis and reducible collagen cross-links.2° This finding appears to corroborate the biomechanical data. Additional histomorphometric studies of the bone-ligament junctions are indicated to evaluate the condition of the insertion sites. We have documented a substantially higher stiffness and ultimate load for the human FATC tested in the anatomical orientation of the ACL than has previously been reported for younger specimens. These values for the specimens under 35 years of age were 242 ± 28 N/mm and 2160 ± 157 N, respectively. This is over 30% higher than those reported by Noyes and Grood,25 and 25% higher than those of Rauch et al. 30 It is difficult to compare our data with these published data because of differences in the orientation of the ACL and the FATC with respect to the direction of tensile load, even though all three studies used similar angles of knee flexion (30° to 45°). It is interesting to note that the ultimate load obtained for FATC in the tibial orientation (1602 ± 167 N) is closer to previously reported values than that obtained in the anatomical orientation. Effects of specimen orientation and the complex anatomy of the ACL may play a role in the failure modes. The fact that the various portions of the ACL are of different lengths makes uniform loading of the entire ACL during tensile difficult if not impossible. Presumably, testing the FATC along the anatomical axis of the ACL, while maintaining its anatomical angles of insertion to the femur and tibia, allows a greater portion of the ACL to be loaded during tensile testing. This premise is substantiated by the higher values of linear stiffness, ultimate load, and energy absorbed at failure for specimens tested in the anatomical orientation than for those tested in the tibial orientation. The contrast in the failure modes between the two specimen orientations is also important. A higher percentage of ligament substance failures occurred for the FATCs tested in the anatomical orientation. Therefore, we believe that the anatomical specimen orientation is a more realistic representation of the strength of the ACL, since a larger portion of ligament is aligned to resist the tensile load. When FATCs were tested in the tibial orientation, there was a higher incidence of
224
insertion site failures. Since the ACL was out of its normal anatomical alignment with respect to the bones during tensile loading, uneven loading would occur and some portions may fail earlier than the others. As a result, the ligament often &dquo;peeled off’ at the insertion site. The complex anatomy of the ACL makes uniform loading of all fiber bundles during the tensile test almost impossible. Therefore, no attempt was made to report mechanical (material) properties of the ACL substance even for the FATC tested in the anatomical ACL orientation. Reasonably uniform stress and strain distribution in the ACL are required in order to achieve more reliable mechanical data (stressstrain curve). We believe that in this case it is simply not justifiable to use cross-sectional area of the entire ACL to calculate tensile stress. Similarly, it is difficult to determine ACL strain since the elongation of the various portions of the ACL would not be uniform. In this study we obtained consistently higher values for stiffness and ultimate load of the FATC in the younger donors. Thus, it appears that maintaining the normal anatomical angles of ACL insertions and applying load along the axis of the ACL is an improvement over arbitrarily selected specimen orientation. The substantial decrease in the structural properties of FATC with aging demonstrates a need for further investigations on ACL homeostasis. Large age-related differences also indicate that there may be significant changes in the tensile properties of ACL allografts with age. The newly obtained load-elongation curves for all three age groups should be added to the current pool of information used in the design and selection of grafts for human ACL replacement in hopes of reproducing normal knee kinematics.
9 Dorlot J-M, Ait Ba Sidi M, Tremblay GM, et al Load elongation behavior of the canine anterior cruciate ligament J Biomech Eng 102: 190-193, 1980 10. Figgie HE, Bahniuk EH, Heiple KG, et al. The effects of tibial-femoral angle on the failure mechanics of the canine antenor cruciate ligament J Biomech
19. 89-91, 1986 11
Torzdli PA, Sherman MF, et al: An in vitro biomechanical evaluation of anterior-posterior motion of the knee Tibial displacement, rotation, and torque J Bone Joint Surg 64A 258-264, 1982 12. Goldberg VM, Burstein AH, Dawson M. The influence of an expenmental immune synovitis on the failure mode and strength of the rabbit anterior cruciate ligament. J Bone Joint Surg 64A. 900-906, 1982 13. Gollehon DL, Torzilli PA, Warren RF: The role of the posterolateral and cruciate ligaments in the stability of the human knee. J Bone Joint Surg
69A: 233-242, 1987 14 Grood ES, Stowers SF, Noyes FR: Limits of movement in the human knee. J Bone Joint Surg 70A. 88-97, 1988 15. Gupta BN, Brinker WO, Subramanian KN: Breaking strength of cruciate ligaments in the dog. J Am Vet Med Assoc 155: 1586-1588, 1969 16. Gupta BN, Subramanian KN, Bnnker WO, et al: Tensile strength of canine cramal cruciate ligaments. Am J Vet Res 32. 183-190, 1971 17. Hollis JM Development and application of a method for determining the in situ forces in anterior cruciate ligament fiber bundles. PhD dissertation, University of California, San Diego, 1988 18. Jackson DW, Grood ES, Arnoczky SP, et al Freeze dned anterior cruciate ligament allografts Preliminary studies in a goat model. Am J Sports Med
295-303, 1987 15: 19.
