Imaging of physeal stress in the upper extremity
(Ab)normal redefined
Kraan, R.B.J.
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2020
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Citation for published version (APA):
Kraan, R. B. J. (2020). Imaging of physeal stress in the upper extremity: (Ab)normal
redefined.
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7
The distal radial physis: exploring normal
anatomy on MRI enables interpretation of
stress related changes in young gymnasts
European Journal of Sport Science 2020 [Epub ahead of print] DOI: 10.1080/17461391.2019.1710263
Rik B.J. Kraan
Laura S. Kox Roelof Jan Oostra P. Paul F.M. Kuijer Mario Maas
Abstract
Objective
Explore the MRI-appearance of the healthy distal radial physis and the distribution of stress-related changes in physeal thickness in young gymnasts to aid in the understanding of the pathophysiological process of stress-related physeal injury.
Methods
Symptomatic gymnasts with clinically suspected overuse injury of the distal radial physis and age and gender matched asymptomatic gymnasts and healthy non-gymnasts underwent an MRI-scan of the wrist. A cartilage-specific sequence was used to obtain three-dimensional reconstructions of the distal radial physis. Heat maps and line charts of these reconstructions visualized distribution of physeal thickness per study group and were used to explore differences between study groups. Symptomatic gymnasts displaying most profound physeal widening (n=10) were analyzed separately.
Results
Twenty-seven symptomatic- (skeletal age 12.9±1.5 years), 16 asymptomatic- (skeletal age 12.8±1.9 years) and 23 non-gymnasts (skeletal age 13.6±1.9 years) were included for analysis. Physes of healthy non-gymnasts had a thin center and increased in thickness towards the borders. Gymnasts demonstrated an increase in thickness of the entire physeal surface. In symptomatic gymnasts increase in physeal thickness was most prominent at the volar side when compared to asymptomatic gymnasts and non-gymnasts.
Conclusion
The healthy distal radial physis is characterized by a thin center surrounded by thicker borders. Stress applied to the wrist during gymnastics causes an overall increase in physeal thickness. Profound thickness increase is present at the volar side of the physis mainly in symptomatic gymnasts. These results can help unravel the pathophysiological mechanism of stress-related physeal injury in gymnasts and aid early injury identification.
Introduction
In the immature skeletal system physeal cartilage is most susceptible to sustain stress-related
damage 1, causing young athletes to be prone for physeal overuse injuries.2 The localization of
these injuries is sport-specific and depends on the biomechanical characteristics of the sport
2. For example, among young gymnasts injuries of the distal radial physis are prevalent as a
result of the repetitive compressive, tensile and rotational stress applied to the wrist during
gymnastics.3-6
The normal physis consists of multiple layers in which chondrocytes rest, proliferate,
hypertrophy and eventually calcify during the endochondral calcification process.7 Two separate
vascular systems supply nutrients to the physeal cartilage cells. The chondrocytes in the resting and proliferative zone are vascularized by the epiphyseal blood supply. On the metaphyseal side the blood supply derives from diaphyseal nutrient and metaphyseal arteries and terminates
in vascular loops in the layer of endochondral ossification.1,7 Stress-related damage to the
multilayered physis or to the metaphyseal vascularization hampers the normal calcification
process causing an accumulation of non-ossified chondrocytes.8-10 This results in widening of
the hypertrophic zone of the physis which can be visualized on radiographs and MRI images
and used to establish the presence or absence of physeal injury.11,12
While this physeal widening is used in the diagnostic workup of physeal injuries, no studies have focused on the distribution of the stress-related changes in physeal thickness. Although
methods for accurate and automatic assessment of articular cartilage are available 13-15,
reliability of these methods for physeal cartilage thickness assessment has not been evaluated yet. Accurate assessment of physeal cartilage thickness can provide insight in the parts of the physis most affected by wrist-loading activities. Subsequently, this knowledge may facilitate early diagnosis of physeal injury and provide understanding of the pathophysiologic and biomechanical factors contributing to stress related physeal pathology of the wrist in gymnasts, which in turn is essential for the development of preventive measures in order to assure healthy
sports participation 16 and to avoid long-term consequences.17
This study aims to explore and visualize the detailed appearance of the normal physis on MRI using three-dimensional segmentations of the distal radial physis and to evaluate the distribution of stress-related changes in physeal thickness as a result of wrist loading in young symptomatic and asymptomatic gymnasts.
