Achilles tendon pain is very common among athletes involved in running and jumping activities as runners, basketball, and soccer players (13,37,42). Despite the high prevalence and the often deleterious consequences of Achilles tendon pain, little is known about the source of pain in this condition. There are many indications that the underlying tendon degeneration starts long before the onset of symptoms and often remains asymptomatic. Cadaver studies revealed a postmortem prevalence of degenerative Achilles tendon changes of 15%–30% (20). Furthermore, spontaneous tendon ruptures mostly occur in people who never had symptoms before (12,19,20). Histopathologically, in these tendons, preexisting degenerative changes are found in almost all cases suggesting a high prevalence of asymptomatic tendinosis (12,20,21).
In vivo, tendon ultrasound has become a commonly used noninvasive procedure to diagnose tendinopathy. In recent years, high-resolution ultrasound examinations have provided evidence of sonomorphological abnormalities of the Achilles tendon in 11%–30% of asymptomatic subjects, it still being unclear whether these are physiological or age- or activity-related adaptation processes or tendon degeneration indicative of a predisposition to clinically manifest tendinopathy (13,15,26,28,30). Especially, the clinical significance of power Doppler blood flow within the tendon remains a matter of debate (16,23,33). Neovascularization, in the beginning, was only identified in degenerated painful tendons so that a direct association with pain was supposed (31,32,38). This was supported by histopathological studies showing nerve fascicles in close relationship to the neovessels (3) as well as by the fact that injections with the sclerosing substance polidocanol, targeting the areas with increased blood flow, gave pain relief (2). However, because neovessels were only found in 47%–64% of symptomatic patients in more recent studies (11,26,35,41,43) and improved ultrasound devices have increasingly yielded evidence of blood flow in tendons of asymptomatic subjects (23,36), the relationship of blood flow and tendinopathy has been questioned. Studies in active athletes recently reported that intratendinous blood flow was dependent on physical activity. In the study of Boesen et al. (6), all badminton players showed Achilles tendon Doppler flow after competing, whereas only 13% had Achilles tendon pain. Hirschmüller et al. (18) found intratendinous blood flow on Achilles tendon power Doppler in more than 30% of asymptomatic long-distance runners, and Malliaras et al. (28) showed abnormality of Achilles tendon Doppler flow in 21% of their examined badminton players. Because Doppler flow was associated with years of badminton competition and hours of weekly competition in their study, they concluded that Achilles tendon Doppler flow may be a response to mechanical load and a sign of asymptomatic tendinopathy rather than an indicator of pain (28). Koenig et al. (23) similarly concluded that intratendinous Doppler activity should not be considered pathological per se because they found evidence of intratendinous blood vessels in all their asymptomatic subjects with morphologically normal Achilles tendons after injection of an ultrasound contrast agent.
Few studies have investigated the prognostic value of abnormal ultrasound findings in asymptomatic Achilles tendons concerning the subsequent manifestation of symptoms (7,13,14). Fredberg and Bolvig (13) identified spindle-shaped thickening of the Achilles tendon as a risk factor for later tendinopathy in elite soccer players. Cook et al. (7,9) found that hypoechoic regions in the patellar tendon were associated with an increased risk of jumper’s knee in elite basketball, netball, football, and cricket players. Controversially, in their 4-yr follow-up study, they did not find a relationship of ultrasonographic patellar tendon abnormalities and clinical outcome (8). The clinical significance of abnormal ultrasound findings in the absence of clinical symptoms is thus still the subject of controversy (23,24). Considering the high incidence of Achilles tendinopathy in running athletes and the often fatal influence on their career, the identification of prognostic factors that are detectable by Doppler sonography seems to be of high clinical interest to potentially prevent the development of symptomatic tendinopathy.
The aim of the present study was therefore to record the Achilles tendon thickness and the vascularization as well as structural abnormalities of the tendon in a large collective of long-distance runners by power Doppler sonography and to evaluate the prognostic value of these parameters concerning the manifestation of midportion tendinopathy (MPT) within a year.
MATERIALS AND METHODS
The study design was a prospective clinical trial. From March 2007 to April 2008, 634 asymptomatic runners were recruited to the study at 23 major national running events. Inclusion criteria were a minimum age of 18 yr, regular running activity, and the absence of Achilles tendon complaints for at least a year. Exclusion criteria included familiar hypercholesterolemia, rheumatic diseases, and a history of Achilles tendon rupture or surgery to the Achilles tendon as well as a history of calcaneal fracture. All subjects took part in the study voluntarily and signed an informed consent form in accordance with the Declaration of Helsinki. The study was approved by the ethics committee of the local university.
