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Significance of Asymptomatic Tendon Pathology in Athletes

Splittgerber, Lauren E., MD; Ihm, Joseph M., MD

Current Sports Medicine Reports: June 2019 - Volume 18 - Issue 6 - p 192–200
doi: 10.1249/JSR.0000000000000600
Training, Prevention, and Rehabilitation/Section Articles
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Symptomatic tendinopathy can be a disabling condition for athletes. Common sites of tendinopathy in athletes include the rotator cuff (RTC), Achilles, and patellar tendons. Advanced imaging modalities, such as magnetic resonance imaging and ultrasound occasionally identify tendinopathic changes in asymptomatic individuals. Such asymptomatic changes have been documented in the RTC, Achilles, and patellar tendons of athletes. In the RTC, tendinopathy, partial-, and full-thickness tears have been demonstrated in asymptomatic athletes, though only small numbers of these athletes may develop symptoms despite prolonged periods of ongoing, competitive play. In the Achilles and patellar tendons, neovascularization, hypoechogenicity, and tendon thickening are commonly noted findings in asymptomatic athletes, and though all have been associated with tendon pain in the literature, there is some inconsistency as to which are the strongest predictors of future tendon pain. Evidence on how best to address or intervene upon such asymptomatic changes is limited.

McGaw Medical Center of Northwestern University/Shirley Ryan AbilityLab, Chicago, IL

Address for correspondence: Joseph M. Ihm, MD, Shirley Ryan AbilityLab, 355 E. Erie Street, Chicago, IL 60611; E-mail: jihm1@sralab.org.

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Introduction

The development of symptomatic tendon pathology can be a serious and disabling condition for athletes at various levels of play across multiple sports. Decreased athletic performance and significant time lost from sport may result from symptomatic tendon pathology, and in some cases, such an injury is career-ending (1–3). Tendon pathology is common among athletes, with certain populations of athletes being at risk for injury at particular sites. Frequent sites of tendinopathy among athletes include the rotator cuff (RTC) tendons, the Achilles tendon, and the patellar tendon. Overhead athletes, such as baseball, tennis, and volleyball players, are predisposed to shoulder injuries, including injuries to the tendons of the RTC (4,5). Athletes who participate in jumping sports, such as basketball and volleyball, have a high incidence of symptomatic patellar tendinopathy (often termed “jumper’s knee”), with estimates as high as 45% in volleyball players and 32% in basketball players (6). Achilles tendinopathy is a commonly reported overuse injury among athletes involved in sports requiring extensive running (7,8).

Advanced imaging modalities, particularly magnetic resonance imaging (MRI) and ultrasound (US), allow for visualization of multiple soft tissue structures, including tendons. The diagnostic accuracy of US and MRI has been found to be high for full-thickness tears of the RTC, with comparable specificity and slightly lower sensitivity among both imaging modalities for diagnosing partial-thickness tears and tendinopathic changes (9). For diagnosis of patellar tendinopathy, US may be more sensitive than MRI, though the two imaging modalities have demonstrated equivalent specificity (10). For the Achilles tendon, both MRI and US have adequate sensitivity to detect pathology when interpreted by an appropriately qualified and experienced clinician (11).

With the frequent use of such imaging modalities to diagnose musculoskeletal conditions in athletes, tendon changes may be found incidentally on advanced imaging. Indeed, the presence of tendon changes in asymptomatic individuals, including athletes, is well documented in the literature (12–14). Such findings raise the question of what constitutes true pathology and creates the challenge of how to best determine the significance of tendon changes when they are noted on imaging, particularly in the absence of symptoms localized to the tendon. However, the presence of asymptomatic changes in tendon morphology on imaging also has stimulated interest in the possible clinical utility of such changes, particularly with regard to prevention of future injury or pain. Given the significant morbidity associated with the development of symptomatic tendon pathology among athletes, the ability to predict or even prevent the onset of symptomatic tendinopathy would be a useful tool for the sports medicine clinician.

