MUSCLE HEALING IN SPORTS INJURIES

– Written by Sandra Mechó, Jaime Isern-Kebschull, Xavier Alomar, Manuel Wong, Alejandro Congo, Carles Pedret, Spain

INTRODUCTION

Injuries affecting myoconnective tissue are very common in sports and generally the athlete is not able to continue with the activity^1,2. In football, muscle injuries constitute approximately one third of the total time-loss injuries^1,3. During the past decade, hamstring injury rates have increased during both training and matches⁴.

It has been also demonstrated that the reinjury rate after a hamstring injury is about 18%. Probably one of the most important factors that can explain this high reinjury rate is the planification of the return to competition (RTC) which is normally faster than the biological healing in a scar tissue quality not prepared enough to withstand the demands of the athlete’s activity in the last stages of the RTC process.

The healing process that follows a muscle injury is completely different from that following a bone fracture. A muscle injury follows a reparative process that will end in a scar tissue that replaces the original but has to work similarly. On the other hand, a bone fracture is followed by a pure regenerative process⁵.

MRI is of great importance in muscle injuries initial diagnosis⁶. Its role in the return to play (RTP) decision making process has also been demonstrated showing statistically significant predictors of reinjury signs in the MRI prior to RTP⁷.

What about the role in the following of the muscle injury healing process? The role of MRI scan in muscle injuries follow-up is also well-documented⁸, but it requires of a very deep knowledge about the anatomy and the basic principles of myoconnective tissue regeneration to use it correctly to assess the quality of the scar tissue evolution and to predict the probability of having an exacerbation or reinjury before full recovery^9-13.

The aim of this article is to review the classification of muscle healing evolution in Sports Injuries based on MRI findings¹⁴ with examples and key points to consider.

MUSCLE HEALING PROPOSED CLASSIFICATION

The classification system proposed is based in the retrospective analysis of 128 cases of acute myoconnective tears that accounted for more than 40 days to RTP. All injuries included initial MRI diagnosis and MRI follow-up that was correlated with clinical findings¹⁴.

Injuries that required surgical treatment and low-grade injuries were not included. 2 to 4 MRI studies were performed in each patient, 310 MRI studies were analyzed at the end. All the MRI studies included proton density (PD) Fat Saturated and T1-weighted sequences in different space planes.

During the analysis two main topics were reviewed:

1. Restitution of the affected tissue architecture (scar appearance) identified by MRI as (Table 1):

• Discontinuity of tissue, no scar changes.
• Linear peripheral repair tissue (Target sign).
• Hypertrophic heterogeneous scar.
• Hypertrophic homogeneous scar.
• Remodeled residual scar (adapted to the morphology of the surrounding connective tissue).

1. Oedema patterns (Table 2):

• Interstitial
• Intermuscular
• Reparative

1. RESTITUTION OF AFFECTED TISSUE ARCHITECTURE

The healing process after a muscle injury is a process that goes through different reparative stages^10,12.

These stages can be detected by MRI:

1^st    Characteristic signs of a myoconnective injury can be observed, with the gap filled with blood and oedema in different spaces, leading to generalized MRI hyperintensity.

2^nd The hyperintensity diminishes, and the gap becomes filled with granulation tissue, forming an immature scar.

3^rd   The granulation tissue is progressively replaced by more fibrous components, resulting in a mature scar (Figure 1).

Throughout the process, tendon tension and the pennation angle of the myofibers gradually recover (Figure 2)^6,7.

4^th   The repaired and remodeled connective tissue forms a scar that is thicker than the native connective tissue (Figure 3)^15-17.

1. OEDEMA PATTERNS

The definition of oedema is an increase of free water or perfusion alterations^18,19.

In a myoconnective injury two different oedema types are the most common ones (Table 2).

• When the free fluid expands to the interstitial space it shows a feathery oedema pattern, INTERSTITIAL OEDEMA.
• When the free fluid expands to the intermuscular or perifascial space it shows a laminar oedema pattern, INTERMUSCULAR.

In case of free tendons, connective tissue without myofibers attached^20,21, the intermuscular or perifascial oedema can be defined as peritendinous oedema.

During the healing process the intensity and amount of these oedemas decreases and a new oedema type can be found. It can be described as an ill-defined oedema surrounding the scar tissue (Table 2). This edema pattern naturally emerges during the healing process as observed in the follow-up studies within our experience, which is why we refer to it as reparative edema. In more mature phases, we believe that this reparative edema transitions into adaptive edema, similar to that described by Kho et al²², indicating muscle activation and sharing the same imaging characteristics as the reparative edema.

Considering the process of the reparation of the myoconnective tissue injured, the oedema variations in the affected myotendinous junction²³ and the correlation with the three stages of the Järvinen classification (destruction, repair, and remodeling stages), a muscle healing classification using MRI has been proposed (Table 3).