20
21
22.
23
24.
ACKNOWLEDGMENTS The authors acknowledge the technical assistance of Jim Marcin and Shuji Horibe, MD. This project was funded by NIH Grant AR-39683 and Baxter Orthopaedics, Irvine, California.
25.
26 27
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J Bone Joint Surg 53A 710-718, 1971 28 Paulos LE, France EP, Rosenberg TD, et al Comparative matenal properties of allograft tissues for ligament replacement Effects of type, age, sterilization and preservation Trans Orthop Res Soc 33 129, 1987 29 Rauch G, Allzeit B, Gotzen L: Tensile strength of the anterior cruciate ligament in dependence on age. Proc Biomechanics of Human Knee Ligaments University of Ulm, Ulm, West Germany, 1987, p 24 30 Rauch G, Allzeit B, Gotzen L: Biomechanical studies on the tensile strength of the anterior cruciate ligament, with special reference to age-dependence. Unfallchirug 91 437-443, 1988 31 Ryan JR, Drompp BW Evaluation of tensile strength of reconstructions of the antenor cruciate ligament using the patellar tendon in dogs. A preliminary report South Med J 59. 129-134, 1966 32 Shino K, Kimura T, Hirose H, et al Reconstruction of the anterior cruciate ligament by allogeneic tendon graft An operation for chronic ligamentous Insufficiency J Bone Joint Surg 68B. 739-746, 1986 33 Sullivan D, Levy IM, Sheskier S, et al: Medial restraints to anterior-posterior motion of the knee J Bone Joint Surg 66A 930-936, 1984 34 Trent PS, Walker PS, Wolf B Ligament length patterns, strength, and rotational axes of the knee joint Clin Orthop 117. 263-270, 1976 35 Vasseur PB, Pool RR, Arnoczky SP, et al Correlative biomechanical and histological study of the cranial cruciate ligament in dogs. Am J Vet Res
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225 36 Viidik A Elasticity and tensile strength of the antenor cruciate ligament in rabbits as influenced by training Acta Orthop Scand 74. 372-380, 1968 37 Woo SL-Y, Hollis JM, Lyon RM, et al On the structural properties of the human anterior cruciate ligament-bone complex from young donors Proc Biomechanics of Human Knee Ligaments. University of Ulm, Ulm, West Germany, 1987, p 23
38. Woo SL-Y, Hollis JM, Roux RD, et al Effects of knee flexion on the structural properties of the rabbit femur-anterior cruciate ligament-tibia complex (FATC) J Biomech 20. 557-563, 1987 39. Yoshiya S, Andnsh JT, Manley MT, et al Graft tension in anterior cruciate ligament reconstruction An in vivo study in dogs. Am J Sports Med 15.
