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Inflammatory and Metabolic Alterations of Kager's Fat Pad in Chronic Achilles Tendinopathy

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Inflammatory and Metabolic Alterations of Kager's Fat Pad in Chronic Achilles Tendinopathy RESEARCH ARTICLE Inflammatory and Metabolic Alterations of Kager's Fat Pad in Chronic Achilles Tendinopathy Jessica Pingel1☯, M. Christine H. Petersen2,3☯, Ulrich Fredberg4,Søren G. Kjær4, Bjørn Quistorff3, Henning Langberg5, Jacob B. Hansen2* 1 Department of Exercise and Nutrition, University of Copenhagen, Copenhagen, Denmark, 2 Department of Biology, University of Copenhagen, Copenhagen, Denmark, 3 Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark, 4 Diagnostic Centre, Silkeborg Regional Hospital, Silkeborg, Denmark, 5 CopenRehab, Department of Public Health, University of Copenhagen, Copenhagen, Denmark ☯ These authors contributed equally to this work. * [email protected] Abstract OPEN ACCESS Background Citation: Pingel J, Petersen MCH, Fredberg U, Kjær Achilles tendinopathy is a painful inflammatory condition characterized by swelling, stiffness SG, Quistorff B, Langberg H, et al. (2015) and reduced function of the Achilles tendon. Kager’s fat pad is an adipose tissue located in Inflammatory and Metabolic Alterations of Kager's Fat Pad in Chronic Achilles Tendinopathy. PLoS ONE 10 the area anterior to the Achilles tendon. Observations reveal a close physical interplay be- (5): e0127811. doi:10.1371/journal.pone.0127811 tween Kager’s fat pad and its surrounding structures during movement of the ankle, sug- ’ Academic Editor: Hazel RC Screen, Queen Mary gesting that Kager s fat pad may stabilize and protect the mechanical function of the ankle University of London, UNITED KINGDOM joint. Received: January 19, 2015 Accepted: April 18, 2015 Aim Published: May 21, 2015 The aim of this study was to characterize whether Achilles tendinopathy was accompanied by changes in expression of inflammatory markers and metabolic enzymes in Kager’sfat Copyright: © 2015 Pingel et al. This is an open access article distributed under the terms of the pad. Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any Methods medium, provided the original author and source are credited. A biopsy was taken from Kager’s fat pad from 31 patients with chronic Achilles tendinopathy Data Availability Statement: All relevant data are and from 13 healthy individuals. Gene expression was measured by reverse transcription- within the paper and its Supporting Information files. quantitative PCR. Focus was on genes related to inflammation and lipid metabolism. Funding: This work was supported by a grant to JBH from the EU FP7 project DIABAT (HEALTH-F2-2011- Results 278373). MCHP was funded in part by The Danish Diabetes Academy supported by The Novo Nordisk Expression of the majority of analyzed inflammatory marker genes was increased in pa- Foundation. tients with Achilles tendinopathy compared to that in healthy controls. Expression patterns β Competing Interests: The authors have declared of the patient group were consistent with reduced lipolysis and increased fatty acid -oxida- that no competing interests exist. tion. In the fat pad, the pain-signaling neuropeptide substance P was found to be present in PLOS ONE | DOI:10.1371/journal.pone.0127811 May 21, 2015 1/13 Kager's Fat Pad in Achilles Tendinopathy one third of the subjects in the Achilles tendinopathy group but in none of the healthy controls. Conclusion Gene expression changes in Achilles tendinopathy patient samples were consistent with Kager’s fat pad being more inflamed than in the healthy control group. Additionally, the re- sults indicate an altered lipid metabolism in Kager’s fat pad of Achilles tendinopathy patients. Introduction Adipose tissue has multiple functions including insulation and structural support, but is first and foremost a key metabolic tissue with profound influence on whole-body homeostasis [1]. Two main types of adipose tissue exist: white adipose tissue, which is the largest energy store of the body, and brown adipose tissue that is specialized in energy dissipation through uncoupled respiration. Adipocytes secrete adipokines, cytokines, and growth factors, acting in endocrine, paracrine or autocrine manners, thereby influencing appetite, insulin sensitivity, metabolism of other tissues and processes like healing, inflammation and tissue degradation [1–4]. Kager’s fat pad, also described as the pre-Achilles fat pad, is a sharply enclosed radiolucent triangle delineated by the flexor halluces longus muscle and tendon (anterior border), the supe- rior cortex of the calcaneus (inferior border) and the Achilles tendon (posterior border) [5]. It has been suggested that the flexor halluces longus part of Kager’s fat pad contributes to moving the bursal wedge during plantar flexion, that the Achilles-associated part protects blood vessels passing through it to supply the Achilles tendon, and that the region near the bursal wedge minimizes pressure changes in the retrocalcaneal bursa [6]. Changes in Kager’s fat pad have