Three-Dimensional Analysis of Bone Morphology of the Rheumatoid Arthritis Elbow

Abstract

Introduction:

Accurate treatment of elbow rheumatoid arthritis (RA) requires understanding the joint destruction pattern. However, comprehensive bone-deformation patterns remain unclear. Thus, we aimed to quantitatively evaluate three-dimensional (3D) deformity in RA elbows compared with normal elbows.

Methods:

The authors created 3D CT models of the distal humerus, proximal ulna, and radial head for 26 elbows with RA (Larsen classification IV) and 26 normal elbows. These models were superimposed onto one reference bone, selected from normal elbows. The intermodel distance was measured at categorized anatomical regions of the individual bones, and the measurements were compared between the RA and normal elbows. Correlation between clinical outcomes, including range of motion and 3D deformities, were also assessed in the RA group.

Results:

RA elbows exhibited notable bone destruction in both the anterior-inferior region of the distal humerus (7.9 to 9.9 mm vs. 9.5 to 12.6 mm) and the trochlear notch (16.7 to 20.1 mm vs. 11.3 to 15.4 mm) compared with normal elbows, with all differences being statistically significant (P < 0.05). The radial head in RA elbow was shortened (2.24 ± 1.97 mm vs. −0.18 ± 0.59 mm; P < 0.05), with osteophyte formation, particularly on the lateral side (P < 0.05). Humeroulnar joint deformity correlated with flexion-extension limitation (R = 0.42 to 0.74), and the radial head correlated with forearm supination limitation (R = 0.57 to 0.58).

Conclusion:

Bone destruction was shown in the anterior-inferior region of the distal humerus and trochlear notch, and the radial head was shortened with osteophyte formation, resulting in a proximal shift of the forearm bones and impaired motion. This provides valuable insights into RA elbow pathology and contributes to advancements in treatment.

Elbow joints are often implicated in the onset of rheumatoid arthritis (RA). Elbow destruction in patients with RA can lead to notable functional disabilities of the upper extremity.¹ Understanding the pattern of joint destruction is important for the accurate diagnosis and treatment of elbow RA. Although three-dimensional (3D) deformity patterns in the wrist, foot, and craniovertebral joints of individuals with RA are extensively documented, there is a paucity of studies examining deformities in the elbow.^2-4 Previous studies have mostly analyzed the deformity pattern of the RA elbow joint surface in two dimensions (2D)^5-10; however, to our knowledge, none have reported its 3D analysis. Previous 2D evaluations have shown that bone resorption of each bone occurs and that the forearm bone burrows into the humerus, but it is unclear what individual bone changes have resulted in these changes. It is difficult to identify detailed bone resorption positions in 2D assessments due to bone overlap and differences in radiographic conditions. By contrast, 3D evaluation made it possible to accurately identify the position of bone resorption.

Nevertheless, the distribution of bone-deformation patterns remains unclear, and the morphological relationships between individual bones have not been directly assessed. The elucidation of the 3D deformity of the elbow in RA will contribute to understanding the pathophysiology of the RA elbow and is important for therapeutic intervention, including specific surgical techniques.¹¹ We hypothesized that elbows with RA would exhibit a typical 3D pattern of joint destruction and herein quantitatively evaluated the 3D deformity in RA elbows compared with that in normal elbows.

Methods

Study Setting

This case-control study compared RA and normal elbows. This study was conducted in compliance with the ethical standards of the Declaration of Helsinki of 1975, as revised in 2000. It was approved by the relevant institutional review board (Protocol Number: 19247-2), and the requirement for written informed patient consent was waived.

Patients

We identified 38 consecutive patients with RA and 39 healthy elbows from individuals who underwent CT before surgery between December 2019 and March 2022. Elbows classified as Larsen grade IV were included. The exclusion criterion was a history of fracture or surgery. Consequently, 26 elbows were included in this study. Data were extracted from medical charts, encompassing physical findings, including elbow (flexion and extension) and forearm (pronation and supination) ranges of motion; elbow pain (categorized as none, mild, moderate, or severe); and elbow stability (classified as stable, moderately unstable, or markedly unstable). We also collected data on the disabilities of the arm, shoulder, and hand score and the Mayo Elbow Performance Score (MEPS).

