Soft-focused extracorporeal shock waves increase the expression of tendon-specific markers and the release of anti-inflammatory cytokines in an adherent culture model of primary human tendon cells

Ultrasound in Medicine and Biology

Volumn 40, Issue 6, 2014, Pages 1204-1215

  De Girolamo, Laura ^a   Stanco, Deborah ^a   Galliera, Emanuela ^a,b   Viganò, Marco ^a   Lovati, Arianna Barbara ^c   Marazzi, Monica Gioia ^b   Romeo, Pietro ^a   Sansone, Valerio ^a,b  

^a IRCCS ISTITUTO ORTOPEDICO GALEAZZI   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c IRCCS POLICLINICO SAN DONATO   (Italy)

Author keywords

Cell proliferation; Cytokines; Soft focused extracorporeal shock waves; Tendinopathy; Tendon cells; Tendon specific markers; Transforming growth factor ; Vascular endothelial growth factor

Indexed keywords

CELL ENGINEERING; CELL PROLIFERATION; CELLS; CYTOLOGY; SHOCK WAVES;

CYTOKINES; TENDINOPATHY; TENDON-SPECIFIC MARKERS; TRANSFORMING GROWTH FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

TENDONS;

CYTOKINE; BIOLOGICAL MARKER; COLLAGEN TYPE 1; MATRIX METALLOPROTEINASE; NITRIC OXIDE; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN A;

ADULT; ANTERIOR CRUCIATE LIGAMENT; ARTICLE; CELL ADHESION; CELL POPULATION; CELL PROLIFERATION; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EXTRACORPOREAL LITHOTRIPSY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TENDON CELL; TISSUE REGENERATION; APOPTOSIS; CELL CULTURE; CYTOLOGY; FLOW CYTOMETRY; METABOLISM; PATHOLOGY; RADIATION; TENDINOPATHY; TENDON;

ADULT; APOPTOSIS; BIOLOGICAL MARKERS; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; CYTOKINES; FLOW CYTOMETRY; HIGH-ENERGY SHOCK WAVES; HUMANS; IN VITRO TECHNIQUES; MATRIX METALLOPROTEINASES; NITRIC OXIDE; TENDINOPATHY; TENDONS; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84899898838     PISSN: 03015629     EISSN: 1879291X     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2013.12.003     Document Type: Article

References (59)