This article will review studies investigating asymptomatic tendon changes found on imaging in athletes, focusing on common sites of tendon pathology: the RTC, the Achilles tendon, and the patellar tendon. In addition to identifying patterns of asymptomatic tendon findings, this article will try to determine whether any of these findings can be applied clinically to better identify athletes at risk for the development of symptomatic tendon pathology. It also will assess if there are interventions that can reduce the risk of morbidity and time lost from sport in the event that asymptomatic tendon changes are found on imaging.

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RTC Tendons

The RTC tendons of asymptomatic individuals, both athletes and nonathletes, have been shown in numerous studies to display tendinopathy and associated findings on imaging modalities including MRI and US. Among nonathletes, multiple studies have shown that there is an association between increasing age and the presence of partial- and full-thickness RTC tears (15–17). Despite the increasing prevalence with age, many of these individuals may remain asymptomatic with preserved function (12).

Studies that have followed nonathlete populations with known RTC tears over time have found that some subjects who were initially asymptomatic go on to develop shoulder pain. One factor that may influence the potential for symptom development is enlargement of an existing tear. Yamaguchi et al. (15) found that enlargement in tear size may predispose to symptom onset, with 50% of subjects who developed shoulder pain showing enlargement of tear size, compared with tear enlargement in only 22% of subjects who remained asymptomatic. Similarly, Mall et al. (18) found that the development of shoulder pain was significantly correlated with progression of RTC tear size over a 2-year period, while subjects who remained asymptomatic demonstrated no significant change in tear size. However, what particular tear size or degree of enlargement is needed before symptoms develop is unclear.

Among athletes specifically, the presence of imaging findings consistent with tendinopathy, partial-, and even full-thickness tears in asymptomatic individuals is well documented (5,19–21), with the dominant shoulder of athletes who participate in asymmetric overhead sports often being more likely to develop changes on MRI (22,23). As can be seen in Table 1, these studies often have few participants and are heterogeneous. Some studies assessed asymptomatic individuals at only one point in time, while others followed athletes over a period of time to see if symptoms developed. Some studies obtained follow-up imaging, while others used only a baseline imaging study and followed the athletes clinically to see if symptoms developed.

Table 1

Table 1

Baseball pitchers are one population of particular interest given the extreme stresses placed on the shoulder during repetitive, high velocity throwing. One factor that may contribute to increased risk of tendinopathy and RTC tears in the throwing shoulder is internal impingement that occurs in the late cocking phase of throwing (23,26). Consistent with this risk factor, articular-sided tears of the supraspinatus and infraspinatus have been found frequently in asymptomatic pitchers (5,21). Studies following asymptomatic throwing and overhead athletes over time, however, have found that a majority do not develop symptoms, even during follow-up periods of up to 5 years of ongoing, competitive play (5,19,24). Following an athlete's retirement from sport, one study found that MRI findings consistent with tendinopathy and partial-thickness tears did not progress to full-thickness tears in any athletes, and occasionally, some of these findings may even resolve in some individuals on repeat imaging years after retirement from sport (25).

In summary, asymptomatic RTC changes are not uncommon among overhead and throwing athletes, but from the studies available, there is no consistent finding that predicts the development of future symptoms even though many asymptomatic athletes have changes that have historically been considered pathologic. Given the small number of subjects in these studies, larger studies with longer follow-up will be useful in determining if these findings predict injury, pain, or functional limitations later in life.

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Achilles Tendon

Asymptomatic abnormalities in the Achilles tendons of athletes also have been well documented in the literature (27–29). Many of these studies utilize US as the imaging modality of choice, and asymptomatic changes that have been noted on US examination of the Achilles tendon include tendon thickening, areas of hypoechogenicity, and neovascularization, the latter of which is most commonly assessed using Doppler US. As outlined in Table 2, there is some inconsistency in the literature for all three of these asymptomatic findings regarding which have been found to be risk factors for the development of symptoms localized to the Achilles tendon.