been observed in a variety of conditions, including cortical destruction of the calcaneus mediat- ed by either a tumor or infection, Os trigonum syndrome [5], accessory soleus muscle [7] and fibroma of the tendon sheath [8]. Radiographical changes in Kager’s fat pad can signal the pres- ence of abnormality [5]. Abnormal conditions involving the posterior ankle may result in in- creased and ill-defined soft tissue density in Kager’s fat pad or the obliteration of its borders. Additionally, patients with chronic pain in the Achilles tendon, Achilles tendinopathy (AT), often show an increased soft tissue density simultaneously with an increased thickness of the Achilles tendon. Despite the common occurrence of pain symptoms and soft tissue alterations in Kager’s fat pad, this region has not been investigated, and detailed knowledge of its role in the pathophysiology of the Achilles tendon is sparse. Another fat pad that has received more attention is the infrapatellar fat pad (IFP), also known as Hoffa’s fat pad. Chronic edema of the IFP is the key pathology of Hoffa’s disease, the edema leading to soft tissue impingement, ischemia, and in the long-term lipomatous tissue ne- crosis [9,10]. IFP contains inflammatory cells and is a source of adipokines, cytokines and growth factors, which might impact disease [11]. Several inflammatory mediators secreted from adipose tissue, including interleukin-1α (IL-1α), IL-1β, IL-6, IL-10, tumor necrosis fac- tor-α (TNF-α), monocyte chemotactic protein-1 (MCP1) and prostaglandin E2, have been shown to be involved in joint diseases [12–14]. Furthermore, one study showed that adiponec- tin (ADIPOQ) induces matrix metalloproteinase-1 and IL-6 expression in synovial fibroblasts [15]. Thus, ADIPOQ might have pro-inflammatory functions in joint diseases [16]. These find- ings underline that, besides being a reservoir for storage of excess calories, adipose tissue plays PLOS ONE | DOI:10.1371/journal.pone.0127811 May 21, 2015 2/13 Kager's Fat Pad in Achilles Tendinopathy an important role in the process of inflammation [12]. Whether these inflammatory cells and mediators are also present in Kager’s fat pad and whether the potential inflammatory state of the fat pad may influence pain and other symptoms of AT patients is still unclear. The aim of the present study was to analyze gene expression changes in Kager’s fat pad of chronic AT patients. Our focus was on genes encoding macrophage markers, adipokines, cyto- kines and growth factors as well as genes involved in lipid and energy metabolism. We provide evidence that patient-derived fat pads display a remarkable inflammatory profile and altered expression of a number of metabolism-related genes. Materials and Methods Subjects The subjects were fully informed and gave their written consent to participate in adherence to the declaration of Helsinki. The study was approved by the Ethical Committee of the capital re- gion of Copenhagen, Denmark (H-1-2009-114). Thirty-one AT patients were recruited for this study. One AT patient had to be excluded due to failure in the process from biopsy to cDNA. In addition, 13 healthy control subjects were recruited. The AT patients were all recreational athletes or persons with physical work with a long history of chronic Achilles tendon pain (sub- ject characteristics are shown in Table 1), on whom conventional conservative treatments, like eccentric training programs, non-steroidal anti-inflammatory drug medication, and corticoste- roid injections, had been tried with no lasting effect. A window of at least 6 months between the most recent last intake of these medications and the present study was ensured in all cases. Control subjects had no previous history of symptoms of Achilles tendon or Kager’s fat pad pain sensation and were without acute or chronic diseases. All AT patients were recruited from the Diagnostic Centre, Silkeborg Regional Hospital, Denmark. Design and biopsy procedure To ensure that all participants were in a resting state, they were asked to abstain from any kind of exercise 24 h prior to the experiment. After arrival to the clinic, body weight and height were recorded before preparation for biopsy. A biopsy of Kager’s fat pad was taken from the subjects placed in a supine position. The subjects were locally anesthetized under ultrasound guidance with 2 ml 1% lidocaine in the peritendinous space from both the medial and lateral side of the tendon. An ultrasound guided biopsy of Kager’s fat pad was taken from the middle of the Kager’s triangle with a semi-automatic biopsy needle [14 GA 9 cm (Angiotech)]. The samples were snap-frozen in liquid nitrogen and stored at -80°C for later RNA isolation. Table 1. Subject characteristics. Subjects Sex Age Height Weight BMI Duration of symptoms (n) (F/M) (years) (m) (kg) (mo.) Controls 13 7/6 29 1.73 71.1 23.5 _ (19–48) (1.6–1.88) (51–94) (19.9–29.0) Patients 30 10/20 49 1.78 91.2 28.8 40 (31–67) (1.6–1.96) (66.7–122) (22.5–38.5) (9–156) Values are presented as mean (min—max). F, female; M, male; BMI, body mass index; mo., months.
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