Knee Surgery, Sports Traumatology, https://doi.org/10.1007/s00167-019-05585-1

ANKLE

Pressure changes in the Kager fat pad at the extremes of motion suggest a potential role in Achilles tendinopathy

F. Malagelada1,2 · J. Stephen3,4 · M. Dalmau‑Pastor2,5,8 · L. Masci6 · M. Yeh4 · J. Vega2,5,7,9 · J. Calder3,4

Received: 29 March 2019 / Accepted: 18 June 2019 © European Society of Sports Traumatology, Surgery, Arthroscopy (ESSKA) 2019

Abstract Introduction The Kager fat pad is one of the largest soft tissue structures local to the ankle , yet it is poorly understood. It has been hypothesised to have a role in Achilles tendinopathy. This study aimed to investigate the pressure areas in the Kager fat pad adjacent to the Achilles tendon and to assess the anatomy and deformation of the Kager fat pad in cadavers. Methods Twelve fresh frozen cadaveric (mean age 44 years, range 38–51) were mounted in a customized testing rig, enabling plantar fexion and dorsifexion of the ankle, with the Achilles tendon loaded. A needle tipped pressure sensor was inserted in two areas of the Kager fat pad under ultrasound guidance (retrocalcaneal bursa and at 3 cm proximal from Achil- les insertion). Pressure readings were recorded at diferent fexion angles. Following testing, the specimens were dissected to expose the Kager fat pad and retrieve it for analysis. MRI images were also taken from three healthy volunteers and the Kager fat pad deformation examined. Results Mean pressures signifcantly increased in all specimens at terminal ankle plantar and dorsi fexion in both regions (p < 0.05). The Kager fat pad was consistently adherent to the Achilles at its posterior aspect for a mean length of 7.7 cm (SD 0.27, 89% of KFP length). The most distal part of the Kager fat pad was the exception and it detached from the Achilles to give way to the retroalcaneal bursa for a mean length of 0.92 cm (SD 0.24, 11% of KFP length). The bursal space is partially occupied by a constant ‘wedge’ extension of Kager fat pad. The mean volume of the whole Kager fat pad was 10.6 ml (SD 3.37). Video and MRI demonstrated that the Kager fat pad undergoes signifcant deformation during plantar fexion as it is displaced superiorly by the Achilles, with the wedge being forced into the retrocalcaneal bursal space. Conclusion The Kager fat pad does not remain static during ankle range of motion, but deforms and its pressure also changes. This observation supports the theory that it acts as a shock-absorber to the Achilles tendon and pathological changes to the fat pad may be clinically important in the development of Achilles tendinopathy.

Keywords Achilles · Ankle · Anatomy · Biomechanics · Cadaver · Fat pad

Electronic supplementary material The online version of this article (https​://doi.org/10.1007/s0016​7-019-05585​-1) contains supplementary material, which is available to authorized users.

* F. Malagelada 5 GRECMIP (Groupe de Recherche et d’Etude en Chirurgie [email protected] Mini-Invasive du Pied), Merignac, France 6 Pure Sports Medicine Clinic, London, UK 1 Department of Trauma and Orthopaedic Surgery, Royal London Hospital, Barts Health NHS Trust, London, UK 7 and Ankle Unit, Hospital Quirón and Clinica Tres Torres, Barcelona, Spain 2 Human Anatomy and Embryology Unit, Department of Pathology and Experimental Therapeutics, University 8 Manresa Health Science School, University of Vic–Central of Barcelona, Barcelona, Spain University of Catalonia, Vic, Barcelona, Spain 3 Fortius Clinic, London, UK 9 European Foot and Ankle Society (EFAS)-Research Committee, Basel, Switzerland 4 Department of Bioengineering, Imperial College London, London, UK

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Introduction Materials and methods

