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Letter to the Editor |
Hannover, Germany
Dear Editor:
I read with great interest the recent work of de Vos et al regarding the use of a neovascularization score to predict clinical severity in Achilles tendinopathy ("The Value of Power Doppler Ultrasonography in Achilles Tendinopathy:A Prospective Study," October 2007, pp 1696–1701). I strongly believe that the visualization of neovascularization as achieved by both color Doppler as well as power Doppler ultrasound gives important new information for the clinician to both detect and directly influence the area of interest in tendinopathy such as at the Achilles level. However, I would like to comment on some of the issues raised by this important work in detail.
Power Doppler, unlike color Doppler, is not dependent on the probe being directionally aligned to the flow and therefore will identify all flow independent of velocity, theoretically improving sensitivity over color Doppler. In vitro validation found power Doppler up to 4 times more sensitive than color Doppler for the detection of microvessels with flow detection in tubes as small as 0.3 mm, where flow may sludge and no flow is seen on color Doppler.15
In 2005, Richards et al from Stoke-on-Trent in the United Kingdom found in a retrospective observational study a positive Spearman correlation (0.84; P < .00001) suggesting a nonlinear relationship between the number of vessels seen on power Doppler and Achilles tendon size.13 They concluded the following: (1) power Doppler shows more tendon microvascularity than color Doppler in Achilles tendinopathy; (2) all microvessels arise on the ventral side of the Achilles tendon; (3) there is a nonlinear relationship between tendinopathy, Achilles tendon size, and the amount of microvascularity, but not between power Doppler and duration of symptoms; and (4) morphologically abnormal adult Achilles tendons were larger than 5.9 mm, and power Doppler flow was only seen in Achilles tendons above 6.5 mm.
However, they found no significant linear Pearson correlation between the number of microvessels on power Doppler and the duration of symptoms in Achilles tendinopathy (r = .25, P = .11) for symptomatic tendons among 52 patients with 55 symptomatic tendons. They counted all visible vessels in the power Doppler examination and found them varying between 0 and 11.
de Vos et al reported the same results at baseline in their recent paper, with 58 patients with 63 symptomatic tendons. They used the Öhberg score,12 with 0 for no vessel visible, 1+ for 1 vessel mostly in the anterior part, 2+ for 2 vessels throughout the tendon, 3+ for 3 vessels throughout the tendon, and 4+ for >3 vessels throughout the tendon, with no correlation of the degree of neovascularization (0–4+) and pain on the visual analog scale. Interestingly, after a 12-week treatment with heavy-load eccentric training with or without an additional night splint, a significant correlation of the level of neovascularization and the visual analog scale score was evident (r = .43, P < .001). To me, there is currently no clear-cut explanation for this discrepancy before and after a 12-week therapeutic intervention. Maybe the classification in 5 or 12 categories based on the reported levels of neovascularization is too narrow to detect a potential correlation of pain and the level of neovascularization given the limited symptomatic patient numbers of 50 to 60 in the current trials. A larger patient cohort with a broader classification system for neovascularization might detect a potential correlation with possible clinical application. On the other hand, mere subjective assessment of pain does not necessarily display the same degree of disease, as the suggested level of baseline neovascularization in color Doppler or power Doppler examinations at rest.
As de Vos et al appropriately cited, physical activity might influence the level of neovascularization after exercise, at least to some degree, as reported by Boesen et al.4 However, one should bear in mind that Boesen et al performed color Doppler optimized for low flow with the Nyquist limit at ± 0.014 m/s, which might be different than power Doppler. Dynamic ultrasound and color Doppler examination has shown that the flow in the neovessels stops during dorsiflexion in the ankle joint.11 Furthermore, all other reported studies were performed at physical rest.13
It is important to point out that patient positioning as well as probe pressure applied might have an influence on the degree of color Doppler and power Doppler neovascularization. Once again, de Vos et al reported the same patient positioning and level of relaxation at baseline and after treatment; therefore, there is no good explanation for the discrepancy in the reported correlations at baseline and after treatment in my view. It would be superb if the authors could comment or at least hypothesize on the underlying mechanism.
Besides the reported color and power Doppler applications, laser Doppler flowmetry has been reported to demonstrate minimal flow in normal Achilles tendons but significantly elevated flow in symptomatic Achilles tendinopathy.3 The initial laser Doppler flowmetry systems were invasive, where monochromatic light transilluminates tissue and the moving blood cells to cause a Doppler shift. However, in the meantime, noninvasive laser Doppler flowmetry is feasible and clinically applied. Using a combined laser Doppler and spectrophotometry system (Oxygen-to-see, LEA Medizintechnik, Giesen, Germany) with a noninvasive probe, we found a significant upregulation of capillary blood flow at the point of pain in symptomatic midportion as well as insertional tendinopathy.9 Twelve weeks of painful eccentric training reduce the tendinopathic capillary blood flow by 35% at the insertion and up to 45% at the mid-portion area.8 This is associated with superior postcapillary venous clearance and sustained tendon oxygenation.
As pointed out by Richards et al,12 it would seem that power Doppler must be detecting larger vessels than laser Doppler flowmetry and that the normal Achilles tendons must be regarded as relatively avascular on conventional ultrasound. Maybe the quantitative microcirculatory mapping using capillary blood flow, tendon oxygenation, as well as venous outflow might detect a potential correlation of patient symptoms with apparative measures in the future. I fully agree with de Vos et al by saying that future studies on this issue are warranted because a standardized validated measurement of neovascularization is needed. I would like to thank de Vos et al for their inspiring work.
