Elsevier

The Veterinary Journal

Volume 194, Issue 3, December 2012, Pages 338-342
The Veterinary Journal

Tendon structure changes after maximal exercise in the Thoroughbred horse: Use of ultrasound tissue characterisation to detect in vivo tendon response

https://doi.org/10.1016/j.tvjl.2012.04.024Get rights and content

Abstract

Investigations into the response of the superficial digital flexor tendon (SDFT) of the Thoroughbred horse to mechanical stimuli have been limited to in vitro cell culture studies focused primarily on gene expression of critical matrix proteins. It is uncertain how well in vitro outcomes translate to the tendon of the horse during exercise. The current study examined changes in tendon structure in response to maximal exercise using ultrasound tissue characterisation (UTC) to scan the SDFT prior to and after competitive racing. UTC uses contiguous transverse ultrasound images to assess the dynamics of the echopattern, which has a close relationship with changes in the 3-D ultra-structure of the tendon.

Using UTC, it was possible to detect subtle changes in the dynamics of the echopattern, with a reduction in pixels that represent aligned and integer collagen tendon bundles on days 1 and 2 post-race when compared to pre-race (P < 0.05). The echopattern of these tendons returned to baseline on day 3. This change in echopattern was not seen in control horses. It was concluded that short-term changes in the SDFT following maximal exercise could be detected using UTC.

Introduction

The superficial digital flexor tendon (SDFT) of the horse accounts for the majority of tendon injuries, reduces performance, requires prolonged recovery periods and predisposes to re-injury. Reported injury incidence ranges from 0.58–9.1 tendon injuries per 1000 race starts (Wilson and Robinson, 1996, Williams et al., 2001, Pinchbeck et al., 2004, Lam et al., 2007), although these figures may be an under-estimate as they only account for injuries that occur during a race meeting. Kasashima et al. (2004) reported that 11% of Thoroughbreds suffered from tendon injury during their career and this may also be an under-estimate as post mortem studies have reported pathological tendon lesions in 26.1% of the sample population (Webbon, 1977).

Horses with a tendon injury can require expensive interventions with up to 12 months to recover, and even then may not return to their previous level of racing (Marr et al., 1993, Smith and Webbon, 2005, Fortier and Smith, 2008). What predisposes some horses to SDFT injury is unknown and research into understanding how the tendon responds to mechanical stimuli is limited.

Molecular biology techniques (e.g. cell culture, microdialysis) have demonstrated that the tendon responds to both loading and stress deprivation (Langberg et al., 2001, Skutek et al., 2001, Lavagnino and Arnoczky, 2005). Research in both human and animal tendon indicates that changes in the expression of matrix proteins and enzymes, such as cytokines, matrix metalloproteinases, collagen and proteoglycans, are critical to this process (Langberg et al., 1999, Langberg et al., 2001, Skutek et al., 2001, Hosaka et al., 2005, Lavagnino and Arnoczky, 2005). However, it is difficult to translate these findings to determine how the in situ tendon reacts to mechanical stimuli.

Ultrasonography (US) is a valuable diagnostic tool for clinicians as it is non-invasive, portable and provides images of tendon structure. The size and structure of the tendon can be assessed qualitatively or (semi)quantitatively (Genovese et al., 1986, Smith et al., 1994, Avella et al., 2009), and echogenicity can be quantified with first-order grey level statistics. US has been used to assess the response of the tendon to long-term exercise. Avella et al. (2009) scanned 263 event horses over two seasons and reported no changes in cross sectional area (CSA) of the SDFT, with similar results observed in other studies (Birch et al., 1999). In contrast, Gillis et al. (1993) performed analysis on first-order grey-level statistics of ultrasound images and tracked echogenicity over a 4 month training period; they noted a trend for decreased echogenicity possibly due to changes in the tendon structure and composition. This study used skeletally immature horses and its application to the adult equine athlete is questionable as mature SDFTs may have a decreased capacity to adapt to mechanical stimuli (Stanley et al., 2007, Smith and Goodship, 2008).