Kager’s fat pad (KFP), also known as the pre-Achilles A total of 12 fresh-frozen cadaveric feet and ankles (mean fat pad, is one of the largest lipomatous structures of the age ± SD = 41.4 ± 10.3 years, range 22–52 years; 6 male) leg. It is located in the posterior ankle joint, occupying with no history of surgery or disease were obtained from a Kager’s triangle, bordered by the Achilles tendon poste- tissue bank. The specimens were preserved in polyethylene riorly, the crural fascia and fexor hallucis longus (FHL) bags, stored frozen at − 20 °C and thawed before use. None muscle anteriorly, and the posterior calcaneal tuberosity at of the specimens showed a degree of ankle stifness beyond its base inferiorly. In an anatomical and histological study, the physiological range of motion (5° of dorsifexion to 40° Theobald et al. showed that the KFP has three regions of plantar fexion). that are closely related to the sides of the triangle. They named those the Achilles-related, the FHL-related, and the bursal wedge adjacent to the calcaneus. They concluded Specimen preparation and loading that the three regions have specialized functions: the FHL part contributes to moving the bursal wedge during plantar The foot and ankle specimens were prepared to enable meas- fexion, the Achilles part protects blood vessels entering urement of pressure in the KFP during ankle plantar- and the tendon, and the bursal wedge is thought to minimize dorsifexion. The gastrocnemius and soleus were identifed pressure changes in the bursa. Despite generic descriptions and a cloth material was surrounded and securely stitched of the KFP in the literature, to the best of our knowledge, to the proximal end of muscles, to provide anchorage for the there are no objective data fully describing the parameters application of load to the Achilles tendon. The proximal tibia of the shape and volume of the KFP. was cut at approximately 40 cm above the joint line and an Close relationship of the KFP with the Achilles tendon intramedullary rod cemented into it. Distally the fbula was has been shown to have a protective efect to the blood secured in an anatomical position using a transverse bone vessels crossing the KFP and the tendon itself. It has been screw to minimize joint excursion. postulated that pressure changes within areas of the KFP The ankle was mounted in a testing rig with the foot may contribute to the process of Achilles tendinopathy or pointing downwards and the second metatarsal pointing tears of the fascia cruris [1, 2]. Equally, excision of part downward, aligned with the shaft of the tibia. Tension was of the KFP during hindfoot endoscopy to create a working applied to the Achilles tendon in its physiological direction area may have biomechanical consequences for ankle joint in relation to the tibial axis. The gastroc-soleus complex was function. Similar studies have been performed to assess the loaded with 62 N, in accordance with prior work [6]. This infrapatellar fat pad of the knee suggesting that it plays a load represents an unloaded open kinetic chain calf raise role in stabilizing the [3]. Around the KFP, pres- with the knee extended. Higher load levels were not used to sure measurements have also been investigated and con- avoid damaging the soft tissues across the tests performed troversy exists as to whether the extremes of motion result on each ankle. Closed kinetic chain motion (by placing a in higher pressure load to the retrocalcaneal bursa and the board across the foot) was also assessed during pilot test- midportion of the Achilles [4, 5]. ing and gave results similar to those of open kinetic chain The aim of this study was to investigate the pressure assessment. This setup has been used previously for ankle changes during ankle range of motion in two areas of joint testing [6]. Kager fat pad, defned in relation to the Achilles tendon: the mid-portion (location of non-insertional Achilles ten- Pressure measurement assessment dinopathy) and the retrocalcaneal bursa (location of inser- tional Achilles tendinopathy). Secondly, it was aimed to evaluate the KFP deformation during ankle motion directly A Gaeltec CTN/4F-HP pressure transducer with a Lemo in vitro, and using magnetic resonance imaging (MRI) 2306 connector (Gaeltec Devices Ltd, Dunvegan, UK) was in vivo. The fnal aim was to re-examine the anatomical used to measure pressure within the KFP. The tip diameter attachments of the KFP, its dimensions and volume using of the sensor was 1.5 mm, with a sensitivity of 1.17 μV/V/ young, fresh cadavers. It was hypothesised that the KFP is kPa. Calibration was determined as per the manufacturer subject to pressure changes throughout the ankle’s range of guidelines. Test re-test readings from the same specimen motion and deformation that is in close relationship with established excellent repeatability with an ICC of 0.97. the Achilles tendon suggesting a potential proprioceptive Under ultrasound guidance, the tip of the sensor was or feedback role of the KFP. introduced through the skin into two regions of the KFP in contact with the Achilles: (a) the midportion; an area of the Achilles located 3 cm proximal to its insertion onto the

