Effect of single intralesional treatment of surgically induced equine superficial digital flexor tendon core lesions with adipose-derived mesenchymal stromal cells: a controlled experimental trial.
Abstract: Adipose tissue is a promising source of mesenchymal stromal cells (MSCs) for the treatment of tendon disease. The goal of this study was to assess the effect of a single intralesional implantation of adipose tissue-derived mesenchymal stromal cells (AT-MSCs) on artificial lesions in equine superficial digital flexor tendons (SDFTs). During this randomized, controlled, blinded experimental study, either autologous cultured AT-MSCs suspended in autologous inactivated serum (AT-MSC-serum) or autologous inactivated serum (serum) were injected intralesionally 2 weeks after surgical creation of centrally located SDFT lesions in both forelimbs of nine horses. Healing was assessed clinically and with ultrasound (standard B-mode and ultrasound tissue characterization) at regular intervals over 24 weeks. After euthanasia of the horses the SDFTs were examined histologically, biochemically and by means of biomechanical testing. AT-MSC implantation did not substantially influence clinical and ultrasonographic parameters. Histology, biochemical and biomechanical characteristics of the repair tissue did not differ significantly between treatment modalities after 24 weeks. Compared with macroscopically normal tendon tissue, the content of the mature collagen crosslink hydroxylysylpyridinoline did not differ after AT-MSC-serum treatment (p = 0.074) while it was significantly lower (p = 0.027) in lesions treated with serum alone. Stress at failure (p = 0.048) and the modulus of elasticity (p = 0.001) were significantly lower after AT-MSC-serum treatment than in normal tendon tissue. The effect of a single intralesional injection of cultured AT-MSCs suspended in autologous inactivated serum was not superior to treatment of surgically created SDFT lesions with autologous inactivated serum alone in a surgical model of tendinopathy over an observation period of 22 weeks. AT-MSC treatment might have a positive influence on collagen crosslinking of remodelling scar tissue. Controlled long-term studies including naturally occurring tendinopathies are necessary to verify the effects of AT-MSCs on tendon disease.
Publication Date: 2017-06-05 PubMed ID: 28583184PubMed Central: PMC5460527DOI: 10.1186/s13287-017-0564-8Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Randomized Controlled Trial
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research paper explores the impact of a single treatment with adipose tissue-derived mesenchymal stromal cells (AT-MSC) on artificially created lesions in horse tendons. The researchers found that treatment with AT-MSC did not significantly improve outcomes compared to treatment with inactivated serum alone.
Method of the Study
- Adipose tissue was identified as a potential source of mesenchymal stromal cells (MSCs) which could be used in treating tendon disease.
- The researchers sought to examine the effects of introducing adipose tissue-derived mesenchymal stromal cells (AT-MSCs) directly into artificial lesions in equine superficial digital flexor tendons (SDFTs).
- A random, controlled and blinded experimental study was designed wherein either cultured AT-MSCs within inactivated serum (referred to as AT-MSC-serum) or just autologous inactivated serum were injected into the lesions created centrally in the SDFTs of nine horses.
- Healing was observed over the course of 24 weeks, being assessed regularly via clinical and ultrasound checks.
Results and Findings
- AT-MSC treatment did not significantly affect clinical and ultrasound observations.
- The histology, biomechanical features and biochemistry of the repaired tissue showed no significant difference between the two treatment methods after the 24 weeks.
- Nevertheless, a significant decrease (p=0.027) was reported in the content of hydroxylysylpyridinoline, a mature collagen crosslink, in serum-treated lesions compared to lesions treated with AT-MSC-serum.
- The stress at failure (p=0.048) and the modulus of elasticity (p=0.001) were found to be lower following AT-MSC-serum treatment compared to normal tendon tissue.
Conclusions
- The researchers concluded that the method of treating surgically-induced tendon lesions in horses with a single injection of cultured AT-MSCs did not demonstrate superior effectiveness to treatment with autologous inactivated serum alone.
- However, the AT-MSC treatment showed possible benefits with regard to collagen crosslinking of the tissue during scar remodeling.
- Further controlled, long-term studies focusing on naturally occurring tendinopathies are necessary to truly validate the effects of AT-MSCs on tendon disease.
Cite This Article
APA
Geburek F, Roggel F, van Schie HTM, Beineke A, Estrada R, Weber K, Hellige M, Rohn K, Jagodzinski M, Welke B, Hurschler C, Conrad S, Skutella T, van de Lest C, van Weeren R, Stadler PM.
(2017).
Effect of single intralesional treatment of surgically induced equine superficial digital flexor tendon core lesions with adipose-derived mesenchymal stromal cells: a controlled experimental trial.
