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Regional Distribution of Articular Cartilage Thickness in the Elbow Joint

A 3-Dimensional Study in Elderly Humans

Miyamura, Satoshi MD, PhD1; Sakai, Takashi MD, PhD2; Oka, Kunihiro MD, PhD1; Abe, Shingo MD, PhD3; Shigi, Atsuo MD4; Tanaka, Hiroyuki MD, PhD1; Shimada, Shoichi MD, PhD1; Mae, Tatsuo MD, PhD1; Sugamoto, Kazuomi MD, PhD1; Yoshikawa, Hideki MD, PhD1; Murase, Tsuyoshi MD, PhD1

doi: 10.2106/JBJS.OA.19.00011
Scientific Articles
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Background: During elbow procedures, reconstruction of the joint (including the articular cartilage) is important in order to restore elbow function; however, the regional distribution of elbow cartilage is not completely understood. The purpose of the present study was to investigate the 3-dimensional (3-D) distribution patterns of cartilage thickness of elbow bones (including the distal part of the humerus, proximal part of the ulna, and radial head) in order to elucidate the morphological relationship among them.

Methods: Two 3-D surface models were created with use of a laser scanner: (1) a cartilage-bone model based on 20 elderly cadaveric elbows exhibiting normal cartilaginous conditions and (2) a bone model that was created after dissolving the cartilage. The 2 models were superimposed, and cartilage thickness was measured as the interval distance on the articular surface. Measurements were made at categorized anatomical points of the individual bones, and 3-D distributions on the entire articular surface were analyzed. The spatial relationship among individual bones was also assessed.

Results: In the distal part of the humerus, the cartilage was thickest in the intermediate region between the capitellum and the trochlea (mean [and standard deviation], 1.27 ± 0.17 mm); in the proximal part of the ulna, it was thickest at the anterolateral edge of the coronoid (2.20 ± 0.39 mm) and the anteroproximal edge of the proximal sigmoid notch (2.49 ± 0.55 mm); and in the radial head, it was thickest at the articular zone on the rim circumference within the dish (1.10 ± 0.17 mm) and on the proximal circumference around the side (1.02 ± 0.17 mm) (p < 0.001 for all). These thicker cartilage regions gathered on the joint center, facing each other.

Conclusions: The present study demonstrated regional variations in elbow cartilage thickness. The combined findings in individual bones showed “cartilage gathering” at the center of the elbow joint, which we believe to be a novel anatomical finding.

Clinical Relevance: An enhanced understanding of elbow cartilage geometry will provide additional insights into elbow procedures in elderly individuals, such as hemiarthroplasties, in which anatomical contours could help to restore normal joint function and improve postoperative outcomes.

1Departments of Orthopaedic Surgery (S.M., K.O., H.T., T. Mae, H.Y., and T. Murase), Neuroscience and Cell Biology (S.S.), and Orthopaedic Biomaterial Science (K.S.), Osaka University Graduate School of Medicine, Suita, Japan

2Department of Orthopaedic Surgery, Yamaguchi University Graduate School of Medicine, Ube, Japan

3Department of Orthopaedic Surgery, Toyonaka Municipal Hospital, Toyonaka, Japan

4Department of Orthopaedic Surgery, Yukioka Hospital, Osaka, Japan

E-mail address for T. Murase: tmurase-osk@umin.ac.jp

Investigation performed at Osaka University Graduate School of Medicine, Suita, Japan

Disclosure: This study was supported by the Japan Agency for Medical Research and Development (project ID 15570777) and the Japan Society for the Promotion of Science KAKENHI (grant number JP 15K10442). The Disclosure of Potential Conflicts of Interest forms are provided with the online version of the article (http://links.lww.com/JBJSOA/A108).

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Joint anatomy reconstruction is closely associated with the functional outcomes of elbow procedures1-6. While reestablishing radiographically visible bone dimensions has been emphasized5,7-12, the contribution of articular cartilage is not well known. The functions of the articular cartilage that covers joint surfaces include absorbing mechanical shock and transmitting the load to the underlying subchondral bone13-15; therefore, reconstructing the cartilaginous articulation to restore elbow kinematics is important. Thus, knowledge of the native cartilage morphology of the elbow joint is useful, and quantification of cartilage thickness is of clinical interest.

