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Achilles Tendons: Clinical Relevance of Neovascularization Diagnosed with Power Doppler US¹

¹ From the Departments of Radiology (M.Z., J.H.) and Orthopedic Surgery (A.M., P.V.), Orthopedic University Hospital Balgrist, Forchstrasse 340, CH-8008 Zurich, Switzerland; private practice (H.P.K., H.Z.); and Institute of Biostatistics, University of Zurich, Switzerland (B.S.). Received December 19, 2001; revision requested January 25, 2002; final revision received August 7; accepted August 22. Address correspondence to M.Z. (e-mail: marco.zanetti@balgrist.ch).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To evaluate the clinical relevance of neovascularization diagnosed with power Doppler ultrasonography (US) in Achilles tendons in patients with chronic achillodynia.

MATERIALS AND METHODS: Forty consecutive patients (mean age, 52 years; age range, 30–72 years) were examined. US was performed bilaterally and repeated after 3 months. Shape and echogenicity were assessed with gray-scale US and vascularization with power Doppler US. All patients were treated conservatively. Clinical assessment was performed after 0, 3, and 6 months by using visual analogue scale (VAS) scores (0, no pain; 100, unbearable pain). The VAS scores were compared with the initial US findings, and analysis of variance was used for repeated measurements.

RESULTS: Neovascularization was present in 30 of 55 painful tendons and in one of 25 asymptomatic tendons. The mean VAS scores at 0, 3, and 6 months, respectively, for tendons with neovascularization were 52, 26, and 20; those for tendons without neovascularization were 39, 19, and 18 (P = .15). Forty-eight painful and nine asymptomatic tendons were spindle shaped. The mean VAS scores at 0, 3, and 6 months, respectively, for the spindle-shaped tendons were 48, 25, and 20; those for normally shaped tendons were 33, 10, and 16 (P = .17). Thirty-five painful and four asymptomatic tendons were inhomogeneous. The mean VAS scores at 0, 3, and 6 months, respectively, for symptomatic inhomogeneous tendons were 54, 29, and 25; those for symptomatic homogeneous tendons were 32, 12, and 9 (P < .001).

CONCLUSION: Although neovascularization is a specific sign for pain, it does not indicate an unfavorable outcome. Conversely, tendon inhomogeneity seems to be associated with an unfavorable outcome.

© RSNA, 2003

Index terms: Extremities, US, 463.12984 • Tendinitis, 456.253 • Tendons, US, 456.253 • Ultrasound (US), power Doppler studies, 463.12984

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Chronic Achilles tendon pain is relatively common, especially in recreational runners but also in nonathletes (1). Ultrasonography (US) has been used for the diagnosis of tendinosis, partial tears, and complete tears (2–5). Color Doppler and power Doppler US provide additional potentially important information about tendon abnormalities (6–8). In patellar tendinosis, for instance, color Doppler US appears to improve confidence in the diagnosis because it demonstrates increased vascularization in abnormal tendons (6). Recently, neovascularization in the Achilles tendon has been demonstrated at color Doppler US in patients with chronic achillodynia (8).

The clinical relevance of such Doppler US findings is not evident, although patients with achillodynia, tendon thickening, and hypoechoic areas have a less favorable outcome, as compared with patients with normal findings at US (5). If neovascularization is a predictor of an unfavorable outcome, color Doppler or power Doppler US could assist the clinician in treatment planning and patient instruction. To our knowledge, no such outcome information is available for patients with neovascularization diagnosed with power Doppler US in the Achilles tendon.

The purpose of this prospective study was to evaluate the clinical relevance of neovascularization diagnosed with power Doppler US in Achilles tendons of patients with chronic achillodynia.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patients
Forty-seven consecutive patients with chronic Achilles tendon pain lasting longer than 4 weeks (mean, 58 weeks; range, 4–208 weeks) were prospectively enrolled in the study. The study was approved by the institutional review board of Orthopedic University Hospital Balgrist. The patients provided written informed consent. All patients meeting the inclusion criteria participated in the study. Patients in whom the onset of symptoms was associated with acute trauma were excluded.

Symptoms were related to sports activities in 20 patients (43%). The sports activities included hiking (n = 9), jogging (n = 7), biking (n = 1), dancing (n = 1), boxing (n = 1), and handball playing (n = 1). In 27 patients (57%), symptoms began without any distinct cause.

Seven patients were subsequently excluded from the study. Two of the seven patients did not undergo follow-up. Five of the seven patients did not send back the final evaluation sheets. The final study cohort included 16 women and 24 men (mean age, 52 years; age range, 30–72 years).

