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. Author manuscript; available in PMC: 2022 May 1.
Published in final edited form as: Phys Sportsmed. 2020 Sep 30;49(2):123–129. doi: 10.1080/00913847.2020.1820846

The role of MRI in evaluating post-operative ACL reconstruction healing and graft mechanical properties: A new criterion for return to play?

SF DeFroda 1, RM O’Donnell 1, PD Fadale 1, BD Owens 1, BC Fleming 1
PMCID: PMC8007665  NIHMSID: NIHMS1629578  PMID: 32897799

Abstract

Disruption of the anterior cruciate ligament (ACL) is a common injury. In active patients, it is routinely treated with ACL reconstruction surgery. Following reconstruction, one of the critical decisions that must be made is the optimal timing of return to sport. While a many of biomechanical, biological, and functional criteria have been proposed to determine return to play, these methods are limited at best. As criteria for return to play are multifactorial, there is a growing need for non-invasive technologies, such as magnetic resonance imaging (MRI), to objectively track graft healing, to better assess the graft itself. Measuring the changes in strength of the healing ligament has been shown to be a reliable means of objectively documenting graft healing in pre-clinical studies. While the initial studies of MR-based modeling of ACL graft healing are promising, this technology is still in its infancy and requires optimization. The goals of this review are: 1) to outline the shortcomings of current return to play criteria, 2) to highlight the ability of MRI to determine the status of ACL graft healing, and 3) to discuss the future of imaging technology to determine return to play and its potential role in the clinical evaluation of patients.

ACL Tears and Return to Play: The Problem

The number of ACL reconstructions performed annually in the US has been increasing in all age groups but most notably in patients less than 15 and over 40 years of age.[1, 2] ACL reconstructions have grown from 32.9 per 100,000 person-years in 1994 to 68.6 per 100,000 person-years in 2016.[3, 4] More recent estimates suggest that there are approximately 200,000 ACL reconstructions performed in the United States annually.[4] With a growing population, and increasing social movement to stay active and exercise, the number of ACL injuries and reconstructions will likely continue to rise. But despite the increase in the number of ACL reconstructions performed annually, re-tear and failure of the graft remains a challenge. While the re-rupture rate quoted in the literature can be variable (0–25%)[5], the larger, more comprehensive studies show rates between 2% and 7.7%.[6–10] While this can be multifactorial in nature, one cause of failure could be return to activity prior to full graft healing and integration.

Currently, there is no consensus regarding the best type of metrics that should be used for determining when an athlete can return to sports. Most are simply based on time post-surgery and/or use physical benchmarks as a rough guide.[11–13] Unfortunately, most tests are assessing the muscles around the knee joint more so than the strength and quality of the healing ACL graft. It has been shown that there is an increased risk of a second ACL tear in the first 12 months after original reconstruction, both with graft failure/tear in ipsilateral knee or ACL tear in the contralateral knee.[14–17] This is especially apparent in female athletes, who are 16 times more likely than matched controls to sustain a tear, including 4 times more likely to have an ipsilateral re-tear and 6 times more likely to suffer a contralateral injury.[14] Even at 24 months, the risk of experiencing an ipsilateral or contralateral tear has been shown to be 6 times greater after return to sport, which again is more profound in females.[16] There is also evidence that supports a psychological element both in the ability to return to sport and the increase in re-rupture rate, with self-reported fear playing a major role.[15, 18] Surgeons and therapists develop rehabilitation programs for athletes to get back to sport[19–22], but despite being a major ar bea of focus, there is still no definitive objective data to tell when an athlete is ready to return to their respective sport. There are many physical, functional, patient reported and psychological tests that have been investigated to determine return to play readiness including but not limited to those shown in Table 1, none of which directly assess the integrity of the graft.[23–26] With so many “tests” to choose from, how do patients, therapists, and physicians know which metrics truly indicate a readiness to return to elite activity.

Table 1.

