651669

research-article2016

CARXXX10.1177/1947603516651669CartilageSchleich et al.

Clinical Research

Thickness Distribution of Glenohumeral Joint Cartilage: A Normal Value Study on Asymptomatic Volunteers Using 3-Tesla Magnetic Resonance Tomography

CARTILAGE 2017, Vol. 8(2) 105­–111 © The Author(s) 2016 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1947603516651669 journals.sagepub.com/home/car

Christoph Schleich1, Bernd Bittersohl2, Gerald Antoch1, Rüdiger Krauspe2, Christoph Zilkens2, and Jörn Kircher1,3

Abstract High-resolution 3-dimensional cartilage-specific magnetic resonance imaging (MRI) was performed at 3 T to test the following hypotheses: (1) there is a nonuniform cartilage thickness distribution both on the proximal humerus and on the glenoid surface and (2) the glenohumeral joint as a combined system is congruent with the level of the joint cartilage surface without substantial radial mismatch. Inclusion of 38 volunteers (19 females, mean age 24.34 ± 2.22 years; range 21-29 years) in a prospective study. Measurements of: cartilage thickness in 3 regions and 3 zones; radius of both circles (glenoid and humeral cartilage) for congruency calculation using 3-T MRI with 3-dimensional dual-echo steady-state sequence with water excitation. A homogenous mean cartilage thickness (1.2-1.5 mm) and slightly higher values for the glenoidal articulating surface radii both in the mid-paracoronar section (2.4 vs. 2.1 cm, P < 0.001) and in the mid-paraaxial section (2.4 vs. 2.1 cm, P < 0.001) compared with the humeral side were observed. The concept of a radial mismatch between the humeral head and the glenoid in healthy human subjects can be confirmed. This study provides normative data for the comparison of joint cartilage changes at the shoulder for future studies. Keywords shoulder, cartilage, MRI, joint space, mismatch, radius

Introduction As is well known, the shoulder joint is an almost nonconstrained joint, gaining its stability from dynamic forces rather than from structural properties. However, even small variations in the anatomy such as glenoid cartilage and bone loss can cause substantial functional changes, including instability and degeneration, which can eventually result in early osteoarthritis (OA).1,2 Since the pioneering work of Walch and Boileau that provided essential basic data about the anatomy of the proximal humerus (and its variability among individuals) and the size and orientation of the glenoid cavity, in particular in the axial plane, including patterns of morphological changes in OA, the anatomy of the glenohumeral joint as a combined system with 2 determinant parts has moved into the focus of attention.3-8 In this matter, 3-dimensional (3D) imaging and computational science have opened the door not only to a new understanding of joint relationships and kinematics but also for the treatment of altered anatomy such as glenoid bone loss.4,9,10 Yet, most imaging studies and 3D reconstruction techniques are based on data derived

from high-resolution computed tomography (CT) scans, which reflect the bony anatomy rather than the cartilaginous joint surface itself, which is the domain of modern magnetic resonance imaging (MRI).4,9-20 Therefore, since the fundamental measurements of cartilage thickness and distribution, which were performed using histological slices or cadaver specimens and a rule more than 30 years ago, there is a lack of information about the particular cartilage distribution and thickness both at the proximal humerus and in the glenoid cavity.21-24

1

Department of Diagnostic and Interventional Radiology, Medical Faculty, University Düsseldorf, Düsseldorf, Germany 2 Department of Orthopedics, Medical Faculty, University Düsseldorf, Düsseldorf, Germany 3 Department of Orthopedic Surgery, Klinik Fleetinsel Hamburg, Hamburg, Germany Corresponding Author: Jörn Kircher, Department of Orthopedic Surgery, Klinik Fleetinsel Hamburg, Admiralitätstrasse 3-4, Hamburg 20489, Germany. Email: [email protected]

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Table 1.  Sequence Parameters. Parameter TR/TE In-plane resolution Slice thickness Flip angle Field of view NEX (number of excitations) Slice gap Bandwidth Basic resolution TA (acquisition time)

Units

3-Dimensional DESS

[ms]/[ms] [mm3] [mm] [°] [mm2]

14.6/5.0 0.5 × 0.5 0.5 25 160 × 160 2

[mm] [Hz/pixel]

0.2 260 256 × 256 18:35

[min:s]

TR = repetition time; TE = echo time; DESS = dual-echo steady-state.

