Imaging of physeal stress in the upper extremity
(Ab)normal redefined
Kraan, R.B.J.
Publication date
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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9
Elite athletes strive for top-level performance, often at or beyond the limits of their physical capacity resulting in a high prevalence of stress-related musculoskeletal injuries.1 Injured athletes
desire to return-to-sports as quickly as possible and therefore request top-level performance from physicians as well. To facilitate this for physeal injured young athletes, the main aim of this thesis was to develop an accurate imaging-based strategy for accurate assessment of the physis. The research in this thesis primarily focused on the distal radial physis, however result can provide guidance for development of diagnostic strategies for similar physeal injuries located in the elbow and/or shoulder.
The AMPHYS protocol: a structured MRI-based diagnostic approach
Assessment of abnormalities in the morphology of anatomic structures is the basis of traditional radiology. In clinical practice a diagnostic image is evaluated for the presence of imaging features that differ from ‘normal’ with respect to the observer’s frame of reference. These findings are, in case of sports radiology, used to determine injury presence and severity. In addition, the prognosis of an athlete’s time necessary to return-to-sports is often based on clinical information combined with imaging findings reported by the radiologist. However, a certain observer-dependent variance is present in the morphologic evaluation of diagnostic images. To minimize this variance, for several musculoskeletal injuries standardized MR imaging assessment protocols have been developed. These protocols demonstrated good reproducibility of findings among observers 2,3 enabling reliable evaluation of injury severity and, if adopted, can provide a uniform
method to compare MRI findings.2,3
As, prior to this thesis, a similar structured approach for assessment of the distal radius was not available, chapter 2 describes the development of such a systematic protocol for distal radial physeal injury: the Amsterdam MRI assessment of the Physis (AMPHYS) protocol. The used approach was based on the methods described by Branci et al. 3 aiming at the development
of an imaging-based diagnostic protocol for athletes with an injury of the pubic symphysis or adductor muscle insertions. In the first development phase of the AMPHYS-protocol all imaging features associated with physeal injury of the distal radius were extracted from medical literature and our institution’s Picture Archiving and Communication System (PACS) and subsequently discussed with several radiological experts in musculoskeletal imaging. The conceived list included features as physeal irregularity 4, epiphyseal bone marrow edema 5,6 and periosteal
bone formation of the metaphysis.6 The experts assessed MRI-scans of healthy and injured
wrists for the presence of all features, however numerous imaging features associated with physeal injury in medical literature were subject to a large interobserver variability. This poor agreement between observers questioned the value of these features in the diagnostic workup of physeal injury.
The main reason to develop the AMPHYS-protocol was to increase reproducibility of imaging findings in daily clinical practice. To achieve this, the final protocol only included the
twelve imaging features with highest interobserver agreement. In addition, a web-based application was created to assist radiologists confronted with MR images of an athlete’s wrist in daily practice, which can be accessed via www.amphys.nl. The application provides information per item and example cases to enable accurate assessment for radiologists with relatively few experience as well. The tools are ready to be used free of charge and implementation is valuable and should thus be encouraged for all institutions with an athletic patient population. However, it should be noted that the AMPHYS-protocol recommends the use of several image sequences that might have to be implemented first.
Redefining the (ab)normal appearance
As mentioned before, clinical assessment of diagnostic images includes the comparison of radiologic images with the ‘healthy’ reference. However, athletes are subject to repetitive (excessive) stress during intensive training regimes causing changes of the musculoskeletal system to occur, even in asymptomatic athletes, if compared to non-athletes.7-10 Images of
athletes can thus not be compared with a ‘healthy’ reference; simply attributing all changes in an athlete’s musculoskeletal system to pathology might introduce treatment or temporary sport cessation that could have been avoided. On the other hand, detecting pathology as early as possible is essential to prevent further damage.