464-470,1987
specimen age and orientation*
WOO,†‡ PhD,
J. MARCUS HOLLIS,† PhD, DOUGLAS J. ADAMS,§ MS, ROGER M. LYON,§ MD, AND SHINRO TAKAI,† MD
From the †Musculoskeletal Research Laboratories,
Department of Orthopaedic Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania, and the §Orthopaedic Bioengineering Laboratory, University of California, San Diego, California Although the
tensile behavior of the human ACL has been studied for many decades, there are only a few published works characterizing its stiffness and strength properties, partly due to the difficulties in procuring young and healthy cadaveric specimens. In addition, its complex anatomy makes the geometric alignment for tensile loading difficult. In 1976, Kennedy et al.19 measured the strength of the isolated ACL in cadavers with a median age of 62 years and reported an ultimate load of 640 N. Trent et al. 34 tested the femur-ACL-tibia complex (FATC) in human knees between 25 and 55 years of age and reported an average stiffness of 141 N/mm and ultimate load of 633 N. In the same year, a landmark article published by Noyes and Grood25 showed the linear stiffness and ultimate load for six FATCs from three young donors between 16 and 26 years of age to be 182 ± 56 N/mm (mean ± SD) and 1730 ± 660 N, respectively. In addition, older specimens from 20 cadaver knees with ages ranging from 48 to 86 years were tested and the corresponding values reduced to 129 ± 39 N/mm and 734 ± 266 N, respectively. The data for the younger knees have since been the basis for matching the tensile properties of autograft and allograft tissues4,24,28 as well as for the design of artificial ligaments for ACL replacement. In a recent consensus workshop on the human ACL, new data on tensile properties of FATC were reported.3o, 37 Rauch et al .21,3’ reported similar data to that of Noyes and Grood,25 while Woo et a1.37 reported higher stiffness and strength values for FATC from younger donors. On the other hand, there exist many published works on the tensile properties of FATC from animals, including rabbits,2,12, 36 dogs, 1,4,6,9,15,16,26,27,31,32.35,39 goats,18 and monkeys.3, 7, 25 In general, the knee flexion angle and the direction of the applied tensile load with respect to the ACL were chosen arbitrarily, in spite of the fact that an early study by
ABSTRACT The structural properties of 27 pairs of human cadaver knees were evaluated. Specimens were equally divided into three groups of nine pairs each based on age: younger (22 to 35 years), middle (40 to 50 years), and older (60 to 97 years). Anterior-posterior displacement tests with the intact knee at 30° and 90° of flexion revealed a significant effect of knee flexion angle, but not of specimen age. Tensile tests of the femur-ACLtibia complex were performed at 30° of knee flexion with the ACL aligned vertically along the direction of applied tensile load. One knee from each pair was oriented anatomically (anatomical orientation), and the contralateral knee was oriented with the tibia aligned vertically (tibial orientation). Structural properties of the femur-ACL-tibia complex, as represented by the linear stiffness, ultimate load, and energy absorbed, were found to decrease significantly with specimen age and were also found to have higher values in specimens tested in the anatomical orientation. In the younger specimens, linear stiffness (242 ± 28 N/mm) and ultimate load (2160 ± 157 N) values found when the femurACL-tibia complex was tested in the anatomical orientation were higher than those reported previously in the literature. These values provide new baseline data for the design and selection of grafts for ACL replacement in an attempt to reproduce normal knee kinematics. *
Presented at the 16th annual meeting of the AOSSM, Sun
Valley, Idaho,
July 1990 $ address correspondence and reprnt requests to: Samo L-Y. Woo, PhD, Department of Orthopaedic Surgery, M-272 Scaife Hall, Urnversity of Pittsburgh,
Pittsburgh,
PA 15261.
217
218
Alm et al/ reported that the strength of the canine FATC at 90° of flexion was affected by the axial rotation of the tibia. Gupta et ail. 16 chose to test the canine FATC with the tibia rotated 90° in order to untwist the ACL. Recently, the ultimate load for the canine FATC was demonstrated to decrease significantly with increasing angle of knee flexion.&dquo; Our laboratory confirmed these findings in rabbits and further demonstrated that the direction of tensile load also played an important role on the structural properties of the rabbit FA TC. 38 To alleviate the geometric complexity of the et al.,5 as well as our laboratory,23 have separated the ACL into individual portions for tensile testing. In this way, the tensile stresses in the ligament would be more uniform, and the mechanical (material) properties of the ligament as represented by the stress-strain curve obtained are more reliable. Our laboratory has recently developed an experimental device whereby the FATC can be oriented and tested at any desired loading direction as well as knee flexion angle.23 Paired porcine knee specimens were tested, and the linear stiffness, ultimate load, and energy absorbed at failure for the FATC in both orientations were determined. These parameters were found to be significantly higher in specimens with the tensile load applied along the anatomical axis of the ACL than in those with the tensile load applied along the long axis of the tibia. The objectives of this study were to examine the effects of 1) donor age and 2) direction of the applied load with respect to specimen orientation on the structural properties of the human FATC. It is hypothesized that if the direction of loading was along the normal anatomical orientation of the ACL, the resulting stiffness and strength values would be higher. In that case, the new data obtained from younger, healthy donors could be used as a basis for selection and design of ACL replacements.
