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Abstract
Objective In this study, structure, blood flow and thickness in the Achilles tendon related to tendon-loading activity were investigated.
Design Examination by ultrasound (US) and colour Doppler (CD) immediately before and after 1 h of floor-ball matchplay.
Setting Sports Medicine Unit, Umeå University, Sweden
Participants 36 Achilles tendons in 18 middle-aged (mean 39 years) recreational male floor-ball players.
Main outcome measurements Structure and high blood flow (HBF)/neovessels (NV) in the tendons were registered. Tendon thickness was measured 3 and 4.5 cm above the upper calcaneus and at the thickest part of the tendon.
Results The US examination showed that 11/36 tendons (30.5%) in nine individuals had structural changes before and after the floor-ball match. In 7/36 tendons (five with structural changes), there were HBF/NV before, and after, the match. In six of these seven tendons, the blood flow was higher after than before the match. In three more tendons (two with structural changes), there were HBF/NV after, but not before, the match.
After the match, mean tendon thickness had decreased significantly in both normal tendons and tendons with structural changes at the 3-cm level (6.0 (1.0) mm to 5.8 (0.9) mm; p<0.019), at the 4.5-cm level (5.7 (1.1) mm to 5.5 (1.0) mm; p<0.044), and at the thickest part (6.6 (1.1) mm to 6.3 (1.2) mm; p<0.000).
Conclusions In about 1/3 of the tendons, there were structural changes, about half of those tendons also had HBF/NV, which was higher after, than before, the match. Mean tendon thickness in both normal tendons and tendons with structural changes had decreased significantly after a 1-h floor-ball match.
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Ultrasonography (US) is a well-known and established method to examine tendons.1 2 The addition of power or colour Doppler (CD) has allowed for evaluation of tendon and peritendinous blood flow,3 4 and has been shown to be useful in the evaluation of the chronic painful tendon.5
Neovessels (NV)/high blood flow (HBF), in combination with structural tendon changes have, during the last years, been shown to be a common finding in patients with chronic tendon pain.5,–,8
There is an ongoing discussion about the understanding and importance of the locally high blood flow.7,–,10 Is the high blood flow a poor sign, or can locally high blood flow be also found in normal and pain-free tendons? In a recent study on elite badminton players, where only Doppler flow (blood flow) and not tendon structure was evaluated, it was shown that most players had high blood flow before and after a game in both pain-free and painful Achilles tendons.10 From this study, it was suggested that the high blood flow was a physiological response to the activity.
Little is known about how the Achilles tendon responds to physical activity in humans. Magnusson and Kjaer11 and Ying et al12 suggested that long-term exercise would cause an increase in thickness of the Achilles tendon, while Hansen et al13 found no such effects of long-term training. Fredberg et al14 found no influence of short-term physical activity on the thickness of the Achilles tendon.
Floor-ball is an indoor team sport that has gained an increased popularity in the Scandinavian countries in recent years. The purpose of the game is to shoot the ball into the other team’s goal with a plastic stick. It is played on both competitive and recreational level, and the playing contains a lot of accelerating–decelerating running movements over the court area, with severe loading of the lower extremities.
This study aimed to investigate structure, blood flow and thickness in the Achilles mid-portion, in recreational middle-aged floor-ball players, immediately before and after a match. The hypotheses were that 1 h of this type of intense tendon-loading physical activity would possibly increase the local blood flow in the Achilles tendon, but have no effects on tendon structure and thickness.
Material and Methods
Participants
A group of 21 male recreationally active floor-ball players that were playing floor-ball together regularly, 1 h/week, were asked to participate in the study. Eighteen of the 21 players (86%) accepted, while two of the remaining three players reported lack of interest for the study, and one had an ankle injury during the time for the study and was therefore excluded.
The 18 examined players had a mean age of 39 (8) years (range 27–52 years), with a mean BMI of 25.5 (3.1) (range 19.3–31.8). The individuals were healthy, on no medication known to negatively affect tendons, and are non-smokers. Their mean amount of sports-related physical Achilles tendon loading activity was floor-ball 2.2 (1.5) h/week (range 1–5 h/week) and other sports 2.2 (2.8) h/week (range 0–11 h/week).