All patients were referred by subspecialist orthopedic foot surgeons working either at an orthopedic university hospital (n = 20) or in private practice (n = 20). All patients were treated conservatively according to a standardized protocol. This treatment protocol included patient education instructions, such as guidelines for proper warm-up, muscle stretching, and reduction or cessation of athletic activity; recommendations for the use of proper equipment, such as good running shoes, orthoses, heel lifts, cushioned soles, or insoles; and local treatment with antiphlogistic medications or physical therapeutic measures such as massage, electrotherapy, and application of heat or ice (9). Steroids were applied neither systemically nor locally.

Visual analogue scale (VAS) scores were used for clinical assessment of pain. The VAS represents a quantitative assessment of subjective factors (10). The VAS is based on a line with an anchor at each end. One anchor was labeled as "no pain," the other as "maximal, unbearable pain." The patient was asked to mark a point on this line to reflect the relative severity of discomfort. The line was 100 mm long, a fact unknown to the patient. The distance in millimeters was measured from the origin of the scale to the marked point to yield a percentage, which represented the VAS score. The VAS scores were noted in absolute values between 0 and 100.

Each patient assigned VAS scores three times: at the first US examination, at 3-month follow-up during the second US examination, and at 6-month follow-up through the mail. VAS scores were recorded separately for the right and the left heel. Pain duration between initial US and complete disappearance of symptoms was noted in weeks. Any surgical interventions at the Achilles tendon and any complete ruptures were noted if they occurred during follow-up.

US Technique
All US examinations were performed by one of two experienced musculoskeletal radiologists (J.H., M.Z.), each of whom had more than 10 years of experience in musculoskeletal US. US examinations were performed bilaterally (ie, in both heels) and were repeated after 3 months of conservative treatment. Patients were examined while they were prone, with the foot hanging over the edge of the examination table. The tendon was examined in both the longitudinal and transverse planes. The transducer pressure was minimized to avoid compression of vessels. Each examination consisted of gray-scale and power Doppler US (Elegra; Siemens Medical Systems, Erlangen, Germany). A linear transducer with a 7.5–9.0-MHz frequency was used.

The conventional US reports included the following findings: shape, normal or spindle; echogenicity, homogeneous or inhomogeneous (Figs 1, 2); maximal anteroposterior diameter of the Achilles tendon; and craniocaudal distance between the location of maximal tendon thickening and the posterior corner of the calcaneal tuberosity. For power Doppler US, the color gain was adjusted until no color signal was present deep to the cortical bone of the calcaneal tuberosity. The pulse repetition frequency was maintained at 1,250 Hz in all cases. New vessel formation within the Achilles tendon was noted. New vessel formation was confirmed by means of demonstration of an arterial blood flow curve at duplex US (Fig 1).

View larger version (113K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Spindle-shaped Achilles tendon with moderate inhomogeneous echoes and neovascularization. (a) Longitudinal power Doppler US image demonstrates neovascularization (shown in red) involving the ventral half of the spindle-shaped Achilles tendon. Moderate echo inhomogeneity is present. (b) Transverse power Doppler US image demonstrates neovascularization (shown in red) within the tendon. The echo inhomogeneity is substantial. (c) Longitudinal duplex US image demonstrates an arterial pulse curve in a small vessel.

View larger version (64K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Spindle-shaped Achilles tendon with moderate inhomogeneous echoes and neovascularization. (a) Longitudinal power Doppler US image demonstrates neovascularization (shown in red) involving the ventral half of the spindle-shaped Achilles tendon. Moderate echo inhomogeneity is present. (b) Transverse power Doppler US image demonstrates neovascularization (shown in red) within the tendon. The echo inhomogeneity is substantial. (c) Longitudinal duplex US image demonstrates an arterial pulse curve in a small vessel.

View larger version (53K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Spindle-shaped Achilles tendon with moderate inhomogeneous echoes and neovascularization. (a) Longitudinal power Doppler US image demonstrates neovascularization (shown in red) involving the ventral half of the spindle-shaped Achilles tendon. Moderate echo inhomogeneity is present. (b) Transverse power Doppler US image demonstrates neovascularization (shown in red) within the tendon. The echo inhomogeneity is substantial. (c) Longitudinal duplex US image demonstrates an arterial pulse curve in a small vessel.

View larger version (102K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Longitudinal power Doppler US scan demonstrates an Achilles tendon with slight spindle shape, homogeneous echoes, and absence of neovascularization.

The prevalence of US abnormalities in the symptomatic and asymptomatic heels was compared. This analysis was performed in only the 25 patients with unilateral pain.