Table 2

Table 2

The role of neovascularization, in particular, in the pathogenesis and symptomatology of tendinopathy has been debated in the literature. Early studies using Doppler US found strong associations between the presence of neovascularization and the presence of Achilles tendon pain (36,37). Such results generated support for the notion that neovascularization may play a role in the development of tendon pain. However, not all studies investigating asymptomatic US findings have found neovascularization to predict tendon pain (28), and other studies (30,31) have questioned the concept that all intratendinous Doppler flow is pathologic, suggesting that at least some component of tendon hyperemia may be a physiologic response to exercise, particularly that which involves tendon loading. However, further investigation into preexercise and postexercise tendon blood flow found that most tendons demonstrating increased blood flow postexercise were rarely otherwise normal in morphology, with most hyperemic tendons also displaying other structural abnormalities on US (32). Furthermore, a large, prospective study of long-distance runners identified several predictors of Achilles tendon pain, the strongest of which was neovascularization in the Achilles tendon on a screening US at the beginning of the study, which conferred a nearly sevenfold increased risk of developing midportion Achilles tendon symptoms at 1-year follow-up (27). Other tendon findings in this study, such as spindle-shaped areas of thickening and hypoechoic defects, were not clear risk factors in this population of runners.

In addition to the use of power Doppler US to detect neovascularization in tendons, contrast-enhanced US (CEUS) also can be used for this purpose as it makes use of microbubble contrast agents to help visualize blood flow and tissue perfusion (38). CEUS is a newer imaging modality being used to investigate neovascularization changes in tendons and may be more sensitive for the detection of neovessels than power Doppler US (33). One study utilizing CEUS found that runners with a history of contralateral Achilles tendon rupture demonstrated significantly increased neovascularization in the uninjured tendon on CEUS (but not on Doppler US) compared with controls who had no history of tendon pathology. Given evidence that an Achilles tendon rupture may increase the risk of rupture in the contralateral tendon (39), these results could indicate early pathologic changes in an as-yet uninjured tendon, however, such a determination would require additional follow-up as all participants in this study were asymptomatic at the time of scanning.

Thus, while some component of intratendinous vascularity may be physiologic, when noted incidentally in asymptomatic athletes, neovascularization may still be considered a risk factor for future symptom development.

The presence of neovessels in the Achilles tendon is not the only feature in asymptomatic tendons that has been associated with the development of Achilles tendon pain. Alterations in the tendon's structure also have been noted in asymptomatic athletes, with US studies showing areas of hypoechogenicity (29) and tendon thickening, particularly when spindle-shaped (14), as being associated with the development of pain in other populations of athletes as well.

The implications of structural changes in asymptomatic tendons also have been investigated with US tissue characterization (UTC), which is a newer technique that was developed in an effort to quantify tendon integrity in a reliable manner (40–42). With the UTC technique, US images are compiled into a three-dimensional block that is then analyzed and classified into one of four echo types (I-IV) based on a validated algorithm that assesses tissue integrity according to varying degrees of fibrillar organization in the tendon. While UTC is currently not widely used in the clinical setting, it has been used in the research setting recently as an attempt to better characterize and quantify some US findings.

One recent study (34) utilizing the UTC technique found that abnormal Achilles tendons (i.e., those that displayed areas of hypoechogenicity and/or tendon thickening on regular, grayscale US) demonstrated similar to greater mean cross-sectional areas of normal, aligned fibrillar tendon structure (echo Types I and II) on UTC compared with normal tendons despite the presence of concomitantly increased mean cross-sectional areas of disorganized tissue (echo Types III and IV) in the abnormal tendons. Furthermore, mean cross-sectional area of aligned fibrillar structure was not significantly associated with tendon symptoms. These findings were taken as a possible counterpoint to the idea that tendon symptoms develop when (presumed) structural compromise of a tendon overwhelms the tendon’s ability to bear load, as even abnormal tendons with large areas of disorganization appeared to have sufficient quantities of appropriately aligned, weight-bearing structure. This could indicate that tendon thickening represents a compensatory response by a stressed tendon wherein the amount of structurally intact tendon tissue is increased to better tolerate load in the presence of areas of disorganization, although further studies will be helpful to confirm such findings using this new imaging technique.

In summary, while a variety of morphological changes have been seen on US examinations of the Achilles tendon in different populations of athletes, certain findings are noted more commonly, including neovascularization, tendon thickening, and hypoechogenicity. Among these three findings, neovascularization may be one of the stronger predictors for the development of tendon symptoms, although hypoechogenicity and spindle-shaped thickening also have been associated with the development of Achilles tendon pain in athletes. The variability in all three of these findings as predictors for future tendon symptoms indicates that caution is necessary in relying on any one as the sole basis for counseling and managing an athlete who demonstrates such asymptomatic findings.