1. Abate M., Silbernagel K.G., Siljeholm C., Di Iorio A., De Amicis D., Salini V., Werner S., Paganelli R. Pathogenesis of tendinopathies: Inflammation or degeneration?. Arthritis Res Ther 2009, 11:235.
2. Andreas B.M., Murrell G.A.C. Treatment of tendinopathy: What works, what does not, and what is on the horizon. Clin Orthop Relat Res 2008, 466:1539-1554.
3. Archambault J., Tsuzaki M., Herzog W., Banes A.J. Stretch and interleukin-1 beta induce matrix metalloproteinases in rabbit tendon cells invitro. JOrthop Res 2002, 20:36-39.
4. Bi Y., Ehirchiou D., Kilts T.M., Inkson C.A., Embree M.C., Sonoyama W., Li L., Leet A.I., Seo B.M., Zhang L., Shi S., Young M.F. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 2007, 13:1219-1227.
5. Chao Y.H., Tsuang Y.H., Sun J.S., Chen L.T., Chiang Y.F., Wang C.C., Chen M.H. Effects of shock waves on tenocyte proliferation and extracellular matrix metabolism. Ultrasound Med Biol 2008, 34:841-852.
6. Chen Y.J., Wang C.J., Yang K.D., Kuo Y.R., Huang H.C., Huang Y.T., Sun Y.C., Wang F.S. Extracorporeal shock waves promote healing of collagenase-induced Achilles tendonitis and increase TGF-beta1 and IGF-I expression. JOrthop Res 2004, 22:854-861.
7. Clegg P.D., Strassburg S., Smith R.K. Cell phenotypic variation in normal and damaged tendons. Int J Exp Pathol 2007, 88:227-235.
8. Cook J.L., Purdam C.R. Is tendon pathology a continuum? A pathology model to explain the clinical presentation of load-induced tendinopathy. Br J Sports Med 2009, 43:409-416.
9. Davis T.A., Stojadinovic A., Anam K., Amare M., Naik S., Peoples G.E., Tadaki D., Elster E.A. Extracorporeal shock wave therapy suppresses the early proinflammatory immune response to a severe cutaneous burn injury. Int Wound J 2009, 6:11-21.
10. De Mos M., van El B., DeGroot J., Jahr H., van Schie H.T., van Arkel E.R., Tol H., Heijboer R., van Osch G.J., Verhaar J.A. Achilles tendinosis: Changes in biochemical composition and collagen turnover rate. Am J Sports Med 2007, 35:1549-1556.
11. Del Buono A., Battery L., Denaro V., Maccauro G., Maffulli N. Tendinopathy and inflammation: Some truths. Int J Immunopathol Pharmacol 2011, 24:45-50.
12. Fredberg U., Stengaard-Pedersen K. Chronic tendinopathy tissue pathology, pain mechanisms, and etiology with a special focus on inflammation. Scand J Med Sci Sports 2008, 18:3-15.
13. Furia J.P., Rompe J.D., Cacchio A., Maffulli N. Shock wave therapy as a treatment of nonunions, avascular necrosis, and delayed healing of stress fractures. Foot Ankle Clin 2010, 15:651-662.
14. Han S.H., Lee J.W., Guyton G.P., Parks B.G., Courneya J., Schon L.C. Effect of extracorporeal shock wave therapy on cultured tenocytes. Foot Ankle Int 2009, 30:93-98.
15. Holfeld J., Kapeller B., Hack F., Tepeköylü C., Dumfarth J., Zimpfer D., Schaden W., Losert U., Grimm M., Macfelda K. IVSWT: How can in-vitro shock wave therapy be performed best? Preliminary results from cardiac cells. Int Soc Med Shockwave Treat Newslett 2009, 5:14-16.
16. Hwang S.M., Chen C.Y., Chen S.S., Chen J.C. Chitinous materials inhibit nitric oxide production by activated RAW 264.7 macrophages. Biochem Biophys Res Commun 2000, 271:229-233.
17. Ireland D., Harrall R., Curry V., Holloway G., Hackney R., Hazleman B., Riley G. Multiple changes in gene expression in chronic human Achilles tendinopathy. Matrix Biol 2001, 20:159-169.
18. Ito K., Fukumoto Y., Shimokawa H. Extracorporeal shock wave therapy as a new and non-invasive angiogenic strategy. Tohoku J Exp Med 2009, 219:1-9.
19. Kingham P.J., Kalbermatten D.F., Mahay D., Armstrong S.J., Wiberg M., Terenghi G. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth invitro. Exp Neurol 2007, 207:267-274.