Stem Cell Res Ther, 8(1), 129.
https://doi.org/10.1186/s13287-017-0564-8 Publication
Researcher Affiliations
- Equine Clinic, University of Veterinary Medicine Hannover, Foundation, Bünteweg 9, 30559, Hannover, Germany. Florian.Geburek@tiho-hannover.de.
- Equine Clinic, University of Veterinary Medicine Hannover, Foundation, Bünteweg 9, 30559, Hannover, Germany.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM, Utrecht, The Netherlands.
- Institute for Pathology, University of Veterinary Medicine Hannover, Foundation, Bünteweg 17, 30559, Hannover, Germany.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM, Utrecht, The Netherlands.
- Pferdeklink Kirchheim, Nürtinger Straße 200, 73230, Kirchheim unter Teck, Germany.
- Equine Clinic, University of Veterinary Medicine Hannover, Foundation, Bünteweg 9, 30559, Hannover, Germany.
- Institute for Biometry, Epidemiology and Information Processing, University of Veterinary Medicine Hannover, Foundation, Bünteweg 2, 30559, Hannover, Germany.
- Department of Orthopedic Trauma, Hannover Medical School, Carl-Neuberg-Straße 1, 30625, Hannover, Germany.
- Laboratory for Biomechanics and Biomaterials, Department of Orthopaedic Surgery, Hannover Medical School, Anna-von-Borries-Straße 1-7, 30625, Hannover, Germany.
- Laboratory for Biomechanics and Biomaterials, Department of Orthopaedic Surgery, Hannover Medical School, Anna-von-Borries-Straße 1-7, 30625, Hannover, Germany.
- , P.O. Box 1243, 72072, Tübingen, Germany.
- Institute for Anatomy and Cell Biology, University of Heidelberg, Im Neuenheimer Feld 307, 69120, Heidelberg, Germany.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM, Utrecht, The Netherlands.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM, Utrecht, The Netherlands.
- Equine Clinic, University of Veterinary Medicine Hannover, Foundation, Bünteweg 9, 30559, Hannover, Germany.
MeSH Terms
- Adipose Tissue / cytology
- Amino Acids / analysis
- Animals
- Collagen / analysis
- Disease Models, Animal
- Elastic Modulus
- Horse Diseases / pathology
- Horse Diseases / therapy
- Horses
- Injections, Intralesional
- Mesenchymal Stem Cell Transplantation
- Mesenchymal Stem Cells / cytology
- Stress, Mechanical
- Tendinopathy / pathology
- Tendinopathy / therapy
- Tendinopathy / veterinary
- Time Factors
- Transplantation, Autologous
- Ultrasonography
References
This article includes 103 references
- Cassel M, Baur H, Hirschmüller A, Carlsohn A, Fröhlich K, Mayer F. Prevalence of Achilles and patellar tendinopathy and their association to intratendinous changes in adolescent athletes.. Scand J Med Sci Sports 2015 Jun;25(3):e310-8.
- Maffulli N, Wong J. Rupture of the Achilles and patellar tendons.. Clin Sports Med 2003 Oct;22(4):761-76.
- Ross MW. Movement. In: Ross MW, Dyson SJ, editors. Diagnosis and Management of Lameness in the Horse. 2. St. Louis: Elsevier Saunders; 2011. pp. 64–80.
- O'Meara B, Bladon B, Parkin TD, Fraser B, Lischer CJ. An investigation of the relationship between race performance and superficial digital flexor tendonitis in the Thoroughbred racehorse.. Equine Vet J 2010 May;42(4):322-6.
- Williams RB, Harkins LS, Hammond CJ, Wood JL. Racehorse injuries, clinical problems and fatalities recorded on British racecourses from flat racing and National Hunt racing during 1996, 1997 and 1998.. Equine Vet J 2001 Sep;33(5):478-86.
- Lam KH, Parkin TD, Riggs CM, Morgan KL. Descriptive analysis of retirement of Thoroughbred racehorses due to tendon injuries at the Hong Kong Jockey Club (1992-2004).. Equine Vet J 2007 Mar;39(2):143-8.
- Riemersma DJ, Schamhardt HC. In vitro mechanical properties of equine tendons in relation to cross-sectional area and collagen content.. Res Vet Sci 1985 Nov;39(3):263-70.
- Stephens PR, Nunamaker DM, Butterweck DM. Application of a Hall-effect transducer for measurement of tendon strains in horses.. Am J Vet Res 1989 Jul;50(7):1089-95.
- Geburek F, Stadler P. [Regenerative therapy for tendon and ligament disorders in horses. Terminology, production, biologic potential and in vitro effects].. Tierarztl Prax Ausg G Grosstiere Nutztiere 2011;39(6):373-83.
- Dyson SJ. Medical management of superficial digital flexor tendonitis: a comparative study in 219 horses (1992-2000).. Equine Vet J 2004 Jul;36(5):415-9.