However, despite its anatomical and clinical importance, few studies have focused on the cartilage distribution of the elbow because of an inability to accurately detect cartilage regions during image analysis in addition to the complexity of cartilage morphology. Most studies have been based on 2-dimensional imaging, including magnetic resonance imaging, and have not extended to the entire articular surface16-20. Furthermore, the regional cartilage dimensions in individual elbow bones have been investigated separately, and, to our knowledge, no study has systematically analyzed the spatial cartilage distribution pattern in a group of individual bones throughout the elbow joint. Consequently, the 3-dimensional (3-D) distribution of elbow cartilage remains unclear and there has been no direct assessment of its morphological relationship among individual bones.

We focused on the anatomical aspects of the elbow joint and hypothesized that there would be regional variations in cartilage thickness in the elbow joint. We constructed 3-D cartilage models from cadaveric elbows of elderly donors to investigate the cartilage distribution patterns of individual elbow bones (including the distal part of the humerus, proximal part of the ulna, and radial head) in order to elucidate the morphological relationships among them. Our findings may be beneficial for joint anatomy reconstruction to restore elbow function in elderly individuals.

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Materials and Methods

This cadaveric study was conducted in accordance with the tenets of the Declaration of Helsinki and received approval from the institutional review board. All specimens were obtained from those who had agreed to be donors. Following in situ computed tomography scanning, 29 elbows from 15 formalin-embalmed cadavers were dissected to expose the articular cartilage surface of the distal part of the humerus, proximal part of the ulna, and radial head. One elbow that had malunited after a fracture and 8 degenerative elbows (defined as those with osteophytes and damage to the articular cartilage surface) were excluded on the basis of visual and radiographic inspection. The remaining 20 elbows (obtained from 6 male and 6 female donors who had had a mean age of 86.2 years [range, 74 to 95 years] at time of death) were included. Four steel spheres were firmly glued to the cortical surface at the distal or proximal third of each bone to serve as landmarks for integrating each digitized data set and surface registration21-24.

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Cartilage-Bone Model

Specimens were scanned with use of a 3-D optical laser scanner (Rexcan CS+ 5.0 Mega pixels; Medit) with an accuracy of ±20 μm to obtain elbow joint dimensions. Scans were processed with use of ezScan7 software (Medit), and 3-D cartilage-bone models were created (Fig. 1-A).

Fig. 1

Fig. 1

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Bone Model

To obtain baseline data for measurements of cartilage, the cartilage dissolution technique was used to create bone models without cartilage25-32. The joint surfaces of the specimens were soaked in 6.0% sodium hypochlorite for 12 to 24 hours to dissolve the articular cartilage29. We visually inspected and checked the cartilage by touching the surface with a surgical probe to ensure that the cartilage was completely dissolved31. Then, cartilage-free bones were rescanned with use of the same procedure, and 3-D bone models were created without cartilage (Fig. 1-B).

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Cartilage Model

Surface model data sets that were obtained with a 3-D laser scanner were analyzed with use of Geomagic Control software (3D Systems) in STL file format. Bone models were superimposed onto the cartilage-bone models to create a 3-D cartilage model with reference to the steel ball registration using the iterative closest point algorithm33, encoding the thickness information on the cartilage-bone model as a thickness map (Figs. 1-C and 1-D).

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Points of Interest

STL data from the cartilage-bone model were imported into Bone Simulator software (Orthree) to define points of interest. On the articular surfaces of individual bones, points at the intersections of planes were set as points of interest based on anatomical landmarks and were saved in STL file format. All definitions and measurements were performed on the right elbow by mirroring the left side, assuming that the elbow joints on both sides are similar in anatomical configuration16-18,34 (Fig. 2; Appendix 1).

Fig. 2

Fig. 2

In the distal part of the humerus, intersection points were categorized as capitellum, intermediate region, and trochlea in the coronal plane. Each category was subdivided further into anterior, inferior, and posterior zones in the sagittal plane (Fig. 2-A).