20. Kuhn C., Angehrn F., Sonnabend O., Voss A. Impact of extracorporeal shock waves on the human skin with cellulite: A case study of an unique instance. Clin Interv Aging 2008, 3:201-210.
21. Kuo Y.R., Wang C.T., Wang F.S., Chiang Y.C., Wang C.J. Extracorporeal shock-wave therapy enhanced wound healing via increasing topical blood perfusion and tissue regeneration in a rat model of STZ-induced diabetes. Wound Repair Regen 2009, 17:522-530.
22. Kuypers F.A., Lewis R.A., Hua M., Schott M.A., Discher D., Ernst J.D., Lubin B.H. Detection of altered membrane phospholipid asymmetry in subpopulations of human red blood cells using fluorescently labeled annexin V. Blood 1996, 87:1179-1187.
23. Léjard V., Brideau G., Blais F., Salingcarnboriboon R., Wagner G., Roehrl M.H., Noda M., Duprez D., Houillier P., Rossert J. Scleraxis and NFATc regulate the expression of the pro-alpha1(I) collagen gene in tendon fibroblasts. JBiol Chem 2007, 282:17665-17675.
24. Leone L., Vetrano M., Ranieri D., Raffa S., Vulpiani M.C., Ferretti A., Torrisi M.R., Visco V. Extracorporeal shock wave treatment (ESWT) improves Invitro functional activities of ruptured human tendon-derived tenocytes. PLoS ONE 2012, 7:e49759.
25. Lui P.P., Chan L.S., Lee Y.W., Fu S.C., Chan K.M. Sustained expression of proteoglycans and collagen type III/type I ratio in a calcified tendinopathy model. Rheumatology (Oxford) 2010, 49:231-239.
26. Maeda T., Sakabe T., Sunaga A., Sakai K., Rivera A.L., Keene D.R., Sasaki T., Stavnezer E., Iannotti J., Schweitzer R., Ilic D., Baskaran H., Sakai T. Conversion of mechanical force into TGF-β-mediated biochemical signals. Curr Biol 2011, 21:933-941.
27. Maffulli N., Ewen S.W., Waterston S.W., Reaper J., Barrass V. Tenocytes from ruptured and tendinopathic Achilles tendons produce greater quantities of type III collagen than tenocytes from normal Achilles tendons: An invitro model of human tendon healing. Am J Sports Med 2000, 28:499-505.
28. Maffulli N., Kader D. Tendinopathy of tendoachillis. JBone Joint Surg Br 2002, 84:1-8.
29. Martini L., Giavaresi G., Fini M., Borsari V., Torricelli P., Giardino R. Early effects of extracorporeal shock wave treatment on osteoblast-like cells: A comparative study between electromagnetic and electrohydraulic devices. JTrauma 2006, 61:1198-1206.
30. Mittermayr R., Hartinger J., Antonic V., Meinl A., Pfeifer S., Stojadinovic A., Schaden W., Redl H. Extracorporeal shock wave therapy (ESWT) minimizes ischemic tissue necrosis irrespective of application time and promotes tissue revascularization by stimulating angiogenesis. Ann Surg 2011, 253:1024-1032.
31. Molloy T., Wang Y., Murrell G. The roles of growth factors in tendon and ligament healing. Sports Med 2003, 33:381-394.
32. Notarnicola A., Moretti B. The biological effects of extracorporeal shock wave therapy (ESWT) on tendon tissue. Muscles Ligaments Tendons J 2012, 2:33-37.
33. Ogden J.A., Tóth-Kischkat A., Schultheiss R. Principles of shock wave therapy. Clin Orthop Relat Res 2001, 387:8-17.
34. Ohran Z., Ozturan K., Guven A., Cam K. The effect of extracorporeal shock waves on a rat model of injury to tendon Achillis. JBone Joint Surg Br 2004, 86:613-618.
35. Pigault C., Follenius-Wund A., Schmutz M., Freyssinet J.M., Brisson A. Formation of two-dimensional arrays of annexin V on phosphatidylserine-containing liposomes. JMol Biol 1994, 236:199-208.
36. Pufe T., Kurz B., Petersen W., Varoga D., Mentlein R., Kulow S., Lemke A., Tillmann B. The influence of biomechanical parameters on the expression of VEGF and endostatin in the bone and joint system. Ann Anat 2005, 187:461-472.
37. Rees J.D., Stride M., Scott A. Tendons-Time to revisit inflammation. BrJ Sports Med 2013 March 9, [Epub ahead of print].
38. Riley G.P., Harrall R.L., Constant C.R., Chard M.D., Cawston T.E., Hazleman B.L. Tendon degeneration and chronic shoulder pain: Changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis. Ann Rheum Dis 1994, 53:359-366.