In addition, we obtained the CT images of 26 normal elbows that were scanned as contralateral controls for surgery from our database. The patients were eligible if they had a healthy elbow imaged for the treatment of fractures or malunited fractures, not RA, and if they had no history of elbow disorders or radiographic evidence of degeneration.

Three-Dimensional CT Model Reconstruction

Using a helical CT scanner (Revolution CT; GE Healthcare), the elbows were scanned while fully extended and the forearms maintained in a neutral position. The CT data were sent to a workstation in the digital imaging and communication in medicine format for analysis. The 3D surface models of the humerus, ulna, and radius were created using a semiautomatic segmentation technique with commercial image processing software (BoneViewer/MvIndex/OV, Teijin Nakashima Medical).

Selection of Reference Bone Model

We selected one reference elbow from among 26 normal elbows by fitting all other bone models, except the reference bone model,¹² to the reference bone. The reference bone was used for analyses because the contralateral side of each RA case could not be used for healthy comparison. Reference bone models were selected for the humerus, ulna, and radius to optimize the overall bone morphology. Specifically, an arbitrarily selected normal model was superimposed onto the remaining 25 normal models by matching the rotation, translation, and scale. Scaling was modified based on the lengths of the medial and lateral epicondyles for the humerus, as well as the bone axis widths for the ulna and radius, serving as indices. The reference bone was chosen based on the smallest dissimilarity, determined by calculating the average symmetric surface distance (ASD) across the 26 normal models.¹³ The ASD is the average of all distances from the polygons to the boundary of the 3D model and vice versa. The images and models were processed using commercial image processing software (BoneViewer/OV) (Figure 1).

Fig. 1.

Illustration showing reference bone selection from normal elbow and reference fitting of other bones.

Points of Interest

The Cartesian coordinate systems of the humerus (X^H, Y^H, and Z^H-axes), ulna (X^U, Y^U, and Z^U-axes), and radius (X^R, Y^R, and Z^R-axes) were determined for the reference bones (Figure 2, see Supplemental Digital Content 1, http://links.lww.com/JG9/A445).¹⁴

Fig. 2.

Illustration showing axis settings. (A) Distal humerus, (B) proximal ulna, and (C) radial head.

In the distal humerus, the sagittal planes were defined as the planes passing through the anatomical points of the (1) capitellum center, (2) lateral trochlear ridge, (3) trochlear groove, and (4) center of the medial trochlea. Seven planes (0°, 30°, 60°, 90°, 120°, 150°, and 180°), including the Y^H-axis, were determined with the X^HY^H plane at 0°/180° and the Y^HZ^H plane at 90°. Subsequently, the points of interest were determined at the intersection of the six planes, with the sagittal planes on the surface of the 3D model, and were categorized into anterior (0° and 30° planes), inferior (60°, 90°, and 120° planes), and posterior (150° and 180° planes) regions (Figure 3, A).¹⁵

Fig. 3.

Illustration showing planes to be evaluated for joint surfaces. A, Distal humerus, (B) proximal ulna, and (C) radial head.

In the proximal ulna, the sagittal plane was defined as the plane passing the anatomical points of the (1) lateral verge of the trochlear notch, (2) ridge of the trochlear notch, and (3) center of the medial trochlear notch. Seven planes are established at 0°, 30°, 60°, 90°, 120°, 150°, and 180°, including the Y^U-axis. The Y^UZ^U plane corresponds to 0°/180°, whereas the X^UY^U plane is positioned at 90°. Subsequently, the points of interest were determined at the intersection of the six planes, with the sagittal planes on the surface of the 3D model, and were categorized into anterior (0° and 30° planes), inferior (60°, 90°, and 120° planes), and posterior (150° and 180° planes) regions (Figure 3, B).¹⁵

For the radial head, the planes were set at 30° from the 0° to the 330° plane around the Y^R-axis. The 0° direction is the direction of the radial styloid process. Within the radial head dish, the most proximal of the vertical Y^R-axis planes is designated as the proximal plane; the most distal plane, as the distal plane; and the middle section, as the middle plane. The intersection of the distal plane with the plane around the Y^R-axis was used as the evaluation point (Figure 3, C).

