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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
Am J Sports Med. Author manuscript; available in PMC Aug 6, 2012.
Published in final edited form as:
PMCID: PMC3412516
NIHMSID: NIHMS394233
Cartilage Pressure Distributions Provide a Footprint to Define Female Anterior Cruciate Ligament Injury Mechanisms
Carmen E. Quatman, PhD,* Ali Kiapour, PhD, Gregory D. Myer, PhD, CSCS,* Kevin R. Ford, PhD,§ Constantine K. Demetropoulos, PhD, Vijay K. Goel, PhD, and Timothy E. Hewett, PhD*§||
Investigation performed at Cincinnati Children’s Hospital, Cincinnati, Ohio; University of Toledo, Toledo, Ohio; and The Ohio State University, Columbus, Ohio
Address correspondence to Timothy Hewett, PhD, 2050 Kenny Road, Suite 3100, Columbus, OH 43221 (Tim.Hewett/at/osumc.edu)
*Departments of Physiology and Cell Biology, Sports Medicine Sports Health & Performance Institute, The Ohio State University, Columbus, Ohio.
Departments of Bioengineering and Orthopaedic Surgery, Colleges of Engineering and Medicine, University of Toledo, Toledo, Ohio.
Cincinnati Children’s Hospital Medical Center Research Foundation, Sports Medicine Biodynamics Center, and Human Performance Laboratory, Cincinnati, Ohio.
§Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio.
||Departments of Orthopaedic Surgery, Family Medicine, and Biomedical Engineering, The Ohio State University, Columbus, Ohio.
Background
Bone bruises located on the lateral femoral condyle and posterolateral tibia are commonly associated with anterior cruciate ligament (ACL) injuries and may contribute to the high risk for knee osteoarthritis after ACL injury. The resultant footprint (location) of a bone bruise after ACL injury provides evidence of the inciting injury mechanism.
Purpose/Hypothesis
(1) To analyze tibial and femoral articular cartilage pressure distributions during normal landing and injury simulations, and (2) to evaluate ACL strains for conditions that lead to articular cartilage pressure distributions similar to bone bruise patterns associated with ACL injury. The hypothesis was that combined knee abduction and anterior tibial translation injury simulations would demonstrate peak articular cartilage pressure distributions in the lateral femoral condyle and posterolateral tibia. The corollary hypothesis was that combined knee abduction and anterior tibial translation injury conditions would result in the highest ACL strains.
Study Design
Descriptive laboratory study.
Methods
Prospective biomechanical data from athletes who subsequently suffered ACL injuries after testing (n = 9) and uninjured teammates (n = 390) were used as baseline input data for finite element model comparisons.
Results
Peak articular pressures that occurred on the posterolateral tibia and lateral femoral condyle were demonstrated for injury conditions that had a baseline knee abduction angle of 5°. Combined planar injury conditions of abduction/anterior tibial translation, anterior tibial translation/internal tibial rotation, or anterior tibial translation/external tibial rotation or isolated anterior tibial translation, external tibial rotation, or internal tibial rotation resulted in peak pressures in the posterolateral tibia and lateral femur. The highest ACL strains occurred during the combined abduction/anterior tibial translation condition in the group that had a baseline knee abduction angle of 5°.
Conclusion
The results of this study support a valgus collapse as the major ACL injury mechanism that results from tibial abduction rotations combined with anterior tibial translation or external or internal tibial rotations.
Clinical Relevance
Reduction of large multiplanar knee motions that include abduction, anterior translation, and internal/external tibial motions may reduce the risk for ACL injuries and associated bone bruises. In particular, prevention of an abduction knee posture during initial contact of the foot with the ground may help prevent ACL injury.
Keywords: bone bruise, ACL, articular cartilage, knee injury
Anterior cruciate ligament (ACL) injury is a common, often devastating, injury. It is well documented that women demonstrate a 4- to 6-fold higher injury rate compared with men participating in similar sports.1,2,15,25 During the ACL injury event, the large external forces that incite ligament disruption likely also lead to violent impact of the tibial and femoral articular cartilage, which transfers into the subchondral bone and often causes a bone bruise “footprint” that is a result of the mechanism of injury (Figure 1).43 Clinical imaging studies of acute ACL injury demonstrate that hyperintense signals in the subchondral tibia and femur (bone bruises) occur in more than 80% of patients who sustain complete ACL disruption.49 Bone bruises are commonly found on the posterolateral tibia and lateral femoral condyle on imaging studies after acute ACL injury (Figure 1) and likely reflect the tibial and femoral cartilage impact that occurs at the time of injury.20,33,49 The locations of bone bruises may provide insight into the directions (anatomic planes) that lead to ACL injury.