PHASE 1: Acute injury

Typical signs of a myoconnective injury have been identified⁶. According to Wangensten and colleagues, this phase usually extends from 1 to 7 days, with minimal changes in oedema extent during the first post-injury week. Disruption of fibers is detectable from the first day and remains consistent throughout the period²⁴.

This phase probably correlates with the destruction phase described by Järvinen.

PHASE 2: Immature scar.

The connective tissue gap is filled with a hypertrophic scar, the center remains hyperintense (soft or immature) in all the sequences and progressively it is surrounded by a hypointense peripheral line, that at the beginning of the phase is fragmented (phase 2a) and at the end it is more uniform (phase 2b). The loss of connective tension is one of the first signs that is recovered (Figure 4).

The feathery oedema and intermuscular oedema progressively decrease. Usually in phase 2b the reparative oedema is well-identified (Figure 5).

This phase probably correlates with the repair phase described by Järvinen.

PHASE 3: Mature scar

The hyperintense center of the scar tissue becomes progressively hypointense with mild reparative oedema associated (phase 3a) and at the end of this stage, the whole scar is homogeneously hypointense, but still hypertrophic (phase 3b) (Figure 6).

We hypothesize that reparative oedema undergoes a transition into a more adaptive oedema, primarily associated with muscle activation. In this mature phase, characterized by increased load demands on the muscle, there is persistent edema which, although indistinguishable from reparative edema on imaging, we interpret as a result of muscle activation²². During this phase the oedema decreases until becoming non-visible (Final Healed Stage). 

This phase probably correlates with the remodeling phase overlapping with the repair phase described by Järvinen.

The T1-weighted sequence is useful to evaluate the maturity grade. The more mature the scar, the more homogeneously hypointense it appears on T1-weighted imaging. Occasionally, hematic changes within the scar can be identified as homogeneous hypointensities on fluid-sensitive sequences. However, when analyzed with the T1-weighted sequence, these changes may present as an intermediate MR signal.

CLINICAL APPLICATION

During the rehabilitation process after an injury, the player’s sensations can be assessed by interview, we can also assess the recovery of function/strength through different tests, but we also need to see how the scar is healing. This point is crucial to understand if the evolution of the scar tissue follows a correct maturation process to withstand the demands of the athlete’s activity⁸.

Myoconnective injuries are typically extensive craniocaudally, which results in different phases of healing at various levels of the same injury. When determining whether an injury is healing properly based on imaging and defining the maturation phase, the most immature section of the scar should be taken into account (Figure 7).

In our experience, it is usually not necessary for the scar to reach phase 3b or the Final Healed Stage to decide on a player’s medical clearance based on imaging. It is more common to consider clearance at phase 3a; however, one critical requirement is the presence of good peripheral organization of the scar. During the healing process, phases overlap, and sometimes scars in phase 3a may still have fragmented or very thin peripheral linear repair tissue (Figure 6a and 6c). Therefore, to consider the scar ready to withstand the demands of activity based on imaging, we must identify at least a phase 3a scar with well-organized periphery (Figure 8).

There are objective MRI features, in our experience, that allow us to think of a delayed healing process or a disbalance between loads and biological repair.

• Maturation delay: It is difficult to determine the exact timing of when each phase occurs. Different factors play a role in the healing process (rehabilitation program, player’s intrinsic factors…) and all of them are not present in the same way in all cases. Generally, from the 3^rd postinjury week a phase 2b-3a scar is the most frequent finding of the healing process. In case that a one month postinjury follow-up MRI shows an immature scar with fragmented periphery is considered a maturation delay in our experience (Figure 9).
• Persistence or recurrence of interstitial or intermuscular oedema: These signs have been described as risk factors for reinjury⁷ (Figure 10)
• Abscense of adaptive oedema:  Adaptive oedema is the ill-defined oedema surrounding the mature scar tissue (Figure 5). When it is present according to our experience it means that there is muscle activation, the identification of a very small amount or the abscense of adaptive oedema is considered indicative of dysfunction at the myotendinous junction (Figure 11).
• Scar rupture: If we sustain a reinjury during the immature scar phase or at the beginning of the mature scar phase the scar itself is affected (Figure 12). If the reinjury happens during the mature scar phase or at the end of the healing process it usually affects the healthy tissue located adjacent to the scar but not the scar itself (Figure 13).

There is an MRI sign that, although it might seem of a high reinjury risk, should not alarm us:

• Adaptive Split: Commonly found in the posterior aspect of the proximal aponeurosis of the hamstrings (Figure 14)

EXCEPTIONS

As has been explained, this classification is primarily based on myoconnective injuries²³. In daily practice different type of injuries can be diagnosed, according to the histoarchitecture affected. In addition to myotendinous injuries, we can find myofibrillar injuries. We have been able to see that this type of injuries do not follow the healing process described in the proposed classification.