For each US finding, sensitivity and specificity with regard to prediction of symptoms at presentation were calculated. The McNemar test was used to determine if the qualitative differences between the symptomatic and asymptomatic heels were significant. A paired t test was used for comparison of the means of continuous data.

A P value of less than or equal to .05 was considered to indicate a statistically significant difference. Commercially available software (StatView, version 4.0; SAS Institute, Cary, NC) was used for all statistical analyses.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Fifteen of the 40 patients had bilateral symptoms, and 25 had unilateral symptoms, which resulted in 55 symptomatic and 25 asymptomatic tendons. In 30 of the 55 painful tendons, neovascularization was present on the initial US images. After 3 months, neovascularization had completely disappeared in eight tendons and had appeared in three tendons that had no signs of neovascularization at initial presentation. A spindle shape was found in 48 of 55 symptomatic tendons, and inhomogeneity was found in 35 of 55 symptomatic tendons. The shape and the echogenicity had not changed in any case at the 3-month follow-up examination (Table 1).

View larger version (26K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Graph shows mean VAS scores for the 55 symptomatic tendons categorized according to presence or absence of neovascularization. This graph demonstrates that tendons with neovascularization were assigned higher VAS scores than were those without neovascularization. However, the difference in the course of the VAS scores was not significant (P = .15, ANOVA for repeated measurements). The small difference at 6 months is notable. Error bars denote standard errors.

View larger version (22K): [in this window] [in a new window] [Download PPT slide]   Figure 4. Graph shows mean VAS scores for the 55 symptomatic tendons categorized according to shape. This graph demonstrates that tendons with a spindle shape were assigned higher VAS scores than were those with a normal shape. However, the difference in the course of the VAS scores was not significant (P = .17, ANOVA for repeated measurements). The small difference at 6 months is notable. Error bars denote standard errors.

View larger version (24K): [in this window] [in a new window] [Download PPT slide]   Figure 5. Graph shows mean VAS scores in the 55 symptomatic tendons categorized according to presence or absence of homogeneity. This graph demonstrates that tendons with inhomogeneous echoes were assigned significantly higher VAS scores than were those with homogeneous echoes (P < .001, ANOVA for repeated measurements). Error bars denote standard errors.

There was a slight positive correlation between maximal tendon diameter and the VAS scores at 0 months (R² = 0.16, P = .002) and 3 months (R² = 0.16, P = .003). There was no significant correlation at 6 months (R² = 0.01, P = .54).

The sensitivity for predicting a symptomatic tendon varied from 52% to 88% for each US finding. Neovascularization was the most specific finding, with one positive finding in the 25 asymptomatic tendons (Table 3). However, all US abnormalities—in terms of shape, echogenicity, and neovascularization—were significantly different in the symptomatic tendons, as compared with those in the asymptomatic tendons (P < .001, McNemar test). The anteroposterior diameters of the tendons were also significantly different (P < .001, paired t test).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Most patients with chronic achillodynia are treated conservatively on the basis of a clinical diagnosis (11). Surgery may be considered when conservative therapy fails. Surgical options include peritenon and tendon débridement; decompression of central core lesions; and tendon augmentation with the plantaris tendon, strips of fascia of the gastrocnemius-soleus complex, or the flexor hallucis longus or flexor digitorum longus tendon (11–13). Imaging of the Achilles tendon is believed to facilitate surgical management because it reveals the nature, extent, and location of the lesion (2,3,14–16).

Technologic advances in color Doppler US and, more recently, power Doppler US have facilitated the detection of small vessels in musculoskeletal structures (17). So far, to our knowledge, little information is available about the clinical relevance of increased vascularity in musculoskeletal structures (7,18). Breidahl et al (17) speculated that power Doppler US improves the clinical relevance of gray-scale US findings, for instance, because it helps to distinguish inflammatory and infectious musculoskeletal fluid collections from those that are noninflammatory.

Neovascularization in Achilles tendons can be diagnosed with both color (8) and power Doppler US. Our hypothesis was that this finding can be used to predict an unfavorable outcome. The presented results demonstrate that neovascularization is a relatively specific US sign for a painful tendon. This abnormality was found in only one asymptomatic contralateral tendon. However, the diagnosis of neovascularization had a limited role in outcome prediction in our series. Tendons with neovascularization were assigned slightly higher mean VAS scores than were normal tendons. However, the difference from normal tendons was not significant. Conversely, tendon inhomogeneity was the only US finding that could be used to predict a significant difference in outcome.