To tackle this problem, the clinical significance of changes in an athlete’s musculoskeletal system as a result of sports should be established. Possibly these ‘abnormalities’ reflect (early) pathology, or result from adaptations necessary to enable symptom-free high-level performance.
Despite the underlined importance of a ‘healthy athlete’ reference for accurate interpretation, prior to this thesis, knowledge of the MR appearance of the healthy adolescent athlete’s wrist as a result of continuous wrist-loading was lacking. We aimed to redefine this appearance and used the AMPHYS-protocol to ensure a structured and reproducible approach.
Interestingly, all features of the AMPHYS-protocol were, to some extent, present in MR images of the distal radius in both healthy non-wrist loading adolescents and asymptomatic (wrist-loading) gymnasts. Chapter 3 demonstrates that, similar to earlier reported studies,11-13
bone marrow edema-like signal intensity is prevalent among the forearm of healthy children. Bone marrow edema is associated with several pathologic conditions,14 however interpretation
of high water content of the bone marrow should be done cautiously in adolescents; maturation dependent processes affect the appearance of the bone marrow,14-16 as for example the red
to yellow bone-marrow conversion results in a change in the marrow’s water content and thus MRI-signal.14 Furthermore, the athlete’s body is subject to a significant quantity of stress, which
may cause reconversion of the bone marrow to its high-water content form.14 We identified
some MR features that were more frequently observed in asymptomatic athletes compared to non-athletes. These features should be further considered, for example by following several
asymptomatic gymnasts over time, obtaining MRI scans at multiple moments during a season. Assessment of these images can reveal if these features should be considered as early pathologic signs and thus enable early identification of physeal injury.
The observed appearances of the healthy- and non-athlete’s wrist were used to identify MR features capable of discriminating between a healthy and injured distal radial physis. Not presence, but signal intensity of epiphyseal and metaphyseal bone marrow edema and thickness of the distal radial physis, if compared to the proximal physis of the first metacarpal bone, appeared to differ between healthy and injured gymnasts. Although validation in large wrist-loading athlete-populations is desirable, these features can be valuable to determine the presence and severity of distal radial physeal injury. Validation should include an assessment of the importance of the different imaging features. Eventually this can lead to the development of a weighted scoring system that ascertains the presence of injury above a certain threshold. The height of the score further yields information on injury severity. Such a score can guide physicians in making treatment decisions in daily practice.
Reliable assessment of the physis: A (semi-)quantitative approach
Despite including imaging features with highest inter-observer reliability in the AMPHYS-protocol, morphologic assessment remains subject to a certain amount of observer dependent bias. This can be further reduced by the use of quantitative imaging techniques; these techniques extract quantifiable information from images as addition to the normal visual representation for the evaluation of injury (or disease) presence, severity and progress.17 The second part of this
thesis explored the possibility of (semi-)quantitative techniques aimed at two features suggested to be valuable in the diagnostic approach of physeal injuries in chapter 4: metaphyseal bone marrow edema and thickness of the distal radial physis.
Chapter 3 and 4 demonstrate that interpretation of bone marrow edema-like signal intensity is challenging; it is prevalent among both healthy non-athletes and asymptomatic athletes 9,10
and is affected by maturational status.14-16 However, as signal intensity of bone marrow edema
was higher in injured gymnasts compared to non-injured gymnasts in chapter 4, and large bone marrow edema volume was suggested to indicate severe injury in patients with an acute anterior cruciate ligament injury 18, chapter 5 evaluates the feasibility of a semi-quantitative approach
for bone marrow edema assessment in physeal injured athletes. To quantify the water content of the bone marrow, Dixon chemical-shift imaging was used which employs the difference in Larmor frequency between water and fat molecules to separately visualize water- and fat-images.19 The proportion of water in the bone marrow can be estimated by calculating the
signal of the water-only images compared to the signal of the combined water- and fat images. In daily clinical practice, this principle is frequently used to evaluate hepatic fat fraction 20 or
involvement of the bone marrow in patients with Gaucher’s disease.21 Chapter 5 demonstrated
assessment in the distal radius and ulna. Furthermore, the proposed method could successfully distinguish between injured and asymptomatic gymnasts as metaphyseal water content was higher in the distal radius of injured gymnasts. Although further validation is necessary, this suggests that Dixon chemical-shift imaging can be an important tool to improve the detection of stress-related physeal injuries.