Methods
All tendons were examined with high-resolution grey scale US and with CD, Acuson Segoia (Siemens) immediately before (within 5 min) and after (within 5 min) the 1-h game. A linear multifrequency (8–13 MHz) probe was used. All tendons were examined by the same experienced doctor. Tendon structure and thickness were recorded. Thickness was measured at three levels, the 3-cm level (from the upper calcaneus), the 4.5-cm level (from the upper calcaneus) and at the thickest part of the tendon. CD was used to diagnose high blood flow/neovascularisation (HBF/NV) inside the tendon, counting the number of visible vessels. Both Achilles tendons were examined.
Pain in the Achilles tendon was estimated and registered before and after the match, on a visual analogue scale (VAS).
Statistical evaluation
The SPSS package (V.11.5, SPSS, Chicago, Illinois, USA) was used for all statistical calculations. Mean and SDs were used to describe data. Differences between groups were calculated using a non-parametric test for independent samples (Mann–Whitney U test). Differences before and after the playing sessions were calculated with Wilcoxon signed ranks test. A p value of <0.05 was considered statistically significant.
Ethical considerations
The study was performed according to the Helsinki declaration; the players were given written and verbal information about the study and gave their written informed consent to participate.
Results
The US examination showed that 11 of the 36 tendons (30.5%) in nine individuals had structural changes before, and after, the 1-h floor-ball playing.
In seven of the tendons (of which five had structural changes), there were HBF/NV before and after the match. In all except one, the blood flow was higher after than before the match. In three more tendons (of which two had structural changes), there were HBF/NV after, but not before, the match.
The mean tendon thickness decreased significantly after match, compared to before, on all measured levels. At the 3-cm level, the thickness decreased from 6.0 (1.0) mm to 5.8 (0.9) mm (p = 0.019), at the 4.5-cm level from 5.7 (1.1) mm to 5.5 (1.0) mm (p = 0.044) and at the thickest part from 6.6 (1.1) mm to 6.3 (1.2) mm (p = 0.000). The same differences were seen in both tendons with and without structural changes.
Tendon pain was not common in the examined group. One of the players reported bilateral Achilles tendon pain during rest before and after the playing session, while two players had no pain during rest before the match, but pain after the playing session (one unilateral, one bilateral). In all the tendons with pain, there were structural changes and/or HBF/NV. The mean estimated pain registered on a VAS among these players was relatively low both before (10.0 (0.0)) and after (15.2 (6.5)) playing.
When comparing players with and without findings of tendon changes and/or HBF/NV, and the players with normal findings, there were no differences in BMI or training amount. However, the players with normal tendons tended to be younger than the players with structural changes (37.4 (7.8) years vs 42.7 (7.5) years, p = 0.093).
Discussion
The current study is done on mainly middle-aged men, mean age 39 years, who all regularly play floor-ball matches together. Floor-ball is played in teams, is a relatively intensive game, including fast runs in different directions, with the purpose to use the stick to shoot the ball into the other team’s goal. Our investigation was done immediately before and after a 1-h match. We believe that the group of individuals studied represents middle-aged recreational athletes, and that the type of activity, floor-ball, is sufficient to put high loads on the Achilles tendon.
In this study, there were structural changes in about one-third of the Achilles tendons, and mean tendon thickness measured at three different sites decreased significantly after the 1-h match in both normal and abnormal tendons (fig 1). There were HBF/NV in 10 tendons, and the blood flow was generally higher after the match. Tendon pain was not a common symptom in this study group.
Achilles tendon midportion in a recreational floor-ball player. (A) Immediately before the 1 hour match, ultrasonography (US) and colour Doppler (CD) show minor structural tendon changes and high blood flow in one region in the ventral tendon. The player is pain-free. (B) Immediately after the match, US + CD show minor structural tendon changes and high blood flow in three regions in the ventral tendon. The player has Achilles tendon pain.
The relationship between high Doppler flow/blood flow and pain has been the focus of recent studies.5 7 8 10 15,–,17 Boesen et al10 investigated elite badminton players and came to the conclusion that a large proportion played with achillodynia; however, only 72 of the invited 320 players participated. In that study, CD flow, but not tendon structure, was evaluated, and the results showed that the majority of the players had high intratendinous Doppler flow before and after match. The high flow was suggested to be a physiological response to activity in a normal tendon, but unfortunately, because tendon structure was not evaluated, it is not known whether these tendons were normal.