Types of Return to Play Criteria

Function Tests Psychological Tests Patient Reported Outcomes Sport Specific Scales/Testing
Range of Motion Testing Anterior Cruciate Ligament-Return to Sport after Injury scale (ACL-RSI) ACL-RSI Conditioning Testing
Lachman’s Test Tampa Kinesiophobia Index International Knee Documentation Committee Questionnaire (IKDC) Agility Testing
Pivot Shift Testing Multidimensional Health Locus of Control Scale Tegner Activity Scale (TAS) Sport Specific Drills (Dribbling, Kicking, Passing, Throwing, etc.)
KT1000/KT2000 Rosenberg Self-Esteem Scale Knee Injury & Osteoarthritis Outcome Score (KOOS) Return to Practice (Non-Contact)
Hop Testing Series Brief Profile of Mood States ADL scales Return to Practice (Full Contact)
Jump testing (Vertical Jump, Broad Jump) Athlete Fear Avoidance Questionnaire Lysholm Knee Scoring Scale Return to Game
Landing Error Scoring Injury Psychological Readiness to Return to Sport (I-PRRS) Knee Self-Efficacy Scale (K-SES)
Isotonic and Isometric Strength Testing
Isokinetic Testing and Analysis
Knee Santy Athletic Return To Sport (K-STARTS)
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Current Techniques to Assess Return to Play

There are three main criteria in which the surgeon should consider when assessing an athlete for return to play (RTP): biomechanical, functional, and biological. From a biomechanical standpoint, the native ACL has an average load to failure of 2160N, versus quadrupled hamstring autograft (4590N), bone-patella tendon-bone (2977N), and quadriceps autograft (2352N).[27–31] However, it is important to note that these values represent cadaveric failure loads, and do not emulate the structural properties of the graft in vivo during the healing process.

Functional testing is the most common current method used to determine whether an athlete is ready for RTP. Functional tests provide a means to evaluate both the quantity (force generated) and quality of movement. A systematic review by Abrams, et al. found 88 studies, with over 4000 patients, evaluating the usefulness of the most common functional tests.[32] The most frequently utilized functional performance test in the studies was hop testing,[33] which was assessed using the limb symmetry index (LSI). Interestingly, the data suggested that there may be some deficit in the operative extremity even in the 6 to 12 month time period, all of which normalized by 24 months.[32] However, there is a disconnect as many athletes are going back to sport by 6 months despite these findings.

The literature has evaluated other tests to determine if they can serve as a guide to whether an athlete is truly ready to return. Some of the other common tests include: jump assessments, closed and open kinetic chain testing, sensorimotor system evaluations (balance/proprioceptive tests), range of motion examinations, sport-specific testing, and lower extremity functional assessments.[23, 24, 32, 34–37] Recently, studies have evaluated a specific battery of tests during the rehabilitation process to try to judge the readiness for an athlete to go back to sport. However, these have not been studied thoroughly to see if injury rates afterwards are reduced.[38, 39] There is no consensus on which functional tests should be used when trying to evaluate when an athlete is ready for return to sport, or what the appropriate “score level” on those tests that indicate it is appropriate to go back to sport. Additionally, these tests are mostly testing the muscular envelope such as the quadriceps and hamstrings, and not the graft itself.

There are also a number of psychological questionnaires that have been used to evaluate patient readiness for sport.[23, 40] ACL injury and surgery carry a significant psychologic effect on an athlete. Psychological readiness to return to sport has been shown to be extremely important. Fear of reinjury is the most common cited reason for not returning to preinjury activity.[35, 41] Self-esteem levels based on patient reported outcome scales have even shown to correlate with patient performance on functional testing and rehabilitation.[25] Females have been found to have a more negative psychologic outlook, with fewer returning to sport compared to males.[42] Younger patients with lower psychologic readiness based on questionnaires have also been shown to be at higher risk of a second ACL rupture.[43]

There is no “gold standard” to determine when an ACL reconstruction or repair is able to withstand the forces needed to return to sport. A systematic review by Harris et al examining 49 studies with 4178 patients found that the most commonly used metrics were: Lysholm score (67% of studies), single-leg hop (31%), isokinetic strength (31%), and KT 1000/2000 (82%).[37] However, only 5% of studies even reported whether patients returned to sport, 90% failed to use any objective criteria for RTP, and 65% used no specific criteria at all. Lastly, 24% failed to report when patients could return to play with no restrictions.[37] A meta-analysis showed equivocal findings when investigating the validity of RTP test batteries and reduction in subsequent ACL tear.[44] Clearly there is no standardized way of determining an athletes ability to RTP that is comprehensive, reproducible, cost effective, and minimally invasive, leaving a lot of confusion in the literature and in patient care.