- Goodship AE, Birch HL, Wilson AM. The pathobiology and repair of tendon and ligament injury.. Vet Clin North Am Equine Pract 1994 Aug;10(2):323-49.
- Stewart MC, Stewart AA. Cell-based therapies in orthopedics.. Vet Clin North Am Equine Pract 2011 Aug;27(2):xiii-xiv.
- Smith RK, Werling NJ, Dakin SG, Alam R, Goodship AE, Dudhia J. Beneficial effects of autologous bone marrow-derived mesenchymal stem cells in naturally occurring tendinopathy.. PLoS One 2013;8(9):e75697.
- Guest DJ, Smith MR, Allen WR. Equine embryonic stem-like cells and mesenchymal stromal cells have different survival rates and migration patterns following their injection into damaged superficial digital flexor tendon.. Equine Vet J 2010 Oct;42(7):636-42.
- Watts AE, Yeager AE, Kopyov OV, Nixon AJ. Fetal derived embryonic-like stem cells improve healing in a large animal flexor tendonitis model.. Stem Cell Res Ther 2011 Jan 27;2(1):4.
- Violini S, Ramelli P, Pisani LF, Gorni C, Mariani P. Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12.. BMC Cell Biol 2009 Apr 22;10:29.
- Park A, Hogan MV, Kesturu GS, James R, Balian G, Chhabra AB. Adipose-derived mesenchymal stem cells treated with growth differentiation factor-5 express tendon-specific markers.. Tissue Eng Part A 2010 Sep;16(9):2941-51.
- Lovati AB, Corradetti B, Cremonesi F, Bizzaro D, Consiglio AL. Tenogenic differentiation of equine mesenchymal progenitor cells under indirect co-culture.. Int J Artif Organs 2012 Nov;35(11):996-1005.
- Tan SL, Ahmad RE, Ahmad TS, Merican AM, Abbas AA, Ng WM, Kamarul T. Effect of growth differentiation factor 5 on the proliferation and tenogenic differentiation potential of human mesenchymal stem cells in vitro.. Cells Tissues Organs 2012;196(4):325-38.
- Raabe O, Shell K, Fietz D, Freitag C, Ohrndorf A, Christ HJ, Wenisch S, Arnhold S. Tenogenic differentiation of equine adipose-tissue-derived stem cells under the influence of tensile strain, growth differentiation factors and various oxygen tensions.. Cell Tissue Res 2013 Jun;352(3):509-21.
- Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells.. Circulation 2004 Mar 16;109(10):1292-8.
- Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators.. J Cell Biochem 2006 Aug 1;98(5):1076-84.
- Richardson LE, Dudhia J, Clegg PD, Smith R. Stem cells in veterinary medicine--attempts at regenerating equine tendon after injury.. Trends Biotechnol 2007 Sep;25(9):409-16.
- Caplan AI. Why are MSCs therapeutic? New data: new insight.. J Pathol 2009 Jan;217(2):318-24.
- Sorrell JM, Baber MA, Caplan AI. Influence of adult mesenchymal stem cells on in vitro vascular formation.. Tissue Eng Part A 2009 Jul;15(7):1751-61.
- Herrero C, Pérez-Simón JA. Immunomodulatory effect of mesenchymal stem cells.. Braz J Med Biol Res 2010 May;43(5):425-30.
- Alves AG, Stewart AA, Dudhia J, Kasashima Y, Goodship AE, Smith RK. Cell-based therapies for tendon and ligament injuries.. Vet Clin North Am Equine Pract 2011 Aug;27(2):315-33.
- Koch TG, Berg LC, Betts DH. Current and future regenerative medicine - principles, concepts, and therapeutic use of stem cell therapy and tissue engineering in equine medicine.. Can Vet J 2009 Feb;50(2):155-65.
- Peroni JF, Borjesson DL. Anti-inflammatory and immunomodulatory activities of stem cells.. Vet Clin North Am Equine Pract 2011 Aug;27(2):351-62.
- Nixon AJ, Dahlgren LA, Haupt JL, Yeager AE, Ward DL. Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis.. Am J Vet Res 2008 Jul;69(7):928-37.
- Taylor SE, Clegg PD. Collection and propagation methods for mesenchymal stromal cells.. Vet Clin North Am Equine Pract 2011 Aug;27(2):263-74.
- Burk J, Gittel C, Heller S, Pfeiffer B, Paebst F, Ahrberg AB, Brehm W. Gene expression of tendon markers in mesenchymal stromal cells derived from different sources.. BMC Res Notes 2014 Nov 20;7:826.