Comparison of echogenicity between serial US scans is difficult as minor changes in amplifier gain, transducer tilt and displacement affect the repeatability (van Schie et al., 1999, van Schie et al., 2000). Ultrasound also has limits of resolution as every US image is a mixture of structural reflections and interfering echoes so only relatively large structures, like secondary tendon bundles (fasciculi), generate reflections, while smaller entities, such as fibrils and cells, will result in interference, each with their specific dynamism in real-time US (van Schie and Bakker, 2000, van Schie et al., 2001). The dynamism of echopatterns over contiguous images is strongly related to changes in the 3-D ultra-structural integrity of tendons, but this is not captured in still 2-D US images.

Ultrasound tissue characterisation (UTC) was developed to address these limitations and to standardise instrumental settings and collection of transverse US images at even distances to create a 3-D ultrasound data-block. In this block, UTC-algorithms quantify the dynamics of echopatterns over contiguous images by intensity and distribution of relative grey levels of corresponding pixels. UTC is based on the close relationship between dynamics of echopatterns and 3-D ultra-structure of collagenous matrices with histomorphology of the tendon tissue specimen as reference (van Schie et al., 2003). As a consequence of standardised data-collection and analysis routines, UTC has shown a high intra- and inter-observer reliability and subtle changes over serial scans can be detected with high reproducibility (van Schie et al., 2010). Previously it has been used for monitoring the progression of tendon lesions and for objective evaluation of repair processes in response to various treatments (van Schie et al., 2009, Bosch et al., 2011).

The aim of this study was to evaluate the short-term tendon reaction in response to maximal exercise (competitive flat racing) by quantifying tendon structure using UTC. We hypothesised that a tendon response to exercise will be detected by UTC when compared to a group of control horses.

Section snippets

Horses

Thirteen Thoroughbred horses (9 males, 4 females; mean ± SD age 3.8 ± 0.6 years) currently in full race training were recruited from a single racing stable and were at the time of the study in full race training. The horses varied in previous race experience (mean ± SD race starts 4.3 ± 3.1) and had not participated in a race during the week before the first scan (previous race start ranged from 1 to 37 weeks with three horses previously un-raced). Horses had neither signs of lameness nor

Results

All tendons scanned prior to racing were normal on grey scale ultrasound and no changes in grey scale ultrasound were seen over the 3 days subsequent to the race. In particular, no focal hypoechoic lesions within the SDFT or clinical signs of tendon injury (i.e. swelling, heat and pain on palpation) were observed throughout the data collection period in both the race and control group. Using UTC, no significant difference was observed between the race and control groups in the proportion of all

Discussion

Since injury to the SDFT is an overuse injury, understanding how the tendon responds to exercise is important. Tendon injuries occur primarily during or after high intensity training or competitive racing (Singer et al., 2008) and the response of the in situ tendon to maximal exercise has not been investigated previously. In this study, significant differences in the echopattern of the SDFT were observed in the race group of horses.

UTC quantifies the dynamics of echopatterns by means of

Conclusions

A short-term response in the structural integrity of the in situ tendon occurred in response to maximal exercise and the tendon responded maximally at 48 h post-race. Future studies should examine the exact nature of the extracellular changes responsible for the decrease in structural integrity post-race. Understanding these concepts may allow for the design of optimal exercise and training schedules and for screening methods to detect early or impending tendon injuries and hence reduce the

Conflict of interest statement

Dr. van Schie developed the UTC imaging used in this study and is a director of the imaging company. He provided support and guidance in the development of the methods and interpretation of the results but the data were collected and analysed without Dr. van Schie’s input and he did not influence the study findings in any way.

Acknowledgements

The authors would like to thank the staff at MC Kent Racing, especially Michael Kent, for access to horses and assistance during ultrasound imaging. This paper was supported by the Australian Centre for Research into Sports Injury and its Prevention, which is one of the International Research Centres for Prevention of Injury and Protection of Athlete Health supported by the International Olympic Committee (IOC).

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