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Patellar Tendon

Similar to the Achilles tendon, most studies assessing the patellar tendons of athletes have utilized US and power Doppler to assess for tendon changes such as thickening, hypoechogenicity, and neovascularization. Populations of interest for assessing the patellar tendon include athletes who participate in sports requiring repetitive jumping, such as basketball and volleyball. As shown in Table 3, multiple studies have found that patellar tendon changes are not uncommon in asymptomatic athletes (13,35,43).

Table 3

Table 3

When structural changes and neovascularization are absent on US examination of the patellar tendon, asymptomatic athletes appear to be at low risk to develop patellar tendon pain even during up to 3 years of ongoing, competitive play (44). When structural changes are noted, not all studies have shown an association between these changes and the development of tendon pain (13), although most have found some association between the presence of tendon changes on US and the development of tendon symptoms (29,35,45). Several studies have found that the presence of hypoechoic defects in athletes is associated with the development of patellar tendon pain (35,45). One of these studies (45) also included a longitudinal assessment of the evolution of structural tendon changes such as hypoechogenicity and thickening. While changes in sonographic appearance were unlikely overall during the 5 months tendons were followed (particularly among tendons that were normal or demonstrated focal hypoechogenicity), certain patterns did emerge among tendons whose appearance changed during the study period. Even though this involved only a small number, tendons that were initially normal were more likely to develop diffuse thickening than a focally hypoechoic area. Tendons that already had a focal area of hypoechogenicity were more likely to change to a diffusely thickened appearance rather than to return to a completely normal appearance (i.e., no hypoechogenicity, no thickening). From these results, it was hypothesized that diffuse tendon thickening may represent a transitional US finding on a continuum between normal sonographic appearance and a potentially more pathologic state in which the tendon displays focal hypoechogenicity, at which point it is more likely to be associated with pain (45).

A recent UTC study (34), discussed previously in relation to the Achilles tendon, also looked at the patellar tendons of its population of athletes. As in the Achilles tendon, findings in patellar tendons that were considered to be abnormal on greyscale US demonstrated an increase in the mean cross-sectional area of normal, aligned fibrillar tendon structure on UTC. These tendons also displayed concomitant, significantly increased areas of disorganization compared to structurally normal tendons. Similarly to the Achilles tendons in the study, the mean cross-sectional area of aligned fibrillar structure of the patellar tendon was not associated with pain, again leading to the hypothesis that overall tendon thickening may be a compensatory feature of some tendons in response to the repetitive loading of sports play.

In addition to hypoechoic defects and tendon thickening, neovascularization has been associated with painful tendons in several studies (46,47). Patellar tendons with neovascularization may not always have observable blood flow within the intratendinous vessels, as one study found that some tendons had only intermittently detectable blood flow (46). Tendons with persistent Doppler blood flow demonstrated longer vessels than those with intermittent Doppler flow, and though both tendons with persistent and intermittent blood flow reported pain, pain intensity was higher among individuals with persistent blood flow compared to those with intermittent blood flow. Thus, both the presence of neovascularization as well as the degree of vascularity (including both the persistence of blood flow and the length of the blood vessels) may have an association with patellar tendon pain.

In summary, the patellar tendon has been shown to display sonographic changes in asymptomatic athletes, particularly those who participate in sports requiring jumping. These changes include neovascularization, focal areas of hypoechogenicity, and tendon thickening, and all of these findings have been associated with pain. Since athletes without structural changes or neovascularization appear unlikely to develop tendon pain over the course of several years of ongoing play (44), the presence of any of these asymptomatic changes could put an athlete at risk for future tendon pain. Focal hypoechogenicity, in particular, may be one of the stronger risk factors for the development of patellar tendon pain and may merit special consideration when found in an asymptomatic athlete (29,45). With regard to tendon thickening, there is some evidence to suggest that this finding may represent a transitional or compensatory state in the setting of repetitive tendon loading and stress (34,45).