- Vidal MA, Kilroy GE, Lopez MJ, Johnson JR, Moore RM, Gimble JM. Characterization of equine adipose tissue-derived stromal cells: adipogenic and osteogenic capacity and comparison with bone marrow-derived mesenchymal stromal cells.. Vet Surg 2007 Oct;36(7):613-22.
- Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue.. Stem Cells 2006 May;24(5):1294-301.
- Dahlgren LA. Fat derived mesenchymal stem cells for equine tendon repair. Regen Med 2009;4(6 Suppl 2):S14.
- Leppänen M, Miettinen S, Mäkinen S, Wilpola P, Katiskalahti T, Heikkilä P, Tulamo RM. Management of equine tendon & ligament injuries with expanded autologous adipose derived mesenchymal stem cells: a clincal study. Regen Med 2009;4(6 Suppl 2):S21.
- Leppänen M, Heikkilä P, Katiskalahti T, Tulamo RM. Follow up of recovery of equine tendon & ligament injuries 18-24 months after treatment with enriched autologous adipose-derived mesenchymal stem cells: a clinical study. Regen Med 2009;4(6 Suppl 2):S21.
- Ricco S, Renzi S, Del Bue M, Conti V, Merli E, Ramoni R, Lucarelli E, Gnudi G, Ferrari M, Grolli S. Allogeneic adipose tissue-derived mesenchymal stem cells in combination with platelet rich plasma are safe and effective in the therapy of superficial digital flexor tendonitis in the horse.. Int J Immunopathol Pharmacol 2013 Jan-Mar;26(1 Suppl):61-8.
- Carvalho AD, Alves ALG, de Oliveira PGG, Alvarez LEC, Amorim RL, Hussni CA, Deffune E. Use of adipose tissue-derived mesenchymal stem cells for experimental tendinitis therapy in equines. J Equine Vet Sci 2011;31(1):26–34.
- Carvalho Ade M, Badial PR, Álvarez LE, Yamada AL, Borges AS, Deffune E, Hussni CA, Garcia Alves AL. Equine tendonitis therapy using mesenchymal stem cells and platelet concentrates: a randomized controlled trial.. Stem Cell Res Ther 2013 Jul 22;4(4):85.
- Patterson-Kane JC, Firth EC. The pathobiology of exercise-induced superficial digital flexor tendon injury in Thoroughbred racehorses.. Vet J 2009 Aug;181(2):79-89.
- Lui PP, Maffulli N, Rolf C, Smith RK. What are the validated animal models for tendinopathy?. Scand J Med Sci Sports 2011 Feb;21(1):3-17.
- Schramme M, Hunter S, Campbell N, Blikslager A, Smith R. A surgical tendonitis model in horses: technique, clinical, ultrasonographic and histological characterisation.. Vet Comp Orthop Traumatol 2010;23(4):231-9.
- van Schie HT, Bakker EM, Cherdchutham W, Jonker AM, van de Lest CH, van Weeren PR. Monitoring of the repair process of surgically created lesions in equine superficial digital flexor tendons by use of computerized ultrasonography.. Am J Vet Res 2009 Jan;70(1):37-48.
- Bosch G, van Schie HT, de Groot MW, Cadby JA, van de Lest CH, Barneveld A, van Weeren PR. Effects of platelet-rich plasma on the quality of repair of mechanically induced core lesions in equine superficial digital flexor tendons: A placebo-controlled experimental study.. J Orthop Res 2010 Feb;28(2):211-7.
- Conze P, van Schie HT, van Weeren R, Staszyk C, Conrad S, Skutella T, Hopster K, Rohn K, Stadler P, Geburek F. Effect of autologous adipose tissue-derived mesenchymal stem cells on neovascularization of artificial equine tendon lesions.. Regen Med 2014;9(6):743-57.
- Cadby JA, David F, van de Lest C, Bosch G, van Weeren PR, Snedeker JG, van Schie HT. Further characterisation of an experimental model of tendinopathy in the horse.. Equine Vet J 2013 Sep;45(5):642-8.
- Rantanen NW. The use of diagnostic ultrasound in limb disorders of the horse: a preliminary report. J Equine Vet Sci 1982;2(2):62–4.
- Reef VB. Musculoskeletal ultrasonography. In: Reef VB, editor. Equine Diagnostic Ultrasound. 1. Philadelphia: W.B. Saunders; 1998. pp. 39–186.
- van Schie JT, Bakker EM, van Weeren PR. Ultrasonographic evaluation of equine tendons: a quantitative in vitro study of the effects of amplifier gain level, transducer-tilt, and transducer-displacement.. Vet Radiol Ultrasound 1999 Mar-Apr;40(2):151-60.
- van Schie HT, Bakker EM, Jonker AM, van Weeren PR. Ultrasonographic tissue characterization of equine superficial digital flexor tendons by means of gray level statistics.. Am J Vet Res 2000 Feb;61(2):210-9.