The objective of this study is to provide normative data about the thickness distribution of hyaline cartilage in healthy human subjects at the glenohumeral joint. Therefore, high-resolution 3D cartilage specific MRI was performed at 3 T to confirm or refute the following hypotheses: (1) there is a nonuniform cartilage thickness distribution both on the proximal humerus and on the glenoid surface and (2) the glenohumeral joint as a combined system is congruent with the level of joint cartilage surface without substantial radial mismatch.

Materials and Methods Study Population This study was approved by the local ethics committee. The principles of the study were carefully explained to all volunteers and a written informed consent was obtained prior to participation. Thirty-eight volunteers (19 females, 19 males, mean age 24.34 ± 2.22 years, range 21-29 years) were included in this prospective study (20 left and 18 right shoulders). Without exception, all participants were in good health, and no volunteer demonstrated any disorder or abnormalities of the glenohumeral joint. Subjects older than 30 years and those involved in high-level sports were excluded a priori to reduce age effects and to minimize the risk of confounding by including undiagnosed cartilage damage in our evaluation.

Magnetic Resonance Imaging Magnetic resonance imaging of the shoulder was performed with a whole-body 3-T system (Magnetom Trio, Siemens Healthcare, Erlangen, Germany) using a flexible 4-channel body matrix phased-array coil. Examination in supine position with the arm at their side in neutral rotation in a stable position using sponges and adjustable straps. The MRI protocol included a 3D dual-echo steady-state (DESS) sequence

with water excitation for morphological cartilage assessment. The DESS sequence combines 2 gradient echoes separated by a refocusing pulse into a single image that increases the signal intensity of both articular cartilage and synovial fluid.25 Details of the imaging parameters are provided in Table 1.

Image Analysis The 3D DESS data sets were transferred to a Leonardo workstation (Siemens Medical Solutions, Erlangen, Germany) to perform further analyses. From each 3D data set, coronal oblique reformats with a slice thickness of 0.5 mm perpendicular to the glenoid surface were generated using multiplanar reconstruction (MPR; Fig. 1). Of these DESS reformats, 3 reformats were selected to assess the glenohumeral cartilage at 3 sections of the joint: (1) anterior, (2) middle, and (3) posterior. Within each section, cartilage thickness measurements were performed on the glenoid and humeral cartilage superiorly, centrally, and inferiorly. To analyze if the glenohumeral joint as a combined system is congruent at the joint cartilage surface level without substantial radial mismatch, a region of interest (ROI) from the head of the humerus was laid in the articular surfaces of the glenoid and humeral cartilage in the paracoronal and paratranversal reformats. Half of the diameter of the ROI was determined to measure the vertical and horizontal radius in the paracoronar and paratransversal slices. The radius of both circles, that is, the glenoid and humeral cartilage, were analyzed in the congruency calculation (Fig. 2). All primary 3D DESS measurements were performed by 1 radiologist with 5 years of experience in musculoskeletal imaging, whereas for the reliability assessment, the analysis was repeated by the former and by a second observer (an orthopedic consultant with 9 years of experience in musculoskeletal imaging) in 10 randomly selected volunteers.

Statistical Analysis SPSS software (Version 22.0; IBM Corp., Armonk, NY, USA) was used for statistical analysis. Cartilage thickness and radius values were reported as means ± standard deviations (SD), median, value range, and 95% confidence intervals. The normality of data was tested by visual inspection using boxplots and scatterplots and statistically using the Kolmogorov-Smirnov and Shapiro-Wilk tests. As the normality assumption was uncertain in portions of the data, Friedman’s test with post hoc analysis was used to identify statistically significant differences between the cartilage thickness in various regions of the glenoidal and humeral cartilage and the radius of the articulating glenoidal and humeral head surface. Interobserver reproducibility of the

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Figure 1.  A measurement of cartilage thickness in the anterior (left), middle (middle) and posterior (right) paracoronar reformats (in this example of the humeral head cartilage). In each section, cartilage thickness was measured superiorly, centrally and inferiorly.

various regions was clinically negligible (mean cartilage thickness ranging from 1.2 to 1.5 mm). Radius measurements (Table 5) revealed slightly higher values for the glenoidal articulating surface both in the mid-paracoronar section (2.4 vs. 2.1 cm, P < 0.001) and in the mid-paraaxial section (2.4 vs. 2.1 cm, P < 0.001) compared with the humeral side. ICC analysis indicated a high degree of interobserver reproducibility in the cartilage thickness (ICC = 0.788, P < 0.001) and radius (ICC = 0.971, P < 0.001) measurements.