After a detailed explanation of the study and signing a written informed consent form, baseline data of the subjects (name, address, phone number, e-mail address, sex, age, height, weight), running-related data (training frequency, intensity and duration, number and results of competitions, record times), and their medical history (actual and previous disorders, injuries, medication and surgery) were documented in preprepared case report forms. Before the subsequent ultrasonographic examination, a resting period of at least 2 h was required to avoid exercise-induced intratendinous blood flow (6,10,18).
For the ultrasonographic examination, two high-resolution power Doppler ultrasonographs (Aplio SSA-770A/80 and Aplio XG SSA-790A; Toshiba, Tokyo, Japan) with 12-MHz multifrequency linear transducers (8–14 MHz) were used. The examination was carried out in a prone position with the feet of the subjects hanging over the edge of the table and ankles passively flexed at 90° and the examiner being blinded to the case history of the subjects (18,39).
The right and left tendons of each subject were scanned in longitudinal and transverse section while the transducer was placed strictly parallel or orthogonal to the fiber direction as previously described (33,35). B-mode abnormalities recorded included spindle-shaped thickening of the tendon, hyper- and hypoechogenicities, and paratenon thickening (B-mode intensification = 80, penetration depth = 3 cm, focus at 0.5 cm). All pathologic findings were documented in longitudinal and transverse section. Subsequently, the diameter of the tendon was measured in the longitudinal section. Therefore, the maximum tendon diameter called “true tendon thickness” (39) was measured at a reference point 3 cm proximal to the calcaneal insertion and at its thickest. The epitenon and paratenon were not included in the measurement. Finally, the tendon was examined for intratendinous microvessels using the broadband power Doppler “advanced dynamic flow” (ADF, Fig. 1; ADF frequency = 10 MHz, pulse repetition frequency = 15.6 kHz, color velocity = 1.2 cm·s−1, color intensity just below the artifact threshold, size of the color box (region of interest, ROI) = 3 cm2 (2 cm × 1.5 cm)). The pressure of the probe was kept to a minimum to avoid obliteration of small vessels (11). Intratendinous power Doppler flow was graded from 0 to 5, scoring 0 (no vessels visible), 1 (1–2 vessels within the ROI), 2 (3–5 vessels within the ROI), 3 (vessels in up to 30% of the ROI), 4 (vessels in 30%–50% of the ROI), and 5 (vessels in >50% of the ROI). This score is a slight modification of the system described by Boesen et al. (5) and Ohberg and Alfredson (31). The examiners were blinded to the case history of the subjects (18).
All subjects, who had agreed to accept follow-up, were contacted twice by e-mail, mail, or telephone in the following year and asked about their training volume, medical history, and any new symptoms at the lower extremities. The interview was based on a standardized questionnaire that inquired time and possible causes of symptom onset, character, and exact location of the pain as well as the course of the symptoms during the day. Symptoms at the Achilles region were questioned in detail to extract subjects experiencing MPT. Because MPT is characterized by pain during tendon load, morning stiffness in the tendon, localized swelling, and tenderness on palpation, subjects were furthermore asked to palpate their tendons for tendon thickening and tenderness on bilateral pressure of the tendon. Subjects allocated to the category MPT had to localize their pain 2–6 cm proximal to the insertion and had to report at least two of the following minor criteria: palpable thickening of the tendon, tenderness on bilateral pressure of the tendon, morning stiffness of the Achilles tendon, or Achilles tendon pain at the beginning of physical activity. The validity of this classification had been tested in a small pilot study in which interviewed subjects were clinically evaluated to verify matching of self-reported symptoms and clinical diagnosis.
After each measuring day, the recorded data were made anonymous and entered in a preprepared database (JMP statistical software package 7.0; SAS Institute, Cary, NC). The power Doppler ultrasonography (PDU) images and short films were saved electronically in Digital Imaging and Communications in Medicine and JPEG formats. All data were evaluated for plausibility directly after entry. After completion of data collection, a more extensive plausibility control with range checks and analysis of normal distribution (Shapiro–Wilk test) was performed. In addition, the data from 100 questionnaires were entered twice as a means of monitoring transfer errors. An error rate of less than 5% was assumed, the actual rate being 1.8%.
Statistical testing of differences between MPT and control (CO) subjects was done by χ2 tests (nonnormal population) using continuity-adjusted χ2 to analyze the differences between the nominal variables and a Mantel–Haenszel χ2 test to calculate the differences in the ordinal variable neovascularization. The differences in tendon thickness were shown using the Spearman rank correlation coefficient. The level of significance was set at α < 5% for all statistical tests.
To address the main hypothesis, influencing factors for the manifestation of Achilles MPT were identified using multiple logistic regression analysis (backward elimination). The strength of the effect was expressed as Wald χ2, biometric and running-related data being initially included in addition to the ultrasound findings. To calculate the risk of symptomatic Achilles tendinopathy for the given influencing factors, odds ratios were applied and can be understood as a good approximation to the relative risk given a small sample size (4).
