- Email: [email protected]
Biomechanics of the Human Triple-Bundle Anterior Cruciate Ligament
Biomechanics of the Human Triple-Bundle Anterior Cruciate Ligament Yuki Kato, M.D., Ph.D., Sheila J. M. Ingham, M.D., Akira Maeyama, M.D., Pisit Lertwanich, M.D., Joon Ho Wang, M.D., Ph.D., Yutaka Mifune, M.D., Ph.D., Scott Kramer, B.S., Patrick Smolinski, Ph.D., and Freddie H. Fu, M.D., D.Sc.
Purpose: To investigate the biomechanics of the intermediate (IM), anteromedial (AM), and posterolateral (PL) bundles in the human anterior cruciate ligament (ACL). Methods: Eighteen human cadaveric knees were tested with a robotic/universal force-moment sensor testing system. Anterior tibial translation (ATT) was determined under an 89-N anterior tibial load. Coupled ATT was determined under a combined rotatory load of 7-Nm valgus and 5-Nm internal rotation torque (pivot moment). Each bundle’s in situ forces were measured under identical external loading conditions. Results: Under anterior load, the PL bundle’s in situ force was highest at 0° and decreased during flexion. Under the anterior load, the AM bundle’s in situ force was significantly higher than the IM and PL bundles’ force at 15°, 30°, and 60°. Under the pivot moment, the AM bundle’s in situ force was significantly higher than the PL and IM bundles’ force at 0° and 15°, and the IM bundle had the lowest in situ force at 0° but higher in situ force than the AM and PL bundles at 30° and 45°. IM and AM bundle removal increased ATT under the anterior load at all angles. Cutting the PL bundle after IM and AM bundle removal (whole ACL removal) significantly increased ATT under the anterior load at 0°, 15°, and 30° of knee flexion and increased coupled ATT under the pivot moment at 0° and 15°. Conclusions: The biomechanical role of each of the 3 ACL bundles (AM, IM, and PL) was measured with a robotic/universal force-moment sensor testing system. The AM bundle stabilized the knee against both the anterior and rotatory loads. The PL bundle stabilized the knee especially near full extension. The IM bundle supported the AM and PL bundles through all flexion angles, especially from 30° to 45°, against the rotatory load. Clinical Relevance: Knowledge of functions of the different ACL bundles will help improve ACL reconstruction techniques to enable restoration of normal knee function.
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From the Departments of Orthopaedic Surgery (Y.K., S.J.M.I., A.M., P.L., J.H.W., Y.M., F.H.F.) and Mechanical Engineering (S.K., P.S., F.H.F.), University of Pittsburgh, Pittsburgh, Pennsylvania, U.S.A.; and Department of Orthopaedic Surgery, Nihon University (Y.K.), Tokyo, Japan. Supported by the Albert B. Ferguson Jr., M.D., Orthopaedic Fund of The Pittsburgh Foundation. F.H.F. received a research grant from Smith & Nephew. The authors report no conflict of interest. Received October 17, 2010; accepted July 27, 2011. Address correspondence to Freddie H. Fu, M.D., Department of Orthopaedic Surgery, University of Pittsburgh, 3471 Fifth Ave, 1010 Kaufmann Bldg, Pittsburgh, PA 15213, U.S.A. E-mail: [email protected] © 2012 by the Arthroscopy Association of North America 0749-8063/10614/$36.00 doi:10.1016/j.arthro.2011.07.019
any surgeons have recently focused on anatomic anterior cruciate ligament (ACL) reconstruction; therefore detailed anatomic studies are required to improve surgical techniques. Several anatomic studies have shown that the ACL can be divided into 2 functional bundles: the anteromedial (AM) bundle and the posterolateral (PL) bundle.1-6 Although this anatomic concept has been widely accepted, other studies have reported that the ACL consists of 3 bundles: AM, PL, and intermediate (IM) bundles.7-10 One study has even shown that the ACL can be divided into 4 bundles: anterolateral, AM, central, and posterior.11 From the anatomic viewpoint, in many animal species, 3 ACL bundles (AM, IM, and PL) are clearly discernible,12,13 although only a few studies have investigated the biomechanical role of
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each of the 3 bundles in animal models.12,13 Studies have shown that the IM bundle plays a subordinate role to the AM and PL bundles in animal models.12,13 Similarly, few studies have determined the biomechanical role of each of the 3 human ACL bundles.7 When anatomic ACL reconstruction is performed, the ACL remnant should be used as a guide for tunnel placement.14 An anatomic study showed a variety of ACL tibial footprints under the 2-bundle ACL concept.15 It is believed that more detailed functional findings would help us understand which position would be optimal for tunnel placement within the ACL footprint. To improve ACL reconstruction, it is important to better understand the biomechanical characteristics of each native ACL bundle. The first purpose of this study was to show the triple-bundle human ACL anatomy. The second purpose was to investigate the biomechanical role of each human ACL bundle. Even if the ACL is divided into 3 functional bundles, we hypothesize that the AM bundle plays the main role in anterior stability and that the PL bundle mainly contributes to rotatory stability, on the basis of previous reports based on the 2-bundle ACL concept.6,16 Furthermore, we hypothesize that the IM bundle plays a supplementary role to the AM and PL bundles, as previous animal studies have reported.12,13 METHODS ACL Triple-Bundle Anatomy and Histologic Analysis To better evaluate triple-bundle ACL anatomy, 10 human cadaveric knees (6 men and 4 women; mean donor age at the time of death, 60.0 years [SD, 3.9 years]) were dissected. According to earlier anatomic studies, the ACL can be divided into 2 bundles (AM and PL) by their differences in tension patterns.1,3,6,17-19 In this study, after careful dissection, the entire ACL, including the ACL insertion site and its connection with the lateral meniscus, was removed. The excised ACL tissues were frozen in 2-methylbutane pre-cooled in liquid nitrogen and then stored at ⫺80°C until cryosectioning to maintain the positional relation between the ACL and its surroundings. Six-micrometer sections were prepared. Masson trichrome staining (IMEB, Chicago, IL) was then performed.