ACL, Butler
MATERIALS AND METHODS
Experimental apparatus An apparatus incorporating multiplanar adjustments for testing human knee specimens was used. The device allows the knee to be oriented in a variety of positions, thus permitting the tensile properties of the FATC to be measured at a preselected orientation and knee flexion angle (Fig. 1). Adjustments can be made such that the direction of applied tensile load can be aligned with the ACL without changing the normal anatomical angles of ACL insertion into the femur and the tibia (Fig. 2a). The apparatus consists of two major components to accommodate the femur and tibia. The femoral component permits the femur to be rotated in the frontal and sagittal planes.21 The entire fem-
also be moved in the transverse (horizontal) plane by adjustments of two sets of linear bearings. The tibial component allows rotational adjustments of the tibia in the frontal and sagittal planes similar to those used for the femoral component. A shaft on rotary bearings, to which the tibia and its mounting cylinder are attached, oral component
provides unrestrained axial tibial rotation. Transverse motion of the tibial component is eliminated by rigidly fixing it to the base of an Instron testing machine (Instron Corp., Canton, MA). The linear bearings of the femoral component and changes in the crosshead position permit alterations of the mediallateral, anterior-posterior (AP), and proximal-distal translations of the femur with respect to the tibia. The frontal and sagittal adjustments and the cylindrical clamps for both the femur and tibia permit alteration of knee flexion angle and internal-external and varus-valgus rotations. This device is also adjustable so that the intact knee specimen can be mounted for AP displacement testing at any desired angle of knee flexion
(Fig. 3).
The stiffness of the apparatus was first determined by securing a 15 cm long section of human femur into the two thick-walled cylinders with three 6 mm diameter transfixing bolts through each end of the bone. The cylinders were made of solid aluminum, with an outside diameter of 82 mm and an ovoid-shaped hole to accommodate the shaft of the bone. The setup was tensile loaded up to 3000 N, and its stiffness was found to be 508 N/mm and linear up to 3000 N.
Specimen preparation of cadaveric human knees were equally divided into three age groups, representing younger, middle, and older aged donors. The younger group consisted of knees from donors aged 22 to 35, with a mean age of 29 years. Seven pairs were from donors who had died following acute trauma (Table 1). The middle-aged group was from donors aged 40 to 50, with a mean age of 45 years. The cause of death for these donors was primarily acute trauma. The older age group was from donors aged 60 to 97, with a mean age of 75 years. The cause of death for this age group was largely due to chronic illness, such as cancer. The paired knee specimens were obtained after routine autopsy, freezing, and storage at -20°C. Prior to testing, each knee was thawed at room temperature for 24 hours, and was then dissected free of all skin and subcutaneous and muscle tissues, leaving the joint capsule and knee ligaments intact. The patella and patellar ligament were removed. The femur and tibia were cut to a length of approximately 15 cm from the joint line, and each was secured into a thick-walled aluminum cylinder using three 6 mm diameter transfixing bolts. The knee specimen, with its mounting cylinders, was then secured within the femoral and tibial components of the testing apparatus (Fig. 1). The soft tissues of all specimens were kept moist throughout the specimen preparation and testing with physiologic saline.
Twenty-seven pairs
Experimental procedure
can
were performed. First, the intact knee specimen was subjected to AP displacement tests to quantify the ACL’s contribution to the stability of each knee. Second,
Two different tests
tensile
testing of the FATC structural properties
was
performed to
examine its
219
1. Schematic diagram of the experimental apparatus used to evaluate the structural properties of the human FATC. Shown is the preparation of a specimen tested in the anatomical orientation. The clamps are oriented so that the tensile load is applied with the FATC specimen remaining in its anatomical position. A, anterior-posterior view; B, medial-lateral view.