Evaluation

Images of the healthy elbows and 26 RA elbows were scaled and fitted to the reference bones of the humerus, ulna, and radius using a surface-based registration method with an iterative nearest-neighbor algorithm. The deformities of individual bones were evaluated by measuring the distance from the y-axis to each evaluation point on the sagittal plane for the humerus and ulna and the axial plane for the radius in 26 normal elbows, including the reference bone model and 26 RA elbows. The radial bone shortening in the radial head was evaluated by measuring the distance from the X^RZ^R plane to the middle plane along the Y^R-axis (Figure 4).

Fig. 4.

Illustration showing joint surface deformity evaluation. (A) Distal humerus, (B) proximal ulna, and (C) radial head. The red models indicate RA, and the white models indicate the reference bone. Yellow lines indicate the distance from the y-axis to the joint surface of the rheumatoid model, and black dotted lines indicate the distance to the joint surface of the reference model. The white arrow in the radius indicates the distance from the X^RZ^R plane of the middle plane on the Y^R-axis. RA = rheumatoid arthritis

Consequently, the measurements were used to compare the normal and RA groups. In addition, we investigated the erosion pattern across the elbow joint by consolidating individual findings.

Statistical Analysis

EZR(Easy R) statistical software was used for statistical analyses. The significance level was set at P < 0.05. Data are presented as mean ± standard deviation unless otherwise noted. The Mann-Whitney U test was used to detect differences in the measurements of the individual bones between the normal and RA groups.

In the RA group, the correlation between clinical outcomes and 3D deformities was evaluated using Spearman rank correlation coefficient. The correlation strength was categorized as mild (R < 0.2), low (R = 0.2 to 0.4), moderate (R = 0.4 to 0.7), or high (R > 0.7).

A priori power analysis was conducted (a = 0.05, 1-b = 0.8, two-tailed test). The requisite minimum sample size for detecting differences was established through a power analysis (α = 0.05, β = 0.2, two-tailed) from a prior study examining bone resorption in RA elbows using plain radiographs (humeral trochlea, distance from the axis of rotation to the articular surface: RA Larsen grades 2 to 5 15.0 ± 4.4 mm, normal 17.9 ± 1.9 mm).¹⁰ We included 24 samples each in the normal and RA groups. This calculation was done using the G*Power software (Universitat Kiel).

Results

Patient Characteristics

The mean age of the participants was 62.7 ± 11.1 years in the RA group and 37.0 ± 8.4 years in the normal group. In the RA group, the mean range of motion was 114.0 ± 26.0° for flexion, −38.9 ± 17.1° extension, 52.0 ± 21.9° pronation, and 41.1 ± 27.6° supination. The mean MEPS was 57.2 ± 17.0, and the mean disabilities of the arm, shoulder, and hand score was 38.6 ± 22.6.

Evaluation of Bone Morphology

In the distal humerus, the RA elbows showed notable bone destruction, particularly in the anterior-inferior region, compared with the normal elbows (Figure 5, A). The measurements of the RA group were markedly lower than those of the control group across all planes, specifically at 0°, 30°, and 60° directions due to bone destruction (P < 0.05 for all); the values for the RA and control groups varied from 8.4 to 9.6 mm and 9.4 to 12.0 mm in the 0° direction; from 7.7 to 9.3 mm and 9.6 to 12.4 mm in the 30° direction; and from 7.9 to 9.9 mm and 9.5 to 12.6 mm in the 60° direction, respectively (Figure 6, A).

Fig. 5.

Illustration showing morphological changes in the elbow with rheumatoid arthritis. (A) Distal humerus, (B) proximal ulna, (C) radial head, and (D) total elbow joint. White arrows indicate bone destruction in each bone, and the wide white arrow indicates the proximal shift of the forearm bone.

Fig. 6.