The proximal part of the ulna was divided into trochlear and proximal sigmoid notches, and points of interest were set for each. Points of the trochlear notch were categorized as coronoid and olecranon in the sagittal plane (Fig. 2-B). On the articular surface of the proximal sigmoid notch, proximal-distal and posterior-anterior rows were categorized as PD1-PD4 and PA1-PA4, respectively (Fig. 2-C).

In the radial head, points of interest were defined as previously described by Yeung et al.35, with some modifications. The articular surface of the radial head was divided into the articular facet, consisting of the radiocapitellar joint (dish), and the peripheral part, consisting of the proximal radioulnar joint (side). The deepest point of the concavity on the dish articular surface was identified and points on the surface of the dish were categorized according to their position relative to the rim of the dish (25% circumference, 50% circumference, 75% circumference, and rim circumference). The safe zone corresponded to the area that did not articulate with the proximal sigmoid notch10,36,37, and the rest of the area was defined as the articular zone. Around the side of the radial head, points along the circumference were categorized according to their position relative to the surface of the dish (level 1, 2, 3, 4, and 5) (Fig. 2-D).

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Evaluation of Cartilage Thickness

STL data for points of interest were imported into Geomagic Control software, and cartilage thickness values were measured at each point of interest on the cartilage surface by determining the spatial minimum distance between the cartilage-bone and bone models. A grouped cartilage thickness value was calculated by averaging the values of all points of interest in a categorized region. Measurement in the computed method was validated with use of 6 samples by comparing with the stereomicroscopic findings at 4 anatomical landmarks (Fig. 3). The mean error of measurement (and standard deviation) between computational and microscopic measurements was 0.024 ± 0.017 mm (mean percentage change, 1.80% ± 1.65%) (Appendix 2).

Fig. 3

Fig. 3

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Statistical Analysis

SPSS (version 23.0; IBM) was used to perform the statistical analyses. The level of significance was set at p < 0.05. The Shapiro-Wilk parametric test was used to test normality of variables.

Cartilage thickness was compared to detect differences among groups and subgroups in the distal part of the humerus and radial head. The unpaired t test or Mann-Whitney U test, with Bonferroni adjustments for multiple comparisons, was used as appropriate. With use of these tests, the average values were compared between the safe zone and the articular zone for each radial head circumference.

In the proximal part of the ulna, we assessed lateral-medial and anterior-posterior (proximal-distal) variation in cartilage thickness in the trochlear notch as well as anterior-posterior and proximal-distal variation in cartilage thickness in the proximal sigmoid notch. Partial Pearson correlation coefficients (r) were determined between cartilage thickness values at each point of interest and the following paired variables (planes) while controlling for other pairs: lateral-medial (planes 6 to 11) and posterior-anterior (C1-C5) in the coronoid, lateral-medial (planes 6 to 10) and distal-proximal (O1-O5) in the olecranon, and posterior-anterior (PA1-PA4) and proximal-distal (PD1-PD4) in the proximal sigmoid notch.

A priori power analyses (α = 0.05, β = 0.1, 2-tailed) were conducted to detect a thickness difference of 0.20 ± 0.15 mm in the distal part of the humerus18,19,38 and radial head17,35,38 and to achieve r > 0.5 in the proximal part of the ulna. A minimum sample size of 13 specimens and 34 separate points of interest was calculated to identify meaningful differences.

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Results

Three-D Cartilage Morphology in Individual Elbow Bones

The cartilage distribution patterns were represented as 3-D thickness maps from a typical subject (Fig. 4). The measurements are detailed in the tables shown in Appendix 3.

Fig. 4

Fig. 4

In the distal part of the humerus, the mean cartilage thickness in the intermediate region (1.27 ± 0.17 mm) was significantly greater than that in the capitellum (1.08 ± 0.14 mm; p < 0.001) and trochlea (0.96 ± 0.16 mm; p < 0.001). Following subdivision, the mean cartilage thickness was significantly greater in the inferior zone than in the anterior and posterior zones in both the capitellum (anterior zone, 1.02 ± 0.14 mm; inferior zone, 1.22 ± 0.18 mm; posterior zone, 0.65 ± 0.25 mm) (anterior zone versus inferior zone, p < 0.001; inferior zone versus posterior zone, p < 0.001) and trochlea (anterior zone, 0.91 ± 0.15 mm; inferior zone, 1.12 ± 0.20 mm; posterior zone, 0.82 ± 0.16 mm) (anterior zone versus inferior zone, p = 0.006; inferior zone versus posterior zone, p < 0.01). In the intermediate region, cartilage in the anterior zone and inferior zone showed similar values and was significantly thicker than that in the posterior zone (anterior zone, 1.34 ± 0.16 mm; inferior zone, 1.40 ± 0.24 mm; posterior zone, 1.06 ± 0.18 mm) (anterior zone versus posterior zone, p < 0.001; inferior zone versus posterior zone, p < 0.001) (Fig. 5).