Figure
displacement testing. AP displacement tests were peron each knee specimen (with all ligaments and joint capsule intact). The knee was oriented with the tibia aligned perpendicular to the applied load (i.e., horizontally) and the femur positioned with the knee at 30° of flexion (Fig. 3). The axial tibial rotation and medial-lateral and proximaldistal translations were unrestrained. We performed cyclic AP drawer tests using a 100 N force applied to the femur at a displacement rate of 20 mm/min. The AP load displacement curves were recorded, and the total AP displacement for the 10th cycle was used. The knee was then flexed to 90°, and the test was repeated. Tensile testing. One knee from each pair was randomly assigned to be tested with the tensile load applied along the axis of the ACL while preserving the normal anatomical angles of ACL insertion into the femur and tibia (anatomical AP
formed
orientation). The contralateral knee was tested with the applied along the long axis of the tibia (tibial orientation) without preserving the anatomical orientation
tensile load
of the ACL. All FATCs were tested at 30° of knee flexion. For specimens tested in the anatomical orientation, the fat pad was removed to allow visualization of the ACL. The femoral and tibial components of the clamps were rotated in the medial-lateral plane and then in the AP plane so as to align the long axis of the ACL with the direction of tensile load (Figs. 2a and 3) while the knee angle was maintained at 30° of flexion. The FATC was then secured in this position. The joint capsule, meniscus, and other soft tissues were then removed, leaving only the ACL. The orientation of the ACL with respect to the line of applied tensile load
checked by means of a plumb line, and minor rotational alignment was done prior to tensile testing. Thus, the direction of tensile loading for this test was aligned with the anatomical axis of the ACL. For the contralateral specimen, which was tested in the tibial orientation, the tibia was secured vertically along the loading axis in both the frontal and sagittal planes (Fig. 2b). The remaining soft tissues around the knee were removed, leaving only the ACL. The femur was translated medially and anteriorly so that the femoral insertion of the ACL was directly above its tibial insertion and the ACL was aligned along the line of tensile load. The FATC was then secured in this position and only vertical elongation along the tibial axis was permitted. The reason for aligning the ligament in this manner was to examine the effects of nonanatomical angles of ACL insertions on the load-elongation properties of the FATC. In other words, although the ACL was aligned in the line of tensile load application, its natural anatomical orientation with respect to the femur and tibia was not maintained. This procedure was different from many previous studies in the literature in which the ACL was often oriented at an angle with respect to the direction of applied tensile load. A small preload of 2.5 N was applied to the FATC after which it was cyclically preconditioned between 0 and 2 mm of deformation at a rate of 20 mm/min. After 10 cycles, the FATC was loaded to failure at a rate of 200 mm/min. The load and elongation were recorded continuously using a strip chart recorder. The resulting load-elongation curve, corrected for the stiffness of the testing apparatus, represented was
220
Figure 3. Schematic diagram demonstrating that the experimental apparatus as described in Figure 1 can be adapted for AP displacement testing of an intact knee at preselected angles of knee flexion. properties of FATC were analyzed using a two-way ANOVA. Significance was set at P < 0.05. RESULTS
Figure 2. Schematic of specimen orientation for tensile testing. a, for the anatomical orientation, the tensile load is applied along the axis of the ACL while the normal anatomical angles of ACL insertion to bone are preserved. b, for the tibial orientation, the femur is moved anteriorly and medially so that the tensile load can be applied in line with the femoral and tibial insertion sites. Note that in this case, the anatomical angles of ACL insertion to bone are distorted. the structural properties of the FATC, and parameters such as the linear stiffness, ultimate load, energy absorbed at failure, and failure mode were documented. Linear stiffness was defined as the linear slope of the load-elongation curve between 3 and 7 mm of elongation. Statistical analysis. The effects of specimen age and knee flexion angle on AP displacement were analyzed statistically using a two-way analysis of variance (ANOVA). Likewise, the effects of specimen age and orientation on the tensile