A total of 634 healthy runners were included in the study. Their baseline data are given in Table 1. At the initial examination, 1268 tendons were examined using power Doppler sonography. The descriptive overview of PDU results is also given in Table 1. One subject could only be examined in B-mode for technical reasons; therefore, the data on neovascularization are derived from 633 subjects.
For the prospective part of the study, 513 of the 634 subjects were contacted by e-mail or postal mail, and 121 were contacted by telephone 6 and 12 months after the initial examination. We received adequate responses from 427 of the study participants, which corresponds to a response rate of 67%. Sixty-one subjects (14%) reported the appearance of new symptoms in the Achilles region within the observation period. In accordance with the defined criteria, 29 subjects were classified as having developed typical MPT and were thus allocated to the MPT group. Three subjects reported symptoms typical of insertion tendinopathy, and in 29 subjects, the symptoms were not clearly classifiable (pain at the musculotendinous junction, etc.). An overview of the subsequent allocation to the defined subgroups CO (still asymptomatic subjects) and MPT (subjects that had developed MPT) is given in Figure 2. Table 2 shows the biometric and running-related baseline data of the subjects in the two groups. The only statistically significant difference in baseline and training characteristics was found for age, which was higher in MPT than for the members of the CO or the total groups (48.1 vs 42.9 yr, P = 0.013). In the comparison of training characteristics between baseline and follow-up, a mean decrease in weekly mileage of −2.6 ± 19 km was found (P > 0.05). Therefore, substantial changes in training habits were not observed. Of the 29 runners who had developed an MPT, 7 had increased their mileage by >10 km·wk−1, 7 did maintain their training level, and 15 had decreased their weekly mileage. Of the latter, eight reported pain while running as the reason for the reduction, and seven reported various other reasons (e.g., “stress at work place”).
The descriptive overview of the PDU findings in the two groups is given in Table 3. Grades of neovascularization higher than grade III were not found. Statistical testing of these data showed that the prevalence of spindle-shaped thickening and hypoechogenicities was significantly higher in subjects who subsequently developed MPT (P < 0.001). In addition, maximum tendon thickness was significantly greater in those subjects who developed MPT (P < 0.001). The test for linear trend furthermore showed that subjects with neovascularization on PDU had a statistically significant increased risk of developing MPT (P < 0.001). Of subjects with neovascularization grade I, 12.1% developed MPT compared with only 1.9% of subjects without neovessels at baseline. The percentage rose only slightly, i.e., to 13.3%, for grade II but up to 50% for grade III, being important that only six subjects were placed in that category. Looked at differently, in 82% of the subjects who developed MPT during the 1-yr observation period, at least one intratendinous vessel was identified on the examination day.
To determine their predictive value concerning the manifestation of MPT, all biometric, running-related, and PDU data were finally evaluated by stepwise multiple logistic regression analyses (Table 4). Neovascularization on PDU thereby proved to have the greatest positive predictive value for the development of MPT and was associated with a 6.9-fold increased risk of developing MPT (P = 0.0001). In contrast, neither biometric data (age, height, weight, body mass index, sex) nor training parameters were identified as predictive factors for the manifestation of tendinopathy. The only other statistically significant predictor was a history of healed Achilles tendon complaints, which was associated with a 3.8-fold increased risk of developing symptomatic MPT. The variable spindle-shaped thickening with a P value of 0.06 and a Wald χ2 of 3.422 was only just eliminated from the analysis. All the other PDU parameters including hyper- and hypoechogenicity were likewise eliminated in the regression model and thus not statistically significant (Table 4).
Because Achilles tendinopathy in professional athletes is often associated with prolonged pain and restricted performance or even with a premature end of their career, Achilles tendinopathy is a dreaded overuse injury in track-and-field athletes. Early diagnosis of a disposition toward tendinopathy is therefore of great practical relevance in high-performance sport. PDU seems to be a suitable tool for this purpose because it is a highly sensitive, inexpensive investigation without significant adverse effects. Even so, prospective studies of the predictive value of power Doppler examination of the Achilles tendon have not yet been conducted in long-distance runners.
To identify the influencing factors relevant to the emergence of symptomatic midportion Achilles tendinopathy, 634 initially asymptomatic runners were followed up for a period of 1 yr. The incidence of Achilles tendon complaints within 1 yr was 14%, 7% being classified as MPT. This percentage correlates well with the published incidence of Achilles tendinopathy of 7%–9% per year in running athletes (17). Referring to the latest figures from Knobloch et al. (22), i.e., a reported incidence of 0.016 disorders per 1000 training kilometers, 14 Achilles tendon disorders were to be expected in the 427 followed subjects given their average weekly mileage of 39 km (2000 km·yr−1), which is a little less than the actual recorded incidence in our study.