Leidschendam, the Netherlands
We would like to thank Dr Knobloch for his interest and comments regarding our study on the value of power Doppler ultrasonography in Achilles tendinopathy.
Recently, a lot has been published about the role of neovessels in chronic tendinopathies. We performed our study to examine whether the degree of neovascularization detected with power Doppler ultrasonography is correlated with clinical severity before and after conservative treatment. There was no significant correlation before treatment, yet after treatment, a correlation was found. We do not have a good explanation for this observation. At present, the role of neovessels in tendinopathy is still unclear. As we do not know exactly where the pain is coming from in chronic tendinopathies, we can only hypothesize about the role of neovascularization in this process. Alfredson1 suggested that the ingrowth of neovessels and their accompanying nerves in the tendinopathic part of the tendon are the source of pain. Eccentric training might decrease the amount of neovascularization. Other authors described a more important role for altered collagen turnover after eccentric exercises in chronic tendinopathy and state that neovascularization is a phenomenon secondary to tendon degradation.10 Alfredson and Öhberg2 found an increase in neovascularization in every patient in the first 3 weeks after treatment with sclerosing injections. After this period, less pain was reported in patients, with a decrease of neovessels; patients with a high neovascularization score reported high pain scores.
We also studied the prognostic role of neovessels in predicting treatment outcome. In our study, neovessels were only found in 63% of the symptomatic tendons at baseline. There was no difference in treatment outcome between tendons with and without neovessels at baseline. Even when the most severe grade (4+, a florid network) was compared with the complete absence of neovessels, the clinical outcome, measured with the Victorian Institute of Sports Assessment-Achilles (VISA-A) questionnaire, was the same. It is frustrating that, despite all the research that has been performed, we cannot inform a patient with florid neovessels in the tendon whether this has any prognostic value.
In daily clinical practice, not every clinician has the opportunity to add power Doppler to the ultrasound examination. In 2005, Richards et al13 published data about the relationship between power Doppler findings and tendon thickness. They included 52 patients with Achilles tendinopathy and concluded that tendons that were less than 6 mm without hypoechogenic areas on ultrasonographic examination did not show flow on color and power Doppler ultrasound. There was a correlation (Spearman correlation, 0.84; P < .00001) between the number of vessels and the size of the tendon.
We also measured tendon thickness with ultrasonographic examination, which was digitally measured at the widest part of the Achilles tendon in the sagittal plane. These data have not been published, but are worth mentioning. There was a positive correlation between tendon thickness and degree of neovascularization at baseline (P < .001) and at 12 weeks’ follow-up (P < .001). In general, more neovessels were detected in thicker tendons, although the thinnest tendon in which neovessels were detectable was 3.5 mm, while the thickest tendon in which neovessels could not be seen was 12.0 mm. Richards et al also found a relationship between tendon size in patients with Achilles tendinopathy and the amount of microvascularity, but in contrast, they reported that a tendon with a thickness >6.5 mm always had detectable neovascularization.
At present, there is insufficient evidence to be able to clearly state the role of neovessels in chronic tendinopathies. We agree with Dr Knobloch that assessment of pain scores does not necessarily correlate with the degree of disease as suggested by the degree of baseline neovascularization in power Doppler examinations at rest.
We would advocate, as supported by Kingma et al,7 the use of validated functional scores instead of just pain scores for assessing outcome in tendinopathy research (VISA-A score by Robinson et al14). In our previous study on the additional value of a night splint to eccentric exercises, we also emphasized the importance of using functional outcome measurements, which may be a cause of the conflicting results between several studies as to the effect of eccentric exercises.6
Another important issue raised by Dr Knobloch is the use of scoring systems for neovessels. There are several scoring systems to evaluate the degree of neovascularization, which are described in our study. Dr Knobloch reported that Richards et al used another scoring system that ranged from 0 to 11. The use of many different scoring systems, none of which have been validated, makes comparing results from different research groups difficult. The lack of a validated scoring system means that any changes in score must also be interpreted with caution and is a major weakness in the field of tendinopathy research. We fully agree with Dr Knobloch that studies concerning the validity and reproducibility of a neovascularization scoring system are needed.
Dr Knobloch stated in his letter that a higher number of patients in combination with a broader classification system might have potential to detect a correlation between pain and neovascularization. We agree that including more patients can increase the chance of detecting a significant correlation. In our experience, determining a neovascularization score is difficult, even when a 5-point scoring system is used. We doubt whether the use of a scoring system with more points would add to the chance of detecting clinically significant correlations. An ideal system should be simple and valid to make it useable in clinical practice. Standardizing as many factors as possible will increase the reliability of the measurement of neovessels.
Some important factors are movements of the probe and the patient causing artifacts, the demarcation of the neovessels (in some cases, it is not clear whether 1 big vessel or 2 small vessels are present), and a possible problem with counting the same vessels twice during evaluation in the longitudinal and transverse planes. Other factors that might influence the amount of neovascularization are mentioned in our article published in The American Journal of Sports Medicine.5
With great interest, we followed the development of noninvasive laser Doppler flowmetry and the addition of spectrophotometry.8,9 Knobloch et al reported that the only limitation was randomly occurring motion artifacts. Another practical disadvantage may be that these techniques are not yet commonly used in the clinical setting. However, we would like to emphasize that it is important to develop new methods for tendon tissue identification. This will hopefully be another step toward unraveling the mysteries of the role of circulation in tendon degeneration and healing.
REFERENCES
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