Methods
Gymnasts aged 12 to 18 years with wrist pain and suspected of having an overuse injury of the distal radial physis were referred by one sports physician. Subsequently, age and
matched asymptomatic gymnasts and non-gymnasts not involved in wrist-loading activities more than twice a week were included. Participants with a growth disturbance or a systemic or oncologic disease of the musculoskeletal system were excluded. The study was approved by the institution’s review board and participants and their parents or guardians signed informed consent prior to participation.
Clinical information
All participants filled in a questionnaire which included biological information (age, sex, body height and body weight), sport participation (primary sports and amount of training hours per week) and symptoms of the wrist (presence and severity on a scale of 1 to 10). Additionally, a research physician (RBK or LSK) performed physical examination of both wrists and hands including palpation, provocation tests (e.g. testing the stability of the distal radio-ulnar joint) and a maximum grip strength test using a hydraulic hand dynamometer.
Imaging
MR-images of one wrist were obtained using a 3.0 Tesla MRI-scanner (Ingenia, Philips Healthcare, Best, the Netherlands). The MRI protocol included a high-resolution cartilage-specific three-dimensional sequence with a voxel size of 0.5*0.5 mm and slice thickness of 1.5 mm. Each scan consisted of 60 slices with a matrix size of 384*384. A digital radiograph of the same wrist was obtained to assess skeletal age using BoneXpert (v2.0.1.3; Visiana, Holte, Denmark, www.
BoneXpert.com)18.
Distal radial physis segmentations
To analyze the configuration of the physes in the different study groups, segmentations of the cartilaginous part of the distal radial physis were used. These segmentations were obtained from earlier work in which changes in distal radial physeal volume between the three study
groups were analyzed.12 In this work the physeal cartilage of each participant was segmented
semi-automatically on MR images derived from the high resolution cartilage-specific sequence.
Segmentations were made in ITK-Snap (Version 3.2.0, October 23, 2014)19 using a method based
on image-intensity thresholding. Subsequently, all segmentations were checked to evaluate if the distal radial physes were segmented correctly and adjusted manually if necessary by one observer blinded for study group. Manual adjustments were necessary in approximately half of the participants and often included small alterations of falsely segmented pixels (i.e. the metaphyseal vascularization was often included in the segmentations as the signal intensity of these pixels approximated that of physeal cartilage). Segmented physis of participants with a
nearly fused distal radial physis (defined as a physeal volume less than 100mm3) were excluded
Post-processing
The three-dimensional segmented distal radial physis of all participants were imported in RStudio (RStudio, version 1.1.453) for post-processing and analysis. Segmentations of participants in whom the right wrist was scanned were rearranged to have all physes to be oriented in the same orthogonal plane.
Two methods were used to evaluate the distribution of physeal thickness in each participant. First, all three-dimensional segmentations were transformed into two-dimensional representations of the physes. This was done by counting the number of voxels in which physeal cartilage was present over one axis (proximal to distal), generating a two-dimensional axial image of the physis in which each pixel represented the physeal thickness in that particular location.
For the second method, physeal thickness was assessed in ImageJ (v1.50i, National Institutes
of Health, USA) 20 using the local thickness method. This is a technique that has been used in the
assessment of articular cartilage and displays the local thickness of a structure as the diameter
of the largest sphere that fits within the structure at that particular location.13,21 These
three-dimensional local thickness maps were also rearranged into two-three-dimensional axial images that represented the maximum thickness at each particular location.