- van Schie HT, Bakker EM, Jonker AM, van Weeren PR. Computerized ultrasonographic tissue characterization of equine superficial digital flexor tendons by means of stability quantification of echo patterns in contiguous transverse ultrasonographic images.. Am J Vet Res 2003 Mar;64(3):366-75.
- van Schie HT, Bakker EM, Jonker AM, van Weeren PR. Efficacy of computerized discrimination between structure-related and non-structure-related echoes in ultrasonographic images for the quantitative evaluation of the structural integrity of superficial digital flexor tendons in horses.. Am J Vet Res 2001 Jul;62(7):1159-66.
- Bosch G, René van Weeren P, Barneveld A, van Schie HT. Computerised analysis of standardised ultrasonographic images to monitor the repair of surgically created core lesions in equine superficial digital flexor tendons following treatment with intratendinous platelet rich plasma or placebo.. Vet J 2011 Jan;187(1):92-8.
- Docking SI, Daffy J, van Schie HT, Cook JL. Tendon structure changes after maximal exercise in the Thoroughbred horse: use of ultrasound tissue characterisation to detect in vivo tendon response.. Vet J 2012 Dec;194(3):338-42.
- Geburek F, Gaus M, van Schie HT, Rohn K, Stadler PM. Effect of intralesional platelet-rich plasma (PRP) treatment on clinical and ultrasonographic parameters in equine naturally occurring superficial digital flexor tendinopathies - a randomized prospective controlled clinical trial.. BMC Vet Res 2016 Sep 7;12(1):191.
- Docking SI, Rosengarten SD, Cook J. Achilles tendon structure improves on UTC imaging over a 5-month pre-season in elite Australian football players.. Scand J Med Sci Sports 2016 May;26(5):557-63.
- de Jonge S, Rozenberg R, Vieyra B, Stam HJ, Aanstoot HJ, Weinans H, van Schie HT, Praet SF. Achilles tendons in people with type 2 diabetes show mildly compromised structure: an ultrasound tissue characterisation study.. Br J Sports Med 2015 Aug;49(15):995-9.
- de Vos RJ, Heijboer MP, Weinans H, Verhaar J AN, van Schie J TM. Tendon structure's lack of relation to clinical outcome after eccentric exercises in chronic midportion Achilles tendinopathy.. J Sport Rehabil 2012 Feb;21(1):34-43.
- Aström M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings.. Clin Orthop Relat Res 1995 Jul;(316):151-64.
- Crevier-Denoix N, Collobert C, Pourcelot P, Denoix JM, Sanaa M, Geiger D, Bernard N, Ribot X, Bortolussi C, Bousseau B. Mechanical properties of pathological equine superficial digital flexor tendons.. Equine Vet J Suppl 1997 May;(23):23-6.
- Majewski M, Ochsner PE, Liu F, Flückiger R, Evans CH. Accelerated healing of the rat Achilles tendon in response to autologous conditioned serum.. Am J Sports Med 2009 Nov;37(11):2117-25.
- Little D, Schramme MC. Ultrasonographic and MRI evaluation of a novel tendonitis model in the horse. Vet Surg 2006;35(6).
- Schmidt H. Die Behandlung akuter und chronischer Sehnenerkrankungen beim Pferd mit hochmolekularer Hyaluronsäure. Dr. med. vet. thesis. Hannover: Tierärztliche Hochschule Hannover; 1989.
- Geburek F, Lietzau M, Beineke A, Rohn K, Stadler PM. Effect of a single injection of autologous conditioned serum (ACS) on tendon healing in equine naturally occurring tendinopathies.. Stem Cell Res Ther 2015 Jun 26;6(1):126.
- Edinger J. Orthopädische Untersuchung der Gliedmaßen und der Wirbelsäule. In: Wissdorf H, Gerhards H, Huskamp B, Deegen E, editors. Praxisorientierte Anatomie und Propädeutik des Pferdes. Hannover: M. u. H. Schaper; 2010. pp. 890–926.
- Genovese RL, Rantanen NW, Hauser ML, Simpson BS. Diagnostic ultrasonography of equine limbs.. Vet Clin North Am Equine Pract 1986 Apr;2(1):145-226.
- Rantanen NW, Jorgensen JS, Genovese RL. Ultrasonographic evaluation of the equine limb: technique. In: Ross MW, Dyson SJ, editors. Diagnosis and Management of Lameness in the Horse. 1. St. Louis: Elsevier; 2003. pp. 166–88.
- Kim YJ, Sah RL, Doong JY, Grodzinsky AJ. Fluorometric assay of DNA in cartilage explants using Hoechst 33258.. Anal Biochem 1988 Oct;174(1):168-76.