Pie charts showing joint surface deformity. Vertical axis shows the distance from the y-axis to the joint surface. Blue band indicates normal elbow, and orange band indicates RA. Red cross sections show notable bone resorption areas in RA compared with normal elbow, whereas blue cross sections show notable bone thickening in RA compared with normal elbow. C, Boxplot of radial shortening. Vertical axis shows the distance from the X^RZ^R plane to the median plane. Blue bar indicates normal elbow, and orange bar indicates RA. RA = rheumatoid arthritis

In the trochlear notch, the RA elbows showed notable bone destruction, particularly in the anterior-inferior region, and osteophyte formation at the tip of the olecranon, compared with normal elbows (Figure 5, B). The values of the RA group were markedly higher than those of the control group across all planes, particularly at 30°, 60° and 90° directions, attributable to bone destruction (P < 0.05 for all); the measurements for the RA and control groups ranged from 16.5 to 18.9 mm and 11.2 to 15.3 mm in the 30° direction; from 16.7 to 20.1 mm and 11.3 to 15.4 mm in the 60° direction; and 14.5 to 19.4 mm and 10.6 to 15.4 mm in the 90° direction, respectively. The values of the RA group tended to be lower than those of the control group, especially in the 180° direction, due to osteophyte formation (ridge of the trochlear notch: RA 5.5 ± 3.4 mm vs. normal 9.3 ± 1.3 mm, P < 0.05, and center of the medial trochlear notch: RA 8.4 ± 4.7 mm vs. normal 12.8 ± 1.3 mm, P < 0.05) (Figure 6, B).

On the radial head, the elbow showed osteophyte formation, particularly on the lateral side. The radial head height of the RA elbow was lower than that of normal elbows (Figure 5, C). The measurements of the RA group were markedly higher than those of the control group, specifically in the 0°, 30°, and 330° directions, due to osteophyte formation (all P < 0.05); the values for the RA and control groups were 13.0 mm and 9.9 mm in the 0° direction; 13.3 mm and 10.7 mm in the 30° direction; and 12.5 mm and 10.6 mm in the 330° direction, respectively. The radial bone length was markedly shortened in the RA group (RA 2.24 ± 1.97 mm vs. normal −0.18 ± 0.59 mm; P < 0.05) (Figure 6, C).

Observation of the deformity of each bone at the elbow joint indicated that the forearm shifted proximally relative to the humerus, resulting in anterior subluxation of the radial head and proximal migration of the olecranon. Osteophytes developed around the humeroulnar, humeroradial, and proximal radioulnar joints (Figure 5, D).

Correlations Between Clinical Function and Bone Morphology

The limitation of flexion angles highly correlated with low bone resorption at 30° from the center of the medial trochlear notch (R = 0.74, P < 0.001) and moderately correlated with low bone resorption at 60° from the trochlear notch ridge (R = 0.46, P = 0.026). The limitation of extension angles correlated moderately with bone thickening at 150° of the lateral verge of the trochlear ridge (R = −0.42, P = 0.048), 120° of the ridge of the trochlear notch (R = 0.45, P = 0.033), and 150° (R = 0.43, P = 0.042) and 180° (R = 0.48, P = 0.024) of the center of the medial trochlear notch. The limitation of the supination angle moderately correlated with bone thickening at 60° (R = −0.58, P = 0.042) and 90° (R = −0.57, P = 0.005) of the radial head. Low MEPS values moderately correlated with low bone resorption at 90° of the trochlear notch ridge (R = −0.55, P = 0.006). The angle of rotation and bone deformities did not correlate. The results of the notable correlations are summarized in Figure 7.

Fig. 7.

Charts showing correlations between clinical findings and three-dimensional measurements.

Discussion

We created a 3D bone model from CT images of patients with RA and quantitatively evaluated the destruction patterns of individual elbow bones (distal humerus, proximal ulna, and radial head) to determine the morphological relationships between these bones. The results showed bone destruction in the anterior-inferior zone of the distal humerus and proximal ulna and shortening of the radius, which suggests that the forearm bone shifts proximally to the humerus. Deformity of the humeroulnar joint is associated with restricted flexion-extension, whereas deformity of the radial head correlated with limitation of forearm supination.

In all sagittal sections of the distal humerus, bone resorption was observed mainly anterior inferiorly, whereas limited bone resorption occurred posteriorly. The same was true for the proximal ulnar articular surface, which showed bone resorption mainly anterior inferiorly, resulting in the deepening of the ulnar trochlear notch, as described by Lehtinen et al.⁹ In the radial head, osteophyte formation was mainly observed in the lateral regions, commonly referred to as the “safe zone,” and the bone length was markedly reduced. Deformities of the RA elbow can be attributed to mechanical factors, as well as immunological factors such as osteopenia and synovitis.^16,17 Mechanical factors may have a greater influence in patients with severe joint destruction, such as those with mucilaginous-type RA.¹⁸ Considering these reports, the bone resorption sites in this study may have been high-load areas for loading or elbow-flexion movements.¹⁹ Because of the high load, the radial head was shortened with crushed osteophytes.