We expected these methods to depict a similar distribution of physeal thickness, however we predicted that the local thickness method would exclude small but relevant irregularities from the measurements as the spheres that are used for calculating the local thickness maps would not infiltrate these irregularities and thus underestimate the physeal thickness in certain locations. As physeal irregularities are important in the assessment of physeal stress we preferred to use the first method to prevent loss of information. To justify the use of the first method we aimed to ascertain that distribution of thickness was similar in both methods by testing if mean physeal thicknesses derived from both methods were correlated. Mean physeal thickness calculated using the two different methods demonstrated a statistically significant positive and consistent correlation in all study groups (correlation coefficient 0.61-0.71, p < 0.01) and therefore results derived with the first method were used for analysis. Scatterplots of the mean physeal thickness per voxel for both methods are depicted per study group in supplementary figure 1. Analyses
To compare the configuration of the changes in physeal thickness, the sizes of all physes were equalized by resizing the two-dimensional axial images to 110 by 40 pixels using nearest-neighbor interpolation. All two-dimensional axial images representing the distal radial physis of individual participants were visualized as heat maps, in which a color scale represented the thickness of the physis in that particular location (blue for the thinnest parts and red for the thickest parts of the physis). The two-dimensional axial images of the participants of the three study groups were used to create three axial images (one for each study group) representing
the mean physeal thickness per study group. In addition, axial images of symptomatic gymnasts with a distal radial physeal volume exceeding the largest volume in the non-gymnasts group (n = 10) were combined and visualized. We assumed that visualizing the distribution of physeal thickness increase in these gymnasts with most profound physeal widening would be helpful to identify those parts of the physis most affected during gymnastics.
Line charts were used to demonstrate the mean thickness per group in the dorsal-to-volar and radial-to-ulnar direction and the relative percentage of increase in physeal thickness of symptomatic and asymptomatic gymnasts compared to non-gymnasts. To explore differences between study groups, the two-dimensional axial images representing the mean physeal thickness per study group were subtracted and visualized with separate heat maps.
Results
Sixty-nine participants (27 symptomatic gymnasts, 18 asymptomatic gymnasts and 24 non-gymnasts) were included in the study. Two asymptomatic gymnasts and one non-gymnast demonstrated a (nearly) fused distal radial physis and were excluded. Consequently, distal radial physis segmentations of 66 participants were used for analysis.
Table 1. Clinical information of participants; Symptomatic
gymnasts Asymptomatic gymnasts Non-gymnasts
Number of participants 27 16 23
Sex – Male (%) 15 (56%) 8 (50%) 12 (52%)
Body height (cm) 159±11 158±9 164±11
Body weight (kg) 47.0±8.4 47.0±8.4 51.8±12.0
Calendar age (years) 14.4±1.3 14.1±1.3 13.6±1.3
Skeletal age (years) 12.9±1.5 12.3±1.5 13.5±1.8
Primary sports Gymnastics Gymnastics Field Hockey (7)
Korfball (5) Soccer (4) Other (6) None (1) Training hours/week 20.8±7.9 20.0±10.8 3.3±1.5* Clinical information
Information of the participants per study group can be found in table 1 and did not demonstrate any statistically significant differences between the three study groups.
Distal radial physeal thickness
In the non-gymnast group, the distal radial physis was thinnest in the center and increased in thickness towards the border (figure 1). The dorsal and radial borders of the healthy physes appeared thicker compared to the volar and ulnar sides (figure 1A and 2).
Symptomatic- and asymptomatic gymnasts demonstrated a similar composition with a thin physeal center compared to the borders (figure 1). However, compared to non-gymnasts the thickness of the entire distal radial physeal surface was increased in both gymnast groups. The ulnar border of the physis was the thinnest border in all gymnasts. In symptomatic gymnasts with the most profound increase in physeal thickness, the thickest part of the distal radial physis was the volar part (figures 1 and 2).
In addition, in non-gymnasts the volar border of the distal radial physis was thinner compared to the dorsal border (volar to dorsal thickness ratio < 1). Both gymnast groups demonstrate a similar thickness at the dorsal and volar borders (volar to dorsal thickness ratio = 1) and gymnasts with most profound increase of distal radial physeal thickness demonstrate a thicker volar border (volar to dorsal thickness ratio > 1) (figure 2).