Figure 1
Figure 1
Magnetic resonance images of bone bruise patterns (lateral femoral condyle and posterolateral tibial plateau) associated with acute anterior cruciate ligament (ACL) injury that the finite element model data are compared to determine relevance of injury (more ...)
The objectives of this study were (1) to analyze tibial and femoral articular cartilage pressure distributions during normal landing and injury simulations and (2) to evaluate ACL strains for conditions that lead to articular cartilage pressure distributions similar to bone bruise patterns associated with ACL injury. We hypothesized that combined anterior tibial shear and knee abduction injury simulations would demonstrate articular cartilage pressure distributions in locations similar to bone bruise patterns found on imaging studies after acute ACL injuries. We also hypothesized that this same kinematics would lead to high ACL strains.
Institutional review board approval and written, informed consent forms were obtained before testing for all patients. A dynamic finite element knee model (Figure 2) (Appendix Figure A-1, available in the online version of this article at http://ajs.sagepub.com/supplemental/) was created from computed tomography and magnetic resonance images of a skeletally mature, young adult, female athlete to determine articular cartilage pressure distributions during normal landing and injury simulations (Abaqus 6.10 software, Simulia, Providence, Rhode Island). Details of model development methods are described in the Appendix (Appendix Tables A1–3 and Figures A1–3, available online).39 Figure 3 demonstrates a flow chart of the methods sequence. The model was subjected to validity evaluations and model simulations to analyze articular pressure distributions during normal landing and injury.
Figure 2
Figure 2
Knee finite element model that demonstrates the femur, tibia, fibula, patella anterior cruciate ligament (ACL), and medial collateral ligament meshes.
Figure 3
Figure 3
Flow chart describing the methods of the study.
The finite element model was subjected to evaluations based on cadaveric experimental data available in the literature and from previous cadaveric tests conducted by some of the current investigators (Appendix Figures A-2 and A-3, available online, provides detailed results). The first criterion for model confirmation was that the Pearson correlation was good (r = .50–.75) to excellent (r > .75) for the model results compared with cadaveric data available in the literature.38,46 The second criterion for model confirmation was that the differences between finite element model simulations and cadaveric data were less than 2 standard deviations (SDs) from the mean of the cadaveric data.31
We observed an excellent correlation (r = .97, P < .001) between the cadaveric results and predicted laxity in the finite element model. The finite element model predicted knee laxity values similar to those of Markolf et al,30 with anterior-posterior, external-internal, and varus-valgus laxities at 0°, 20°, and 45° of knee flexion for the finite element model within 2 SDs of the predicted mean for the cadaveric investigations. We used data from 10 human cadaveric lower extremities tested by Sohn et al48 to confirm the articular cartilage pressure distributions for the finite element model during weightbearing conditions. We observed a correlation (r = .888, P < .01) between the finite element predictions and the cadaveric data for articular cartilage pressures, with the model results within 2 SDs of the mean of the cadaveric data (Appendix Table A-3, available online). Markolf et al28 also examined combined loading states that generate high ACL forces (varus-valgus, internal-external tibial rotation, and anterior tibial force). These loading conditions were repeated in the model (knee flexion angles of 0°–40°). Again, an excellent correlation (r = .92, P < .001) was observed between the finite element predicted forces and the cadaveric results (Appendix Figures A-2 and A-3, available online). The finite element data were within 2 SDs of the reported cadaveric means for each testing condition.
The femur and tibia were divided into 6 separate sections each in order to describe articular cartilage pressure distributions (Figure 4). These sections were defined as anterior-lateral (AL), anterior-medial (AM), middle-lateral (ML), middle-medial (MM), posterior-lateral (PL), and posterior-medial (PM) by drawing a sagittal plane divider and 2 frontal plane dividers (Figure 4). This technique was previously described in detail and was adapted to allow for comparisons to current clinical techniques for localizing articular cartilage abnormalities (International Cartilage Repair Society format).4,39 Because the PL tibial and ML femoral sections are the most common bone bruise locations after ACL injury, articular cartilage contact pressure locations in the PL and ML sections were considered likely ACL injury mechanisms (Figures 1 and and55).33 Peak ACL strains were identified for each condition that resulted in peak articular cartilage pressures in the PL tibia and ML femur. Peak ACL strain was determined by the midsub-stance ACL element that had the maximum critical value.
Figure 4
Figure 4
Illustration of the sections used to describe pressure locations that demonstrate articular cartilage pressures during a loading scenario. The various colors indicate the stresses in the menisci and articular cartilage (further description in Figure 5 (more ...)