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Clinical Applications for Asymptomatic Tendon Abnormalities

As outlined in the above sections, there is ample evidence in the literature to support the presence of tendon changes in athletes across multiple sports at varying levels of play who remain asymptomatic. Such evidence underscores the importance of clinical context when interpreting MRI and US examinations performed on athletes to avoid misinterpretation of asymptomatic tendon changes that could lead to inappropriate treatments or loss of playing time. Nonetheless, asymptomatic imaging findings can still raise significant levels of concern for the possibility of future symptoms or injury, and a challenge thus arises in trying to determine how to address such findings to protect the health of the athlete’s tendon while still maximizing his or her ability to participate in his or her chosen sport(s) at the highest level possible.

Among overhead and throwing athletes, MRI findings suggestive of tendinopathy or even identification of partial- and full-thickness tears of the RTC tendons have been documented in asymptomatic athletes (5,19). While aspects of overhead and throwing sports may place these athletes at increased risk of injury to the RTC tendons, characteristic imaging findings in samples of these athletes have shown that these findings may not be associated with symptoms. Furthermore, the risk of developing RTC pain in the presence of asymptomatic imaging findings appears to be small, even over a period of up to 5 years of ongoing, competitive play (19). Though multiple studies in nonathlete populations have identified RTC tear progression as a risk factor for the development of pain in a previously asymptomatic individual (16,18), limited evidence with follow-up imaging in athletes has suggested that asymptomatic RTC tendinopathy and partial-thickness tears may not progress to full-thickness tears even with a follow-up period of up to 6 years (25).

Asymptomatic tendon changes in the Achilles and patellar tendons are prevalent in athletes, with runners and soccer players being among those who show changes in the Achilles tendon (14,27), while patellar tendon changes are common among asymptomatic basketball and volleyball players (43,46). One factor that seems to have a strong association with pain in both the Achilles and patellar tendons is neovascularization. Multiple studies have found that the presence of neovessels in tendons is associated with pain in symptomatic populations (36,46,47), and among asymptomatic populations of athletes, the presence of neovessels may be a risk factor for the presence or development of tendon pain (27). Despite some debate in the literature (28,30), in the Achilles tendon in particular, neovascularization may be the US finding that conveys the strongest risk of future tendon pain, with one study showing a nearly seven-fold increased risk of pain development in asymptomatic tendons that displayed neovascularization (27). It remains notable that not all studies have found this association (28), so caution must be maintained when interpreting the significance of such incidental findings in an athlete.

Of the other changes that have been noted on US, focal hypoechogenicity seems to be one of the stronger risk factors for pain development in the patellar tendon (29,45), though again, not all studies have demonstrated this (13). Within the Achilles tendon, there also is some evidence that areas of focal hypoechogenicity may be a risk factor for development of pain (29), though this may not be as significant a risk factor for symptom development as neovascularization (27).

A discussion regarding the significance of Achilles and patellar tendon thickening is interesting in that some studies (34,45) have suggested that thickening may represent a transitional state or adaptive response by the tendon. Nonetheless, there also is some evidence that tendon thickening is associated with the development of tendon pain in some populations (14,28,35), but these findings are inconsistent with other studies (29). With this in mind, tendon thickening may be seen as an indicator that a tendon is under stress from repetitive loading, but why some thickened tendons seem to compensate for this stress and remain asymptomatic while others go on to develop pain remains unclear.

In conclusion, given the apparent limited clinical significance of asymptomatic RTC tendon findings and the inconsistency of the predictive value of various asymptomatic imaging changes seen in both the Achilles and patellar tendons, care should be taken to avoid ordering unnecessary imaging studies, and using imaging studies as a screening tool to assess the health of tendons in asymptomatic athletes should be limited or discouraged.

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Considerations in Treating Asymptomatic Tendinopathy in Athletes

As discussed above, though several asymptomatic findings have been associated with subsequent development of tendon pain, the question still remains as to how to address such findings if identified in an athlete. In cases of symptomatic Achilles tendinopathy, eccentric exercises are well established treatments (48–50); in cases of symptomatic patellar tendinopathy, eccentric protocols also have been shown to have some benefit (51,52). Given these results in symptomatic populations, it would seem intuitive that eccentric strengthening protocols could be used in asymptomatic populations who are at risk for the development of Achilles and patellar tendon pain.