C | Symptomatic gymnasts B | Asymptomatic gymnasts
A | Non-gymnasts D | Gymnasts with thickest physes
Volar Dorsal Volar Dorsal Volar Dorsal Volar Dorsal Radial Ulnar
Figure 1. Distal radial physeal thickness per study group (A: non-gymnasts (n = 23), B: asymptomatic
gym-nasts (n = 16), C: symptomatic gymgym-nasts (n = 27), D: symptomatic gymgym-nasts with most profound increased physeal thickness increase (n = 10) demonstrated by heat maps with a color scale (red represents thickest and blue represent thinnest parts of the physis).
Changes in physeal thickness
Compared to non-gymnasts the distal radial physis in both symptomatic and asymptomatic gymnasts was increased in all locations (figure 3). In both gymnasts groups, the increase in thickness is most distinct at the dorsal and volar parts of the physis compared to the center. However, while the extent of physeal widening in asymptomatic gymnasts appears similar at the dorsal and volar sides, in symptomatic gymnasts widening is most pronounced at the volar side (figure 3). This is further delineated by the comparison in physeal thickness between symptomatic and asymptomatic gymnasts; at the dorsal side the distal radial physeal thickness is comparable in both groups, however especially the volar side of the physis is thicker in symptomatic gymnasts. This difference is larger when the most profound widened physes are compared with asymptomatic gymnasts demonstrating a large increase at the volar side of the physis (figure 2).
5 7 9 11
Dorsal Location Volar
Mean thi ck nes s (i n v oxel s)
Mean thickness | dorsal to volar direction
A
3 5 7 9
Radial Location Ulnar
Mean thi ck nes s (i n v oxel s)
Mean thickness | radial to ulnar direction
B
30% 60% 90%
Dorsal Location Volar
% increase compared to non-gymnasts
C
Study Group Most severe cases Symptomatic gymnasts Asymptomatic gymnasts Non-gymnasts
Figure 2. Thickness of the distal radial physis per study group in dorsal-to-volar direction (A) and
radi-al-to-ulnar direction (B) and increase in thickness per study group demonstrated as percentage compared to physeal thickness in non-gymnasts (C).
Volar Dorsal Radial Ulnar Volar Dorsal A | Subtraction
Asymptomatic - Non-gymnasts Symptomatic - Non-gymnastsB | Subtraction
Volar
Dorsal Dorsal Volar
C | Subtraction
Symptomatic - Asymptomatic-gymnasts Gymnasts with thickest physes D | Subtraction - Asymptomatic-gymnasts
Figure 3. Differences in physeal thickness between asymptomatic (A) and symptomatic gymnasts (B)
compared to non-gymnasts; and between symptomatic gymnasts (C) and gymnasts with profound physeal widening (D) compared to asymptomatic gymnasts demonstrated by heat maps with a color scale (red represents largest and blue represents smallest differences between groups).
Discussion
The healthy distal radial physis is characterized by a thin center and becomes thicker towards the border, especially at the volar and radial borders. In both symptomatic and asymptomatic gymnasts the physeal center remains the thinnest part with the entire physeal surface demonstrating an increase in thickness. In symptomatic gymnasts with suspected physeal injury the volar part of the physis appears to be most affected by the wrist-loading activities during gymnastics.
Method of thickness assessment
Several methods have been developed for the automatic assessment of articular cartilage
thickness, but have not been tested on physeal cartilage.13-15 These methods appear to be
particularly sensitive to irregularities in the articular surface.13,14 The shape of the physis is undulating and irregular compared to articular cartilage, especially in athletes with stress-related
physeal injury.11 When the aforementioned methods are used to evaluate physeal thickness,
relevant irregularities and thus valuable information will be discarded.