Biologically, it has been shown that the graft initially loses strength during the healing process.[45, 46] This loss occurs over the first 6–12 weeks of healing while the graft undergoes hyperproliferation and revascularization via an acute inflammatory phase.[46–49] It has been shown that 3 weeks after bone-patellar tendon-bone graft implementation, the graft-tunnel wall interface is the weakest component, whereas at 6 weeks, the midsubstance of the graft becomes the weakest link.[46–48] There is still large debate about when the ACL graft fully “heals”. Previous research in animal models which included ligament biopsy at various stages of healing has shown that tendon autografts undergo a “ligamentization” process after reconstruction.[50, 51] In humans, a similar process was seen.[52–55] The implanted grafts progressively lose their tendon specific biologic properties and exhibit more ligamentous histologic properties over time.[52–55] Authors have broken this process into four discrete phases: early, remodeling, maturation, and quiescent.[52–55] Overall, cellularity slowly returned to the values of intact ACLs at 3–6 months, while vascularity returned to values of intact ACLs at 6–12 months.[49, 52–55] Three out of five of these studies showed that the “maturation” phase did not begin until about 12 months[53–55], and one showed that the maturation phase did not begin until 18 months after implementation[52]. There is literature that the graft continues to the maturation process up to the 2 year point.[56, 57] However, as we know, athletes are returning to sport well before the one-year post-operative time point. Determining, whether a graft is “healed”, or “matured” would necessitate a biopsy, which in the real world is not feasible. Thus, using any type of histological criteria to tell if a player’s graft is ready to return to sport is not plausible. While performing failure testing of a healing graft is possible using pre-clinical models, these methods are not possible in real life patients. This necessitates the need for minimally invasive yet reproductible techniques to evaluate graft healing and maturation.

Potential Role of MRI To Determine Return to Play Readiness

Magnetic resonance imaging (MRI), is a tool which has been investigated as a tool to assess both the quality and quantity of soft tissues.[58–66] MRI has both the ability to assess tissue quality via normalized signal intensity, with lower signal intensity corresponding to more organized tissue, and normalized graft volume or cross-sectional area, which can be used to determine the mechanical properties of the healing tissue.[64, 67] More specifically, the linear combination of graft volume and mean signal intensity has been found to correlate with in situ structural properties (while using a custom software, IDL; ITT Visual Information Solutions, Boulder, CO) (Figure 1).[67] The signal intensity is a direct measurement of water content within the graft, which has been linked to collagen organization and hence tensile strength of the graft.[68] Prior studies have shown that increased vascularity and water content early in the graft healing process result in a higher signal intensity, corresponding with less tensile strength. As the graft matures the signal intensity then decreases.[64, 65, 67, 68] The normalized graft volume (Figure 2) represents the quantity of tissue, which also relates to the overall strength of the healing graft.

Figure 1.

Figure 1.

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ACL segmentation following MRI.A. Two-dimensional segmentation in sagittal plain. This is done for all slices containing ACL tissue. B. 3-D representation of ACL including graft in the tibial tunnel. C. Exclusion of the tibial tunnel

Figure 2.

Figure 2.

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3D representation of ACL segmentation to determine graft volume. Sagittal MRI demonstrating the volume segmentation of the ACL (orange), as well as the medial and lateral tendon length (measurements). Cross section represents coronal plane of the 3-D image.

Correlation of MRI parameters with ACL healing

One of the first studies attempting to correlate MRI and biomechanical properties of healing grafts was performed in 2001 by Weiler et al. The authors determined the mechanical properties of healing split achilles tendon grafts by performing a MRI, calculating the signal to noise ratio in the center of the graft, and correlating it to the structural properties such as load to failure and linear stiffness.[69] It was found that higher signal intensity on MRI correlated with decreased mechanical properties, with immunohistochemistry confirming that the amount of signal enhancement correlated with the vascular status of the graft during remodeling.[69] Signal to noise ratio calculations, however, can have inherent error since they are dependent both on acquisition sequences and the type of MRI scanner used.[67] This study also only performed a 2-D assessment of the midsubstance of the graft from a central slice and did not perform and entire 3-D assessment.[69] Parameters less dependent on image acquisition are needed to more accurately determine the in vivo properties of the healing ACL graft.