Figure 5
Figure 5
Injury conditions that resulted in peak articular cartilage contact pressure locations in the posterolateral tibia and lateral femur. A, combined abduction tibial rotation and anterior tibial translation injury conditions. B, the articular cartilage pressure (more ...)
Kinematic and kinetic data during a drop vertical jump maneuver from female athletes before their athletic seasons were used as baseline input for the finite element model. Mean kinematic and kinetic data at initial contact during landing from a drop vertical jump for athletes who went on to subsequent injury (INJ) after testing (n = 9 knees) and control (CTRL) (n = 390 knees) athletes (who did not have subsequent ACL injury) were used as baseline input for the model.16 Methods for biomechanical data collection are described in Ford et al9 and Hewett et al.16 A static trial was used as the athlete’s neutral (zero) alignment with subsequent measures relative to this position.10
Three-dimensional coordinates for the tibial and femoral markers were identified from the in vivo data (see Ford et al for marker placement) and used to define baseline input rotational and translational boundary conditions for the finite element model at corresponding node locations.9,16 The coordinate system described by Grood and Suntay14 was used to define the knee joint coordinate system of the finite element model with respect to the 3-dimensional knee joint motions, and a geometric center axis was used to apply flexion rotations.34 A vertical ground-reaction force was applied to the finite element model as a compressive force across the tibiofemoral joint. A 600-N quadriceps tension and 400-N hamstrings tension were applied to the model to simulate in vivo muscle resistance and compressive joint forces.46,51 Baseline “normal” landing conditions included a knee abduction angle of 5° (INJ) or −3.4° (CTRL) with a 20° knee flexion angle and a vertical ground-reaction force (600 N) for both groups.16
We used the finite element model to simulate ACL injury mechanisms for each group (INJ, CTRL) by single planar loading conditions for abduction rotation (abduction of the tibia relative to the femur), internal tibial rotation, external tibial rotation, and anterior tibial translation (Figure 3). Combined injury conditions were examined for combined abduction/anterior tibial translation, abduction/internal tibial rotation, abduction/external tibial rotation, anterior tibial translation/internal tibial rotation, and anterior tibial translation/external tibial rotation. Because video analyses indicate that female athletes have 4° higher abduction angles compared with their initial contact angle during the ACL injury event, abduction injury simulations consisted of a 4° increase in abduction angle relative to baseline initial contact landing conditions.22 Anterior tibial translation injury simulations consisted of 6-mm increases in anterior tibial translation. Normal anterior tibial translation laxity is approximately 3 mm (depending on flexion angle and applied force), and ACL deficiency leads to an increase of 3 mm (or more) of anterior tibial translation laxity compared with the healthy contralateral limb.6,29,30 Internal and external tibial rotation injury simulations included 9° increases in the respective rotations because weightbearing axial rotations are approximately 5° to 7° in each direction, and Olsen et al36 reported approximately 9° of internal or external rotation of the tibia during ACL injury.47 The articular cartilage contact pressure locations were determined for each injury scenario and compared with the common bone bruise locations after acute ACL injury.
Table 1 summarizes the location of peak articular cartilage pressure distributions during normal (noninjury producing) landing, isolated single-plane injury conditions, and combined injury conditions. Peak articular pressures that matched the typical bone bruise pattern associated with ACL injury were found for the following conditions in the INJ group: combined abduction/anterior tibial translation, anterior tibial translation/internal tibial rotation, or anterior tibial translation/external tibial rotation and isolated anterior tibial translation, external tibial rotation, or internal tibial rotation (Figure 5). Only the combined abduction/anterior tibial translation condition resulted in articular cartilage pressure locations isolated to the quadrants similar to bone bruise patterns (Table 1). Although other conditions resulted in peak pressures that occurred in the PL and ML quadrants, the patterns overlapped into other quadrants as well (Table 1). No injury conditions in the CTRL group led to peak pressures in the locations that matched the typical bone bruise pattern (Table 1 and Figure 5).
TABLE 1
TABLE 1
Section Locations of Articular Cartilage Pressure Distributions for Each Injury Condition for Injury (INJ) and Control (CTRL) Groupsa
The increases in ACL strains from normal landing conditions for the scenarios that resulted in peak articular cartilage distributions similar to bone bruises associated with the ACL are listed in Table 2. The highest ACL strain occurred in the combined abduction/anterior tibial translation condition with a 4.6-fold (358%) increase from normal landing conditions in the INJ group. Combined anterior tibial translation/internal tibial rotation for the INJ group also resulted in high ACL strains (3.9-fold, 289% increase in strain relative to normal landing conditions). Combined anterior tibial translation/external tibial rotation resulted in a 3.7-fold (270%) increase to ACL strain for the INJ group, and combined abduction/external tibial rotation for the INJ group resulted in a 2.0-fold (99%) increase in ACL strain. Isolated anterior tibial translation, internal tibial rotation, and external tibial rotation resulted in a 3.6-fold (264%) increase, 1.2-fold (16%) increase, and 0.8-fold (16%) decrease from the normal landing condition ACL strain, respectively.