1 3 Knee Surgery, Sports Traumatology, Arthroscopy calcaneum and (b) the retrocalcaneal bursa; at the insertion fexion to full dorsifexion. The participants were asked of the Achilles on the calcaneum. The sensor was inserted to keep the desired position of the ankle during the time under ultrasound vision by an experienced ultrasonographer. required for the obtention of images. The images were made The tip was located at the midpoint of the Achilles width in into a movie, by taking the same sagittal slice from scans the coronal plane and in the two previously mentioned areas taken at diferent fexion angles. in the sagittal plane. Once the tip of the sensor was placed IRB approval was obtained from the local Research appropriately the pressure measurements were taken in dif- Ethics Committee of Imperial College London (Number: ferent ankle degrees of dorsi- and plantar fexion. R18048). Full ankle range of motion was measured for each speci- men using a goniometer. Mean ankle dorsifexion was 17.5° Statistical analysis (SD 7.7°, range 5°–30°), and mean plantar fexion range was 34.1° (SD 8.0°, range 20°–45°), similar to prior ankle ranges Data were analyzed in SPSS (v 22; IBM). After a Shap- of motion reported among younger populations [7]. Pressure iro–Wilk test, all data were found to be normally distributed measurements were taken with the foot in neutral alignment and assessed with parametric analysis. A one-way ANOVA (plantigrade), full dorsifexion, full plantar fexion, and mid- was performed to compare for diferences in KFP pressure in range plantar fexion. each area across the diferent fexion angles assessed. Where signifcant, a paired t test was then performed to compare In vitro deformation and anatomical study the diferences in pressure across individual fexion angles. Signifcance level was set to p < 0.05. The skin and subcutaneous fat were removed, taking care not to penetrate the fascia overlying the Achilles fat pad. Once the KFP was visible from the medial and lateral areas, pho- Results tographs were taken with a ruler in the photograph to allow correction of magnifcation, and ImageJ (National Institutes Pressure measurements across range of motion of Health, Bethesda, MD) was used to make photographic measurements [8]. ImageJ has previously been found to There was a signifcant diference in mean pressure identi- demonstrate high reliability to 0.1 mm. For IFP measures in fed across diferent fexion angles in the KFP in both areas the current study, it was confrmed to have a mean test re- assessed (p < 0.05). Mean pressures from mid-range fexion test diference of 0.1 ± 0.05 mm (mean ± standard deviation), angles (PG and 50% PF) signifcantly difered when com- with ICC of 0.98 [9]. pared to terminal range angles (full PF and full DF) for both Videos were also taken of the deformation of the KFP measured points (Achilles mid-portion and retrocalcaneal through ankle range of motion. A small window was created bursa) (all: p < 0.05) (Fig. 1; Table 1). in the retrocalcaneal bursa to allow for visualization of the No signifcant diferences were found between full DF bursal wedge portion of the KFP. The gastrocnemius muscle and full PF or between PG and 50% PF in any of the two was then detached from the deep posterior compartment of measured points. the leg proximally and working its way distally, the KFP was freed of any attachments to the Achilles. In two specimens and prior to the detachment of the gastrocnemius, the KFP was only detached from its anterior attachment to the FHL in one specimen and from its posterior attachment to the Achilles in another. At this point the ankle was mobilized throughout its entire range to assess for any KFP motion and specifcally for the bursal wedge motion. Finally the KFP was completely removed from its attachments and its dimen- sions were documented. Volumetric measures were obtained based on Archimedes principle. The KFP was placed in a measuring cylinder flled with water and the rise in the water level after immersing the object was recorded [10]. Fig. 1 Pressure measurements. Chart with the results of pressure measurements in the retrocalcaneal bursa (bursa) and within the MRI study Kager’s fat pad at the level of the midportion of the Achilles tendon (mid-portion), throughout diferent points of ankle range of motion. DF dorsifexion, PG plantigrade, PF plantar fexion. The mean pres- Three healthy volunteers had their ankle scanned in a 3 T sures signifcantly increased in the extremes of motion (full PF, full MRI scanner (Siemens) in 10° increments from full plantar DF) when compared to mid-range values (PG, 50% FP) (p < 0.05)

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Table 1 Comparison of mean Areas assessed Ankle fexion points compared pressures and SD experienced across diferent fexion angles in Full DF − PG PG − 50% ROM 50% ROM − full PF PG − full PF the KFP in both areas assessed Mid-portion of Achilles 10.6 ± 11.09 11.15 ± 14.6 − 7.34 ± 6.05 − 6.8 ± 4.22 P value < 0.05 < 0.05 < 0.05 < 0.05 Retrocalcaneal bursa 5.25 ± 5.07 4.24 ± 5.34 − 4.64 ± 2.5 − 5.66 ± 6 P value < 0.05 < 0.05 < 0.05 < 0.05

Values expressed in MPa DF dorsifexion, PF plantigrade, 50% ROM mid-range of motion, PF plantar fexion

Fig. 2 KFP and surrounding structures. Posterior view of ankle dis- wedge extension of KFP (2), muscle fbers of gastroc-soleus complex section with the tendo Achilles refected and the KFP detached from (3), anterior aspect of tendo Achilles (4) retrocalcaneal bursal space all its insertions except for those to the calcaneal tuberosity. KFP (1), (5)