For this reason, T2 relaxation times are a valuable resource in evaluation of graft healing. T2 relaxation is dependent on the proteoglycan and water content of the graft, which is directly associated with graft healing.[70–72] Fleming et al examined the relationship between signal intensity and graft volume looking at BTB ACLR grafts in 9 Nubian goats. This was accomplished by scanning the specimens with a 3T MR scanner and determining the T2 relaxation time using a T2-relaxometry imaging protocol, as well as the graft volume using a graphic workstation (Vitrea workstation; Vital Images, Minnetonka, MN ). Using a custom software (IDL; ITT Visual Information Solutions, Boulder, CO), the manually segemented ACL was mapped in the T2 sequence to evaluate the volume and this was compared to the T2 relaxation time to find the mean T2 time of the graft midsubstance.[67] The authors also normalized volume to T2 relaxation time in hopes of getting more accurate measurements by considering both MRI measurements and graft T2 properties.[67] It was shown that there was a significant relationship between graft volume and failure load which was even greater when normalized to the T2 relaxation time.[67] Additionally, stiffness and graft volume had a significant correlation which remained significant with normalization. AP laxity was only significantly correlated with graft volume when normalized.[67] This study was important in demonstrating proof of concept of predicting structural properties of ACL grafts when combining MRI volumetric and signal intensity metrics. However, the echo times were too long for use with normal ligament and tendon tissues.

In a follow-up study by Biercevic et al, MRI was used to determine graft properties of Yucatan mini pigs at 15 and 52 weeks post-surgery.[64] The study utilized T2* weighted MRI to determine the intra-articular graft volume and signal intensity (grayscale) followed by mechanical testing of the harvested ligaments. The study showed that both volume and signal intensity significantly predicted structural properties (maximum load, yield load, linear stiffness) with the combination of these two parameters in a regression model improving the predicted mechanical properties.[64] This was an important study in allowing for the development of a predictive algorithm for calculating the mechanical properties of healing ACL grafts. An additional follow-up study by Biercevicz et al sought to examine if this same technique could be used to examine humans to determine in vivo if the signal intensity and volume measures used to predict the graft properties correlated with clinical outcomes.[73] While it was obviously not possible to test the reconstructed ligaments to failure, patient 1-legged hop was used as a surrogate for mechanical strength. Combining graft volume and signal intensity in a multiple regression model correlated with 1-legged hop at both 3 and 5 years, demonstrating these MRI parameters as a possible way to assess for graft strength in vivo.[73] These parameters also showed positive correlation with better patient reported outcomes in the form of 4 of 5 of KOOS subscores.[73]

While promising there are still limitations to this technology. One concern is that the signal intensity values may not be reproducible across varying magnets. For instance, the measurement of signal intensity is limited by its dependence on image acquisition, meaning it may vary based on MRI sequence parameters, scanner manufacturer, which can cause variability depending on where the scan is performed.

More advanced MRI techniques hold the promise of shorter scan times with less magnet to magnet variability. T2* relaxometry is one such MRI sequence with this potential.[60, 62] Post surgical MRI evaluation with T2* relaxometry using shorter echo times offers a noninvasive method of investigating graft maturation. [63–65, 73] The measurement of signal intensity by itself is dependent on image acquisition parameters and machine manufacturer, rendering the data to be protocol, magnet, and institution specific, limiting its utility as an easily employed criteria for return to play.[62] T2* image acquisition offers a solution to this problem. Values acquired with this sequence are inherent to tissue type, and have been shown to correlate with collagen organization and tissue vascularity, making it ideal for highly organized structures such as ligaments and tendons.[74, 75] Biercevicz et al further examined this by obtaining MRI exams 52 weeks after bio-enhanced ACL repair in a porcine model and performing T2* mapping of the ligaments.[76] Their study found that T2* values significantly predicted maximum load, yield load, and linear stiffness with a similar correlation to their previous studies utilizing signal intensity.[76] The authors concluded that this could be the first step in developing a standardized way to assess graft healing across institutions regardless of acquisition parameters and magnet type. A follow-up study by the same group investigated the relationship between T2* relaxometry and the semi-quantitative histology healing ACL repair tissue.[77] A porcine model was once again used, and imaged at 52 weeks to obtain T2* relaxation values as well as ligament volume. The ligaments then underwent histologic examination using the advanced Ligament Maturity Index (LMI).[77] Both the T2* and volume of healing ligaments significantly predicted the total LMI score as well as cell, collagen, and vessel sub-scores with lower T2* and higher volume associated with higher histological scores.[77] This provided another important step in validating this imaging modality for the evaluation of healing of ACL tissue.

