Microstructural and Mechanical Properties of the Posterior Cruciate Ligament: A Comparison of the Anterolateral and Posteromedial Bundles

Wright, Jon O. MD; Skelley, Nathan W. MD; Schur, Reid P. BS; Castile, Ryan M. BS; Lake, Spencer P. PhD; Brophy, Robert H. MD

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.16.00032
Scientific Articles
Abstract

Background: The microstructural organization (collagen fiber alignment) of the posterior cruciate ligament (PCL), which likely corresponds with its functional properties, has only been described qualitatively in the literature, to our knowledge. The goal of this study was to quantify the tensile mechanical and microstructural properties of the PCL and compare these qualities between the anterolateral and posteromedial bundles.

Methods: Twenty-two knee specimens from 13 donors (8 male and 5 female; mean age [and standard deviation] at the time of death, 43.0 ± 4.1 years; mean body mass index, 30.0 ± 6.7 kg/m2) were dissected to isolate the PCL, and each bundle was split into 3 regions. Mechanical testing of each regional sample consisted of preconditioning followed by a ramp-and-hold stress-relaxation test and a quasi-static ramp-to-failure test. Microstructural analysis was performed with use of a high-resolution, division-of-focal-plane polarization camera to evaluate the average direction of collagen orientation and the degree to which the collagen fibers were aligned in that direction. Results were compared between the anterolateral and posteromedial bundles and across the regions of each bundle.

Results: The anterolateral and posteromedial bundles demonstrated largely equivalent mechanical and microstructural properties. Elastic moduli in the toe and linear regions were not different; however, the posteromedial bundle did show significantly more stress relaxation (p = 0.004). There were also few differences in microstructural properties between bundles, which again were seen only in stress relaxation. Comparing regions within each bundle, several mechanical and microstructural parameters showed significant relationships across the posteromedial bundle, following a gradient of decreasing strength and alignment from anterior to posterior.

Conclusions: The PCL has relatively homogenous microstructural and mechanical properties, with few differences between the anterolateral and posteromedial bundles. This finding suggests that distinct functions of the PCL bundles result primarily from size and anatomical location rather than from differences in these properties.

Clinical Relevance: These properties of the PCL can be used to assess the utility of graft choices and operative techniques for PCL reconstruction and may partly explain limited differences in the outcomes of single-bundle compared with double-bundle reconstruction techniques for the PCL.

Author Information

1Departments of Orthopaedic Surgery (J.O.W., N.W.S., S.P.L, and R.H.B.), Mechanical Engineering and Materials Science (R.P.S., R.M.C., and S.P.L.), and Biomedical Engineering (S.P.L.), Washington University in St. Louis, St. Louis, Missouri

2Department of Orthopaedic Surgery, Beaumont Health, Royal Oak, Michigan

E-mail address for R.H. Brophy: brophyr@wudosis.wustl.edu

Article Outline

The posterior cruciate ligament (PCL) is the primary restraint to posterior translation of the tibia relative to the femur1-3 and is composed of 2 bundles: the anterolateral and the posteromedial2,4-6. Considerable research has been dedicated to investigating PCL anatomy and function, as PCL disruptions can be associated with knee instability and altered knee kinematics7-11.

While a large proportion of PCL injuries can be treated nonoperatively12-17, high-grade isolated PCL injuries and multiligament knee injuries may be treated operatively with reconstruction11,17-20 or, less commonly, repair9,21-23. Previous research characterizing the mechanical properties of the PCL has been limited by sample-preparation techniques, imaging technology, and the understanding of tissue mechanics at the time24-27. In addition, the microstructural organization (collagen fiber alignment) of the PCL, which likely corresponds with its functional properties, has only been described qualitatively in the literature, to our knowledge25.

The purpose of the present study was to quantify the tensile mechanical and microstructural properties of the PCL bundles under dynamic tensile loading. We used a novel polarization imaging technique to allow for real-time analysis of collagen fiber alignment during mechanical testing. On the basis of previous findings in both the anterior cruciate ligament (ACL)28,29 and the PCL27,30, we hypothesized that the anterolateral and posteromedial bundles would exhibit distinct mechanical and microstructural properties.