There are studies on volleyball players, another group of athletes with high tendon loading activity, having similar structural tendon changes and HBF/NV as seen in mid-portion Achilles tendinopathy.7 8 In these studies, it was shown that the amount of Doppler flow varies from time to time, and there was not a strict correlation between the combination structural changes plus Doppler flow and pain. However, the severity of tendon pain was demonstrated to correlate with Doppler flow.8 Öhberg et al5 have reported a strong correlation between locally high Doppler flow in the region with structural tendon changes and chronic pain in patients with mid-portion tendinopathy. On the other hand, de Vos et al,16 who studied the correlation between neovascularisation score and clinical severity, found no such correlation before treatment with eccentric training. However, in that study, after 12 weeks of treatment with eccentric training, a correlation was found. In the study by Öhberg et al,5 neovascularisation score and clinical severity was not evaluated. In painful Achilles tendons, Zanetti et al18 found that power Doppler flow was associated with hypoechoic regions in the tendon, and Richards et al19 found a relationship between power Doppler flow and a greater Achilles tendon anterioposterior diameter. Altogether, the results of the above-cited studies indicate that the finding of Doppler flow in a structurally changed tendon does not necessarily implicate that there is tendon pain. Interestingly, it has been demonstrated from animal studies that after injury, there is an interaction between neovascularisation and axonal regeneration, and neovascularisation has been shown to precede the axonal regeneration.20 Therefore, theoretically, in some structurally changed tendons with HBF/NV, the nerve growth might still not be sufficient enough to cause pain. Furthermore, in certain individuals the condition might heal before nerve ingrowth. From a prospective study on young volleyball players, in about one-third of the players that had structural tendon changes and neovascularisation in the patellar tendon at inclusion, pain gradually evolved.21
In the current study, only two pain-free tendons with normal structure had HBF/NV before and after the 1-h match. This is in contrast to the findings by Boesen et al10 who found high blood flow before and after badminton in the majority of elite badminton players. However, again, from the study by Boesen et al,10 there is no information about tendon structure, and it might be that the majority of the badminton players also had structural tendon changes. The findings in our study anyhow indicate that there are few tendons with high HBF/NV alone, without structural tendon changes and/or pain. Is it because the ultrasound (US) examination was not good enough to pick up minor structural tendon changes? Would MRI have shown signal changes in these two tendons? Because neovascularisation has been indicated to come relatively late in the sequential pattern of changes in tendinopathy/tendinosis,22 it might be that also in these two tendons, there were minor structural tendon changes that our US examination could not register.
We found that the Achilles tendon thickness had decreased significantly at all three measured sites, after being compared to before the 1-h floor-ball match. Measurements were done at 3 and 4.5 cm, and at the thickest part, above the calcaneal tendon insertion. The findings were stable, with small interindividual differences. The results, that are conflicting with our hypothesis and previous studies,11,–,14 are interesting and indicate that tendon thickness is varying in relation to Achilles tendon loading activity. It can be speculated how, and why, tendon thickness can vary. It is known that glucose-amino glycans, a tendon matrix component, are hydrophilic and attract fluid.23 Theoretically, the hydrophilic tendon matrix might release fluid during tendon loading activity, resulting in a decreased tendon thickness. There might possibly be a pump mechanism during tendon loading activity. Further studies are needed to evaluate tendon thickness under different conditions, such as rest and loading.
In summary, there were structural changes in about one third of the Achilles tendons in middle-aged recreational floor-ball players, and about half of them also had HBF/NV that were higher after than before the match. Mean tendon thickness in both normal tendons and tendons with structural changes had decreased significantly after a 1-h floor-ball match.
What is already known on this topic
High blood flow/neovessels in combination with structural tendon changes is a common finding in Achilles tendons with chronic pain. Findings in direct relation to tendon loading activity have not been fully clarified.
What this study adds
There was higher blood flow after exercise in the majority of Achilles tendons with structural changes and high blood flow/neovessels, but not in the majority of normal tendons.
Achilles tendon mid-portion thickness decreased significantly after exercise in both normal tendons and tendons with structural changes.
Acknowledgments
Financial assistance was received from the Swedish Research Council for Sports and from the County Council of Västerbotten.
References
Footnotes
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Competing interests None.