Physical Activity Increases Synovial Fluid in Ankle Tendon Sheaths: an Adjustment of MR Criteria is Needed

<jats:title>Abstract</jats:title>         <jats:p><jats:bold>Objectives: </jats:bold>To compare the amount of fluid in synovial sheaths of the ankle before and after running. Our hypothesis was that this amount would increase, and that the threshold for what is normally acceptable should be adjusted after physical activity.<jats:bold>Methods: </jats:bold>Twenty-one healthy volunteers (n=42 ankles) ran for 40 minutes on a treadmill. They underwent 3T MRI before and immediately after running using a dedicated ankle coil. The images were stored and subsequently measured in a standardized way and independently read by two readers for fluid in the tendon sheaths in the retro and inframalleolar area. Statistics were performed for each tendon (Wilcoxon signed rank test), and also for the pooled data. Intraclass correlation coefficients were calculated.<jats:bold>Results: </jats:bold>For reader 1, for all tendons the values after running increased without reaching statistical significance. For reader 2 this was not the case for all tendons but for most. When all the data were pooled (n=800 measurements), the statistical difference before and after running was significant (p&lt; 0.001).<jats:bold>Conclusion: </jats:bold>Data pre and post running show a trend of increasing synovial fluid, however not significant for each individual tendon. The pooled data for all tendons, (n=800) show a statistically significant increase after running (p&lt; 0.001). The clinical implication is that the threshold for normally acceptable fluid should be adjusted if the patient undergoes an MR study after recent physical activity.</jats:p>

section_content: Tendons typically contain a synovial sheath. This is not the case everywhere, however. Examples where such a sheath is absent include the exor carpi ulnaris, patellar tendon, Achilles' tendon, and the dorsal tendons at the ngers and toes [1] [2] [3] [4] [5] [6] [7]. 

One question that arises is what are the limits of normal tendon sheath uid in the ankle. Too much uid may indicate mechanical overuse, infection, or a rheumatological condition. A few studies have addressed this topic of normal synovial uid especially in the ankle [1] [2] [3] [4] [5] [6] [7]. 

In this article we focus on the ankle tendons. Previous reports have given indications of the amount of uid that can be expected in a normal person without any known underlying condition. Fluid was quite common and rather important around the medial tendons. It was minimal and usually absent around the peroneal tendons. In the normal situation uid was never observed in the anterior tendon group. 

Reference values are available in several publications [2, 3, 4, 5, 8, and 9 ]. 

Our research question was whether increased athletic would increase tendon sheath uid. Our hypothesis was that it indeed would increase tendon sheath uid, and hence that the normal values could change [10, 11, 12, 13, 14]. We would try to demonstrate this with MR imaging. 

To study this type of research question is rather complicated and an experimental context was designed. 

We decided to perform MR of both ankles in 21 volunteers before and after running for 40 minutes on a treadmill.
section_name: Introduction

section_content: Our study was approved by the IRB of our hospital. Written informed consent was obtained from the volunteers. They also lled out a questionnaire to make sure they had no underlying rheumatologic condition, ankle pain or trauma, or previous severe injury or surgery to the ankle. Conditions that would make the experiment unsafe were also assessed. The investigators were available to answer any questions and monitor the experiment. 

The volunteers were also weighed and their length was obtained, allowing subsequent calculation of BMIs. MRI in the three orthogonal planes was obtained with a PD FS sequence on a Philips 3T Achieve system (Philips, Best, The Netherlands). Imaging parameters were as follows: TR 2969 ms; TE 30 ms; NA 2; slice thickness 2. 5 mm. A dedicated ankle coil was used allowing maximum reproducibility of patient positioning before and after running. 

After pre-exercise imaging the patient started running on a treadmill at intensity setting nr 3 (Domyus T520, Decathlon, Villeneuve-d'Ascq, France). The investigators continuously monitored the volunteers for injury, pain, or feeling unwell. After running, the same imaging sequences where repeated immediately with exactly the same imaging parameters. All images were stored on PACS (Agfa, Mortsel, Belgium). 

None of the investigators made any immediate assessments or interpretations of the obtained images. Positioning consistency and image quality were ascertained by a certi ed RT (three different RTs performed the studies; 15, 20, 25 years of work experience). 

For the interpretation session the transverse images were used, however the other planes were used to ascertain that the measurements were performed in the most similar position possible for the pre and post images. The measurements that were obtained included TP, FD, FH, PL, and PB. For each tendon a retro-as well as inframalleolar measurement was obtained. The exact measurement positions are further detailed in Table 1. The largest dimension of uid was used, in exactly the same position pre and post running. The images were interpreted by two MSK radiologists (8 and 20 years of experience) independently [ Fig. 1 2 3 4 5 6 7 ]. 

The pre and post image set was analyzed simultaneously to make sure each measurement was performed in exactly the same location for both image sets. The readers were blinded to which image was pre and which was post. The images were thus presented to the viewers in a randomized fashion.
section_name: Materials and methods

section_content: All participants performed the experiment successfully without pain, injury, or becoming unwell. 

