Normalized STEAM-based diffusion tensor imaging provides a robust assessment of muscle tears in football players: preliminary results of a new approach to evaluate muscle injuries

Acute muscle injuries are very common in elite and non-elite athletes, and tears due to indirect active traumatic events especially have a high prevalence [1, 2]. In the last decades, the clinical evaluation of muscle strains has increasingly been associated with imaging-based assessment [2, 3]. Several grading systems of muscle injuries have been proposed in the clinical and radiological literature [4‐6] and recently the Munich Consensus Statement highly recommended the use of an accurate terminology about muscle lesions [7]. Nevertheless, the prevalent MRI-based classification is still based on a rough quantification of the amount of torn fibres [8] preventing a high imaging-based accuracy in both therapeutic and prognostic management of patients [9]. Diffusion tensor imaging (DTI) [10‐12] has been successfully used to investigate muscle tears on an animal model (i.e. dystrophic and wild mice) [13] as well as in patients (i.e. two patients with acute muscle tears) [14]. Even though DTI allows an accurate assessment of muscle anatomy [15‐18] and disorders [13, 14, 19‐21], it is affected by challenges (i.e. short T2 relaxation times of muscle) [22] and artifacts [23‐25]. The development of new techniques for muscle fibre-tracking is, therefore, an active field of research [26‐28]. Promising results were recently obtained using a Stimulated Echo Acquisition Mode (STEAM) sequence, which, among other advantages, is hardly affected by eddy current distortions and enables long diffusion times without strong T2-induced signal-to-noise ratio (SNR) loss via the application of mixing time (TM) [25, 29].

Despite the above-mentioned encouraging results and technical improvements, to the best of our knowledge a prospective study applying STEAM-DTI for investigating acute muscle tears in athletes has not been performed yet. Therefore, the main aim of this study was to assess and quantify acute muscle tears affecting the lower limb of professional football players with STEAM-DTI. As it has been demonstrated that in athletes differences between the muscles of the preferred and non-preferred leg occur [30‐33], the second aim of this study was to evaluate the impact of a normalization of the data by deriving a ratio between injured and healthy areas on the injured limb and healthy areas on the contralateral extremity.

Five out of the eight investigated patients showed an injury of the thigh and three one of the calf. Seven lesions affected the right side and one the left. Two tears were rated as minor partial and six as moderate [7] (Table 1).

Our results suggest that normalized DTI/fibre-tracking metrics obtained via artifact-corrected STEAM-DTI are insensitive to possible bias due to laterality, being thus well suited for quantitative diagnostic assessment of muscle tears.

Acute muscle tears are characterized by alterations of the myofibrillar structure and inflammation [39, 40]. DTI is uniquely sensitive to changes in the magnitude and directionality of intramuscular water diffusivity occurring in acute muscle tears. Hence, these alterations are expected to be easily detected and quantified by this technique. Our results show an absence of significant differences (i.e. besides higher AD on the injured side) comparing entire and injured muscles. This is consistent with observations by McMillan et al. on an animal model for injuries of the tibialis anterior [13]. Indeed, these authors found significant differences in DTI metrics only comparing wild and dystrophic mice with muscle injury or comparing injured and non-injured dystrophic animals, whereas differences between injured and non-injured wild animals did not occur [13].

In contrast, Zaraiskaya et al. [14] showed significant differences in FA, MD and eigenvalues (i.e. λ₁,λ₂,λ₃) comparing DTI measures from entire healthy muscles (i.e. eight volunteers) with those obtained in ROIs drawn in injured muscle areas of the calves of four patients (i.e. two with haematomas and two with muscle tears). These results are in accordance with the differences in FA, MD, RD and AD found in our population comparing the injured areas with the healthy ones (i.e. ipsi- and contralateral ROIs), even if it has to be taken into account that the presence of oedema may lead just to an apparent decrease of AD and FA [41].

Zaraiskaya et al. performed fibre tracking only in healthy controls, but no such data were presented for patients [14]. Froeling et al. [35] evaluated fibre-tracking changes at different time points in marathon runners, but performed no separate assessments for muscle strains already visible on anatomical images (i.e. T2w images). To the best of our knowledge, there are no previous studies that have investigated fibre-tracking metrics (i.e. number, length and volume of tracked fibres) of muscle tears. In our cohort, no differences in fibre tracking emerged, either in the entire muscle, or in the ROI-based analyses. The tracked muscle fibres of the injured side turned out to be significantly less numerous (-55 %) and shorter (-39 %) only after normalization of the data. Considering that in athletes an asymmetry in the characteristics and metabolic activity of muscle belonging to the dominant and non-dominant side has been shown [30‐33], it appears reasonable that the laterality is a biasing factor in quantitative DTI assessments in muscles. The results obtained after applying the normalization seem to confirm this assumption, as differences in length, number and volume of the tracked fibres due to the injury were apparent only in normalized data.

Our study results are preliminary and could not yet validate the fact that STEAM-DTI brings any additional benefits compared to conventional MRI. Since one of the more challenging aspects of muscle tear assessment is represented by the prognosis of the recovery interval [42], we strongly believe that the application of the ratio could also provide essential benefits for the longitudinal evaluation of muscle strains during the recovery phase and thus improve the prediction of the recovery interval and reduce the risk of recurrence.

Despite our very promising results, there are some limitations to our study. All patients were scanned within 1 week after the injury; however, DTI/fibre-tracking metrics may change quite quickly (e.g. inflammation may occur in a few days). Thus, a more standardized recruitment (i.e. a fixed number of days after the injury for all patients) may be beneficial, especially for entire muscle analyses. Despite the evidence that in volunteers different ranges of DTI metrics values occur in different muscles [15, 16], in the present study separate analyses according to the injured muscles were not performed, because of the low number of examined patients. Future studies including larger patient populations should focus on muscle-specific analyses to provide even more accurate results. Nevertheless, normalization will certainly also reduce such differences between muscle groups.

Finally, the quite long acquisition time (i.e. ca. 8 min) might represent a limit with very extensive lesions, since motion artifacts may occur. However, recent developments in simultaneous-multi-slice (SMS) DTI have translated into ~threefold acceleration of clinically available DTI sequences [43]. SMS was not yet implemented into our STEAM-DTI sequence when our study was performed, but future studies aiming for larger FOVs should directly benefit from this new technology.

In conclusion, STEAM-based DTI allowed a precise assessment of the injured fibres in athletes especially when a ratio between the injured and the contralateral muscles was applied. Aiming to improve the current imaging-based classification of muscle tears and to increase the accuracy of the therapeutic and prognostic management of injured athletes, future studies including a larger population and evaluating muscle tears, also during follow-up, are necessary.