The regression analysis identified intratendinous microvessels and preexisting healed Achilles tendon disorders as statistically significant influencing factors in the development of tendinopathy, whereas neither anthropometric nor running-related parameters had any effect. The anthropometric findings confirm those of Longo et al. (27), who conducted a more recent study to investigate the relationship between biometric and running-related data from 178 master track-and-field athletes and the manifestation of chronic Achilles tendinopathies and who also found no significant effects for the parameters age, sex, height, weight, or sports discipline on the development of tendinopathy. The relationship between biometric data and tendinopathy in runners was also investigated by Taunton et al. (40) in a retrospective study. In this study, logistic regression revealed that an age of older than 35 yr was a significant factor in men, the odds ratio of 0.355 being very low. Increased risk was unrelated to increasing age in women. In the present study, the subjects in the category MPT were statistically significantly older than the subjects in the control group, but the variable age was eliminated in regression analysis. Because it has already been proven that degenerative changes are more frequent as age increases, but age was not identified as a risk factor for the manifestation of tendinopathy, it has to be assumed that tendon degeneration is more often asymptomatic in older than in younger people.
Similarly, gender was not found to be a significant factor favoring the development of achilles tendinopathy (AT). Although it has often been reported that men are more frequently affected by AT (40), regression analysis did not yield a significant value for the variable gender (27). The explanation for the preponderance of male AT patients might therefore rather be a generally higher number of male runners and the participation of more men than women at competitive events (25).
Concerning ultrasound parameters, the prospective study of Fredberg and Bolvig (13), which investigated predictors for the manifestation of Achilles and patellar tendinopathy in elite soccer players, showed that spindle-shaped thickening was linked to a 45% risk of developing AT symptoms. In the present study, the incidence of spindle-shaped thickening was significantly higher in the MPT group. Even if regression analysis yielded a P value of 0.06 for the variable spindle-shaped thickening, which was slightly above the level of significance, we consider this variable relevant. Spindle-shaped thickening seems to be the most relevant B-mode parameter of predictive value concerning symptomatic tendinopathy, whereas neither absolute tendon thickness nor hypoechogenicities were associated with an increased risk in the regression analysis. The investigation by Fredberg and Bolvig controversially showed that hypoechogenicities of the patellar tendon are associated with a 17% risk of tendinosis, which supports the results reported by Cook et al. (8) for patellar tendons of basketball players. However, this could not be confirmed for the Achilles tendon in running athletes.
The most important result of the present study was that the prognostic factor with the highest odds ratio was neovascularization within the tendon. This was interestingly already found for neovascularization I°, corresponding to 1–2 tiny vessels. Because the higher grades were much rarer, the finding that grade I was even the most significant parameter must most likely be attributed to the smaller sample size for more severe cases. In any case, it has to be concluded from regression analysis that the detection of neovessels within the Achilles tendon, independent of the number of vessels, is linked to an increased risk of symptomatic Achilles tendinopathy. Therefore, it has to be assumed that neovascularizations are not, as is frequently suggested, part of an adaptation process (5,6) but rather indicators of an early manifestation of tendinosis and a predisposition to clinically manifest tendinopathy.
Because the only prognostically relevant factor identified in B-mode was spindle-shaped thickening, it seems worthwhile, although more expensive and time-consuming, to conduct PDU for risk stratification of symptomatic Achilles tendinopathy in runners. If PDU should be used for early diagnosis of yet-asymptomatic tendinopathy, the question arises as to whether the progression of degeneration culminating in symptomatic tendinopathy can be prevented. Eccentric training has been used successfully as a physiotherapeutic approach in the treatment of manifest tendinosis for many years (1,21,29). It was shown that that successful treatment using this approach led not only to normalization of tendon structure (34) but also to a clear reduction in the number of microvessels (32). In a prospective randomized pilot study, Fredberg et al. (14) conducted prophylactic eccentric training for one season with Danish elite soccer players but found no evidence that the training program had an effect on the manifestation of Achilles tendinopathy. They actually identified an increased risk of patellar tendinopathy in the group doing eccentric training. Because there are quite a few important differences of patellar and Achilles tendinopathy, a reevaluation concerning Achilles tendinopathy in runners might reveal different results and should therefore be conducted. Because the presented study identified neovascularizations as the most important prognostic factor, prophylactic sclerosing therapy might also be considered in high-level athletes.
The authors thank Toshiba Medical Systems for their provision of an additional ultrasound device during the running events as well as the doctoral thesis students involved in data collection. They also thank Mr. Duncan Cummins for language support and proofreading of the article.
There was no financial funding received for this study.
The authors disclose professional relationships with companies or manufacturers who will benefit from the results of the present study.
The authors have no conflicts of interest to disclose.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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Keywords:©2012The American College of Sports Medicine
MIDPORTION; TENDINOPATHY; NEOVASCULARIZATION; PROGNOSIS