To our knowledge, the present study is the first to report changes in morphological parameters based on ultrasound imaging before and after a prolonged ski mountaineering racing. Changes in tendon thickness, CSA, and echogenicity revealed an immediate response of the tendon to acute loading. These findings provide further evidence of the behavior of the tendon during loading, particularly, its ability to react immediately to a high-intensity training stimulus.
Ski mountaineering is a high-impact sport that engages the entire musculoskeletal system. In particular, the AT, which is involved in the steep ascending phase, is put under tension from repetitive ankle-knee movements. This repetitive loading pattern could induce an acute response of the tendons, which seems to be attributed more to the load magnitude and contraction intensity than to the type of contraction [8
]. The present study showed a significant reduction in tendon thickness and CSA between the pre-race measurement and each of the three post-race evaluations.
In a previous evaluation of AT thickness during eccentric and concentric exercises in healthy participants [11
] and various in vitro studies, [21
] cyclic loading has been proposed to exude water from the tendon with a consequent decrement in tendon dimensions. Whereas the water content present in the core of the tendon moves toward the peritendinous space [24
Our findings are in line with previous studies and tendon gray scale values are consistent with those of the morphological parameters, showing increased levels for the dominant, and for the non-dominant leg. (Table 1
Tendon images showed a brighter internal pattern when subjected to a high-intensity load, compared with pre-race measurements. This brightness of the B-mode image could be related to the reduced water content within the tendon, as fluids in ultrasound images appear darker than connective tissues. This water movement can be attributed to the realignment and stretching of collagen fibrils during mechanical loading [11
]. The increased compressive force within the tendon and reduction of the interfibrillar space generate fluid movement outside of the tendon as a consequence of positive hydrostatic pressure.
Similarly, the present study showed a significant reduction in the CSA of the AT, confirming that repetitive loading can exude water from the tendon, and even the CSA is affected by this change in water content. Previous studies have reported an unchanged AT CSA after running or passive stretching [26
]; however, in the present study, the athletes were subjected to a prolonged race with a comparatively higher tendon stimulus. Moreover, in the recent systematic review of Bohm et al., [8
] the authors suggest that material properties of tendons (i.e., stiffness and Young’s modulus) react earlier to loading compared to morphological properties (i.e., CSA). However, in that systematic review, the immediate effect of loading was not evaluated, and early tendon changes are considered to occur after 8–12 weeks of intervention.
Tendon structure and properties differ across the body. Given the wide range of functional requirements during human movement, morphology and behavior can vary between tendons. The. PT is shorter and stiffer than the AT even if both are mainly designed for the storage and release of elastic energy [28
Although some studies have reported a difference in the stiffness and CSA of the PT after resistance training, [6
] there is a paucity of literature evaluating the changes in morphological parameters induced by acute exercise.
The load applied to the quadriceps muscle-tendon unit, and more specifically, the PT, during downhill ski sports (i.e., alpine skiing and ski mountaineering) is mostly due to the necessity to maintain a flexed-knee position and modify the knee angle during different trajectories [20
]. An acute response of the tendon tissue could be present, given the amount of strain generated during the downhill period, in which complete stress relief of the PT is not possible, owing to the absence of an unloading phase, as occurs in other more cyclic physical activities.
In the present study PT thickness and CSA were unchanged immediately after the races. Conversely, gray scale values of the PT showed a significant increase between the pre-race measurements and the end of the third race. The morphological properties of the PT were unchanged after the 3 days of racing, indicating a difference in its behavior in comparison to the AT.
Owing to the differences in function and type of loading during the activity, the stimulus induced by ski mountaineering was not sufficient to elicit changes in PT thickness and CSA. Hypertrophy of the PT following years of training in specific sports and in response to high-intensity, resistance training has been shown [6
]. In contrast, no change in the morphological properties of the PT has been reported after alpine skiing training of 12 weeks [20
]. The differences between studies could be attributed to the behavior of the tendon, which undergoes changes only when a certain load threshold is overcome.
In the present study, the load applied to the tendon was probably not high enough to enable a morphological acute response in comparison to the high-intensity training proposed in previous studies [7
]. Moreover, hypertrophy of the PT seems to occur in a specific region of the tendon as opposed to its entire length. Hypertrophy has been observed, especially near the osteo-tendinous junction [7
]. In the present study, the central part of the tendon was evaluated. Any possible change in the morphological properties of the PT away from the evaluation site could have been missed following this measurement protocol. However, we cannot rule out any PT response within the measurement error of the US imaging.
A significant difference was observed in the echogenicity of the PT. As reported for the AT measures, the gray scale levels were increased after each of the three races, showing a change in the internal pattern of the tendon. Similar to the AT, an increase in gray levels resulting in a “brighter” tendon is likely related to the movement of fluid from within the core of the tendon to the peritendinous space. A previous study, [13
] using a slightly different methodology to evaluate the PT echogenicity, showed a similar increase in gray scale values after a squatting exercise session. Although this phenomenon in the PT are less described in the literature, changes in the internal pattern of the PT possibly occur prior to morphological changes. These early changes in material properties, without morphological changes, could be attributed to changes in the alignment of collagen fibers, loss of collagen crimping, [29
] and the cellular response [30
] due to loading.
Moreover, is important to remark that given the PT is less exposed to sliding and friction load compared to AT, the extent of peritendinous structure and the fluid present between the paratenon and the epitenon are probably reduced. The lack of morphological changes in the PT reported in this study could be related to a minor fluid movement in a tendon where peritendinous structures and fluid are less present. Differences in peritendon extent and size between the two tendons should be further investigated.
The presented study has some limitations that needs to be acknowledge. Reliability of the ultrasound echo intensity technique was evaluated only on AT; no data on PT are available. Ultrasound measurements were obtained at a standardized site in the mid-Achilles and PT; region-specific morphological changes could not have been confirmed by this study. Furthermore, baseline values were taken the day before the start of the three-day race. Due to logistical aspects, the recording of baseline measurements immediately before each of the three races was not possible. We could not have evaluated whether the morphological parameters returned to baseline values after rest; neither could we have excluded a cumulative effect of the different races. Lastly, there is a lack of control group; incidental walking has shown to be sufficient to induce Achilles tendon thickness changes [31
] therefore a control group could have highlighted possible differences between high and low load activities.
The AT and PT of healthy athletes are highly responsive to an acute increase in mechanical load. An exhausting ski mountaineering race seems to reduce the thickness and CSA of the AT, and increase tendon echogenicity. Conversely, the PT showed increased tendon echogenicity without any notable change in morphological parameters. The differences in anatomy and function between the two tendons and the opposite loading patterns of ski mountaineering could explain the differences between their structures during acute loading.
Tendon fluid flow and tendon loading are known to be important to provide nutrition at the tendon and stimulate the remodeling [11
Given the importance of fluid movement in the tendon, it can be speculated that the ability to react to the mechanical load, showing immediate structural and morphological changes, could be the normal behavior of the tendon that protect the structure against the risk of overload.
The sample analyzed in this study had a very high level of training, it could be interesting to evaluate if tendons of persons with a lower level of training, subjected to an acute load, shows the same behavior.
If the importance of the fluid movement as a protective factor to limit tendon overload will be confirmed by future studies, an easy and low-cost technology able to early detect these changes could be helpful to personalize the training load of athletes during the season.