Therefore, a technique that included physeal irregularities is preferred and was used in this study after adequate validity compared to the local thickness method was ensured. This fairly simple technique of counting the number of pixels that compose the physeal cartilage in a proximal-to-distal direction for each location was feasible because the physis is a (relatively) flat disc. As articular cartilage often has a convex shape, it has to be mentioned that this study’s method is not suitable for the assessment of articular cartilage.
The normal growth plate
The radiological appearance of the healthy distal radial physis has been described before 22,23,
but the configuration of the different areas of the unfused physis including the anatomical configuration with a relatively thin center compared to the borders have not been reported previously. Several studies have described the effect of maturation on the thickness of the
different physeal areas.22,24,25 In general, physeal cartilage thickness depends on the balance
between chondrocyte proliferation and endochondral calcification during normal growth.7 Craig
et al. explored the healthy distal femoral and proximal tibial physes using three-dimensional physeal reconstructions and described that surface area and volume increase during childhood
and plateau through adolescence.24 Eventually, if maturation approaches, a process starts that
causes the physis to narrow and eventually close.7,26 Sasaki et al. described that this closing
process is initiated at the central part of the physis in the distal femur and proximal tibia.25 Kraus
et al. described a similar pattern in the distal radius and hypothesized that this might be the
result of a relatively weak blood supply in the central area of the physis.22 In addition to this, the
results of our study suggest that the anatomical configuration of the healthy physis including a relatively thin center may also contribute to the described early central closure.
Stress-related changes in physeal thickness
Alexander et al. described that the zone of hypertrophy near the region of endochondral
calcification is the part of the physis most susceptible to stress-related changes.8 A second
vulnerable area is the metaphysis just below the physis; during the normal calcification process the physeal cartilage is replaced by primary spongiosa starting with resorption of cartilage cells
causing a transient vulnerability for stress at this location.8
An earlier study showed that increased thickness of the distal radial physis is present in both symptomatic and asymptomatic gymnasts, suggesting that increased physeal thickness as a result of wrist-loading activities during gymnastics is present to some extent in all gymnasts,
regardless of symptoms.12 It is unclear if changes in asymptomatic gymnasts reflect early physeal
damage, or physiologic adaptations of the body to resist the stresses applied to the wrist. In 1985, Roy et al. explored the presence of physeal widening in 21 gymnasts using conventional radiographs and described that, in line with the results of our study, especially the radial and
volar parts of the physis were affected.27 While increased thickness of the entire physeal surface
was present in gymnasts with and without symptoms in our study, the present study showed that the volar part of the physis was affected mainly in symptomatic gymnasts. In contrast to non-gymnasts and asymptomatic gymnasts, gymnasts with profound physeal widening demonstrated a volar to dorsal thickness ratio of more than 1 and therefore it should be further evaluated if severe widening of the volar side of the physis indicates the presence of true pathology.
We considered two possible explanations for the mainly volar-sided changes in distal radial physeal thickness in symptomatic gymnasts: vascular anatomy and biomechanics.
The major part of the metaphyseal blood supply in long bones derives from a central
diaphyseal nutrient artery.7,28 Several metaphyseal arteries entering the distal radius at different
locations provide the rest of the metaphyseal blood supply.29 The supplying arteries form a
large anastomotic interosseous network of arterial loops that end at the zone of endochondral
calcification.29,30 This metaphyseal vascularization plays an important role in the induction of the
normal endochondral calcification process.9,10 Damage to this network of arteries causes a local
(temporary) disruption in the calcification process.9 Consequently, the presence of anatomical
variations in this vascularization might cause the metaphyseal blood supply at the volar side to be more easily disrupted. However, these anatomical variations have never been reported and therefore we consider the increase in physeal thickness more likely to be attributed to differences in stress applied to the different physeal areas.