Fig. 5

Fig. 5

In the proximal part of the ulna, the mean thickness values in the coronoid, olecranon, and proximal sigmoid notch were 1.04 ± 0.51, 0.78 ± 0.30, and 0.92 ± 0.67 mm, respectively. The trochlear notch had a small area with thinner cartilage, known as the “bare area” (0.27 ± 0.14 mm). In the coronoid of the trochlear notch, cartilage thickness increased as it moved laterally (r = −0.45; p < 0.001) and anteriorly (r = 0.39; p < 0.001), with a peak at the anterolateral edge (2.20 ± 0.39 mm). Conversely, cartilage was evenly distributed on the articular surface in the olecranon (Fig. 6-A). In the proximal sigmoid notch, cartilage thickness increased as it moved anteriorly (r = 0.64; p < 0.001) and proximally (r = −0.73; p < 0.001), with a peak at the anteroproximal edge (2.49 ± 0.55 mm) (Fig. 6-B).

Fig. 6

Fig. 6

Within the dish of the radial head, the cartilage thickness of the rim circumference (1.10 ± 0.17 mm) was significantly greater than that at all of the inner circumferences (deepest, 0.73 ± 0.15 mm; 25%, 0.73 ± 0.16 mm; 50%, 0.77 ± 0.14 mm; 75%, 0.86 ± 0.14 mm) (p < 0.001 for all) (Fig. 7-A). The cartilage thickness values in the articular zone were higher than those in the safe zone at the 75% circumference (p < 0.01) and tended to be higher at the rim circumference (Fig. 8-A). Around the side of the radial head, the cartilage thickness values consecutively decreased and were significantly different from level 1 to level 5 (level 1, 1.02 ± 0.17 mm; level 2, 0.71 ± 0.15 mm; level 3, 0.52 ± 0.11 mm; level 4, 0.42 ± 0.09 mm; level 5, 0.28 ± 0.07 mm) (p < 0.001 for all) (Fig. 7-B). The articular zone cartilage was significantly thicker than the safe zone cartilage at all levels (p < 0.001 for all) (Fig. 8-B).

Fig. 7

Fig. 7

Fig. 8

Fig. 8

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Morphology of the Cartilage Distribution Pattern throughout the Elbow Joint

The thicker cartilage regions in individual bones gathered at the center of the elbow joint, facing each other. The thicker areas in the distal part of the humerus (intermediate region) were faced with the counterpart in the ulnar trochlear notch (anterolateral edge of the coronoid), where the ulnotrochlear joint articulates, and were also faced with the articular zone on the rim circumference within the dish of the radial head, where the radiocapitellar joint articulates. The thicker cartilage areas in the anteroproximal edge of the proximal sigmoid notch and in the articular zone on proximal circumferences around the side of the radial head faced each other at the point where the proximal radioulnar joint articulates (Figs. 9 and 10).

Fig. 9

Fig. 9

Fig. 10

Fig. 10

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Discussion

Using a laser scanner, we created cartilage models from cadaveric elbows and quantified the distribution of cartilage thickness throughout the elbow. We found that thicker cartilage areas in individual elbow bones gathered at the joint center, facing each other. The combined findings revealed that the thicker cartilage regions were associated with articulation of the 3 joints of the elbow (Fig. 10).