AP displacement tests. Typical load-displacement curves obtained from AP displacement testing of the intact human knees are shown in Figure 4. The AP displacement, defined as the total displacement between 100 N of anterior and 100 N of posterior load, was 45% and 34% higher at 30° of flexion than at 90° for the younger-aged and middle-aged specimens, respectively, but only 12% higher for the older group (Table 2). Two-way ANOVA revealed a significant effect of flexion angle on the AP displacement (P < 0.001) but not of specimen age (P > 0.10). There was no significant interaction between age and flexion angle (P > 0.10), indicating no interdependence between specimen age and knee flexion angle. Tensile testing. Typical load-elongation curves for the paired FATC from the younger age group tested in the anatomical and tibial orientations are shown in Figure 5. The two curves show that the structural properties of the
221 TABLE 1
History of cadaver donors
Figure 5. Typical load-elongation curves for paired FATC from a younger donor demonstrating the differences in results between the anatomical and tibial orientations. different modes of failure of the FATC were observed: 1) avulsion of bone at the insertion site, 2) insertion site failure but without bony fragment, and 3) ligament substance failure of collagen fibers. The modes of failure were found to be different between specimen orientations. The tensile load-elongation curves for all FATC specitested are plotted in Figure 6. Both donor age and the specimen orientation had a significant effect on the resulting structural properties of the FATC (Table 3). For specimens tested in the anatomical orientation, the values of stiffness were 242 ± 28 N/mm, 220 ± 24 N/mm, and 180 ± 25 N/ mm for the younger, middle, and older aged specimens, respectively. For specimens tested in the tibial orientation these values reduced to 218 ± 27 N/mm, 192 ± 17 N/mm, and 124 ± 16 N/mm. A two-way ANOVA showed a significant effect of age on the linear stiffness (P < 0.001), with the younger specimens having a higher linear stiffness than the older specimens (Table 3). The linear stiffness for the FATCs tested in the anatomical orientation was 11%, 15%, and 45% higher than those tested in the tibial orientation for the younger, middle, and older aged specimens, respectively, although statistical significance was not shown (P 0.07) for the effect of specimen orientation. There was not a significant correlation between age and orientation (P > 0.50), indicating that the differences documented between age groups were independent of the specimen orientation. The ultimate load for the younger specimens tested in the anatomical orientation (2160 ± 157 N) was found to be 44% higher than that of the middle-aged group (1503 ± 83 N), and 328% higher than that of the older group (658 ± 129 mens
Figure 4. Typical load-displacement curves for a young knee during AP displacement testing at 30° and 90° of flexion. TABLE 2 Effects of specimen age and knee flexion angle on the AP displacement of intact knees (mean ± SEM) -
=
FATC were affected by the specimen orientation. The FATCs tested in the anatomical orientation resulted in a higher linear stiffness, ultimate load, and energy absorbed at failure than those tested in the tibial orientation. Three
222 TABLE 3 Effects of specimen age and orientation on the structural properties of the FATC (mean ± SEM)
Figure 7. The effect of specimen age on FATC ultimate load. Data on ultimate load as a function of specimen age and orientation using a least squares curve fit demonstrated that the strength of FATC decreases in an exponential manner. The values of energy absorbed at failure followed the same trend as for the linear stiffness. The younger specimens absorbed more energy at failure than did the older specimens, while the specimens tested in the anatomical orientation absorbed only slightly more energy at failure than those tested in the tibial orientation (Table 3). Statistical analysis revealed that energy absorbed was significantly affected by age (P < 0.001), and although energy absorbed was similarly affected by specimen orientation, statistical significance was not shown (P 0.06). Again no significant interaction was found between age and orientation (P > =
Figure 6. The load-elongation curves for FATC tested at 30° of flexion in the (a) anatomical orientation and (b) tibial orientation for younger, middle, and older human donors.
N). A decrease related to increasing age was also seen for those tested in the tibial orientation. For the younger FATCs tested in the anatomical orientation, the value was 35% higher than that for the tibial orientation (1602 ± 167 N), but the difference diminished with increasing age (Fig. 7). Statistically, both specimen age and orientation had a significant effect on the ultimate load (P < 0.001 and P < 0.05, respectively; Table 3). There was no significant correlation between age and specimen orientation (P > 0.10), indicating that the differences due to age and specimen orientation were
independent.
0.10). The older specimens had a higher incidence of substance failure (12/18, or 67%) than the younger (5/18, or 28%) or middle (8/18, or 44%) aged specimens regardless of the specimen orientation (Fig. 8). Several of the specimens from younger donors (9/18, or 50%) failed by avulsion of a piece of bone directly under the tibial insertion. FATCs tested in the anatomical orientation failed predominantly by midsubstance tear for older specimens (7/9, or 78%) or bony avulsion for younger specimens (6/9, or 67%). The FATCs tested in the tibial orientation had a higher incidence of insertion failure by sequentially &dquo;peeling off’ individual fiber bundles (13/27, or 48%) than those tested in the anatomical orientation (1/27, or 4%).
223
elongation behavior of the ligament would prevent a direct correlation between the results of tensile testing and the AP
displacement test. The study of tensile testing
of the FATC has identified
two important factors that influence the structural properties of the human FATC-specimen age and orientation. The large decreases in linear stiffness and ultimate load, as well as energy absorbed at failure, of the FATC with increasing age are similar to the previous findings by others.25, 30 These large reductions are due to many factors. The decrease
in types and levels of physical activity with age, the physical condition of older donors, and the changes in joint geometry
Figure 8. Histograms of modes of failure of human FATC tested in the (a) anatomical and (b) tibial orientations from the younger, middle, and older human donors studied. DISCUSSION The AP displacement of intact human knees under ±100 N drawer force in all three age groups studied was greater at 30° than at 90° of knee flexion. This finding correlates with data from previous in vitro and in vivo studies.’,&dquo;,&dquo;, 14,22,33 Fukubayashi et al.ll and Gollehon et a1.13 reported maximum total AP displacement (approximately 13 mm) at 30° for knees subjected to specimen orientation and loading similar to those used in this study. Our data further suggest that the intact knee stability in the AP direction does not change significantly with age. On the other hand, tensile testing of the FATC revealed significant effects of specimen age. The apparent difference between the two tests is presumably due to the fact that the AP displacement test assesses the behavior of the intact knee, which includes the contribution of all periarticular soft tissue structures of the knee such as the menisci, joint capsule, collateral and cruciate ligaments, etc. Also, the level of load experienced by the ACL during this test is small, and only a portion of the ACL may be loaded.&dquo; During the tensile test, only the ACL is loaded, and a larger portion of it would be under load. In addition, comparable load levels between these two tests are unknown. These differences, together with the nonlinear tensile load-
and knee kinematics with aging are some of the causes. The higher incidence of substance failures in the older specimens suggests a more rapid deterioration of the ligament substance than of the insertion sites with increasing age. Preliminary biochemical analysis of the ACL substance revealed significant decreases in collagen synthesis and reducible collagen cross-links.2° This finding appears to corroborate the biomechanical data. Additional histomorphometric studies of the bone-ligament junctions are indicated to evaluate the condition of the insertion sites. We have documented a substantially higher stiffness and ultimate load for the human FATC tested in the anatomical orientation of the ACL than has previously been reported for younger specimens. These values for the specimens under 35 years of age were 242 ± 28 N/mm and 2160 ± 157 N, respectively. This is over 30% higher than those reported by Noyes and Grood,25 and 25% higher than those of Rauch et al. 30 It is difficult to compare our data with these published data because of differences in the orientation of the ACL and the FATC with respect to the direction of tensile load, even though all three studies used similar angles of knee flexion (30° to 45°). It is interesting to note that the ultimate load obtained for FATC in the tibial orientation (1602 ± 167 N) is closer to previously reported values than that obtained in the anatomical orientation. Effects of specimen orientation and the complex anatomy of the ACL may play a role in the failure modes. The fact that the various portions of the ACL are of different lengths makes uniform loading of the entire ACL during tensile difficult if not impossible. Presumably, testing the FATC along the anatomical axis of the ACL, while maintaining its anatomical angles of insertion to the femur and tibia, allows a greater portion of the ACL to be loaded during tensile testing. This premise is substantiated by the higher values of linear stiffness, ultimate load, and energy absorbed at failure for specimens tested in the anatomical orientation than for those tested in the tibial orientation. The contrast in the failure modes between the two specimen orientations is also important. A higher percentage of ligament substance failures occurred for the FATCs tested in the anatomical orientation. Therefore, we believe that the anatomical specimen orientation is a more realistic representation of the strength of the ACL, since a larger portion of ligament is aligned to resist the tensile load. When FATCs were tested in the tibial orientation, there was a higher incidence of
224
insertion site failures. Since the ACL was out of its normal anatomical alignment with respect to the bones during tensile loading, uneven loading would occur and some portions may fail earlier than the others. As a result, the ligament often &dquo;peeled off’ at the insertion site. The complex anatomy of the ACL makes uniform loading of all fiber bundles during the tensile test almost impossible. Therefore, no attempt was made to report mechanical (material) properties of the ACL substance even for the FATC tested in the anatomical ACL orientation. Reasonably uniform stress and strain distribution in the ACL are required in order to achieve more reliable mechanical data (stressstrain curve). We believe that in this case it is simply not justifiable to use cross-sectional area of the entire ACL to calculate tensile stress. Similarly, it is difficult to determine ACL strain since the elongation of the various portions of the ACL would not be uniform. In this study we obtained consistently higher values for stiffness and ultimate load of the FATC in the younger donors. Thus, it appears that maintaining the normal anatomical angles of ACL insertions and applying load along the axis of the ACL is an improvement over arbitrarily selected specimen orientation. The substantial decrease in the structural properties of FATC with aging demonstrates a need for further investigations on ACL homeostasis. Large age-related differences also indicate that there may be significant changes in the tensile properties of ACL allografts with age. The newly obtained load-elongation curves for all three age groups should be added to the current pool of information used in the design and selection of grafts for human ACL replacement in hopes of reproducing normal knee kinematics.
9 Dorlot J-M, Ait Ba Sidi M, Tremblay GM, et al Load elongation behavior of the canine anterior cruciate ligament J Biomech Eng 102: 190-193, 1980 10. Figgie HE, Bahniuk EH, Heiple KG, et al. The effects of tibial-femoral angle on the failure mechanics of the canine antenor cruciate ligament J Biomech
19. 89-91, 1986 11
Torzdli PA, Sherman MF, et al: An in vitro biomechanical evaluation of anterior-posterior motion of the knee Tibial displacement, rotation, and torque J Bone Joint Surg 64A 258-264, 1982 12. Goldberg VM, Burstein AH, Dawson M. The influence of an expenmental immune synovitis on the failure mode and strength of the rabbit anterior cruciate ligament. J Bone Joint Surg 64A. 900-906, 1982 13. Gollehon DL, Torzilli PA, Warren RF: The role of the posterolateral and cruciate ligaments in the stability of the human knee. J Bone Joint Surg
69A: 233-242, 1987 14 Grood ES, Stowers SF, Noyes FR: Limits of movement in the human knee. J Bone Joint Surg 70A. 88-97, 1988 15. Gupta BN, Brinker WO, Subramanian KN: Breaking strength of cruciate ligaments in the dog. J Am Vet Med Assoc 155: 1586-1588, 1969 16. Gupta BN, Subramanian KN, Bnnker WO, et al: Tensile strength of canine cramal cruciate ligaments. Am J Vet Res 32. 183-190, 1971 17. Hollis JM Development and application of a method for determining the in situ forces in anterior cruciate ligament fiber bundles. PhD dissertation, University of California, San Diego, 1988 18. Jackson DW, Grood ES, Arnoczky SP, et al Freeze dned anterior cruciate ligament allografts Preliminary studies in a goat model. Am J Sports Med
295-303, 1987 15: 19.
20
21
22.
23
24.
ACKNOWLEDGMENTS The authors acknowledge the technical assistance of Jim Marcin and Shuji Horibe, MD. This project was funded by NIH Grant AR-39683 and Baxter Orthopaedics, Irvine, California.
25.
26 27
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