Anatomy In full dorsiflexion the bursal wedge moved out and in full plantar flexion it moved into this space. This bursal In all specimens, the KFP was adherent to both the Achil- wedge had adhesions onto the calcaneus superiorly and les posteriorly (mean length of 7.7 cm, SD 0.27), and the mediolaterally that seem to dictate the movement of the FHL muscle and fascia anteriorly (mean length of 10 cm, wedge in accordance to calcaneal movement (Fig. 3). In SD 2.03), leaving only an area of separation in the retro- two of the specimens, (2/12: 16.7%) an arterial branch calcaneal bursa (mean length of 0.92 cm, SD 0.24). The was identified communicating the KFP and tibialis artery KFP is, therefore, adherent to the Achilles tendon for a through the fascia cruris. The mean volume of the whole mean of 89% of its length and the bursal space represents KFP is of 10.6 ml (SD 3.37). The video shows changes in the remaining 11%. The KFP constantly formed a tongue- the shape of the KFP throughout ankle range of motion, like extension at the retrocalcaneal bursal space that was being particularly evident at the extreme of dorsiflexion moving in and out of the space between the Achilles and when the KFP is seen to bulge both medially and later- calcaneus during range of motion. The mean dimen- ally as the Achilles closes the space occupied by the KFP sions of the bursal wedge were 0.76 cm (SD 0.27) length (Fig. 4) (Video 1). (from its base to the tip) and 0.99 cm (SD 0.34) width at On the anterior aspect of the KFP an extension of the fatty its base which corresponds to its widest point (Fig. 2). tissue was found to pass under an arch of the fascia cruris to

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MRI study

The video created using images of the sagittal slices from the scans demonstrates the deformation undergone by the KFP during ankle motion. In all cases, when achieving full dorsifexion, the anteroposterior dimensions throughout the length of the KFP become narrower compared to the plan- tigrade position. In full plantar fexion the antero-posterior dimensions remain grossly unchanged from the plantigrade position. Those volunteers that achieved higher degrees of dorsifexion also showed higher amount of KFP narrowing relative to the widest dimension observed. Although all KFP appear triangular shaped in MRI scans, there is variability of these triangles among the examined healthy individuals (Video 2).

Discussion

The most important fnding of this study is the quantifca- Fig. 3 ‘Wedge’ extension. Posterior view of ankle dissection with the tion in human cadavers for the pressure changes experienced tendo Achilles refected to expose the KFP. Note the retrocalcaneal within the KFP throughout ankle range of motion. The bursal space between the calcaneal tuberosity and the attachment of motion of the KFP and its bursal wedge has been dynami- the Achilles tendon (a) and the ‘wedge’ extension identifed as a con- stant fnding in all our dissections (b) cally documented in cadavers and in vivo with the use of MRI. The new anatomical fndings described including attachments of the KFP with its neighbouring structures support its function as a shock absorber in the ankle. The motion and signifcant deformation experienced by the KFP is guided by its insertions and the musculotendinous struc- tures that surround it. It is, therefore, reasonable to assume that any surgical or traumatic injury to those or the KFP itself will afect the motion and function of this part of the ankle. It had been hypothesised that the bursal wedge helps to minimize pressure changes in the retrocalcaneal bursa and our results support this hypothesis [11]. It appears that for the same position of the ankle, pressure measurements are reduced in the retrocalcaneal bursa when compared to the midportion of the TA. In both the bursal and the midportion areas there is a signifcant increase in pressure when reach- ing the extremes of passive ankle plantar- or dorsifexion in comparison to the midrange of motion. This fnding presents the possibility of the KFP having a proprioceptive role. This maybe an important consideration when developing physi- Fig. 4 Changes in shape of KFP during ankle motion. Posterior view otherapy protocols for treatment of Achilles related condi- of ankle dissection showing the KFP in full plantar fexion, neutral position, and full dorsifexion where the KFP bulges out medially and tions. Extreme end ranges of motion (full plantar fexion laterally (yellow dotted lines) or full dorsifexion) should be avoided as these could be detrimental for the Achilles or surrounding KFP. Dissection of the specimens allowed for identifcation of extend onto the posterior ankle capsule (Fig. 5). Macroscopi- the close relationship and adhesions between the KFP and cally, the fat consistency and appearance were diferent in the Achilles posteriorly as well as the FHL muscle anteri- the Achilles-related area in comparison to the FHL-related orly. Only in the posterior distal corner of the KFP was this area which was more fbrous. adhesion with the Achilles interrupted to give way to the