First, regarding the radiocapitellar joint, our findings showed that the cartilage thickness on the rim circumference within the dish of the radial head was significantly greater than that on all of the inner circumferences, similar to the results reported by Yeung et al.35. The articular zone cartilage was thicker than the safe zone cartilage in the outer circumferences and, facing this area, the cartilage in the intermediate region of the distal part of the humerus was thicker as well. These findings indicated that thicker cartilage along the rim may help to increase radiocapitellar stability secondary to concavity compression onto the concave articular dish1,35,39-41. Second, thicker cartilage in the ulnotrochlear joint was distributed from the anterolateral edge of the coronoid to the anteroproximal edge of the proximal sigmoid notch and faced the intermediate region of the distal part of the humerus. This asymmetrically distributed pattern was in line with the knowledge that the ulnotrochlear joint is an asymmetrical trochoid joint having an obliquity to the axis of rotation42. Third, in the proximal radioulnar joint, there was a thicker cartilage area in the anteroproximal edge of the proximal sigmoid notch, which was faced by the articular zone cartilage on the proximal circumferences around the side.

Taken together, our findings indicated that the thicker cartilage regions in individual bones gathered at the joint center. We believe that this spatial “cartilage gathering” is a novel anatomical finding, which led us to speculate that the cartilage might thicken in the area where individual bones gather, as if to fill the joint gap to fit the complex structures and stabilize the joint43,44. In terms of flexion-extension motion, articulation reportedly contributes more to elbow stability in the flexed position42. Our results showed that cartilage thickens in the anterior zone of the distal part of the humerus and in the coronoid of the trochlear notch, where the closest relationship of the cartilage surfaces during elbow flexion provides a certain degree of joint stability45-48. These trends should be constant in this age range as long as normal cartilaginous conditions exist.

Our findings are clinically relevant to anatomical implant and prosthesis designs. Considering the spatial variability of cartilage in implant design can replicate normal human articular surface anatomy, thus restoring joint kinematics, maximizing contact area with the native articular surfaces, and potentially leading to improved postoperative outcomes35,49. Several studies have experimentally revealed that subtle change in prosthetic configuration affects joint biomechanics1,39-41; thus, small differences in cartilage thickness would be clinically meaningful. This concept is applicable to radial head replacement, distal humeral hemiarthroplasty, and capitellar arthroplasty in several clinical scenarios, including severe fractures, isolated degeneration at the radiocapitellar joint, and osteonecrosis5. Next, anatomical knowledge of cartilage thickness is useful for treating fractures. Regarding the development of arthritis, joints are believed not to tolerate step-offs of more than the cartilage thickness50-53; therefore, fractures occurring in thinner cartilage regions may be more susceptible to posttraumatic arthritis, potentially lowering the threshold for surgical treatment compared to fractures in regions with thicker cartilage.

Furthermore, an understanding of the spatial cartilage anatomy may help to elucidate elbow osteoarthritis. Unpredictable incongruity resulting from articular roughness with joint instability is assumed to contribute to osteoarthritic progression54; nevertheless, there is a paucity of literature that supports these theories. Our results not only provide important information to predict the articular roughness such as posttraumatic step-offs and surface irregularities associated with degenerative conditions but also provide a possible explanation regarding joint instability42,45-48.

The present study had some limitations. First, we used formalin-embalmed cadavers. Formalin fixation can lead to dehydration of the cartilage; however, several researchers have reported that formalin fixation has no measurable effects on cartilage thickness or on geometric configuration within a joint21,23,25,31,55,56. Furthermore, our measurements corresponded with those in previous in vivo cartilage studies16-19. Second, a true difference may have been overlooked due to the relatively small sample size and the study design assuming a large effect size. Also, the subjects were sampled without considering potential differences in age and sex.

In conclusion, we identified regional variations in cartilage thickness of the distal part of the humerus, proximal part of the ulna, and radial head in the elderly. Additionally, we found that thicker cartilage of individual bones gathered at the elbow joint center (“cartilage gathering”), which we believe to be a novel anatomical finding. Our findings provide additional insight that is invaluable for elbow surgery to restore normal function.

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Appendix

Supporting material provided by the authors is posted with the online version of this article as a data supplement at jbjs.org (http://links.lww.com/JBJSOA/A109).

Note: The authors would like to thank Ryoji Nakao and Taro Adachi for their skillful technical support and excellent contributions to this study. They would also like to acknowledge Yasunobu Nakamura for his statistical support.

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