In chapter 6 and 7 the value of a quantitative approach for the assessment of stress-related changes in distal radial physeal thickness was explored. An increase in thickness is often associated with physeal pathology 22-24 and emerges as the result of stress-related disturbance
of the normal endochondral ossification process.25,26 Within the physis a continuous process
of chondrocyte proliferation and hypertrophy takes place; the absence of ossification leads to an accumulation of chondrocytes which can be observed on MR images as widening of the cartilaginous part of the physis.26
The methods for quantitative evaluation of physeal thickness included semi-automatic segmentation of the cartilaginous part of the distal radial physes on cartilage-specific MR images with subsequent three-dimensional reconstruction. First, volume assessment of the reconstructed physes demonstrated that stress-related thickness increase is present in gymnasts with and without an injury of the distal radial physis. Comparing physeal volume of gymnasts with non-gymnasts is therefore not useful in daily clinical practice. However, largest increases in physeal volume were observed in injured gymnasts. This underlines that assessment of the amount of thickness increase may be valuable for detecting physeal injuries.
Further analysis of the distribution of physeal widening revealed that stress-related thickness increase was especially present at the volar side of the distal radial physis. In the evaluated gymnastic population in chapter 7, especially a volar part of the physis thicker than the dorsal part suggested the presence of physeal pathology. Apparently, during gymnastics, the majority of injurious stresses are applied to the volar part of the distal radius.
The next step towards successful prevention of physeal injuries is unraveling which stresses (and thus which gymnastic exercises) inflict most damage to the physis. In physeal injuries of the elbow and shoulder occurring as a result of throwing, most likely excessive rotational and traction forces result in physeal damage.27,28 However, in contradiction to overhead throwing, in
gymnastics a major part of the activities include weight bearing. A detailed (to be performed) analysis of gymnastics’ biomechanics can evaluate which stresses are applied to the different parts of the physis. Combining the results of this analysis with an examination of historic training information and physeal thickness increase per gymnast might reveal if physeal injuries are primarily induced by repetitive traction, rotation or compression. Eventually this can guide coaches to adjust and better balance wrist-loading exercises and training, for example during the growth spurt when the physis is extra vulnerable for stress-related damage.29
Future directions: clinical implementation …
Sports-injury research should always be centered around the injured athlete’s interests in order to optimize significance of findings for daily practice. The developed AMPHYS-protocol is ready to use as diagnostic tool and structured assessment of MR-images of the distal radial physis. Structured reporting using the AMPHYS-protocol may decrease the observer-dependent variance, especially when using the reference application at www.amphys.nl. It enables assessment of detailed data on the status of the distal radius and consistent use in each athlete suspected of having a physeal injury is therefore recommended. In addition, if multiple MR scans are indicated over time, follow up of the injury (or the effect of initiated treatment) is facilitated as the progression of the injury can be easily evaluated. This is essential to enable physicians to provide injured athletes with specific information on injury status and severity and prognostic information on expected time to return to sports.
We consider a future imaging-based diagnostic strategy for physeal injuries of the distal radius to include both morphologic and (semi-)quantitative approaches in order to optimize diagnostic accuracy. However, as the studies in this thesis only explore the clinical utility and feasibility of both (semi-)quantitative techniques, validation in larger study populations is necessary prior to implementation of these techniques. In addition, the techniques are ready to use for research purposes but implementation in daily clinical practice will require radiologists to have access to the additional quantitative information simultaneously with morphologic evaluation of the images. This requires fully automatic preprocessing and information extraction from images without the radiologist having to perform additional actions to prevent loss of expensive time in daily clinical practice. With the current developments in both algorithms and infrastructure these solutions should be within reach. Furthermore, the extraction of quantifiable features as demonstrated in this thesis provides interesting opportunities to develop machine learning algorithms that can predict the presence and severity of injuries. This requires a lot more MR images, but can further assist in the diagnostic workup of physeal injuries.