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Materials and Methods

Study Design

Human cadaveric tissues were handled in accordance with the Washington University School of Medicine in St. Louis body-donation policy. Institutional review board approval was not needed for the cadaveric study design. Inclusion criteria consisted of cadavers from patients who were <55 years of age at the time of death and had a body mass index (BMI) of <43 kg/m2. Exclusion criteria consisted of knee samples with a history of trauma, surgery, or instability as well as those from patients with recorded genetic conditions that could affect bone or ligament composition. Power analysis demonstrated that 14 PCLs (a total of 84 regional samples) would be required to avoid a type-II error with β = 0.20 and α = 0.05.

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Harvest Technique

Twenty-two knee specimens from 13 donors (8 male and 5 female; mean age [and standard deviation] at the time of death, 43.0 ± 4.1 years; mean BMI, 30.0 ± 6.7 kg/m2) fitting the selection criteria were acquired (Table I). Ligament tissues were kept hydrated with phosphate-buffered saline (PBS) solution during all stages of this study, including dissection, sample preparation, and mechanical testing.

Soft tissues were removed, leaving only the ACL, PCL, menisci, and meniscofemoral ligaments intact. An oscillating saw was used to split the femoral condyles, starting in the trochlear groove. The split was completed near the PCL and ACL attachments with use of an osteotome for better control, preserving the osseous attachments of the PCL in order to maintain proper ligament orientation. After the condyles were separated, the synovium was removed to differentiate the PCL from the anterior and posterior meniscofemoral ligaments. The meniscofemoral ligaments, when present, were carefully dissected from the PCL and sharply dissected from their femoral attachments (Fig. 1). In 6 knees, an oblique fascicle of fibers was noted just posterior to the bulk of the posteromedial bundle, as described in a previous anatomical study4. Since these fascicles were too small for testing, they were discarded.

The division between the bundles of the PCL was identified on the basis of previous descriptions of PCL structural orientation, anatomical landmarks, and the behavior of each bundle under joint flexion and extension2-4,6,31. The division was bluntly developed at the femoral attachments, and then it was bluntly extended down to the tibial attachments. Once the bundles were separated, 2 incisions were made in each bundle in the coronal plane, just inferior to the femoral insertion, and they were extended down to divide each bundle into 3 regions. Each region was then marked at the lateral aspect of the femoral insertion to maintain orientation throughout testing and was detached from bone.

The 6 regions were numbered by anteroposterior orientation: region 1 (most anterior) through region 6 (most posterior), with regions 1 to 3 composing the anterolateral bundle and regions 4 to 6 composing the posteromedial bundle. The regions were thinned into approximately 600-μm regional samples with use of a freezing-stage sliding microtome. Cross-sectional area was measured with use of a 3-dimensional (3D) laser scanning system and a custom MATLAB program (The MathWorks), and the mean cross-sectional area of each regional sample was recorded for subsequent stress calculations.

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Sample Testing

Each regional sample was harvested, and the ends were affixed to small pieces of sandpaper using cyanoacrylate. Four 0.5-mm-diameter brass beads (Small Parts) were attached with cyanoacrylate to the central portion of each sample to provide points of reference for strain tracking and microstructural analysis.

Testing was performed with use of a tensile testing machine (TestResources). The sandpaper ends of the samples were placed in custom aluminum clamps with corresponding sandpaper footings to provide the necessary force transference without compressing or compromising the tissue itself, and the clamps were then attached to the actuators of the testing machine. The mechanical testing system was integrated with a custom-built quantitative polarized light imaging system that consisted of a fiber optic backlight (Dolan-Jenner); a circularly polarizing film (Dolan-Jenner); and a high-resolution, division-of-focal-plane polarization camera32,33.