During gymnastics the wrist is subject to compressive, tensile and rotational forces resulting
in a high prevalence of physeal injury of the distal radius.5,6 Several studies state that the
multilayered physis is most vulnerable to shear stress 8,31-33 and tension 32, while the metaphyseal
vascularization is vulnerable to both shear stress and compression.8,32 Damage to both the
multilayered physis and the metaphyseal vascularization can cause widening of the physis
due to an accumulation of chondrocytes in the zone of hypertrophy.8 In addition, repetitive
traction during gymnastics may possibly initiate effects analogous to physeal distraction therapy,
which uses continuous traction for the management of growth arrest 34, and affects physeal
thickness including widening of the hypertrophic zone.35 As the zone of hypertrophy is the most
vulnerable part of the physis due to the increased cell size and relatively decreased amount of
intercellular matrix which causes resistance to shear stress 1,8, widening of this zone may cause
the physis to be even more easily damaged if stresses are continued to be applied.
Stress-related injuries of the proximal humeral physis and the medial humeral apophysis appear similar to distal radial physeal injury on diagnostic images and are common in
demonstrated that shear stress resulting from rotational forces is predominant during the overhead motion in baseball and suggested these stresses are responsible for physeal injuries
in young baseball pitchers.31 Comparable biomechanical studies exploring the magnitude
of compressive, tensile and rotational forces at the different areas of the distal radial physis in gymnastics are currently lacking. These studies are necessary for the interpretation of the physeal thickness increase and to identify which stresses (and thus gymnastic exercises) are most physically demanding for the wrist.
Strengths and limitations
We explored the configuration of physeal injuries in the wrist in a specific population at risk with a high training intensity. Symptomatic gymnasts were referred by a sports physician when an injury of the distal radial physis was clinically suspected, risking that in some symptomatic gymnasts no physeal injury was present after all. To reduce the effect of this potential bias, we separately analyzed the physis of ten symptomatic gymnasts demonstrating most profound physeal widening defined as a physeal volume exceeding the largest physeal volume in the healthy non-gymnasts. In addition, the study population was relatively small and as not all physes had the same configuration in some locations the combined arrays per study groups are based on data from a few physes. However, as anatomical configuration of distal radial physes has never been assessed in a similar way, exploration of the proposed method may be useful for larger studies in the future. Finally, the MR images used for physeal segmentation had relatively low through-plane resolution of 1.5 mm. Although this resolution was considered sufficient for this study, it should be noted that higher resolution yields more accurate segmentations, especially when imaging younger individuals with smaller physes.
Clinical implications
This study showed that the volar side of the distal radial physis is most affected in young gymnasts with wrist pain. This finding may be the first step in exploring the pathophysiological mechanisms responsible for stress-related injuries of the physis. Future work should focus on the biomechanics of gymnastics and identify which stresses are mainly applied to the different areas of the physis. In addition, while this study evaluated physeal changes as a result of wrist-loading during gymnastics in general, it would be interesting to unravel the effects of individual gymnastic disciplines (e.g. floor exercise, vault and pommel horse) on the morphology of the distal radial physis. This information may eventually help to prevent the occurrence
of physeal injuries.16 For example, preventive measures may be aimed at the avoidance of
specific movements that appear to be most stressful, e.g. the use of soft mats that cause extra
dorsiflexion 27 or the asymmetrical hand placement that increases rotational strain.37
In addition, the demonstrated difference in thickness at the volar side of the physis between symptomatic and asymptomatic gymnasts and the presence of a positive volar to dorsal
thickness ratio of more than 1 in gymnasts with most profound physeal thickness increase should be further explored. If larger studies confirm this finding, evaluating volar thickness and the volar to dorsal thickness ratio may be important for the (early) detection of stress-related physeal injury and to discriminate between a healthy and injured distal radial physis in daily clinical practice.
Conclusion
The healthy distal radial physis is characterized by a thin center compared to the borders. Stress applied to the wrist during gymnastics causes an overall increase in physeal thickness. Severe thickness increase is present at the volar side of the physis mainly in symptomatic gymnasts and gymnast with profound physeal thickness increase demonstrated a volar to dorsal thickness ratio of more than 1. These results may be useful for future studies exploring the pathophysiological mechanism and for early identification of stress-related physeal injury in gymnasts.
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