- Dudhia J, Scott CM, Draper ER, Heinegård D, Pitsillides AA, Smith RK. Aging enhances a mechanically-induced reduction in tendon strength by an active process involving matrix metalloproteinase activity.. Aging Cell 2007 Aug;6(4):547-56.
- Fleiss JL. The design and analysis of clinical experiments. New York: Wiley; 1986.
- Marx C, Silveira MD, Beyer Nardi N. Adipose-derived stem cells in veterinary medicine: characterization and therapeutic applications.. Stem Cells Dev 2015 Apr 1;24(7):803-13.
- Eyre D. Collagen cross-linking amino acids.. Methods Enzymol 1987;144:115-39.
- Last JA, Armstrong LG, Reiser KM. Biosynthesis of collagen crosslinks.. Int J Biochem 1990;22(6):559-64.
- Eyre DR, Koob TJ, Van Ness KP. Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography.. Anal Biochem 1984 Mar;137(2):380-8.
- Fu SC, Chan KM, Rolf CG. Increased deposition of sulfated glycosaminoglycans in human patellar tendinopathy.. Clin J Sport Med 2007 Mar;17(2):129-34.
- Parkinson J, Samiric T, Ilic MZ, Cook J, Feller JA, Handley CJ. Change in proteoglycan metabolism is a characteristic of human patellar tendinopathy.. Arthritis Rheum 2010 Oct;62(10):3028-35.
- Birch HL, Bailey AJ, Goodship AE. Macroscopic 'degeneration' of equine superficial digital flexor tendon is accompanied by a change in extracellular matrix composition.. Equine Vet J 1998 Nov;30(6):534-9.
- Estrada RJ, van Weeren R, van de Lest CHA, Boere J, Reyes M, Ionita JC, Estrada M, Lischer CJ. Effects of Autologous Conditioned Plasma (R) (ACP) on the healing of surgically induced core lesions in equine superficial digital flexor tendon. Pferdeheilkunde 2014;30(6):633–42.
- Lin YL, Brama PA, Kiers GH, DeGroot J, van Weeren PR. Functional adaptation through changes in regional biochemical characteristics during maturation of equine superficial digital flexor tendons.. Am J Vet Res 2005 Sep;66(9):1623-9.
- Batson EL, Paramour RJ, Smith TJ, Birch HL, Patterson-Kane JC, Goodship AE. Are the material properties and matrix composition of equine flexor and extensor tendons determined by their functions?. Equine Vet J 2003 May;35(3):314-8.
- Silver IA, Brown PN, Goodship AE, Lanyon LE, McCullagh KG, Perry GC, Williams IF. A clinical and experimental study of tendon injury, healing and treatment in the horse.. Equine Vet J Suppl 1983 Jul;(1):1-43.
- Crevier N, Pourcelot P, Denoix JM, Geiger D, Bortolussi C, Ribot X, Sanaa M. Segmental variations of in vitro mechanical properties in equine superficial digital flexor tendons.. Am J Vet Res 1996 Aug;57(8):1111-7.
- Caniglia CJ, Schramme MC, Smith RK. The effect of intralesional injection of bone marrow derived mesenchymal stem cells and bone marrow supernatant on collagen fibril size in a surgical model of equine superficial digital flexor tendonitis.. Equine Vet J 2012 Sep;44(5):587-93.
- Manferdini C, Maumus M, Gabusi E, Piacentini A, Filardo G, Peyrafitte JA, Jorgensen C, Bourin P, Fleury-Cappellesso S, Facchini A, Noël D, Lisignoli G. Adipose-derived mesenchymal stem cells exert antiinflammatory effects on chondrocytes and synoviocytes from osteoarthritis patients through prostaglandin E2.. Arthritis Rheum 2013 May;65(5):1271-81.
- Ceserani V, Ferri A, Berenzi A, Benetti A, Ciusani E, Pascucci L, Bazzucchi C, Coccè V, Bonomi A, Pessina A, Ghezzi E, Zeira O, Ceccarelli P, Versari S, Tremolada C, Alessandri G. Angiogenic and anti-inflammatory properties of micro-fragmented fat tissue and its derived mesenchymal stromal cells.. Vasc Cell 2016;8:3.
- Shen H, Kormpakis I, Havlioglu N, Linderman SW, Sakiyama-Elbert SE, Erickson IE, Zarembinski T, Silva MJ, Gelberman RH, Thomopoulos S. The effect of mesenchymal stromal cell sheets on the inflammatory stage of flexor tendon healing.. Stem Cell Res Ther 2016 Sep 27;7(1):144.
- Dahlgren LA. Management of tendon injuries. In: Robinson NE, Sprayberry KA, editors. Current Therapy in Equine Medicine. 6. St. Louis: Saunders Elsevier; 2009. pp. 518–23.