Planning of imaging was organized as such that each participant immediately underwent MR when his running session ended. There were 12 men (57 %) and 9 women (43%). The mean age was 24. 7 years. 

All the measurements obtained for all tendons pre and post are shown in table 2 and 3. The data were compared by a Wilcoxon signed rank test. This Table also shows the 95 % con dence intervals, the delta (and con dence interval), and the p-value for this speci c tendon. Statistical signi cance was calculated for each tendon separately. Since the number of cases per tendon remained small, we also calculated statistical signi cance for all measurements pooled. This calculation thus related to 800 cases. The rst table relates to reader 1, and the second table to reader 2 [Fig 1 -7]. Intraclass correlation coe cients were calculated between both readers. BMI was calculated for each volunteer. 

All the measurements pre and post were largest for both readers for the TP and FH, followed by the FD, and peroneal tendons but in their inframalleolar location. 

For all tendons pooled the delta was small and ranged from 0. 00 to 0. 14 mm. None of the observed differences for both readers per tendon was statistically signi cant. For reader 1 all measurements post running showed a trend to be higher than pre-running. For reader 2 most values after running showed a trend to be higher, but not all. There was a trend for the post measurement to be larger, although not reaching statistical signi cance per tendon. 

When the calculation was performed on the pooled data (n=800 cases) the result was signi cant, however (p< 0. 001), with the measurement post running being higher. 

The mean BMI of the volunteers was 23,2 (N). The BMI range was 19-32. Three individuals were in the obese range, and 3 in the overweight range, all the others having a BMI in the normal range.
section_name: Results

section_content: Several synovial sheaths, in the normal situation contain some synovial uid. Generally, a sheath is present where the tendon(s) make a turn or are subject to increased mechanical forces. The presence of tendon sheath uid therefore in itself is not necessarily abnormal. 

The normal amount of uid in tendon sheaths has been the subject of several investigations, some using MR, some US. In our opinion, the ones using US may have been awed as it may be quite di cult to differentiate normal hypoechoic tendon retinacula from hypoechoic tendon uid. This is less of a problem with MRI, where uid is hyperintense and retinacula and sheaths exhibit hypointense signal on all pulse sequences. Increased uid may be the cause of mechanical issues, tendon damage, infection, and rheumatological disorders. 

Our measurements pre-running is in accordance with those of previous investigations [1] [2] [3] [4] [5] [6], pointing to the fact that uid is particularly common in the medial tendons in the normal situation, and to a lesser degree in the peroneal tendons. In the anterior tendon group uid is never present in the normal situation. 

Our present investigation has a physiological implication, but more so a clinically relevant implication. If physical activity increases joint uid our threshold for considering uid as pathological should be adjusted following such activity. 

Although it may be argued that for each tendon individually our pre and post imaging values were not statistically signi cant, signi cance was obtained when the data were pooled (to 800 cases). Our number of cases per tendon is not su cient to show a signi cant difference per tendon. However, devising an experiment such as this is quite time consuming, and it would not be realistic to image e. g., 150 volunteers in this way. Probably an even better experiment would be to image this number of marathon runners before and after their contest, but this also is not realistic. 

Our study has several limitations. Our number of volunteers was limited. Nevertheless, there was a consistent trend for the measurements to increase after running and when the data were pooled, they became statistically signi cant. Second, our set up was experimental using a treadmill. Running outside on uneven terrain or for longer distances would likely be more signi cant. 

MR positioning before and after running may have changed slightly, although every effort was made to avoid this by meticulous positioning by highly experienced RTs. 

The distribution of uid in the sheath is a three-dimensional phenomenon and ideally the total volume in the entire sheath could have been measured. This would imply heavy computing and segmentation of images which was beyond our capabilities. It can be criticized that we obtained only one measurement in the transverse plane. However, we de ned the measurement site precisely and also evaluated the paired images to measure exactly at the same location. Our study population was also rather heterogeneous, some individuals having a BMI out of the normal range. We believe, however, this in itself would not affect our measurements and is rather representative of a general population. We also omitted the anterior tendon group since it has been repeatedly shown that uid never occurs in the normal situation. Finally, the observed differences were often small, and it could be argued that measurement bias played a role. Nevertheless, as mentioned before there was a quite consistent trend for an increase post running. 

Flexor hallucis tendon. Note obvious increase uid after running along medial and lateral margin (arrows). 

Flexor digitorum. Images in inframalleolar area. Note subtle increase after running in synovial uid (arrows).
section_name: Discussion

section_content: Availability of data and materials: provided in the tables of the manuscript Competing interests: no competing interest to disclose Funding: no funding

section_name: Abbreviations

section_content: In conclusion, there was a statistically signi cant difference in synovial sheath uid before and after running, when all obtained data were pooled (n=800). 

Therefore, we suggest that if a patient is imaged after physical activity (such as running, jogging, tness), the threshold of what can be accepted as a normal amount of synovial uid should be adjusted.