Ligament samples were preloaded to 0.1 N to remove slack, and specimen gauge length was measured before each sample was tested. Testing consisted of 10 cycles of preconditioning by stretching the samples from 1.5% to 4.5% strain, a ramp-and-hold stress-relaxation test (a 5% strain step and dwell time of 300 seconds), and a quasi-static ramp-to-failure test at a strain rate of 1% per second. Images were acquired at approximately 18 frames per second throughout testing for optical strain and fiber-alignment analysis.

When the circularly polarized light passes through the tissue, the light becomes linearly polarized to some degree in the direction of the collagen fibers in the tissue. This system uses a custom-made division-of-focal-plane polarization imaging camera that can acquire polarization data at high resolution, in real time, to determine the amount (degree of linear polarization [DoLP]) and direction (angle of polarization [AoP]) of polarization after the light passes through the tissue sample32,34. The DoLP value corresponds to how much of the light has been polarized by passing through the tissue, and it represents the distribution of collagen fibers (relative degree of isotropy and anisotropy) within each pixel. The AoP value is the average direction of the linear polarization of the light after the light passes through the tissue, and it represents the average direction of collagen alignment contained within each pixel (averaged through the thickness of the sample). Therefore, each pixel has a direction (AoP) and strength (DoLP) of collagen alignment. For quantitative analysis (Fig. 2), the DoLP and AoP values can be extracted from within a region of interest, defined in this study as the tissue bordered by the 4 brass beads attached to each sample, and they are compared across different groups by calculating the standard deviation of the AoP (representing the degree of variation in orientation angle in each region of interest) and the mean DoLP (representing the mean strength of collagen alignment in each region of interest)28,29,34,35.

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Data and Statistical Analysis

A custom MATLAB program was used to optically track the surface beads and calculate 2-dimensional (2D) Lagrangian strain with use of tensor algebra. Stress was calculated as force divided by the mean initial cross-sectional area of each sample. With use of the least-squares method, a bilinear curve fit was applied to the stress-strain data in order to quantify the elastic modulus in the toe and linear regions as well as the stress and strain values corresponding to the transition point of the bilinear curve fit.

Images corresponding to distinct time points during the stress-relaxation test and quasi-static ramp-to-failure test were selected for analysis. For each image, the mean DoLP and standard deviation of the AoP were calculated in the region of interest defined by the 4 beads. For the quasi-static ramp-to-failure test, these values were then interpolated to calculate alignment parameters corresponding to specific points on the corresponding stress-strain curve, namely zero strain (immediately prior to initiation of the ramp-to-failure test), transition strain (the intersection point of the bilinear curve fit of the stress-strain data), and linear strain (defined as 2 times the transition strain within the linear portion of the stress-strain curve).

With use of Shapiro-Wilk normality tests, the data were determined to be non-normally distributed; therefore, nonparametric statistical analyses were used and the data are presented as the median and interquartile range in each data figure. A linear mixed model was used to identify significant differences between anterolateral and posteromedial bundles with use of JMP software (SAS Institute). This statistical approach accounted for dependence of multiple test samples (6 subsections) taken from each ligament and multiple PCLs (left and right) taken from a given donor. To evaluate variation of properties across the regions of each bundle, linear regression parameters were estimated after appropriately adjusting for the dependencies in the samples (as in the inter-bundle analysis), thus appropriately defining the degrees of freedom for statistical tests. Linear mixed models were fit with use of standard restricted maximum likelihood (REML) estimation procedures, and significance was set at p < 0.05.

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Results

The anterolateral and posteromedial bundles of the PCL demonstrated similar mechanical and microstructural properties. Elastic moduli calculated during the quasi-static ramp-to-failure test for both toe and linear regions were not significantly different between bundles (Fig. 3-A). In the stress-relaxation test, peak and equilibrium stresses were similar for the anterolateral and posteromedial bundles (Fig. 3-B); however, both percent relaxation and rate of relaxation were found to be significantly different, with more relaxation in the posteromedial than in the anterolateral bundle (p = 0.004; Table II). Based on the time-dependent normalized stress, the inter-bundle difference was significant from the first time point calculated after the ramp through the end of testing (the 5% strain step) (p < 0.05; Fig. 3-C).