This thesis is centered around imaging as diagnostic tool for physeal injury assessment, however eventually sports-physicians and hand surgeons guide athletes with a physeal injury of the wrist and prescribe treatment if necessary. To ensure optimal care for athletes intensive collaboration between clinicians and radiologists is essential. Structured physeal assessment using the AMPHYS protocol increases interpretability of imaging findings and thereby will facilitate communication and teamwork between radiologists and clinicians. The imaging-based diagnostic methods developed in this thesis will thus be valuable for clinicians. The use of these methods combined with an athlete’s history and physical examination will provide a solid base for shared treatment decision making.
… and further developments for the wrist and beyond
As elite athletes are involved in extensive training schedules, focusing on elite-level athletes in this thesis ensured optimal evaluation of wrist-loading on the MR appearance of the distal radial
physis. Usage of the imaging protocol should however not be limited to elite athletes as the described imaging methods are valuable for recreational athletes; the redefined appearance of the healthy athlete’s wrist facilitates interpretation of MR images in these athletes as well. However, as the wrists of elite-level athletes are subject to a larger amount of stress, the methods of this thesis should be validated for recreational athletes. This will increase the impact of the developed imaging techniques on (sports) society significantly.
Multiple morphologic and quantitative imaging features were demonstrated to be valuable in the diagnostic interpretation of MR imaging of the healthy and injured distal radial physis, however several steps have to be made to optimize the imaging-based strategy for use in daily clinical practice. Further research should focus on two essential topics that will be described below: providing prognostic information to injured athletes and enhancing early diagnosis to prevent physeal injuries from deteriorating and decreasing time to return to sports.
Currently, treatment of stress-related physeal injury of the distal radius includes prescription of temporary sports cessation and rest for a standardized period of time. In case of an injury, athletes desire prognostic information on the time period of their injury, often exemplified by the question if participation in a certain competition will be possible. To be able to provide this information, a longitudinal project should monitor both described morphologic and quantitative MR imaging features at multiple time points after the injury occurred. This information can provide insight in the healing process of the physis during periods of rest and enable the estimation of injury severity and time to recovery much more accurate. The athlete can then be provided with an athlete-specific and personalized advise on return-to-sports or specific activities.
This thesis illustrated that the difference between symptomatic and asymptomatic gymnasts is not arbitrary; the MR appearance of the asymptomatic gymnasts’ distal forearm is clearly affected by repetitive wrist-loading and should not be compared with a normal ‘healthy’ reference. The pathological significance of MR features resulting from wrist-loading should be explored in a longitudinal research project; if these MR features are signs of early pathology, they will enable early diagnosis of physeal injuries. Subsequently, despite MRI being an expensive imaging technique, it may be considered as surveillance tool in young vulnerable elite-gymnasts in order to guide training intensity, for example during important periods of the season.
We intended our research to contribute to prevention of physeal injuries of the upper extremity as well. In particular by contributing to the first steps in the ‘sequence of prevention’ established by van Mechelen et al., which include accurate establishment of injury incidence and severity.25 For the distal radial physis we described methods that, provided that further
validation is done, contribute to early identification, and thus secondary prevention. If imaging features can identify early biological changes to the musculoskeletal system, these features can essentially be considered as imaging biomarkers for stress-related injury. In addition, the imaging-based methods can be used for the first two steps of van Mechelen’s primary injury
prevention sequence 30; the proposed techniques enable accurate assessment of incidence and
prevalence of distal radial physeal injury and, as aforementioned, combining the distribution of stress-related physeal widening with biomechanical information can eventually increase the pathophysiological understanding of physeal injuries.