Though there are limited studies that assess treatment protocols for those with asymptomatic tendon findings, Fredberg et al. (53) conducted a large, randomized controlled trial that examined the efficacy of a prophylactic eccentric training and stretching program on the Achilles and patellar tendons. A total of 209 initially asymptomatic professional soccer players were followed over a 12-month period, with randomization into the study group, which performed the prescribed eccentric training and stretching protocol, or the control group, which did not perform an eccentric protocol as part of routine training. At the conclusion of the season, the eccentric training program was found to reduce the frequency of US abnormalities in the patellar tendon, but not in the Achilles tendon. However, the eccentric training protocol did not reduce the risk of onset of pain in either the patellar or Achilles tendon, and in fact was found to increase the risk of pain among players with preseason patellar tendon changes on screening US.

Interestingly, then, the current, limited evidence suggests that not only are prophylactic eccentric protocols not effective for the prevention of injury to the Achilles tendon, it seems that such protocols could even be detrimental in the setting of asymptomatic patellar tendon changes (53). Given the efficacy of rehabilitation programs in the treatment of symptomatic tendinopathy, more research is needed before this question can be answered completely, and a challenge remains regarding how best to counsel and manage asymptomatic athletes with imaging findings that may be risk factors for the development of tendon pain.

With some question of whether or not specific exercise programs can be used to prevent tendon pain from developing in the presence of asymptomatic tendon changes, one alternative strategy could involve evaluating the athlete for other, potentially modifiable risk factors to optimize other conditions for tendon health. This may include correction of certain extrinsic risk factors such as training errors, with adjustments that may include optimization of technique in certain tendon-loading activities like jumping or landing mechanics (54), or adjustments to the volume of training (55).

Other intrinsic factors also may play a role in the development of tendinopathy. Genetic risk factors have been implicated by a number of studies, and while these are not modifiable risk factors, a number of other intrinsic risk factors may be targets for intervention, such as muscle inflexibility, joint laxity, and decreased strength (56). Weight and body composition also have been associated with tendon injuries, and the association of adiposity with tendon pathology has been thought to be possibly due to the influence of low-grade inflammation on the tendon that may be present in individuals with increased amounts of adipose tissue (57,58). Though many athletes may not traditionally be thought of as having excess adipose tissue, those who are identified as having significant adiposity or other factors related to metabolic syndrome should be counseled about lifestyle modifications as a way to possibly decrease risk of tendon injury or development of symptoms.

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Conclusion

Asymptomatic changes are commonly seen in the tendons of athletes, with certain populations of athletes being at risk for morphologic changes and pain at particular sites, which may be related to the unique demands of the athlete’s particular sport or some other intrinsic or extrinsic risk factor. While many abnormalities noted in the RTC tendons of overhead and throwing athletes appear to remain largely asymptomatic over extended periods, certain findings in the patellar and Achilles tendons among other groups of athletes, especially jumping and running athletes, respectively, may predate the development of tendon symptoms in some individuals, although there remains some inconsistency in the literature as to which asymptomatic tendon changes may best predict future symptom development. As with many musculoskeletal injuries, there are likely multiple environmental factors that will play a role in the development of pain, with imaging findings being only one aspect to consider.

While the identification of asymptomatic findings in athletes’ tendons may provide some insight, strong evidence as to how to prevent the development of symptoms in the presence of these findings is not yet robust. As the predictive value of asymptomatic findings remains limited, care should be taken to avoid unnecessary imaging to assess asymptomatic tendons when possible. If such asymptomatic tendon changes are noted incidentally on imaging, any decision to intervene before symptoms develop should be carefully considered with regard to the athlete’s unique athletic goals, clinical situation, and health. In many cases, it may be most appropriate to educate the athlete on what the asymptomatic findings imply and recommend close observation to monitor for any future symptom development so as to provide timely, early interventions when clinically appropriate.

The authors declare no conflict of interest and do not have any financial disclosures.

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