One challenge with T2* relaxation time is that because it is related to collagen fibril organization and the amount of tissue healing, that the degree of collagen organization will vary with time. The duration of T2* acquisition times predict healing with varying ability depending on the overall organization of the tissue (mature ligament versus scar tissue). One study found that the ACL volume with the shortest T2* relaxation times contributed the most to the predicted strength of healing ligaments.[76] Beveridge et al combined short and long T2* relaxation times at 6, 12, or 24 weeks in a porcine model to better characterize both organized (short T2* time), and disorganized (longer T2* time) to more accurately predict the structural properties of the healing ACL in the hopes of developing a temporal linear predictive model irrespective of the stage of healing.[59] The study found that the structural properties as predicted by a multiple linear regression model based on both short and long T2* relaxation times over the healing period were in closest agreement with the measured values of the structural properties. This indicated that due to the healing ACL containing both organized and disorganized collagen that change over time, that both long and short T2* relaxation times should be used for the most accurate model of graft healing.[59] These methods continue to be refined to give the most accurate in vivo prediction of graft healing. As these methods have been developed using the pig model, work is ongoing to translate the T2* mapping models to human ACLs and ACL grafts.

However, we know that graft maturation and healing is only a portion of the complex interplay between biology, function, and psychology with regards to the ability to return to play. Clearly, current return to play methods are lacking completeness. We are hopeful that as MRI techniques such as T2* relaxometry continue to improve, that future return to play protocols will include MRI evaluation in addition to include passing a series of function tests to ensure neuromuscular optimization, and patient reported testing to confirm psychological readiness to return to sport confidently. Ultimately optimizing the aforementioned MRI techniques can help guide return to play, particularly in those patients who may reach their functional milestones early, by truly evaluating the degree of healing of the ligament with a goal for successful, injury free return to play. Additionally, depending on which sequences are ultimately acquired (T2 relaxation, T2*, T1 STIR, etc.) MRI can take a significant amount of time (30 minutes or longer). Future studies should aim at examining early time points (6–12 months), and determining the best MRI sequence balancing speed, fidelity and reproducibility. Ultimately, these imaging modalities show promise for potentially being able to determine the strength of the healing ligament to better guide physicians return to play criteria.

Summary

While there have been many advances in the surgical techniques, and post-operative protocols following ACL reconstruction, there still remains a grey area with regards to the best way to determine ligamentous “healing” and when a patient is ready to return to play. While functional, and clinical assessments exist to determine return to play, these metrics don’t truly assess graft strength and healing but more likely focus on the overall muscular envelope and patients ability to perform various physical tasks without a definite ability to evaluate the ability of the reconstructed graft to withstand physical activity. MRI has the potential to serve as an effective tool in evaluating the in vivo characteristics of the ligament while using measurements such as graft volume and signal intensity to extrapolate the mechanical strength of a ligament, which could help influence the decision to allow an athlete to return to play, especially when combined with the pre-existing functional and clinical outcome metrics. Ultimately more work is needed in this area to perfect the imaging sequences and processing techniques, but this is an exciting area of research which may ultimately help guide return to play.

Acknowledgement

We gratefully acknowledge the support from the National Institutes of Health [NIAMS 3R01-AR065462, NIGMS 5P30 GM122732 (Bioengineering Core of the COBRE Centre for Skeletal Health and Repair)], the RIH Orthopaedic Foundation, and the Lucy Lippitt Endowment.

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