Due to the thorough exploration of all imaging-based possibilities for the distal radius, this thesis does not yet provide a ready-to-use diagnostic strategy for physeal injuries of the elbow and shoulder. However, as imaging features of physeal injuries at these locations appear similar to distal radial physeal injury on MRI 24, we suppose that the described methods, obviously
with slight modifications, can be valuable for the elbow and shoulder as well. This thesis can therefore be regarded as a first step in the direction of a diagnostic imaging strategy for the elbow and shoulder. To confirm this, the methods should be validated in an athletic population in which overuse (physeal) injuries of the shoulder and/or elbow are common. To direct these future research projects, a systematic literature review was conducted and established that overuse injuries of the elbow and shoulder were prevalent in young athletes involved in several overhead sports including baseball, softball and tennis. Athletes involved in these sports should be included to test the clinical utility of the described imaging techniques for physeal injuries of the elbow and shoulder.
The bigger picture
Prevalence of overuse injuries involving the musculoskeletal system and not only the physis is high among young athletes.1 Overuse injuries result from sports-participation beyond the
boundaries of an athlete’s physical limits 31, thus decreasing the intensity of training regimes and
eliminate excessive repetitive stress may be considered as a relatively easy method to prevent overuse injuries. Although the approach of simply decreasing the amount of training hours is too simple 32, several preventive measures are based on reduction of training intensity; for
example in youth baseball the amount of pitches a pitcher can throw is limited and the number of (mandatory) resting days after a certain amount of thrown balls is specified.33,34 Keeping
track of the exact amount of thrown pitches can distract an athlete during training. However, innovative methods can simplify training load monitoring, for example through innovative smart devices integrated in an athlete’s outfit that, in the case of baseball, can automatically count the number of thrown pitches.
Despite the proven value, adherence to the pitch-count limit is poor among young baseball players.35,36 The lack of adherence is however not surprising; the reduction or alteration of
training routines necessary to comply to the preventive guidelines may introduce a disadvantage compared to opponents adhering less strictly to the guidelines. In addition, young athletes are prepared to take risks in their desire to reach the top 37,38 and might be too young to understand
the consequences of potential overuse injuries. Parents of young athletes can be passionate about their child reaching a professional status and the additional financial consequences, i.e.
receiving a scholarship based on sports-performance creating the possibility to go to university,
39 and coaches are often judged on the performance of their athletes and may therefore be
willing to violate the preventive guidelines, especially in important periods in the season. Although the adherence might be poor, merely the presence of preventive guidelines increases awareness of sports injuries among young athletes, parents and coaches. Awareness itself may have a decreasing effect on the prevalence of overuse injuries, as coached might be more mindful in arranging training schedules, and could be further encouraged by (inter) national sports federations through education programs for athletes, coaches and parents (for example by successful adult athletes or federation appointed sports physicians). To optimize adherence to new to be developed preventive guidelines, these guidelines have to be feasible to be implemented in daily training schedules. Therefore, collaboration between researchers, athletes, coaches, team-physicians and (inter)national sports federations is essential. The International Olympic Committee underlined this by appointing nine centers of excellence for prevention of injury and protection of athlete healthy in 2014 of which one is based in Amsterdam (Amsterdam Collaboration on health & Safety in Sports). Furthermore, in the Amsterdam UMC high quality healthcare for athletes is centralized in the Academic Center for Evidence Based Sports-Medicine (ACES). ACES collaborates with several national sports federation, with the national Olympic committee and is official partner of TeamNL. The centralized approach ensures top-level healthcare and produces the opportunity to perform innovative team-based research projects with quick implementation in daily clinical practice.
Although injury-free sports-participation is an illusion, the aforementioned collaborations should be encouraged to prevent avoidable (stress-related) injuries among young athletes and enhance safe sports participation. For athletes at risk of physeal injury of the upper extremity,
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