Discussion

Figure 2.  Radius measurements of glenoidal (white) and humeral (red) shoulder joint cartilage in paraxial (left) and paracoronar (right) slices.

cartilage thickness and radius measurement was quantified with the intraclass correlation coefficient (ICC) using a pairwise correlation model with absolute agreement. P values less than 0.05 were considered to be statistically significant.

Results The cartilage thickness values in the posterior region of the humeral head were slightly lower when compared with those in other aspects of the glenohumeral joint (Tables 2-4). Otherwise, the difference in the cartilage thickness among

The most striking result of our study is the remarkable difference in joint surface radii between the humeral head and the glenoid both in the frontal and axial planes. The differences in the frontal plane are 3 ± 0.3 mm and 2 ± 0.3 mm in the axial plane mean that (1) there is a radial mismatch between the flatter glenoid surface and the more curved humeral head and (2) this mismatch is greater in the frontal than in the axial plane (the ratio between the radius of the humeral head and the glenoid is 0.875 in the frontal and 0.92 in the axial plane). Although the absolute values appear to be small, they are in fact very relevant because they underline the biomechanical theory that the glenohumeral joint represents a force-locked dimeric ball-and-socket joint.26 Early joint replacement pioneers such as Charles Neer designed their components with a high degree of conformity based on the assumption of the “ball and socket” principle that was widely accepted at that time.27-32 A quantitative analysis of Soslowsky et al.33 in 1992 using precise stereophotogrammetry in 32 freshly frozen human cadavers

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Table 2.  Thickness Measurements of Glenoidal and Humeral Head Cartilage. Joint Partner Glenoid

Region Anterior

Middle

Posterior

Humeral Head

Anterior

Middle

Posterior

Superior Central Inferior Superior Central Inferior Superior Central Inferior Superior Central Inferior Superior Central Inferior Superior Central Inferior

Mean ± SD (mm)

Median (mm)

MinimumMaximum (mm)

95% CI (mm)

Normal Distribution

1.4 ± 0.2 1.5 ± 0.2 1.5 ± 0.1 1.4 ± 0.2 1.5 ± 0.2 1.5 ± 0.2 1.4 ± 0.2 1.4 ± 0.2 1.4 ± 0.2 1.5 ± 0.5 1.5 ± 0.4 1.5 ± 0.3 1.5 ± 0.3 1.4 ± 0.2 1.3 ± 0.2 1.3 ± 0.2 1.3 ± 0.2 1.2 ± 0.2

1.5 1.5 1.5 1.5 1.5 1.5 1.5 1.4 1.4 2.0 1.3 1.4 1.4 1.4 1.3 1.3 1.3 1.3

1.1-1.7 1.2-1.8 1.2-1.8 1.1-1.7 1.0-1.7 1.1-1.8 1.0-1.7 1.0-1.6 1.0-1.7 1.0-2.0 1.1-2.5 1.0-2.5 1.1-2.4 0.8-1.8 1.0-1.7 0.8-1.6 1.0-1.7 1.0-1.6

1.4-1.5 1.4-1.5 1.5-1.6 1.4-1.5 1.4-1.5 1.4-1.5 1.3-1.5 1.3-1.4 1.3-1.5 1.4-1.7 1.3-1.6 1.3-1.6 1.4-1.6 1.3-1.4 1.2-1.3 1.2-1.3 1.2-1.4 1.2-1.3

No No No No No No No No No No No No No No Yes Yes No No

Table 3.  Pairwise Cartilage Thickness Comparisons Between Regions of the Glenoid That Revealed Statistically Significant Differences. Glenoid Region 1

Mean ± SD Region 1 (mm)

Posterior-inferior

1.4 ± 0.2

Posterior-central

1.4 ± 0.2

Posterior-superior

1.4 ± 0.2

Glenoid Region 2

Mean ± SD Region 2 (mm)

P

Anterior-inferior Anterior-central Anterior-inferior Anterior-central Anterior-inferior Anterior-central

1.5 ± 0.1 1.5 ± 0.2 1.5 ± 0.1 1.5 ± 0.2 1.5 ± 0.1 1.5 ± 0.2

Thickness Distribution of Glenohumeral Joint Cartilage.

High-resolution 3-dimensional cartilage-specific magnetic resonance imaging (MRI) was performed at 3 T to test the following hypotheses: (1) there is ...
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