- Frisbie DD, Smith RK. Clinical update on the use of mesenchymal stem cells in equine orthopaedics.. Equine Vet J 2010 Jan;42(1):86-9.
- Otsu K, Das S, Houser SD, Quadri SK, Bhattacharya S, Bhattacharya J. Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells.. Blood 2009 Apr 30;113(18):4197-205.
- Awad HA, Boivin GP, Dressler MR, Smith FN, Young RG, Butler DL. Repair of patellar tendon injuries using a cell-collagen composite.. J Orthop Res 2003 May;21(3):420-31.
- Taylor SE, Smith RK, Clegg PD. Mesenchymal stem cell therapy in equine musculoskeletal disease: scientific fact or clinical fiction?. Equine Vet J 2007 Mar;39(2):172-80.
- Godwin EE, Young NJ, Dudhia J, Beamish IC, Smith RK. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon.. Equine Vet J 2012 Jan;44(1):25-32.
- Geburek F, Mundle K, Conrad S, Hellige M, Walliser U, van Schie HT, van Weeren R, Skutella T, Stadler PM. Tracking of autologous adipose tissue-derived mesenchymal stromal cells with in vivo magnetic resonance imaging and histology after intralesional treatment of artificial equine tendon lesions--a pilot study.. Stem Cell Res Ther 2016 Feb 1;7:21.
- Burk J, Berner D, Brehm W, Hillmann A, Horstmeier C, Josten C, Paebst F, Rossi G, Schubert S, Ahrberg AB. Long-Term Cell Tracking Following Local Injection of Mesenchymal Stromal Cells in the Equine Model of Induced Tendon Disease.. Cell Transplant 2016 Dec 13;25(12):2199-2211.
- Pacini S, Spinabella S, Trombi L, Fazzi R, Galimberti S, Dini F, Carlucci F, Petrini M. Suspension of bone marrow-derived undifferentiated mesenchymal stromal cells for repair of superficial digital flexor tendon in race horses.. Tissue Eng 2007 Dec;13(12):2949-55.
- Hraha TH, Doremus KM, McIlwraith CW, Frisbie DD. Autologous conditioned serum: the comparative cytokine profiles of two commercial methods (IRAP and IRAP II) using equine blood.. Equine Vet J 2011 Sep;43(5):516-21.
- Dabareiner RM, Carter GK, Chaffin MK. How to perform ultrasound guided-tendon splitting and intralesional tendon injections in the standing horse. In: 46th Annual Convention of the AAEP. Lexington: American Association of Equine Practitioners; November 26–29 2000.
- Avella CS, Smith RKW. Diagnosis and management of tendon and ligament disorders. In: Auer JA, Stick JA, editors. Equine Surgery. 4. St. Louis: Elsevier Saunders; 2011. pp. 1157–79.
- Jann H, Stashak TS. Equine wound management. In: Stashak TS, Theoret CL, editors. Equine Wound Management. Ames: Wiley-Blackwell; 2008. pp. 489–508.
- Bosch G, Moleman M, Barneveld A, van Weeren PR, van Schie HT. The effect of platelet-rich plasma on the neovascularization of surgically created equine superficial digital flexor tendon lesions.. Scand J Med Sci Sports 2011 Aug;21(4):554-61.
- Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation.. Knee Surg Sports Traumatol Arthrosc 2001 Jul;9(4):233-8.
- Kristoffersen M, Ohberg L, Johnston C, Alfredson H. Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment.. Knee Surg Sports Traumatol Arthrosc 2005 Sep;13(6):505-8.
Citations
This article has been cited 20 times.- Quintero D, Perucca Orfei C, Kaplan LD, de Girolamo L, Best TM, Kouroupis D. The roles and therapeutic potentialof mesenchymal stem/stromal cells and their extracellular vesicles in tendinopathies.. Front Bioeng Biotechnol 2023;11:1040762.
- El-Husseiny HM, Mady EA, Helal MAY, Tanaka R. The Pivotal Role of Stem Cells in Veterinary Regenerative Medicine and Tissue Engineering.. Vet Sci 2022 Nov 21;9(11).
- Viganò M, Ragni E, Marmotti A, de Girolamo L. The effects of orthobiologics in the treatment of tendon pathologies: a systematic review of preclinical evidence.. J Exp Orthop 2022 Apr 8;9(1):31.
- Melotti L, Carolo A, Elshazly N, Boesso F, Da Dalt L, Gabai G, Perazzi A, Iacopetti I, Patruno M. Case Report: Repeated Intralesional Injections of Autologous Mesenchymal Stem Cells Combined With Platelet-Rich Plasma for Superficial Digital Flexor Tendon Healing in a Show Jumping Horse.. Front Vet Sci 2022;9:843131.
