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Use of Adipose Tissue-Derived Mesenchymal Stem Cells for Experimental Tendinitis Therapy in Equines

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Use of Adipose Tissue-Derived Mesenchymal Stem Cells for Experimental Tendinitis Therapy in Equines View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Journal of Equine Veterinary Science 31 (2011) 26-34 Journal of Equine Veterinary Science journal homepage: www.j-evs.com Original Research Use of Adipose Tissue-Derived Mesenchymal Stem Cells for Experimental Tendinitis Therapy in Equines Armando de Mattos Carvalho MSc a, Ana Liz Garcia Alves PhD a, Patrícia Galvão Gomes de Oliveira MSc a, Luis Emiliano Cisneros Álvarez MSc b, Renée Laufer Amorim PhD c, Carlos Alberto Hussni PhD a, Elenice Deffune PhD d a Department of Veterinary Surgery and Anesthesiology, School of Veterinary Medicine and Animal Science, São Paulo State University, Botucatu, São Paulo, Brazil b Department of Animal Reproduction and Veterinary Radiology, School of Veterinary Medicine and Animal Science, São Paulo State University, Botucatu, São Paulo, Brazil c Department of Clinical Veterinary, School of Veterinary Medicine and Animal Science, São Paulo State University, Botucatu, São Paulo, Brazil d Blood Center, Botucatu Medical School, São Paulo State University, Botucatu, São Paulo, Brazil abstract Keywords: Superficial digital flexor tendon lesion is an important cause of lameness in equine Equine athletes. Although numerous treatments have been described, few are effective at Tendinitis promoting significant improvement in the quality of the extracellular matrix. Therefore, Mesenchymal stem cells great potential remains for recurrence and in certain cases, an abrupt end to the horse’s Adipose tissue Tendon repair athletic career. Recently, several experiments have focused on the therapeutic potential Collagenase of mesenchymal stem cells (MSCs) in cases of tendon lesions. This study aimed to evaluate the effect of adipose tissue-derived MSCs in the treatment of induced tendinitis of the superficial digital flexor tendon in horses by clinical, ultrasonographic, histo- pathological, and immunochemical analyses. Tendinitis was induced in both thoracic limbs of eight mares by administration of collagenase solution and adipose tissue was collected from the tail base for MSCs isolation and expansion, which were used during cellular therapy on only one limb 30 days after lesion induction. No differences occurred between the groups regarding the clinical and ultrasonographic analyses; however, histopathological evaluation revealed a significant improvement in tendon fiber orga- nization and diminished inflammatory infiltrate, whereas immunohistochemical analysis showed increased expression of type I collagen in the treated group as compared with controls. The cellular therapy model implanted in this experiment promoted increased perivascular inflammatory infiltrate, fibroblastic density, neovascularization, and quali- tative healing improvement of tendon extracellular matrix, in terms of fiber orientation and type I/III collagen ratio; moreover, it was considered to be a safe and viable process. Ó 2011 Elsevier Inc. Open access under the Elsevier OA license. 1. Introduction because of its high incidence, prolonged recovery period, and high rate of recurrence [2]. Possible explanations for Tendinitis of the superficial digital flexor tendon (SDFT) the slow healing of tendons and, in the majority of cases, is an extremely important affliction for equine athletes in the resulting formation of mechanically inferior extracel- all types of sports [1]. Tendinitis is an important cause of lular matrix are probably because of the fact that tendon is lameness and diminished performance in equine athletes a minimally vascularized tissue, presents cells that exhibit diminished mitotic activity, and the presence of few Corresponding author at: Armando de Mattos Carvalho, MSc, progenitor cells in the tissue [3,4]. Department of Veterinary Surgery and Anesthesiology, School of Veteri- Recurrences are related to the nonregeneration of nary Medicine and Animal Science, São Paulo State University (UNESP), Rubião Júnior, Botucatu 560, São Paulo, Brazil. tendon tissue and the production of a matrix of collagen E-mail address: [email protected] (A. de Mattos Carvalho). fibrils that are smaller in diameter and of inferior quality, 0737-0806 Ó 2011 Elsevier Inc. Open access under the Elsevier OA license. doi:10.1016/j.jevs.2010.11.014 A. de Mattos Carvalho et al. / Journal of Equine Veterinary Science 31 (2011) 26-34 27 showing a reduced number of crosslinks [3]. Therapies that and Animal Science, São Paulo State University, Brazil, and promote healthy tendon tissue regeneration should was performed under international guidelines for the care produce a reduction in recurrence rates as compared with and use of