The observation of deformity for each bone in the elbow joint suggests a proximal shift in the forearm bone relative to the humerus, which results in joint incompatibility and periarticular osteophyte formation. The proximal shift of the forearm bone relative to the humerus also suggests that the radial head subluxes anteriorly and the olecranon shifts proximally.⁹ Anterior subluxation of the radial head acts as a mechanical block to extension and flexion.^20,21 Progressive proximal migration of the olecranon can form a fork-like deformity in the humeral pulley and may be a risk factor for medial humeral condyle fractures.^6,22 The occurrence of these shifts throughout the elbow because of resorption in each bone is a novel finding (Figure 5).

The correlation results between bone morphological changes and clinical symptoms demonstrated that the limitation of flexion motion correlated with low bone resorption in the anterior part of the ulnar trochlear notch, and limitation of extension correlated with low bone resorption in the posterior part of the humeral trochlea and ulnar trochlear notch. These findings suggested impingement due to osteophyte formation in the relevant parts. In addition, greater osteophyte formation on the dorsolateral side of the radial head correlated solely with the restriction of forearm supination. This observation indicates potential impingement at the proximal radioulnar joint, a notion supported by previous studies demonstrating an improvement in restricted motion after radial head resection.²³ In the inferior region of the center of the middle trochlear notch, high bone resorption negatively correlated with the MEPS. The MEPS, which includes a range of motion as a variable, may reflect the correlations between ulnar deformities and both flexion and extension limitations.

Therefore, this study's findings are clinically relevant. Understanding the progression of destructive changes in the rheumatoid elbow has intrinsic value to the clinician and surgeon. Second, it can serve as a warning sign for potential fractures. Resorption of the base of the ulnar trochlear notch increases the risk of olecranon fractures.¹⁰ Third, understanding the deformities can elucidate insight into the kinematics and help in selecting appropriate implants and designing more anatomical implant geometries. For instance, in cases where bone resorption occurs in the anterior lower part of the humerus, opting for noncemented fixation may pose challenges, requiring meticulous implant selection.

This study has some limitations. First, the degree of bone destruction varied even among the Larsen IV cases, and we did not differentiate between the resorptive and ankylosing types, which are two characteristic patterns of bone destruction in the RA elbow.⁵ In addition, each RA case differed in terms of the number of years since onset and treatment history. This may have led to case bias, in which the deformity in each case may have had a notable effect on the results, although our results are consistent with those of previous reports.^9,10 Second, errors may have occurred in the fitting of the bone models, although the fitting was done using a uniform method for the specific model used as the reference bone. Third, the mean age of the normal group differed from that of the RA group. However, this could be considered a suitable healthy elbow without elbow arthropathy. A control group with the same mean age would provide more robust comparisons to assess morphological changes. This study used retrospective data, although longitudinal data tracking progression over time would provide valuable insights into the pathophysiology. We will consider subsequent follow-up longitudinal studies to investigate the correlation between morphological alterations and clinical disease progression in the future.

Conclusion

In conclusion, we characterized bony deformities of the distal humerus, proximal ulna, and radius of RA elbows by 3D analysis.

• (1)In the distal humerus, bone destruction was located at the anterior-inferior region.

• (2)In the trochlear notch, bone destruction was located at the anterior-inferior region, and osteophyte formation was located at the tip of the olecranon.

• (3)The radial head showed shortening and osteophyte formation on the lateral side.

• (4)Overall, these bony changes led to a proximal shift of the forearm relative to the humerus, resulting in anterior subluxation of the radial head and proximal migration of the olecranon.

This unique deformity pattern is a novel anatomical observation. These findings offer valuable insights into the pathology of the RA elbow and contribute to advancements in treatment.

Supplementary Material

jagrr-9-e24.00384-s001.docx ^{(532KB, docx)}