Tendon inhomogeneity on US images may represent tendinosis or a partial tear. In this study, we did not attempt to distinguish between tendinosis and partial tear. This differentiation is hardly possible with currently used imaging methods (4). In the literature (1,11,12,19), there is broad discussion about terminology. Tendinosis, tendinitis, partial tear, and tendinopathy are simultaneously used for apparently similar clinical and imaging abnormalities. There appears to exist a consensus that these lesions should not be called tendinitis because of the lack of inflammatory cells in those cases in which histologic examination results were available (1,19,20).

Analogous to its use in describing inflammation in the patellar tendon, the term tendinosis may be the most suitable term for characterizing a thickened tendon with slight inhomogeneity (21). Tenocyte hyperplasia, prominent neovascularization with endothelial hyperplasia, loss of longitudinal collagenous architecture, and microtears with collagen fiber separation were found in histologic specimens in patients with patellar tendinosis (22). Similar abnormalities with alterations in fiber structure, focal variations in cellularity, and neovascularization have also been found histologically in thickened and inhomogeneous Achilles tendons (1). Movin et al (20) found neovascularization in 26 of 40 tendon specimens obtained during semiquantitative histologic analysis of painful Achilles tendons. The prevalence of neovascularization in our investigation was 55% (30 of 55 painful tendons), which is consistent with these results.

The importance of tendon inhomogeneity in outcome analysis that was observed in this study is in accordance with the results of previous studies (5,14). In a retrospective study with 33 patients (5), a statistically significant difference was found in the full recovery time between normal tendons and enlarged tendons and tendons with hypoechoic lesions. Nehrer et al (14) reported that patients without US changes had a significantly better clinical outcome after conservative treatment. They also emphasized that patients with tendon thickening and circumscribed lesions of the echogenicity had higher rates of spontaneous tendon tears. On the basis of our study results, analysis of the echogenicity is more important than is the detection of neovascularization.

The use of power Doppler US for prediction of outcome in patients with long-standing Achilles tendon pain is probably not as relevant as is the use of gray-scale US. Therefore, we cannot recommend the general use of power Doppler US for the assessment of chronic achillodynia. Additional power Doppler US adds cost to gray-scale US. Cost considerations for US are relevant, although a single examination is inexpensive. In Germany, the overall cost of US exceeds those of computed tomography and magnetic resonance imaging because of the large numbers of examinations performed (23).

The absence of neovascularization in some of the symptomatic tendons in our study is in contrast with the results of a previous study (8) in which all patients with chronic achillodynia demonstrated neovascularization. The inclusion criteria were identical and patients were included in a consecutive fashion in both investigations. Part of the difference may result from the fact that neovascularization is a dynamic finding that may be most pronounced during acute exacerbation of pain and then disappear at inconstant rates. This finding is supported by the fact that during the first 3 months changes in neovascularization were demonstrated in the patients in our study. Another explanation may be the influence of stretching or relaxing the Achilles tendon during passive motion of the foot. Ohberg et al (8) found that intratendinous blood flow ceased in the stretched Achilles tendon when the foot was in dorsiflexion. However, in our standard examination, the tendon was not stretched.

Ohberg et al (8) also found that neovascularization was more pronounced in the ventral side of the thickened tendon. This observation fits with our findings. Although we did not specifically assess for the location of neovascularization, we confirmed the predominance of neovascularization in the ventral side of the tendon (Fig 1). The predominance of ventrally sided neovascularization may be important when the tendon is débrided. It can be hypothesized that these vessels should be retained to ensure sufficient tendon regeneration or repair.

A limitation of this study was that there may be a potential correlation between right and left measurements when pain is present in both heels. A patient who has scored one heel would have that score as a reference on which to base the potential pain score for the other heel. However, the main focus of this study was outcome analysis. The course of decrease in pain should not be influenced.

In conclusion, neovascularization of Achilles tendons seems to be associated with pain but not with an unfavorable outcome. Tendon inhomogeneity appears to be more relevant with regard to the outcome.

	FOOTNOTES

 
Abbreviations: ANOVA = analysis of variance, VAS = visual analogue scale

Author contributions: Guarantor of integrity of entire study, M.Z.; study concepts, M.Z.; study design, all authors; literature research, M.Z., H.P.K.; clinical studies, M.Z., J.H.; data acquisition, M.Z.; data analysis/interpretation, all authors; statistical analysis, B.S.; manuscript preparation, M.Z.; manuscript definition of intellectual content, M.Z., J.H.; manuscript editing, J.H.; manuscript revision/review and final version approval, all authors.

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2272012069v1 227/2/556    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Zanetti, M. Articles by Hodler, J. Search for Related Content PubMed PubMed Citation Articles by Zanetti, M. Articles by Hodler, J.