experimental animals. All the mares were those that promote the formation of scar tissue [5]. submitted to the same procedures, with differences only in Knowledge concerning tendon repair and its implica- the time of biopsy. To further improve the elucidation of the tions for the athletic capacity of the individual horses experiment, the horses were divided into two groups of affected by tendinitis has stimulated research regarding four mares each: Group A (GA), in which the mares were new therapies applied to this tissue. Cellular therapy using submitted to ultrasound examinations at 0, 2, 4, 6, and 8 mesenchymal stem cells (MSCs) has shown promising weeks and a bilateral biopsy of the digital flexor tendon results in several published works [1,2,6,7]. In cases of performed 60 days after lesion induction; and Group B tendon lesion in horses, the majority of published data have (GB), in which the mares were submitted to ultrasound focused mainly on the therapeutic potential of MSCs derived examinations at 0, 2, 4, 6, 8, 10, to a maximum of 21 weeks from bone marrow and adipose tissue, even though studies and a bilateral biopsy of the digital flexor tendon after indicate the possibility of other sources of MSCs in adult lesion induction for posterior histopathological and tissue, including brain tissue, dermis, periosteal, skeletal immunohistochemical analyses. The tendon biopsies were muscle, synovial, trabecular bone, and vascular tissue [8]. obtained on days 60 and 150 after collagenase application The most abundant and accessible source of stem cells is to investigate tendon healing evolution. adipose tissue [9], justifying the expressive interest in the development of cellular therapy involving this source. 2.2. Tendinitis Induction The stromal vascular fraction is a heterogenous cell population derived from adipose tissue that includes All the mares were subjected to lesion induction in the endothelial and epithelial cells, preadipocytes, and certain SDFT of both thoracic limbs in the region of the middle one- progenitor cells. These progenitors, adipose-derived MSCs, third of the metacarpal region. Lesion induction was ach- have shown multiple differentiation potential similar to ieved by local administration of 2.5 mg or 690 IU of type I bone marrow-derived MSCs [10]. collagenase (Collagenase type 1: C-0130, Sigma Pharma- MSCs implantation causes an increase in the number of ceutical, St. Louis, MO, USA) diluted in 1.0 mL of sterile progenitor cells than normally present in tendon tissue, water, guided by ultrasound equipment (Logiq 3, General thereby improving the potential for regeneration [11]. The Electric, Sangdaewon-Dong, Korea), similar to the method immunomodulatory properties of MSCs translate into anti- described by Maia et al. [14]. Prior sedation of the mares inflammatory effects in vivo and numerous animal studies was achieved with 10% xylazine (Sedazine, Fort Dodge, have demonstrated that exogenously administered MSCs Campinas, São Paulo, Brazil) at a dosage of 0.8 mg/kg, the attenuate inflammation and facilitate regeneration of region around the collection site was shaved and asepti- injured tissue [12]. cally prepared, and local anesthesia was performed by Till recently, existing reports have only described the perineural blockage of the lateral and medial palmar nerves clinical use of adipose tissue-derived MSCs isolated from in the proximal metacarpal region, using 2 mL of 2% lido- horses and expanded in the laboratory, as outlined by caine chlorhydrate (Xylestesin, Cristália Produtos Químicos Leppänen et al. [13]; however, no controlled study of e Farmacêuticos Ltda, Itapira, São Paulo, Brazil) without the equine tendon therapy using these cells exists. To investi- application of a vasoconstrictor at each point. gate this, collagenase was used to induce tendinitis in the SDFT, followed by adipose tissue collection for the isolation 2.3. Adipose Tissue Collection of mononuclear cells and posterior culture of progenitor cells. After intralesional implantation of MSCs in the treated The region above the dorsal gluteal muscle, at the base group, clinical, ultrasonographic, histological, and immu- of the tail, was chosen as the adipose tissue collection site nohistochemical analyses were conducted to compare the because of the availability of material, the absence of large treatment and control groups. It is our hypothesis that the veins, and easy access. The mares were sedated with injection of progenitor cells improves tendon healing by xylazine (1 mg/kg, i.v.), followed by infiltration of the skin increasing the number of stem cells at the lesion site, and subcutaneous tissues with an anesthetic, 2% lidocaine thereby favoring the synthesis of extracellular matrix chloride, using an inverted L-block. An incision of approx- similar to healthy tendon tissue, the reduction in tendon imately 10 cm
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