TABLE 2
TABLE 2
Change in Peak Anterior Cruciate Ligament (ACL) Strain for Injury Conditions (Relative to Normal Landing) That Resulted in Articular Cartilage Contact Pressure Locations in Posterolateral Tibia and Lateral Femoral Condylea
Bone bruises are commonly associated with ACL injuries, and the resultant location of these bone bruises (commonly found on the lateral femoral condyle and posterolateral tibia) provides evidence to the injury mechanism. We developed and evaluated a finite element model of a knee of a young female athlete to analyze tibial and femoral articular cartilage pressure distributions during normal landing and injury simulations. The objectives of this study were (1) to analyze tibial and femoral articular cartilage pressure distributions during normal landing and injury simulations and (2) to evaluate the ACL strains for conditions that lead to articular cartilage pressure distributions similar to bone bruise patterns associated with ACL injury.
The tibiofemoral osteokinematic planar (sagittal, frontal, transverse motions) contributions to the mechanisms of ACL injury are a current debate in recent journal articles and symposia at sports medicine conferences.24,40,41,50,52 Video studies of ACL injuries provide evidence of 2 predominant loading patterns: (1) valgus collapse of the knee (a combination of knee valgus, hip internal rotation, and tibial rotation) or (2) anterior tibial shear.3,21,40 Systematic reviews of the literature related to ACL injury mechanisms by Shimokochi et al45 and Quatman et al41 concluded that ACL injuries are more likely to occur because of multiplanar rather than single-planar mechanisms, in which anterior tibial shear, valgus knee collapse, and internal or external tibial rotations represent the most likely contributors to the injury mechanism. Despite the large amount of literature related to ACL injury, the relationship and additive nature of these multiplanar loading conditions to ACL strain and injury remain unclear.
In vivo biomechanical data and video analyses indicate that increased lower extremity abduction loads and movements are associated with increased ACL strain and risk of injury.3,17,21,22 Data from the current investigation support abduction as a component of the ACL injury mechanism. Although isolated abduction injury simulations did not result in the typical bone bruise pattern, combined abduction/anterior tibial translation and combined abduction/external tibial rotation lead to articular cartilage pressure distributions on the lateral femur and posterolateral tibia. In addition, the current study demonstrated that combined abduction/anterior tibial translation, anterior tibial translation/internal tibial rotation, anterior tibial translation/external tibial rotation and isolated anterior tibial translation, external tibial rotation, or internal tibial rotation only resulted in peak pressure distributions occurring in the areas similar to the bone bruise pattern associated with ACL injury in athletes who had an abduction angle of 5° at initial contact during landing (INJ group). Thus, these lateral tibial and femoral bone bruises likely result from lateral compression of the femur and tibia. The more posterior tibial location of the bone bruise relative to the femur is most likely to result from abduction combined with either anterior tibial translation or internal or external tibial rotation during the injury event.
Most ACL injuries occur under weightbearing conditions, and modeling studies indicate that the ACL can impinge on the notch during combined abduction/external tibial rotation.12 Results from this study also indicate that external tibial rotation combined with anterior tibial translation or abduction rotation in an athlete who lands with an abducted knee posture may result in a bone bruise pattern that has been associated with ACL injuries. An abducted knee posture at initial contact is likely important for this type of mechanism because combined anterior tibial translation/external tibial rotation in the CTRL group did not result in the classic bone bruise pattern. However, the ACL strain for combined abduction/external tibial rotation was lower than the abduction/anterior tibial translation condition ACL strain.
Anterior shear of the proximal tibia is the most obvious ACL loading mechanism, and decreasing knee flexion angles increase the anterior shear force at the tibia.28,44 As video studies indicate that noncontact ACL injuries usually occur at low flexion angles, and women have been reported to have less knee flexion during sports movements, it is theorized that a powerful quadriceps force at low knee flexion angles could produce enough anterior shear force at the tibia to cause ACL rupture. Although anterior tibial translation conditions led to high ACL strains, isolated anterior tibial translation conditions only resulted in the typical bone bruise pattern in the INJ group that had an abducted knee posture during initial contact of landing from the jump. Moreover, there were high articular cartilage pressures noted on the medial aspect of the joint as well.