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Fig. 5 Extension under arch of fascia cruris. a Posterior ankle dissec- evident (1). b–c The tunnel formed by this fascial arch is occupied by tion down to the level of superfcial fascia. After excision of tendo an extension of the Kager’s fatty tissue (4) that enters the deep poste- Achilles (2) and Kager’s fat pad, the arch created by the deep fascia is rior compartment (3) retrocalcanealbursal space. Dynamic evaluation confrmed an increase in pressure values in both groups, similar to our the efect of the Achilles and the FHL in driving the move- fndings. In their study, however, no pressure measurements ment of the KFP. Alteration of this anatomic confguration were obtained from the area adjacent to the Achilles mid- during surgery or injuries in the vicinity of the KFP (i.e. portion that could confrm or refute the same hypothesis in crural fascia or Achilles tendon tears), hindfoot endoscopy cases of midportion tendinopathy. Our results corroborate may have implication due to the disruption of normal KFP this possibility due to the similar pattern of increased pres- motion. It is worth highlighting that the specimens used sure seen in the extremes of ankle motion. These fndings were of young cadavers (mean 41.4 ± 10.3 years) which is and other previous studies support the general idea that the the age when pathologies like Achilles tendinopathy and retrocalcaneal bursa functions as a bufer to decrease local fascia cruris tears around the ankle are generally encoun- pressure and friction although the mode of action for this tered [1, 12]. pressure reduction is unclear [11, 13]. Likewise, an infamed Pressure in the retrocalcaneal bursa has been investigated and fuid-flled bursa in retrocalcaneal bursitis creates higher previously in vivo study, on a single individual, using a pressures in the bursa that seem to impair the physiologic cannula commercialized for monitoring arterial blood pres- “bufer” efect [4, 14]. This further supports the hypothesis sure [5]. In contrast with our results, the authors found that that in pathologic cases the retrocalcaneal bursa experiences increasing ankle dorsifexion did not result in an increase some degree of hypertension due to the infammation and in pressure in the retrocalcaneal bursa. The discrepancy in increased fuid produced by the bursitis. fndings could be as a result of the difering test protocols A further study assessed pressure changes in the periten- applied. In the in vivo test, the authors applied a maximum dinous area ventral to the Achilles in healthy, young indi- of 50 N of passive dorsifexion but it is possible that maxi- viduals [15]. They found a linear decrease in pressure with mum dorsifexion was not reached by this force and, there- increasing active isometric torque in the plantar direction. fore, the results may not be comparable to those of the cur- This study confrmed that when actively contracting the rent study, where pressure in full dorsifexion was measured calf muscles, a negative pressure is experienced in the KFP in each specimen. Further studies with greater participant area. The discrepancy between the positive pressure experi- numbers should seek to investigate this further. enced in our study when evaluating passive movement and There is evidence that in patients with retrocalcaneal bur- the negative pressure experienced during active movement sitis, the pressure in the retrocalcaneal bursa is increased demonstrates that the KFP functions in conjunction with compared to control patients sufering from midportion the muscular units surrounding it. It is likely that the con- Achilles tendinopathy [4]. In this comparative study by traction of muscular fbres and its corresponding reduction Lohrer et al., the efect of dorsifexion was associated with in volume will cause a negative pressure efect and this is

1 3 Knee Surgery, Sports Traumatology, Arthroscopy transmitted between the interrelated FHL muscle, the KFP, Ethical approval This article does not contain any studies with human and the Achilles. Further investigation on the anatomical participants or animals performed by any of the authors. and physiological relationships between the KFP and its sur- rounding structures is warranted. There are some limitations to this study. First, despite the References efort to load the muscles in a physiological manner to mimic the efects of gait, the in vitro testing characteristics may 1. Webborn N, Morrissey D, Sarvananthan K, Chan O (2015) Acute be lower and less adaptable than those estimated to occur tear of the fascia cruris at the attachment to the Achilles tendon: a new diagnosis. Br J Sports Med 49:1398–1403 in vivo. Second, the pressure sensor was introduced within 2. 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These fndings and the accurate dynamic description ogy. Champaign, IL, pp 164–253 14. Canoso JJ (1998) The premiere enthesis. J Rheumatol help to understand the function of the KPF and may have 25:1254–1256 implications in heel pain related conditions. 15. Langberg H, Skovgaard D, Bülow J, Kjaer M (1999) Negative interstitial pressure in the peritendinous region during exercise. J Appl Physiol 87:999–1002 Funding This study was part of and was made possible thanks to the Publisher’s Note “ESSKA-AFAS Pau Golanó Research Fellowship” awarded to Franc- Springer Nature remains neutral with regard to esc Malagelada by ESSKA-AFAS under the supervision of Mr James jurisdictional claims in published maps and institutional afliations. Calder at Fortius Clinic, London, UK. Further funding was provided by Fortius Research and Education Foundation, London, UK.

Compliance with ethical standards

Conflict of interest The authors declare that they have no confict of interest.

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