During the quasi-static ramp-to-failure test, the mean DoLP increased and the standard deviation of the AoP decreased with increasing strain in both bundles, demonstrating reorganization of collagen fibers under tensile loading. In addition, larger changes occurred from “zero” to “transition” than from “transition” to “linear” in both bundles, indicating that most collagen realignment occurred during the toe-region portion of the stress-strain curve. However, no significant inter-bundle microstructural differences were observed (Fig. 4). Nonetheless, similar to findings with the mechanical properties, significant inter-bundle differences in microstructural properties were observed during the stress-relaxation test (p < 0.05). While the mean DoLP was not different between bundles at peak or equilibrium (Fig. 5-A and Table II), the standard deviation of the AoP was significantly different at both peak (p = 0.018) and equilibrium (p = 0.018), and the percent change of the AoP standard deviation over the hold period also showed significant inter-bundle differences (p = 0.009; Fig. 5-B and Table II).

Although overall properties of the bundles were quite similar, several notable differences were found in intra-bundle comparisons in both mechanical and microstructural properties. Intra-bundle comparisons of mechanical properties of regional samples showed several significant linear relationships across posteromedial regions: linear modulus in the quasi-static ramp-to-failure test (p = 0.042) as well as both peak stress (p = 0.043) and equilibrium stress (p = 0.037) in the stress-relaxation test (Fig. 6 and Table II). All values decreased moving posteriorly. However, no significant intra-bundle relationships were found across anterolateral regions.

Similarly, intra-bundle comparisons of microstructural properties showed significant linear relationships across posteromedial regions (p < 0.05) but not across anterolateral regions (Fig. 7 and Table II). All measured parameters, except percent change of the mean DoLP during the stress-relaxation test, were found to have significant linear regressions across posteromedial regions (p < 0.05 for all and p < 0.001 for most; Table II), with the mean DoLP decreasing and the AoP standard deviation increasing moving posteriorly, a finding consistent with the trend seen in the mechanical properties. Notably, while no regressions reached significance across anterolateral regions, several regressions in both the mean DoLP and the AoP standard deviation trended (p < 0.20) in the same direction as the significant regressions found across posteromedial regions (Table II).

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Discussion

The anterolateral and posteromedial bundles of the PCL have very similar microstructural and mechanical properties under tensile loading. These findings are in contrast to previous studies of the ACL24,28,29,36, including our own28,29, which found significant regional and bundle variation in the properties of that ligament. The regional variation of these properties in the PCL appears to be much more subtle. Our findings suggest that the distinct functions of the bundles arise more from differences in size and mechanical dynamics due to geometry than from differences in underlying material and microstructural properties.

Values in the literature for mechanical properties of the PCL, based on cadaveric studies with different testing and harvesting techniques, vary greatly24-27; this variation makes drawing conclusions about the differences between bundle properties based on tissue-level values alone challenging. An advantage of the present study compared with prior work is that we were able to evaluate the behavior of the collagen microstructure of the ligaments in real time, simultaneously with mechanical testing. Previous studies were unable to simultaneously examine these variables27,30,37. The current study provides a more complete picture of ligament behavior and shows only small inter-bundle differences under dynamic loading. Additionally, the mean patient age of samples in this study was much lower than in previous studies, an important distinction since studies have demonstrated that cell proliferation, metabolism, and collagen orientation all decrease with aging38-40.

Since the anterolateral bundle was traditionally considered the dominant PCL bundle17,27,41,42, single-bundle techniques for reconstruction historically attempted to recreate this bundle alone. The findings from our study suggest that any so-called dominance of the anterolateral bundle results from greater mass and geometric orientation and location rather than any significant mechanical or microstructural differences between the 2 bundles, in contrast to conclusions of prior studies17,27. Moreover, our findings are consistent with recent studies suggesting co-dominance of the PCL bundles7,43. These findings may help to explain why smaller case studies have shown that there are similar clinical outcomes between single and double-bundle constructs for PCL reconstruction44-46 despite biomechanical differences between these constructs47-52.