Cadaveric data indicate that combined knee abduction with internal tibial rotation, external tibial rotation, or anterior tibial forces leads to considerably larger ACL forces than internal or anterior tibial forces alone.28 For the current study, the ACL strains were higher for tibial abduction conditions coupled with anterior tibial translations or internal tibial rotations than isolated abduction, anterior translation, or internal tibial rotation conditions. Thus, multiplanar load conditions appear to be additive for ACL strains and likely increase risk of ACL injury.
The underlying microstructural damage to the articular cartilage and subchondral bone that occurs as a result of the large impact forces sustained by the tibia and femur may lead to cartilage thinning and osteochondral defects, in addition to the acute consequences of an initial ACL injury and concomitant bone bruise. This damage may serve as a precursor to osteoarthritis that accelerates the progression of degenerative changes in the knee.7,11,18,27 Recent reports also indicate that ACL injuries/reconstructions not only affect anterior-posterior stability but also knee joint motion in all 6 degrees of freedom. This multi-planar loss of knee stability may alter the tibiofemoral cartilage contact, which in combination with a commonly reported torn meniscus, may represent a secondary causative factor for knee osteoarthritis subsequent to ACL deficiency.19 The characterization of the kinematic and kinetic variables that contribute to ACL injury is essential in the design of the most effective prevention strategies. If bone bruise footprints can be utilized to define ACL injury mechanisms, specific neuromuscular training interventions designed to prevent the lower extremity mechanics that contribute to these bruise patterns may help athletes avoid the disability associated with posttraumatic knee osteoarthritis.
Limitations
All models have inherent limitations, and there are likely differences between experimental conditions and the real-world biomechanics of sports. High loading rate simulations are challenging and may require model simplifications, and it may not be possible to fully confirm injury models under these conditions. Inherent damage associated with injury biomechanics limits a researcher’s ability to conduct robust high rate mechanical characterization on any single specimen. However, we used both information from a large in vivo cohort study and data provided by the finite element model to extend the existing knowledge base and to appraise working hypotheses about reducing injury risk (both ACL and associated bone bruises) without reporting exact stress and strain results. Instead, the relationships between structures and changes in the locations of concentrated forces were evaluated between test conditions to help us understand, but perhaps not accurately predict, exact articular cartilage stresses. The methodology utilized in this study is both innovative and unique in that it embraces a new “in sim” methodological approach that shifts the current experimental paradigm to incorporate a multifaceted integration of in vivo, in vitro (cadaveric), and in silico (computer modeling) methods.42 In sim methodology can be used to provide a platform for a more comprehensive understanding of the complex joint biomechanics that occur during ACL injury.42 This model serves as an initial step in the development of a model to evaluate ACL injury mechanisms. Further development will focus on the incorporation of high rate and injury biomechanics data, not available at this stage. As this is a preliminary study and given the limited validation data to represent high loading conditions, only the location of pressure distributions associated with injury mechanisms is reported at this point. This model is needed to guide further study.
The results of this study support a valgus collapse injury mechanism that results from tibial abduction rotations combined with anterior tibial translation or external or internal tibial rotations. Reduction of knee abduction motions is possible with neuromuscular training that may help decrease the risk for ACL injury and associated bone bruises in female athletes.13,15,26,35 The large impacts sustained by the tibia and femur during ACL injuries may be a significant precursor event that accelerates the progression of degenerative changes in the knee. As demonstrated by the results of this study, the lateral tibial and femoral bone bruises associated with acute ACL injury may occur as a result of lateral joint compression. The more posterior location of bone bruises on the tibial plateau relative to the femur may indicate that the tibia shifts anteriorly or rotates internally relative to the femur during the injury event. Prevention programs that target reduction of large knee abduction, anterior translation, and internal and external tibial motions during sports activities may help reduce the risk for sustaining ACL injuries with associated bone bruises.
Acknowledgments
The authors thank Keith Kenter, Catherine Quatman-Yates, Jason Levine, Ata Kiapour, Krishna Mallik, Mark Paterno, Laura Schmitt, and Sam Wordeman for their stimulating discussions about these topics.
Footnotes
References 3, 5, 8, 22, 23, 28, 32, 36, 37, 53.
For reprints and permission queries, please visit SAGE’s Web site at http://www.sagepub.com/journalsPermissions.nav
One or more authors has declared the following potential conflict of interest or source of funding: National Institutes of Health grants R01-AR049735, R01-AR056259, and R03-AR057551. Funding support from the University of Toledo College of Medicine Pre-Doctoral Fellowship, the American College of Sports Medicine Foundation Plus One Active Research Grant on Wellness Using Internet Technology.
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