- Yano M, Nasti A, Seki A, Ishida K, Yamato M, Inui H, Ogawa N, Inagaki S, Ho TTB, Kawaguchi K, Yamashita T, Arai K, Yamashita T, Mizukoshi E, Inoue O, Takashima S, Usui S, Takamura M, Honda M, Wada T, Kaneko S, Sakai Y. Characterization of adipose tissue-derived stromal cells of mice with nonalcoholic fatty liver disease and their use for liver repair.. Regen Ther 2021 Dec;18:497-507.
- Palumbo Piccionello A, Riccio V, Senesi L, Volta A, Pennasilico L, Botto R, Rossi G, Tambella AM, Galosi L, Marini C, Vullo C, Gigante A, Zavan B, De Francesco F, Riccio M. Adipose micro-grafts enhance tendinopathy healing in ovine model: An in vivo experimental perspective study.. Stem Cells Transl Med 2021 Nov;10(11):1544-1560.
- Gaesser AM, Underwood C, Linardi RL, Even KM, Reef VB, Shetye SS, Mauck RL, King WJ, Engiles JB, Ortved KF. Evaluation of Autologous Protein Solution Injection for Treatment of Superficial Digital Flexor Tendonitis in an Equine Model.. Front Vet Sci 2021;8:697551.
- Meeremans M, Van de Walle GR, Van Vlierberghe S, De Schauwer C. The Lack of a Representative Tendinopathy Model Hampers Fundamental Mesenchymal Stem Cell Research.. Front Cell Dev Biol 2021;9:651164.
- Harman RM, Marx C, Van de Walle GR. Translational Animal Models Provide Insight Into Mesenchymal Stromal Cell (MSC) Secretome Therapy.. Front Cell Dev Biol 2021;9:654885.
- Depuydt E, Broeckx SY, Van Hecke L, Chiers K, Van Brantegem L, van Schie H, Beerts C, Spaas JH, Pille F, Martens A. The Evaluation of Equine Allogeneic Tenogenic Primed Mesenchymal Stem Cells in a Surgically Induced Superficial Digital Flexor Tendon Lesion Model.. Front Vet Sci 2021;8:641441.
- Ribitsch I, Oreff GL, Jenner F. Regenerative Medicine for Equine Musculoskeletal Diseases.. Animals (Basel) 2021 Jan 19;11(1).
- Tsai SL, Nödl MT, Galloway JL. Bringing tendon biology to heel: Leveraging mechanisms of tendon development, healing, and regeneration to advance therapeutic strategies.. Dev Dyn 2021 Mar;250(3):393-413.
- Jankowski M, Dompe C, Sibiak R, Wąsiatycz G, Mozdziak P, Jaśkowski JM, Antosik P, Kempisty B, Dyszkiewicz-Konwińska M. In Vitro Cultures of Adipose-Derived Stem Cells: An Overview of Methods, Molecular Analyses, and Clinical Applications.. Cells 2020 Jul 27;9(8).
- Voga M, Adamic N, Vengust M, Majdic G. Stem Cells in Veterinary Medicine-Current State and Treatment Options.. Front Vet Sci 2020;7:278.
- Kunze KN, Burnett RA, Wright-Chisem J, Frank RM, Chahla J. Adipose-Derived Mesenchymal Stem Cell Treatments and Available Formulations.. Curr Rev Musculoskelet Med 2020 Jun;13(3):264-280.
- Lim WL, Liau LL, Ng MH, Chowdhury SR, Law JX. Current Progress in Tendon and Ligament Tissue Engineering.. Tissue Eng Regen Med 2019 Dec;16(6):549-571.
- Shojaee A, Parham A. Strategies of tenogenic differentiation of equine stem cells for tendon repair: current status and challenges.. Stem Cell Res Ther 2019 Jun 18;10(1):181.
- Smieszek A, Kornicka K, Szłapka-Kosarzewska J, Androvic P, Valihrach L, Langerova L, Rohlova E, Kubista M, Marycz K. Metformin Increases Proliferative Activity and Viability of Multipotent Stromal Stem Cells Isolated from Adipose Tissue Derived from Horses with Equine Metabolic Syndrome.. Cells 2019 Jan 22;8(2).
- Moro LN, Amin G, Furmento V, Waisman A, Garate X, Neiman G, La Greca A, Santín Velazque NL, Luzzani C, Sevlever GE, Vichera G, Miriuka SG. MicroRNA characterization in equine induced pluripotent stem cells.. PLoS One 2018;13(12):e0207074.
- Olivera R, Moro LN, Jordan R, Pallarols N, Guglielminetti A, Luzzani C, Miriuka SG, Vichera G. Bone marrow mesenchymal stem cells as nuclear donors improve viability and health of cloned horses.. Stem Cells Cloning 2018;11:13-22.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists