http://informahealthcare.com/cts ISSN: 0300-8207 (print), 1607-8438 (electronic) Connect Tissue Res, Early Online: 1–7 ! 2015 Informa Healthcare USA, Inc. DOI: 10.3109/03008207.2015.1026437

Effect of taurine on rat Achilles tendon healing Ovunc Akdemir1, William C. Lineaweaver2, Turker Cavusoglu3, Erdal Binboga4, Yigit Uyanikgil3, Feng Zhang5, Mahmut Pekedis6, and Tugay Yagci7

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Department of Plastic, Reconstructive, and Aesthetic Surgery, Kemerburgaz University, Istanbul, Turkey, 2Joseph M. Still Burn and Reconstructive Center, Brandon, MS, USA, 3Department of Histology and Embryology, Ege University, Izmir, Turkey, 4Department of Biophysics, Ege University, Izmir, Turkey, 5Department of Plastic and Reconstructive Surgery, University of Mississippi Medical Center, Jackson, MS, USA, 6Department of Mechanical Engineering, Engineering Faculty, Ege University, Izmir, Turkey, and 7Department of Orthopedic Surgery, Sisli Etfal Hospital, Istanbul, Turkey Abstract

Keywords

Taurine has anti-inflammatory and antioxidant characteristics. We have introduced taurine into a tendon-healing model to evaluate its effects on tendon healing and adhesion formation. Two groups of 16 rats underwent diversion and repair of the Achilles tendon. One group received a taurine injection (200 mg/ml) at the repair site, while the other group received 1 ml of saline. Specimens were harvested at 6 weeks and underwent biomechanical and histological evaluation. No tendon ruptured. Average maximum load was significantly greater in the taurine-applied group compared with the control group (p50.05). Similarly, average energy uptake was significantly higher in the taurine-applied group compared with the control group (p50.05). We observed no significant differences in stiffness in both groups (p40.05). After histological assessment, we found that fibroblast proliferation, edema, and inflammation statistically decreased in the treatment group (p50.05). These findings could indicate greater tendon strength with less adhesion formation, and taurine may have an effect on adhesion formation.

Antiadhesion, fibrosis, taurine, tendon healing, rats

Introduction Delayed tendon healing and tendon adhesions are still found to be among the complications that occur most often after tendon repair. After tendon injury, the process of healing or tissue repair starts. This process begins with a local inflammatory reaction characterized by edema, vasodilatation in the tissue, and tendon pain on movement and at rest. In addition, the recruitment of inflammatory cells and the production of humoral mediators, such as cytokines and eicosanoids, occur locally (1–5). Taurine was so named because it was first isolated from the bile of the ox (Bos Taurus) (6). The modern era of research on taurine may be considered to have been introduced by the seminal and thorough review of Jacobsen and Smith that appeared in this journal in 1968 (7). Since then, the increase in the range of phenomena with which taurine has been associated has been a little short of astounding. Taurine is a powerful antioxidant (8). It has been seen, in vitro, that taurine decreases the CD11b receptor in neutrophils, preventing the creation of induced glucose formation and apoptosis in endothelium (i.e. protecting tissues). These effects can minimize inflammation and

Correspondence: Ovunc Akdemir, Department of Plastic, Reconstructive and Aesthetic Surgery, Kemerburgaz University, Istanbul 34160, Turkey. Tel: +90 532 204 3139. E-mail: [email protected]

History Received 13 August 2014 Revised 16 February 2015 Accepted 23 February 2015 Published online 24 April 2015

scarring in injured tissue (9–11). Previously, we also presented the effects of 200 mg/kg taurine on ischemia– reperfusion injury (8). For that reason, we used same dosage to present anti-inflammatory and anti-adhesive effects. This study investigates the effects of taurine on tendon healing in rats and presents a model of Achilles tendon repair.

Material and methods Thirty-two legs of 16 male Sprague–Dawley rats weighing between 380 and 420 g were used in this study. The National Research Council’s guidelines for the care and use of laboratory animals were followed. The rats were anesthetized using pentobarbital administered by intraperitoneal injection (50 mg/kg). Sixteen rats with repaired Achilles tendons were randomly divided into two groups of eight. In the sham group (Group 1), saline was injected into each Achilles tendon at the repair site. In the treatment group (Group 2), taurine was injected into each Achilles tendon at the repair site.

Surgical procedure After shaving the legs of each animal, each Achilles tendon was cut through a skin incision. The Achilles tendon was approached by a posterior skin incision and freed from the surrounding tissue. After cutting the tendon with a scalpel at

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5 mm above its insertion to the calcaneus, it was sutured using a Kessler stitch with 5/0 prolene (an epitendinous suture was not used) (12). After the Group 1 tendons were sutured, they were irrigated with 1 ml saline. After the Group 2 tendons were sutured, a 1 ml powder taurine was dissolved in normal saline and was made into a 200 mg/kg solution, which was then injected into the tendons. The skin of each animal was sutured with 4/0 prolene. Following surgical intervention, no wound dressing was applied. The mobilization was not limited after surgery. Subjects were followed for 6 weeks. The left legs from each group were used for biomechanical analysis (n ¼ 8), and the right legs from each group were used for histopathologic and immunohistochemical analysis (n ¼ 8).

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Biomechanical analysis At the end of the sixth week, biomechanical tests were performed by the application of a tensile load at a speed of 5 mm/min on the tensile test machine model (Autograph AGIS 100 kN, Shimadzu Co., Kyoto, Japan) (Figure 1). It should be noted that the tensile machine has a capability to test the maximum 100 kN load (maximum load). A tensile machine test is displacement controlled, in that the sample is extended and the load required for this extension is measured. We used 5 kN Shimadzu Loadcell (Shimadzu Co., Kyoto, Japan) to obtain signal data with low noises. The tendons were dissected free from the extraneous soft tissue and harvested together with the calcaneal bones and parts of the gastrocnemius and soleus muscle complex. Two ends of the tendons were fixed on the test machine. The calcaneal bone with tendon was mounted and fixed on the base plate of the machine, and the other was fixed to a force plate of the machine. Prior to the experiment, the dimensions of the tendon were measured so that they could be used as Figure 1. (A) Sham group sample prior to biomechanical analysis. (B) Treatment group sample prior to biomechanical analysis. (A1) The appearance of sham group sample during biomechanical analysis. (B1) The appearance of treatment group sample during biomechanical analysis.

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parameters in biomechanical evaluation. Here, the tendon cross-sectional areas were measured with a calibrated micrometer. It is also noted that a circular cross section was assumed. In addition, the initial gage length of the tendon was measured with a caliper. The measurements were sampled at 1707.06 Hz. During the test, all ruptures in tendons occurred at the excised and repaired region. The biomechanical behaviors of the tendons, such as maximum load (N), tendon stiffness (N/mm), energy uptake (J), elastic modules (MPa), and maximum stress (MPa), were studied. Elastic modules could be defined as the ratio of the stress along an axis over the strain along that axis of stress. Here the stress could be the true stress or the engineering stress. The true stress is determined by the instantaneous load acting on the instantaneous cross-sectional area. The engineering stress is the load divided by this initial cross area. While the tendon is pulling, the length increases, but its area shrinks. At any load, the true stress is the load divided by the cross area at that instant. Unless the area is being monitored continuously during the test, it is difficult to calculate true stress. However, it can be also calculated approximately by the formulation given as follows: P E ¼ Ao T ¼

P ð1 þ "E Þ Ao

"E ¼

l  lo lo

  l "T ¼ ln lo

DOI: 10.3109/03008207.2015.1026437

where lo, l, P, E, T, "E, and "T, are initial length, ultimate length, load applied, engineering stress, true stress, engineering strain, and true strain, respectively. It is noted that the curves for engineering stress and true stress are identical to the yield point. In this way, Young’s modulus was calculated by dividing the tensile engineering stress to the tensile engineering strain in the elastic (initial, linear) portion of the stress–strain curve as follows:

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E P=Ao Plo ¼ ¼ "E DL=lo Ao DL

where E is Young’s modulus (modulus of elasticity), A0 is the original cross-sectional area of the tendon, P is the force applied to the tendon under tension, DL is the amount by which the length of the tendon changes, and L0 is the original length of the tendon. Before conducting the experiment, L0 and A0 (areas at the repair section) were measured. The other variables (P and DL) were extracted from the force– displacement curves after completing the experiment. A typical force–displacement curve obtained for a rat Achilles tendon sample is shown in Figure 2, and the strain–stress curve is given in Figure 3. Here, the noise ratio is approximately in the range of ±0.2 N. It can be seen that the curve shows a non-linear shape. The curve can be divided in three domain parts. The initial domain is characterized by a low stiffness of the tendon, which reflects that the collagen fiber is stretching to approximately 20%. The second domain, which exhibits a linear trend, starts. Here, the slope of the stress–strain curve is almost constant. Note that the elastic module was calculated in this region. An additional increment in tendon strain results in fiber tissue failure so that the tension in the tendon decreases. The area-under-the-stress– strain diagram represents the energy uptake, demonstrating the energy required to cause the tendon to rupture. The collagen in connective tissue has organized fibers that transmit the energy of the muscle to the bone. Here, the idea is to explore whether the taurine has an advantage in tendon healing in terms of energy uptake, which reflects the organization of fibers (Figure 3).

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under ketamine+xylasine anesthesia after intracardiac fixation with 4% paraformaldehyde, weighed, post-fixed for 24 h, and processed for paraffin embedding. Paraffin sections were cut into 5 mm thick slices in microtome (Leica RM 2145, Leica Biosystems, Buffalo Grove, IL) and stained with routine hematoxylin–eosin (H&E) and Mallory tricrome histostains. The sections were examined under a highperformance light microscope (40 and 100 magnification). According to the modified Verhofstad scoring (8), the samples were examined within the five parameters, including polymorphonuclear leukocyte (PMN), fibrosis, fibroblast proliferation, edema, and vascularity (Table 1). Immunohistochemical analysis Immunohistochemical expression was analyzed using antifibronectin antibodies (Dako A0245, DAKO Corporation, Carpenteria, CA). Briefly, paraffin sections were immersed in xylene overnight and incubated in methanol containing 1% H2O2 to reduce endogenous peroxidase activity. Sections were kept in sodium citrate solution in the microwave oven at 90 W for 5 min and at 360 W for 15 min. After washing in 0.2 M Tris–HCl, including 0.5% Triton X, the sections were exposed to the mouse anti-fibronectin primary antibody (Dako A0245, DAKO Corporation, Carpenteria, CA), antiINOS (SigmaN7782, Sigma, Taufkirchen, Germany), and anti-Desmin (Dako D33-N1526, Dako North America, Inc., Via Real Carpinteria, CA). Sections were then incubated with mouse monoclonal PAP complex (DAKO Corporation, Carpenteria, CA; 1:200 dilutions) and reacted with 0.05% diaminobenzidine (Zymed Histostain Plus Ref/Cat no. 859643 San Francisco, CA) and 0.01% H2O2. Immunoreaction was assessed by light microscopy (Olympus BX-51 light microscope, Olympus C-5050 digital camera, Olympus Corporation, Tokyo, Japan) at a magnification of 40–100. Statistical assessment

Histopathological and immunohistochemical analyses were made at the end of the biomechanical analysis. Thereafter, at the end of 6-week recovery period, tendons were removed

The statistical analysis of the obtained data was performed using SPSS 14.0 (SPSS Inc., Chicago, IL) package program. The Mann–Whitney U test was used for histopathologic assessment. The p values50.05 are regarded as statistically significant. The Wilcoxon Signed Rank tests were performed to determine biomechanical variables, such as mean maximum load, tendon stiffness, and energy uptake; elastic modules and maximum stress for both groups were

Figure 2. A typical displacement–force curve of the rat Achilles tendon.

Figure 3. A typical strain–stress curve of the rat Achilles tendon.

Histopathologic analysis

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Table 1. Histopathologic evaluation of the Verhofstad-modified scoring table (8). Score

Fibrosis

PMN

Edema

Fibroblast proliferation

Vascularity

0 1 2 3

None Superficial Pronounced Massive

Normal Light Pronounced Massive

None Light Pronounced Dense

None Light Pronounced Dense

None Light Pronounced Dense

PMN, polymorph nuclear leukocyte. 0: none; 1: mild; 2: moderate; 3: severe.

Table 2. Averaged geometrical and biomechanical properties of the Achilles tendons for taurine applied and sham groups. Taurine (n ¼ 8)

Variable

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Geometrical properties Structural properties Material properties

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Section area (mm ) Gauge length (mm) Maximum load (N) Stiffness (N/mm) Energy uptake (J) Elastic modules (MPa) Maximum stress (MPa)

2.42 14.60 47.95 11.04 0.11 69.05 21.40

(0.15) (1.26) (9.27) (2.02) (0.03) (12.67) (4.13)

Sham (n ¼ 8)

p Value

2.27 14.20 40.45 11.11 0.09 69.42 18.05

0.060 0.470 0.025* 0.890 0.012* 0.900 0.025*

(0.13) (0.80) (4.50) (1.41) (0.034) (8.82) (3.85)

Data presented as mean (standard deviation). *p50.05.

Table 3. Histopathologic evaluation of the Verhofstad-modified scoring table. Groups Sham (N ¼ 8) Treatment (N ¼ 8)

Fibrosis

Fibroblast proliferation

Edema

PMN infiltration

Vascularity

2.55 ± 0.52* 0.5 ± 0.53

2.66 ± 0.5* 1.37 ± 0.51

2.33 ± 0.5* 0.25 ± 0.46

2.77 ± 0.44* 0.37 ± 0.51

1.22 ± 0.97 2.75 ± 0.46*

PMN, polymorph nuclear leukocyte. *p50.05 statistically significant higher.

significantly different. Data were presented as mean ± SD and supported with graphics and tables. All analyses were performed with a 95% confidence interval in the Statistical Package for Social Sciences (SPSS Inc., Chicago, IL). p50.05 was regarded as statistically significant.

group (p50.05). Mean vascularity was significantly higher in the taurine group compared with the sham group (p50.05; Figure 4).

Results

The aim of tendon repair is the restoration of the mechanical functions of the tendon. The tendon rupture is a definitive but relatively minor failure of tendon repair. The greatest obstacle against a successful outcome is the adhesion formation that leads to a loss of the gliding surface during the healing process (13). The type of injury, coarse manipulation during repair, traumatized tendon sheaths, ischemia of the tendon, immobilization, repairs with gaps, and sheath excision are factors that cause adhesive bands around the repaired tendon and limit the excursion (14). The challenge with this clinical problem is to reconcile the competing needs of limiting scarring between the tendon and surrounding soft tissues while allowing scarring in the tendon to achieve wound healing (15). Numerous strategies have been used experimentally to reduce formation of the bands of scar tissue that form adhesions. These approaches can be grouped into those modifying the wound-healing response (16–20) and those interposing physical or chemical barriers between the tendon and the surrounding soft tissues (21–26). Various biologic materials (e.g. paratenon, tunica vaginalis, fibrin film, vein grafts, arterial grafts, and fascial patch grafts) and synthetic

No tendons ruptured. All rats were alive at 6 weeks. The results of the biomechanical assessment The geometrical properties of the sham and treatment groups are given in Table 2. The results showed no significant difference between the two groups in terms of section area of the tendons (p40.05). Mean maximum load and maximum stress were significantly greater in the taurine group compared with the sham group (p50.05). Similarly, mean energy uptake was significantly higher in the taurine-applied group compared with the sham group (p50.05). We observed no significant differences in stiffness or elastic modules in both groups (p40.05). The results of the histopathologic assessment The histopathologic properties of the Achilles tendons are represented in Table 3. Mean fibrosis, fibroblast proliferation, edema, and PMN infiltration were significantly greater in the sham group compared with the taurine-applied

Discussion

DOI: 10.3109/03008207.2015.1026437

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Figure 4. (A) Tendon appearance of the sham group (H & E staining, 40 magnification). (B) Tendon appearance of the treatment group (H & E staining, 40 magnification). (C) Tendon appearance of the sham group (Mallory-Tricrome staining, 100 magnification). (D) Tendon appearance of the treatment group (Mallory-Tricrome staining, 100 magnification).

materials (e.g. metal tubes, cellophane, celloidin, polytef, polyethylene, Millipore cellulose tube, polytetrafluoroethylene, and silicon sheaths) have been used to make barriers for reducing adhesion (27,28). Some of these alloplastic and biological materials have led to unsuccessful results by causing serious inflammatory response and adhesions and some disabled diffusion and healing, leading to the necrosis of the tendon (28). Biomechanical agents have also been tried to prevent adhesions, such as antihistamines (29), steroids (30), and nonsteroid anti-inflammatory drugs (e.g. ibuprofen) (31), beta-amino propionitrile (32), hyaluronate (i.e. sodium hyaluronate or hyaluronic acid) (33), collagen-enriched topical solutions (34), fibrin sealants (17), and 5-FU (35) are some examples. However, the perfect method has not been achieved yet (28). Taurine is known to demonstrate antioxidant and antiinflammatory effects in tissues by decreasing the lipid peroxidation and neutrophil adhesion (8,36,37). Taurine also prevents changes in membrane permeability after the oxidant damage (38). No side effects have been recorded in the literature related to the use of taurine. Sılaeva et al. (39) have shown that the most effective treatment with taurine is a 200 mg/kg dose through intraperitoneal or intravenous administration. This dosage is also used for antioxidant and antiinflammatory effects (8). Our study examined the effects of taurine on tendon healing. The parameters of maximum load, energy uptake, and maximum stress were significantly increased in the taurine group. When the sham group and the test group were histopathologically compared, it was found that the levels of fibroblasts, PMN, edema, and fibrosis in the sham group were higher than that of the taurine group. Fibronectin, with its muldomain structure, plays a role as ‘‘master organizer’’ in the matrix assembly as it forms a bridge between cell surface

receptors (e.g. integrins and compounds such as collagen, proteoglycans, and other focal adhesion molecules). It also plays an essential role in the assembly of fibrillin-1 into a structured network. Laminins contribute to the structure of the extracellular matrix (ECM) and modulate cellular functions such as adhesion, differentiation, migration, stability of phenotype, and resistance toward apoptosis. The primary role of fibrinogen is in clot formation. But after conversion to fibrin by thrombin, it also binds to a variety of compounds, particularly to various growth factors. As such, fibrinogen is a player in cardiovascular and extracellular matrix physiology (40). Soeda et al. (41) have shown that taurine and its breakdown products (taurolidine, taurocholate, etc.) prevent fibronectin expression; they stimulate plasminogen and decrease fibrin formation (41). Thus, the formation of adhesion in tissues decreases. Tarhan et al. (42) have applied taurolidine for increasing peritoneal fibrinolysis to prevent intra-abdominal adhesion formation. Immunohistochemically, fibronectin immunoreactivity was higher in the sham group in comparison with the treatment group, and it was found to be dense in small areas (Figure 5A and B). In the INOS coloring, it was found that the INOS expression was highly consistent with the fibrosis in the sham group (Figure 5C and D). In the desmin coloring, immune coloring was detected where the skeletal muscle connects tendons. In the treatment group, immunoreactivity in the adhesion zones was found to be higher in comparison with the sham group (Figure 5E and F). Biomechanical characterization of connective tissues such as tendons has been a research subject for a long time (42). Many biomechanical constitutive models to describe material behavior of the tendon generally assume incompressibility due to the difficulty of measuring the instantaneous crosssectional area of the tendon during tensile loading (43–46). Eppel et al., in their study, predicted the cross-sectional area

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Figure 5. (A) Tendon appearance of the sham group (Fibronectin staining, 100 magnification). (B) Tendon appearance of the treatment group (H & E staining, 100 magnification). (C) Tendon appearance of the sham group (INOS staining, 100 magnification). (D) Tendon appearance of the treatment group (INOS staining, 100 magnification). (E) Tendon appearance of the sham group (Desmin staining, 40 magnification). (F) Tendon appearance of the treatment group (Desmin staining, 40 magnification).

instantaneously with the hypothesis of constant volume during loading (47). However, these approaches do not reflect the material behavior of tissue experimentally (48). In our study, as a limitation, a constant cross-sectional area was assumed while determining the biomechanical parameters due to the difficulty of measuring the instantaneous cross-sectional area of the tendon during tensile loading, similar to the studies reported above. However, the volume of fibrous connective tendon tissue changes when subjected to uniaxial extension because of the large Poisson ratio. In other words, the Poisson ratio shows the volume loss in the tissue during loading. Recently, Swedberg et al. (48) demonstrated an isotropic model for compressibility of the tendon. Vergari et al. (49), in their study, found that the difference between engineering and true stress corresponded to a cross-sectional area percentage variation of 7.1–13.6% at tendon failure. In the future, we will explore the effects of taurine on the Poisson ratio during instantaneous tensile loading by designing an experimental setup to monitor the cross-sectional area of the Achilles tendon for more accurate biomechanical evaluation. In conclusion, many treatments have been tried to prevent tendon adhesion. In our study, the biomechanical,

histopathological, and immunohistochemical results for the taurine group shows us that taurine may reduce scar formation and increase the strength of tendon repairs. If the results here translate to the human tendon, taurine could be useful as a locally injected adjunct to clinical tendon rupture. However, any reference to a possible effect on adhesion formation should be excluded, as this effect has not been tested in the current study and represents simply an opinion of the authors.

Declaration of interest The authors report that they have no conflicts of interest. The authors alone are responsible for the content and writing of this article.

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Effect of taurine on rat Achilles tendon healing

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Effect of taurine on rat Achilles tendon healing.

Taurine has anti-inflammatory and antioxidant characteristics. We have introduced taurine into a tendon-healing model to evaluate its effects on tendo...
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