The myofibrillar or muscular injuries definition is: rupture that occurs at a distance from the tendon or aponeurosis without direct involvement of them²³. The tissue that heals consists purely myofibers, therefore these injuries do not follow the healing process that we define by MRI. We are unable to detect a linear repair peripheral tissue characteristic of the immature phase. Sometimes, persistent interstitial oedema may be observed (Figure 15), and in the final healed stage, sometimes it may be impossible to clearly define the residual scar.

Although in the proposed classification, 14% of the injuries included in the sample were myofascial¹⁴, this type of injury poses a challenge when defining the different phases of healing. The affected myoconnective junction is not always visible on MRI, and the resulting scar is typically very thin, making it difficult to identify the linear peripheral reparative tissue, whether fragmented or not, or the progressive maturation of granulation tissue within the scar.

In these cases, scar monitoring is primarily useful for detecting warning signs, such as the persistence or recurrence of oedema. We have limited sensitivity in defining the temporal boundary between the mature and immature phases (phase 2b-3a). Consequently, the stages are ultimately summarized as the immature phase, when the scar is poorly defined and predominantly hyperintense, and the mature phase, when the scar appears predominantly hypointense (Figure 16).

Another exception to our classification is the proximal tendinous complex of the Rectus Femoris. It is formed by the direct tendon and the indirect tendon, that then converge into a common tendon^16,17,25-28. Probably the cause of the non-uniform healing in this complex is the distribution of forces in different directions, due to the distinct trajectory of each myoconnective junction that comprises it and the possible anatomical patterns that the indirect tendon can present²⁹. In the final stage of healing, we may observe heterogeneous scars without a properly organized periphery (Figure 17).

Again, in this region, scar monitoring should not focus primarily on evaluating its maturation but rather on identifying warning signs, such as the persistence or appearance of edema or changes in scar uniformity that may suggest re-tearing.

A reflection on this classification is that it outlines the general milestones of the healing process; however, each location within each muscle belly exhibits its own particularities, which could be further studied to complement it. For example, in our previous work, we analyzed these specific features in the hamstring tendons³⁰. 

POSSIBLE APPLICATION BY ULTRASOUND

US and MR imaging offer excellent spatial and contrast resolution to perform a detailed evaluation of muscles and connective tissue³¹. 

During the healing process the histoarchitecture of the muscle changes and until the scar begins to appear uniform, it exhibits moderate anisotropy artifact on ultrasound which may be related to the maturation of the scar. Anisotropy as a characteristic of normal tendons disappears during the initial destruction phase and recovers as the healing process advances to a mature scar. A clearer delineation of planes or reduced blurring can be observed as the scar progresses. But it is very difficult to pinpoint the transition specially between mature and immature scar tissue.

As we have indicated previously, when evaluating the healing process, we not only consider the scar but also the progression of oedema. The interstitial and intermuscular oedemas gradually disappear and become nearly impossible to detect by US although, some residual changes in the interstitial space among muscles bellies may help monitor the resolution of the oedema. Reparative oedema, as we have mentioned, is not free fluid that expands to any space; it is a feature that has only been described through MRI¹⁴ and hardly detected by US (Figure 18).

Therefore, we do not believe that ultrasound can approach the spatial resolution of MRI in assessing scar quality and the subtle changes in the surrounding edema. If we rely solely on ultrasound to monitor the healing process of an injury, it can lead to errors that, in professional athletes, may result in very complex situations.

CONCLUSION

Although progress has been made in diagnosing and understanding myoconnective injuries, the incidence of muscle injuries, particularly in the hamstrings, continues to rise. Ensuring adequate biological healing time remains a major challenge. The proposed classification by experts demonstrates that the MRI can show variations in the healing process that allow us to define when the scar is mature. It helps identify delayed maturation, poor scar adaptation, or re-tear. However, distinguishing healing phases in myofascial or myofibrillar injuries and detecting them by ultrasound remains difficult, highlighting the need for further research.

Sandra Mechó^1,2,3

Jaime Isern-Kebschull⁴

Xavier Alomar^2,3

Manuel Wong³

Alejandro Congo¹

Carles Pedret⁵

1               Department of Radiology

Hospital de Barcelona-SCIAS

Barcelona, Spain

2              Department of Radiology

Centres Mèdics Creu Blanca

Barcelona, Spain

3              Medical Department of Futbol Club Barcelona (FIFA Medical Center of Excellence) and Barça Innovation Hub

Barcelona, Spain.

4              Department of Radiology

Hospital Clinic de Barcelona

Barcelona, Spain

5              Sports Medicine and Imaging Department

Clinica Diagonal

Esplugues de Llobregat, Spain

Contact: mechomeca@gmail.com

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