The implications for operative treatment of PCL injury are not entirely clear. With only small differences in mechanical and microstructural properties between the bundles, the benefit of the double-bundle technique, if any, likely arises from the use of more tissue and from more closely reapproximating the native ligament geometry, potentially providing more natural kinematics47-50,53. In this study, the only parameters that were significantly different between bundles were related to stress-relaxation, namely less relaxation and less dispersed collagen alignment for the anterolateral bundle compared with the posteromedial bundle (Figs. 3 and 5). These results agree with those of our previous studies of ACL bundles and collagen gel tissue analogs, which showed faster relaxation and greater overall total relaxation for less aligned samples29,54. Thus, the PCL bundles exhibit some differences in time-dependent viscoelastic behavior, with a slightly more viscous response for the posteromedial bundle. While it is possible that these differences could have some relevance to injury risk, the clinical implications are not directly obvious because in vivo viscoelasticity will depend on other factors not evaluated in this study, such as physiological water content, anatomical orientation, and degree of prestress in the bundles. In addition, relatively small differences in viscoelastic behavior may not be as clinically important as other parameters measured in this study, such as elastic moduli and stresses.

Similar to the findings of previous studies of the ACL and PCL29,30, in our study we found that the collagen microstructure within each bundle was not entirely homogenous. Our data show that, at least within the posteromedial bundle, there is a gradient from anterior to posterior in both microstructural and mechanical properties, with collagen in the anterior portion of the bundle more highly aligned and more resistant to tensile forces and with both properties decreasing moving posteriorly. These findings correspond with those of a previous report of increased collagen density in the anterior portions of knee ligaments in general and the ACL bundles in particular30. The current study, however, was powered to detect differences between the bundles rather than between regions; therefore, these trends were not fully elucidated, especially in regard to the anterolateral bundle. Further studies would be required in order to fully evaluate intra-bundle variation and whether a linear gradient in the properties of a reconstructed posteromedial bundle could enhance clinical outcomes.

There are a number of limitations to the current study. One important limitation results from anatomical variation. While our study averaged the bundle properties across all of the different anatomical variants, it is possible that material properties may be affected by the variations, especially in light of findings suggesting that the meniscofemoral ligaments, when present, may support the role of the PCL in restraining the knee55. Our sample size was not large enough to adequately compare the differences between anatomical variants, and further studies would be needed to fully characterize them. However, we believe this limitation to be of questionable clinical importance, as identifying which anatomic variant a given patient had prior to a PCL injury would likely be impossible unless the patient had had imaging prior to the injury. Also, while dissection was performed systematically to minimize differences between specimens, the anatomical variants invariably resulted in some inter-specimen differences between the sections of the posteromedial bundle, and these were subsequently identified as regions 4, 5, and 6. Finally, in order to prepare samples for testing, multiple freeze-thaw cycles were required. There is the theoretical possibility that freezing may alter the tissue, but previous research has suggested that limited freeze-thaw cycles do not cause meaningful changes in ligamentous tissue properties56.

Despite these limitations, to our knowledge, this is the first study to report both the microstructural and mechanical properties of the PCL. This ligament has relatively homogenous properties, with only small differences in stress-relaxation behavior between the anterolateral and posteromedial bundles and only subtle regional variation across each bundle. This information may help to guide graft choice and operative techniques for PCL reconstruction. Further research is warranted to assess which techniques and grafts most closely recreate the microstructure of the native PCL as well as to determine the impact of anatomical variation of the ligament, if any, on these findings.

NOTE: Samples were collected through the Mid-America Transplant Services Center (St. Louis, Missouri).

Investigation performed at Washington University in St. Louis, St. Louis, Missouri

Disclosure: The authors indicated that no funding was received in support of this study. The Disclosure of Potential Conflicts of Interest forms are provided with the online version of the article.

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