universal force-moment sensor (UFS) testing system. Computed tomography of the specimens was performed before testing to ensure the absence of osseous abnormalities, deformities, or osteoarthritis. All specimens were frozen at ⫺20°C and thawed the night before testing. The knees were left intact, and the specimens were kept moist with saline solution during the testing to prevent soft-tissue exsiccation. The femur and tibia were then cut approximately 20 cm from the joint line, and the surrounding skin and muscles that were more than 10 cm away from the joint line were removed to expose the bone. The specimens were subsequently secured within custom-made aluminum cylinders by use of an epoxy compound (3M Bondo, Atlanta, GA) and rigidly fixed to the robotic/ UFS testing system.12,20-23 To prevent slippage between the epoxy and the specimens in the rig, the epoxy was screwed through several holes with thread grooves made into the aluminum cylinder. Transection Technique Arthroscopy was performed in all specimens with a 30° arthroscope. The surgical approach included a 3-portal technique with the anterolateral, AM, and accessory medial portals.24-26 All the specimens were arthroscopically dissected by a single trained surgeon (Y.K.). In this study the extension of the inner edge of the anterior horn of the lateral meniscus was considered the anterior border of the PL bundle (Fig 1). A discrete boundary between the IM and AM bundles can be observed after careful removal of all the soft tissue surrounding the ACL.27 Fibrous-like soft tissue was found from the lateral meniscus to the lateral side of the anterior aspect of the ACL. There was a wrinkle
Biomechanics We tested 18 fresh-frozen human cadaveric knees (13 men and 5 women; mean donor age at the time of death, 53.5 years [SD, 6.7 years]) using a robotic/
FIGURE 1. Tibial insertion site anatomy of ACL. (LM, lateral meniscus; MM, medial meniscus.)
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FIGURE 2.
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Each ACL bundle was identified and then selectively sectioned under arthroscopic vision.
in the anterior aspect of the ACL in all specimens. This wrinkle was defined in this study as the border between the IM and AM bundles. Thus each of the 3 ACL bundles was identified and separated with a periosteal elevator and selectively sectioned by use of the Vulcan EAS Electrothermal Arthroscopy System (Smith & Nephew Endoscopy, Andover, MA) (Fig 2). Robotic/UFS Testing System A CASPAR Stäubli RX90 robot (Orto MAQUET, Rastatt, Germany) was used to manipulate the joint. A UFS testing system (model 4015; JR3, Woodland, CA) was used to measure the forces and moments for 6 df. The robotic system was capable of controlling the displacement and the force/moment applied to the knee in all 6 df based on a mathematic description of knee kinematics and kinetics.20,21,28 Control and data acquisitions were performed by use of a personal computer and the MATLAB programming environment (The MathWorks, Natick, MA). The robot arm had a repeatability of motion within ⫾0.02 mm at each joint. According to the manufacturer, the UFS testing system has reliability within ⫾0.2 N and ⫾0.1 Nm. Testing Protocol The experimental protocol and acquired data are outlined in Table 1. After a specimen was attached to
the robotic/UFS testing system, the path of passive flexion-extension of the intact knee was determined from full extension to 90° of flexion by moving the tibia through 1° increments of flexion while minimizing the forces and moments. This path served as the reference position from which knee kinematics were measured and provided the starting position for the recorded kinematics. For this study, the loading conditions included (1) an 89-N anterior tibial load with the knee at full extension and at 15°, 30°, and 60° of flexion and (2) a
TABLE 1.
Experimental Protocol and Data Acquired
Step
Knee Status
Loading Condition
Data Acquired
1 2
Intact ACL IM deficient
Applied 2 loads Repeat kinematics
Intact knee kinematics In situ force of IM bundle IM-deficient knee kinematics In situ force of AM bundle IM-/AM-deficient knee kinematics In situ forces of PL bundle and ACL ACL-deficient knee kinematics
Applied 2 loads 3
IM/AM deficient
Repeat kinematics Applied 2 loads
4
ACL deficient
Repeat kinematics Applied 2 loads
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combined rotatory load of 7 Nm of valgus torque and 5 Nm of internal tibial torque at full extension and at 15°, 30°, and 45° of knee flexion. The anterior tibial load was used because the ACL is a major restraint to anterior tibial translation (ATT) and corresponds to the Lachman test and the anterior drawer test. The force of 89 N is equivalent to that used in the KT-1000 arthrometer (MEDmetric, San Diego, CA).29 The combined valgus and internal tibial torque were chosen to simulate the pivot-shift test.30,31 The remaining 5-df kinematics of the knees in an intact state was determined in response to both loading conditions. To observe the roles of the 3 bundles, they were cut in sequential order before retesting using the same criteria. After the intact knees (intact group, n ⫽ 18) were tested, the IM bundle of all knees was cut first (IM-deficient group, n ⫽ 18). The AM bundle was cut next (IM-/AM-deficient group, n ⫽ 18), followed by cutting of the PL bundle (ACL-deficient group, n ⫽ 18). The in situ force in each ACL bundle was determined after careful arthroscopic transection of each ACL bundle. ATT (in millimeters) in response to the external loads was measured at subsequent states (intact, IM deficient, IM/AM deficient, and ACL deficient). The previously recorded positions of the intact knee were reproduced by the robotic manipulator on the ACL-deficient knee, and the UFS testing system measured new forces and moments. On the basis of the superposition principle, the difference between the forces of the intact and ACL-deficient knees was determined to be the in situ force in the ACL.23 To assess changes in knee kinematics associated with ACL deficiency, the same external loads previously applied to the intact knee were again applied to the ACL-deficient knee and the resulting kinematics was measured.
for the ANOVA test and P ⱕ .017 for the pair-wise comparisons. All statistical data were calculated with the statistical software package SPSS, version 17.0 (SPSS, Chicago, IL). RESULTS Anatomy and Histologic Analysis Careful dissection and histologic analysis showed the presence of connective soft tissue from the lateral meniscus to the anterior part of the ACL in all specimens (Fig 3). This soft tissue divides the anterior part of the ACL into 2 other bundles, the IM bundle and the AM bundle. Histologic findings, especially those observed in cross sections, could not clearly show that
Statistical Analysis Because all variables were measured within the same specimen, statistical analyses of the kinematics and in situ forces were performed by use of a 2-factor repeated-measures analysis of variance (ANOVA) that evaluated knee state and flexion angle. Multiple comparisons with the Bonferroni post hoc test were performed to compare means among groups (IM, PL, AM, and intact ACL) and to compare differences between the intact, IM-deficient, IM-/AM-deficient, and ACL-deficient conditions at specific angles of knee flexion. Statistical significance was set at P ⱕ .05
FIGURE 3. Connective tissue from the lateral meniscus to the anterior of the ACL divides the AM bundle from the IM bundle. This can be seen during (A) histology (Masson trichrome staining; original magnification, ⫻40) and (B) arthroscopy.
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force at 0° of knee flexion, but the IM bundle had a higher in situ force than the PL bundle at 15° of knee flexion. Furthermore, the IM bundle had a higher in situ force than the AM and PL bundles at 30° and 45° of knee flexion (Fig 4B). ATT During Anterior Tibial Load: After the IM bundle was sectioned, no significant change was found in ATT in response to the anterior load. On sectioning of the AM bundle, ATT increased significantly at 15°, 30°, and 60° of knee flexion. When the PL bundle was sectioned, ATT increased significantly at 0°, 15°, and 30° of knee flexion (Fig 5A). Coupled ATT During Combined Rotatory Load: When only the IM bundle was sectioned, the coupled ATT increased in response to the combined rotatory load, but no significant difference was seen. When the ACL was completely sectioned, coupled ATT increased significantly at 0° and 15° of knee flexion. There was a significant difference in coupled ATT
FIGURE 4. In situ forces in response to (A) anterior tibial load and (B) combined rotatory load.
there were borders among the 3 bundles. Even a coronal section could not show the clear border between the AM and IM bundles. Biomechanical Analysis In Situ Forces During Anterior Tibial Load: There was no significant in situ force difference in response to anterior load between the AM and PL bundles at 0° of knee flexion, although the PL bundle had a higher in situ force. The IM bundle had the lowest in situ force at 0° and 15° of knee flexion. The AM bundle had a significantly higher in situ force than the IM and PL bundles at 15°, 30°, and 60° of knee flexion. The PL bundle had the lowest in situ force at 30° and 60° of knee flexion (Fig 4A). In Situ Forces Under Combined Rotatory Load: The AM bundle had a significantly higher in situ force in response to the combined rotatory load than the PL and IM bundles at 0° and 15° of knee flexion. The PL bundle had the lowest in situ force at 15°, 30°, and 45° of knee flexion. The IM bundle had the lowest in situ
FIGURE 5. (A) ATT in response to anterior tibial load. (B) Coupled ATT in response to combined rotatory load. (DEF, deficient.)
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between the IM-deficient and ACL-deficient knees at 0° of knee flexion (Fig 5B). DISCUSSION The biomechanical roles of the AM, IM, and PL bundles of the ACL were measured in this study. We have shown that the AM bundle stabilizes the knee against both anterior and rotatory loads, that the PL bundle stabilizes the knee especially near full extension, and that the IM bundle plays a supplemental role to the AM and PL bundles through all flexion angles, especially from 30° to 45°, against a rotatory load. A recent biomechanical study has indicated that ATT at higher degrees of knee flexion is limited by the AM bundle fibers whereas ATT at lower flexion angles is limited by the PL bundle fibers.6 Our study showed similar findings, in that ATT at 0° and 15° of knee flexion under external loads increased more when the PL bundle was cut. Other biomechanical studies have shown that an increase in laxity, implied by significantly increased ATT during a pivot moment, is higher if the PL bundle is cut than if the AM bundle is cut6,16; despite this, these studies do not suggest that the AM bundle does not play a role in rotational stability. Our study, however, has shown that sectioning of the AM bundle also causes an increase in laxity during the combined rotatory load, suggesting that the AM bundle, in addition to the PL bundle, plays an important role in rotational stability. At full extension of the knee joint, the AM and PL bundles work equally, but as the knee is flexed, the AM bundle is mainly working. This study has also shown that the IM bundle plays an important role under pivot moments at 30° and 45° of knee flexion. This suggests that the IM bundle plays a secondary role not only to the AM bundle but also to the PL bundle. Although Norwood and Cross9 described that the AM bundle contributes to anterolateral stability whereas the IM bundle adds to anterior and AM stability and the PL bundle assists in PL stability, Amis and Dawkins7 showed that each bundle contributes to anterior stability at different flexion angles. The results of our study are in concordance with these studies because the results show that each bundle contributes to anterior stability at different knee flexion angles. Iwahashi et al.8 evaluated the “functional length” of the 3 ACL bundles and found that they were not isometric, supporting the idea that the contributions of each bundle, including the IM bundle, to knee stability depend on the angle of knee flexion. As a previous study has mentioned, the advan-
tages of a robotic testing system include kinematic measurements when the knee is artificially restrained.32 Most importantly, this advanced method has the advantage of collecting experimental data from the same cadaveric knee specimen under different experimental conditions (such as intact, IMdeficient, IM-/AM-deficient, and ACL-deficient knee states), thus reducing the effect of interspecimen variation and significantly increasing the statistical power of the data through allowing the use of repeated-measures ANOVA for data analysis. In this study a histologic analysis was performed before the biomechanical testing to better understand triple-bundle ACL anatomy. A previous study has shown a septum between the AM and PL bundles in the fetal ACL2; however, we could not visualize a clear septum between the ACL bundles. The cleavage that we showed, which looked like a septum between the AM and IM bundles on histologic imaging (Fig 3A), might be an artifact caused by the staining, although a wrinkle in the anterior aspect of the ACL was seen arthroscopically in all specimens. This might be explained by the existence of soft tissue from the lateral meniscus to the anterolateral portion of the ACL. We have shown that the IM bundle can be divided from the AM and PL bundles not anatomically but functionally. This result would advocate a triplebundle ACL reconstruction as reported by Shino et al.10 However, we believe that anatomic tunnel placement is more important than multiple-bundle reconstruction, such as double- or triple-bundle ACL reconstruction. We found that the magnitude of the in situ force of the IM bundle was almost isometric and low, although it was relatively higher than that of the AM and PL bundles under the pivot moment at 30° and 45° of knee flexion. As a practical proposition, when double-bundle ACL reconstruction is performed, the tibial AM tunnel should be positioned toward the AM side (AM bundle footprint in a narrow sense) and not the anterolateral side (IM bundle footprint in a narrow sense). To ensure correct anatomic ACL reconstruction, it is imperative that ACL anatomy and biomechanics are fully understood. We hope the results of this study will add to the existing knowledge and help surgeons to improve ACL reconstruction techniques. There were some limitations of this study. First, the results at 90° of knee flexion could not be shown. Because the full extension angle was not always 0° of knee flexion, the full-extension angle of each specimen was measured by use of an angle gauge. The
HUMAN TRIPLE-BUNDLE ACL BIOMECHANICS mean full-extension angle of all knee specimens was 3.5° (SD, 1.9°), ranging from 0° to 8°. Over 90° was too deep to be examined with the robotic/UFS testing system used. In the future, testing should be done at more detailed knee flexion angles. Second, dissection of the 3 bundles depended on human evaluation and, as such, was prone to error. To minimize this, the same experienced surgeon (Y.K.) with previous experience in animal dissections performed all the dissections.12,13 To prevent any unknown bias, the bundles should have been cut in different sequential order. However, we believed that it was important to identify and cut the IM bundle first for consistency, because the IM bundle contacts both the AM bundle (in a narrow sense) and PL bundle and is thought to be a lateral part of the AM bundle in a broad sense. In addition, the accuracy of cutting each bundle under arthroscopic control must be considered, although we believe our arthroscopic distinction was no less accurate than an open dissection. Third, the applied external loads in this study were lower than the loads used in previous biomechanical studies.6,30,31,33-37 Nonetheless, even with lower applied external loads, we were able to show both significant differences and the trends that occur after each bundle is sectioned. Finally, no prior sample size analysis or post hoc power analysis was performed, and despite the fact that statistically significant results were found, the large number of variables evaluated could increase the type II error. CONCLUSIONS The biomechanical role of each of the 3 ACL bundles (AM, IM, and PL) was measured with a robotic/ UFS testing system. The AM bundle stabilized the knee against both the anterior and rotatory loads. The PL bundle stabilized the knee especially near full extension. The IM bundle supported the AM and PL bundles through all flexion angles, especially from 30° to 45°, against the rotatory load. Acknowledgment: The authors thank Monica LindeRosen, B.S., and Chad A. Hume for their technical assistance.
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Purpose: To investigate the biomechanics of the intermediate (IM), anteromedial (AM), and posterolateral (PL) bundles in the human anterior cruciate ligament (ACL). Methods: Eighteen human cadaveric knees were tested with a robotic/universal force-moment sensor testing system. Anterior tibial translation (ATT) was determined under an 89-N anterior tibial load. Coupled ATT was determined under a combined rotatory load of 7-Nm valgus and 5-Nm internal rotation torque (pivot moment). Each bundle’s in situ forces were measured under identical external loading conditions. Results: Under anterior load, the PL bundle’s in situ force was highest at 0° and decreased during flexion. Under the anterior load, the AM bundle’s in situ force was significantly higher than the IM and PL bundles’ force at 15°, 30°, and 60°. Under the pivot moment, the AM bundle’s in situ force was significantly higher than the PL and IM bundles’ force at 0° and 15°, and the IM bundle had the lowest in situ force at 0° but higher in situ force than the AM and PL bundles at 30° and 45°. IM and AM bundle removal increased ATT under the anterior load at all angles. Cutting the PL bundle after IM and AM bundle removal (whole ACL removal) significantly increased ATT under the anterior load at 0°, 15°, and 30° of knee flexion and increased coupled ATT under the pivot moment at 0° and 15°. Conclusions: The biomechanical role of each of the 3 ACL bundles (AM, IM, and PL) was measured with a robotic/universal force-moment sensor testing system. The AM bundle stabilized the knee against both the anterior and rotatory loads. The PL bundle stabilized the knee especially near full extension. The IM bundle supported the AM and PL bundles through all flexion angles, especially from 30° to 45°, against the rotatory load. Clinical Relevance: Knowledge of functions of the different ACL bundles will help improve ACL reconstruction techniques to enable restoration of normal knee function.
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From the Departments of Orthopaedic Surgery (Y.K., S.J.M.I., A.M., P.L., J.H.W., Y.M., F.H.F.) and Mechanical Engineering (S.K., P.S., F.H.F.), University of Pittsburgh, Pittsburgh, Pennsylvania, U.S.A.; and Department of Orthopaedic Surgery, Nihon University (Y.K.), Tokyo, Japan. Supported by the Albert B. Ferguson Jr., M.D., Orthopaedic Fund of The Pittsburgh Foundation. F.H.F. received a research grant from Smith & Nephew. The authors report no conflict of interest. Received October 17, 2010; accepted July 27, 2011. Address correspondence to Freddie H. Fu, M.D., Department of Orthopaedic Surgery, University of Pittsburgh, 3471 Fifth Ave, 1010 Kaufmann Bldg, Pittsburgh, PA 15213, U.S.A. E-mail: [email protected] © 2012 by the Arthroscopy Association of North America 0749-8063/10614/$36.00 doi:10.1016/j.arthro.2011.07.019
any surgeons have recently focused on anatomic anterior cruciate ligament (ACL) reconstruction; therefore detailed anatomic studies are required to improve surgical techniques. Several anatomic studies have shown that the ACL can be divided into 2 functional bundles: the anteromedial (AM) bundle and the posterolateral (PL) bundle.1-6 Although this anatomic concept has been widely accepted, other studies have reported that the ACL consists of 3 bundles: AM, PL, and intermediate (IM) bundles.7-10 One study has even shown that the ACL can be divided into 4 bundles: anterolateral, AM, central, and posterior.11 From the anatomic viewpoint, in many animal species, 3 ACL bundles (AM, IM, and PL) are clearly discernible,12,13 although only a few studies have investigated the biomechanical role of
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each of the 3 bundles in animal models.12,13 Studies have shown that the IM bundle plays a subordinate role to the AM and PL bundles in animal models.12,13 Similarly, few studies have determined the biomechanical role of each of the 3 human ACL bundles.7 When anatomic ACL reconstruction is performed, the ACL remnant should be used as a guide for tunnel placement.14 An anatomic study showed a variety of ACL tibial footprints under the 2-bundle ACL concept.15 It is believed that more detailed functional findings would help us understand which position would be optimal for tunnel placement within the ACL footprint. To improve ACL reconstruction, it is important to better understand the biomechanical characteristics of each native ACL bundle. The first purpose of this study was to show the triple-bundle human ACL anatomy. The second purpose was to investigate the biomechanical role of each human ACL bundle. Even if the ACL is divided into 3 functional bundles, we hypothesize that the AM bundle plays the main role in anterior stability and that the PL bundle mainly contributes to rotatory stability, on the basis of previous reports based on the 2-bundle ACL concept.6,16 Furthermore, we hypothesize that the IM bundle plays a supplementary role to the AM and PL bundles, as previous animal studies have reported.12,13 METHODS ACL Triple-Bundle Anatomy and Histologic Analysis To better evaluate triple-bundle ACL anatomy, 10 human cadaveric knees (6 men and 4 women; mean donor age at the time of death, 60.0 years [SD, 3.9 years]) were dissected. According to earlier anatomic studies, the ACL can be divided into 2 bundles (AM and PL) by their differences in tension patterns.1,3,6,17-19 In this study, after careful dissection, the entire ACL, including the ACL insertion site and its connection with the lateral meniscus, was removed. The excised ACL tissues were frozen in 2-methylbutane pre-cooled in liquid nitrogen and then stored at ⫺80°C until cryosectioning to maintain the positional relation between the ACL and its surroundings. Six-micrometer sections were prepared. Masson trichrome staining (IMEB, Chicago, IL) was then performed.
universal force-moment sensor (UFS) testing system. Computed tomography of the specimens was performed before testing to ensure the absence of osseous abnormalities, deformities, or osteoarthritis. All specimens were frozen at ⫺20°C and thawed the night before testing. The knees were left intact, and the specimens were kept moist with saline solution during the testing to prevent soft-tissue exsiccation. The femur and tibia were then cut approximately 20 cm from the joint line, and the surrounding skin and muscles that were more than 10 cm away from the joint line were removed to expose the bone. The specimens were subsequently secured within custom-made aluminum cylinders by use of an epoxy compound (3M Bondo, Atlanta, GA) and rigidly fixed to the robotic/ UFS testing system.12,20-23 To prevent slippage between the epoxy and the specimens in the rig, the epoxy was screwed through several holes with thread grooves made into the aluminum cylinder. Transection Technique Arthroscopy was performed in all specimens with a 30° arthroscope. The surgical approach included a 3-portal technique with the anterolateral, AM, and accessory medial portals.24-26 All the specimens were arthroscopically dissected by a single trained surgeon (Y.K.). In this study the extension of the inner edge of the anterior horn of the lateral meniscus was considered the anterior border of the PL bundle (Fig 1). A discrete boundary between the IM and AM bundles can be observed after careful removal of all the soft tissue surrounding the ACL.27 Fibrous-like soft tissue was found from the lateral meniscus to the lateral side of the anterior aspect of the ACL. There was a wrinkle
Biomechanics We tested 18 fresh-frozen human cadaveric knees (13 men and 5 women; mean donor age at the time of death, 53.5 years [SD, 6.7 years]) using a robotic/
FIGURE 1. Tibial insertion site anatomy of ACL. (LM, lateral meniscus; MM, medial meniscus.)
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FIGURE 2.
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Each ACL bundle was identified and then selectively sectioned under arthroscopic vision.
in the anterior aspect of the ACL in all specimens. This wrinkle was defined in this study as the border between the IM and AM bundles. Thus each of the 3 ACL bundles was identified and separated with a periosteal elevator and selectively sectioned by use of the Vulcan EAS Electrothermal Arthroscopy System (Smith & Nephew Endoscopy, Andover, MA) (Fig 2). Robotic/UFS Testing System A CASPAR Stäubli RX90 robot (Orto MAQUET, Rastatt, Germany) was used to manipulate the joint. A UFS testing system (model 4015; JR3, Woodland, CA) was used to measure the forces and moments for 6 df. The robotic system was capable of controlling the displacement and the force/moment applied to the knee in all 6 df based on a mathematic description of knee kinematics and kinetics.20,21,28 Control and data acquisitions were performed by use of a personal computer and the MATLAB programming environment (The MathWorks, Natick, MA). The robot arm had a repeatability of motion within ⫾0.02 mm at each joint. According to the manufacturer, the UFS testing system has reliability within ⫾0.2 N and ⫾0.1 Nm. Testing Protocol The experimental protocol and acquired data are outlined in Table 1. After a specimen was attached to
the robotic/UFS testing system, the path of passive flexion-extension of the intact knee was determined from full extension to 90° of flexion by moving the tibia through 1° increments of flexion while minimizing the forces and moments. This path served as the reference position from which knee kinematics were measured and provided the starting position for the recorded kinematics. For this study, the loading conditions included (1) an 89-N anterior tibial load with the knee at full extension and at 15°, 30°, and 60° of flexion and (2) a
TABLE 1.
Experimental Protocol and Data Acquired
Step
Knee Status
Loading Condition
Data Acquired
1 2
Intact ACL IM deficient
Applied 2 loads Repeat kinematics
Intact knee kinematics In situ force of IM bundle IM-deficient knee kinematics In situ force of AM bundle IM-/AM-deficient knee kinematics In situ forces of PL bundle and ACL ACL-deficient knee kinematics
Applied 2 loads 3
IM/AM deficient
Repeat kinematics Applied 2 loads
4
ACL deficient
Repeat kinematics Applied 2 loads
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combined rotatory load of 7 Nm of valgus torque and 5 Nm of internal tibial torque at full extension and at 15°, 30°, and 45° of knee flexion. The anterior tibial load was used because the ACL is a major restraint to anterior tibial translation (ATT) and corresponds to the Lachman test and the anterior drawer test. The force of 89 N is equivalent to that used in the KT-1000 arthrometer (MEDmetric, San Diego, CA).29 The combined valgus and internal tibial torque were chosen to simulate the pivot-shift test.30,31 The remaining 5-df kinematics of the knees in an intact state was determined in response to both loading conditions. To observe the roles of the 3 bundles, they were cut in sequential order before retesting using the same criteria. After the intact knees (intact group, n ⫽ 18) were tested, the IM bundle of all knees was cut first (IM-deficient group, n ⫽ 18). The AM bundle was cut next (IM-/AM-deficient group, n ⫽ 18), followed by cutting of the PL bundle (ACL-deficient group, n ⫽ 18). The in situ force in each ACL bundle was determined after careful arthroscopic transection of each ACL bundle. ATT (in millimeters) in response to the external loads was measured at subsequent states (intact, IM deficient, IM/AM deficient, and ACL deficient). The previously recorded positions of the intact knee were reproduced by the robotic manipulator on the ACL-deficient knee, and the UFS testing system measured new forces and moments. On the basis of the superposition principle, the difference between the forces of the intact and ACL-deficient knees was determined to be the in situ force in the ACL.23 To assess changes in knee kinematics associated with ACL deficiency, the same external loads previously applied to the intact knee were again applied to the ACL-deficient knee and the resulting kinematics was measured.
for the ANOVA test and P ⱕ .017 for the pair-wise comparisons. All statistical data were calculated with the statistical software package SPSS, version 17.0 (SPSS, Chicago, IL). RESULTS Anatomy and Histologic Analysis Careful dissection and histologic analysis showed the presence of connective soft tissue from the lateral meniscus to the anterior part of the ACL in all specimens (Fig 3). This soft tissue divides the anterior part of the ACL into 2 other bundles, the IM bundle and the AM bundle. Histologic findings, especially those observed in cross sections, could not clearly show that
Statistical Analysis Because all variables were measured within the same specimen, statistical analyses of the kinematics and in situ forces were performed by use of a 2-factor repeated-measures analysis of variance (ANOVA) that evaluated knee state and flexion angle. Multiple comparisons with the Bonferroni post hoc test were performed to compare means among groups (IM, PL, AM, and intact ACL) and to compare differences between the intact, IM-deficient, IM-/AM-deficient, and ACL-deficient conditions at specific angles of knee flexion. Statistical significance was set at P ⱕ .05
FIGURE 3. Connective tissue from the lateral meniscus to the anterior of the ACL divides the AM bundle from the IM bundle. This can be seen during (A) histology (Masson trichrome staining; original magnification, ⫻40) and (B) arthroscopy.
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force at 0° of knee flexion, but the IM bundle had a higher in situ force than the PL bundle at 15° of knee flexion. Furthermore, the IM bundle had a higher in situ force than the AM and PL bundles at 30° and 45° of knee flexion (Fig 4B). ATT During Anterior Tibial Load: After the IM bundle was sectioned, no significant change was found in ATT in response to the anterior load. On sectioning of the AM bundle, ATT increased significantly at 15°, 30°, and 60° of knee flexion. When the PL bundle was sectioned, ATT increased significantly at 0°, 15°, and 30° of knee flexion (Fig 5A). Coupled ATT During Combined Rotatory Load: When only the IM bundle was sectioned, the coupled ATT increased in response to the combined rotatory load, but no significant difference was seen. When the ACL was completely sectioned, coupled ATT increased significantly at 0° and 15° of knee flexion. There was a significant difference in coupled ATT
FIGURE 4. In situ forces in response to (A) anterior tibial load and (B) combined rotatory load.
there were borders among the 3 bundles. Even a coronal section could not show the clear border between the AM and IM bundles. Biomechanical Analysis In Situ Forces During Anterior Tibial Load: There was no significant in situ force difference in response to anterior load between the AM and PL bundles at 0° of knee flexion, although the PL bundle had a higher in situ force. The IM bundle had the lowest in situ force at 0° and 15° of knee flexion. The AM bundle had a significantly higher in situ force than the IM and PL bundles at 15°, 30°, and 60° of knee flexion. The PL bundle had the lowest in situ force at 30° and 60° of knee flexion (Fig 4A). In Situ Forces Under Combined Rotatory Load: The AM bundle had a significantly higher in situ force in response to the combined rotatory load than the PL and IM bundles at 0° and 15° of knee flexion. The PL bundle had the lowest in situ force at 15°, 30°, and 45° of knee flexion. The IM bundle had the lowest in situ
FIGURE 5. (A) ATT in response to anterior tibial load. (B) Coupled ATT in response to combined rotatory load. (DEF, deficient.)
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between the IM-deficient and ACL-deficient knees at 0° of knee flexion (Fig 5B). DISCUSSION The biomechanical roles of the AM, IM, and PL bundles of the ACL were measured in this study. We have shown that the AM bundle stabilizes the knee against both anterior and rotatory loads, that the PL bundle stabilizes the knee especially near full extension, and that the IM bundle plays a supplemental role to the AM and PL bundles through all flexion angles, especially from 30° to 45°, against a rotatory load. A recent biomechanical study has indicated that ATT at higher degrees of knee flexion is limited by the AM bundle fibers whereas ATT at lower flexion angles is limited by the PL bundle fibers.6 Our study showed similar findings, in that ATT at 0° and 15° of knee flexion under external loads increased more when the PL bundle was cut. Other biomechanical studies have shown that an increase in laxity, implied by significantly increased ATT during a pivot moment, is higher if the PL bundle is cut than if the AM bundle is cut6,16; despite this, these studies do not suggest that the AM bundle does not play a role in rotational stability. Our study, however, has shown that sectioning of the AM bundle also causes an increase in laxity during the combined rotatory load, suggesting that the AM bundle, in addition to the PL bundle, plays an important role in rotational stability. At full extension of the knee joint, the AM and PL bundles work equally, but as the knee is flexed, the AM bundle is mainly working. This study has also shown that the IM bundle plays an important role under pivot moments at 30° and 45° of knee flexion. This suggests that the IM bundle plays a secondary role not only to the AM bundle but also to the PL bundle. Although Norwood and Cross9 described that the AM bundle contributes to anterolateral stability whereas the IM bundle adds to anterior and AM stability and the PL bundle assists in PL stability, Amis and Dawkins7 showed that each bundle contributes to anterior stability at different flexion angles. The results of our study are in concordance with these studies because the results show that each bundle contributes to anterior stability at different knee flexion angles. Iwahashi et al.8 evaluated the “functional length” of the 3 ACL bundles and found that they were not isometric, supporting the idea that the contributions of each bundle, including the IM bundle, to knee stability depend on the angle of knee flexion. As a previous study has mentioned, the advan-
tages of a robotic testing system include kinematic measurements when the knee is artificially restrained.32 Most importantly, this advanced method has the advantage of collecting experimental data from the same cadaveric knee specimen under different experimental conditions (such as intact, IMdeficient, IM-/AM-deficient, and ACL-deficient knee states), thus reducing the effect of interspecimen variation and significantly increasing the statistical power of the data through allowing the use of repeated-measures ANOVA for data analysis. In this study a histologic analysis was performed before the biomechanical testing to better understand triple-bundle ACL anatomy. A previous study has shown a septum between the AM and PL bundles in the fetal ACL2; however, we could not visualize a clear septum between the ACL bundles. The cleavage that we showed, which looked like a septum between the AM and IM bundles on histologic imaging (Fig 3A), might be an artifact caused by the staining, although a wrinkle in the anterior aspect of the ACL was seen arthroscopically in all specimens. This might be explained by the existence of soft tissue from the lateral meniscus to the anterolateral portion of the ACL. We have shown that the IM bundle can be divided from the AM and PL bundles not anatomically but functionally. This result would advocate a triplebundle ACL reconstruction as reported by Shino et al.10 However, we believe that anatomic tunnel placement is more important than multiple-bundle reconstruction, such as double- or triple-bundle ACL reconstruction. We found that the magnitude of the in situ force of the IM bundle was almost isometric and low, although it was relatively higher than that of the AM and PL bundles under the pivot moment at 30° and 45° of knee flexion. As a practical proposition, when double-bundle ACL reconstruction is performed, the tibial AM tunnel should be positioned toward the AM side (AM bundle footprint in a narrow sense) and not the anterolateral side (IM bundle footprint in a narrow sense). To ensure correct anatomic ACL reconstruction, it is imperative that ACL anatomy and biomechanics are fully understood. We hope the results of this study will add to the existing knowledge and help surgeons to improve ACL reconstruction techniques. There were some limitations of this study. First, the results at 90° of knee flexion could not be shown. Because the full extension angle was not always 0° of knee flexion, the full-extension angle of each specimen was measured by use of an angle gauge. The
HUMAN TRIPLE-BUNDLE ACL BIOMECHANICS mean full-extension angle of all knee specimens was 3.5° (SD, 1.9°), ranging from 0° to 8°. Over 90° was too deep to be examined with the robotic/UFS testing system used. In the future, testing should be done at more detailed knee flexion angles. Second, dissection of the 3 bundles depended on human evaluation and, as such, was prone to error. To minimize this, the same experienced surgeon (Y.K.) with previous experience in animal dissections performed all the dissections.12,13 To prevent any unknown bias, the bundles should have been cut in different sequential order. However, we believed that it was important to identify and cut the IM bundle first for consistency, because the IM bundle contacts both the AM bundle (in a narrow sense) and PL bundle and is thought to be a lateral part of the AM bundle in a broad sense. In addition, the accuracy of cutting each bundle under arthroscopic control must be considered, although we believe our arthroscopic distinction was no less accurate than an open dissection. Third, the applied external loads in this study were lower than the loads used in previous biomechanical studies.6,30,31,33-37 Nonetheless, even with lower applied external loads, we were able to show both significant differences and the trends that occur after each bundle is sectioned. Finally, no prior sample size analysis or post hoc power analysis was performed, and despite the fact that statistically significant results were found, the large number of variables evaluated could increase the type II error. CONCLUSIONS The biomechanical role of each of the 3 ACL bundles (AM, IM, and PL) was measured with a robotic/ UFS testing system. The AM bundle stabilized the knee against both the anterior and rotatory loads. The PL bundle stabilized the knee especially near full extension. The IM bundle supported the AM and PL bundles through all flexion angles, especially from 30° to 45°, against the rotatory load. Acknowledgment: The authors thank Monica LindeRosen, B.S., and Chad A. Hume for their technical assistance.
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