39. Rompe J.D., Kirkpatrick C.J., Kullmer K., et al. Dose-related effects of shock waves on rabbit tendon Achilles: A sonographic and histological study. JBone Joint Surg Br 1998, 80:546-552.
40. Sansone V., D'Agostino M.C., Bonora C., Sizzano F., de Girolamo L., Romeo P. Early angiogenic response to shock waves in a three-dimensional model of human microvascular endothelial cell culture (HMEC-1). JBiol Regul Homeost Agents 2012, 26:29-37.
41. Schaden W., Thiele R., Kölpl C., Pusch M., Nissan A., Attinger C.E., Maniscalco-Theberge M.E., Peoples G.E., Elster E.A., Stojadinovic A. Shock wave therapy for acute and chronic soft tissue wounds: A feasibility study. JSurg Res 2007, 143:1-12.
42. Schäffer M., Weimer W., Wider S., Stülten C., Bongartz M., Budach W., Becker H.D. Differential expression of inflammatory mediators in radiation-impaired wound healing. JSurg Res 2002, 107:93-100.
43. Schulze-Tanzil G., Mobasheri A., Clegg P.D., Sendzik J., John T., Shakibaei M. Cultivation of human tenocytes in high density culture. Histochem Cell Biol 2004, 122:219-228.
44. Shyy J.Y., Chien S. Role of integrins in cellular responses to mechanical stress and adhesion. Curr Opin Cell Biol 1997, 9:707-713.
45. Skutek M., van Griensven M., Zeichen J., Brauer N., Bosch U. Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol 2001, 86:48-52.
46. Speed C.A. Extracorporeal shock-wave therapy in the management of chronic soft-tissue conditions. JBone Joint Surg Br 2004, 86:165-171.
47. Stojadinovic A., Elster E.A., Anam K., Tadaki D., Amare M., Zins S., Davis T.A. Angiogenic response to extracorporeal shock wave treatment in murine skin isografts. Angiogenesis 2008, 11:369-380.
48. Tartour E., Pere H., Maillere B., Terme M., Merillon N., Taieb J., Sandoval F., Quintin-Colonna F., Lacerda K., Karadimou A., Badoual C., Tedgui A., Fridman W.H., Oudard S. Angiogenesis and immunity: A bidirectional link potentially relevant for the monitoring of antiangiogenic therapy and the development of novel therapeutic combination with immunotherapy. Cancer Metastasis Rev 2011, 30:83-95.
49. Tsai W.C., Tang S.T., Liang F.C. Effect of therapeutic ultrasound on tendons. Am J Phys Med Rehabil 2011, 90:1068-1073.
50. Tsuzaki M., Guyton G., Garrett W., Archambault J.M., Herzog W., Almekinders L., Bynum D., Yang X., Banes A.J. IL-1 beta induces COX2, MMP-1, -3 and -13, ADAMTS-4, IL-1β and IL-6 in human tendon cells. JOrthop Res 2003, 21:256-264.
51. Van der Jagt O.P., Van der Linden J.C., Schaden W., Van Schie H.T., Piscaer T.M., Verhaar J.A., Weinans H., Waarsing J.H. Defocused extracorporeal shock wave therapy as potential treatment for osteoporosis. JOrthop Res 2009, 27:1528-1533.
52. Vetrano M., d'Alessandro F., Torrisi M.R., Ferretti A., Vulpiani M.C., Visco V. Extracorporeal shock wave therapy promotes cell proliferation and collagen synthesis of primary cultured human tenocytes. Knee Surg Sports Traumatol Arthrosc 2011, 19:2159-2168.
53. Vulpiani M.C., Trischitta D., Trovato P., Vetrano M., Ferretti A. Extracorporeal shockwave therapy (ESWT) in Achilles tendinopathy: A long-term follow-up observational study. JSports Med Phys Fitness 2009, 49:171-176.
54. Wang C.J. An overview of shock wave therapy in musculoskeletal disorders. Chang Gung Med J 2003, 26:220-232.
55. Wang C.J., Wang F.S., Yang K.D., et al. Shock wave therapy induces neovascularization at the tendon-bone junction: A study in rabbits. JOrthop Res 2003, 21:984-989.
56. Wang F.S., Wang C.J., Chen S.M., et al. Superoxide mediates shock wave induction of ERK-dependent osteogenic transcription factor (CBFA1) and mesenchymal cell differentiation toward osteoprogenitors. JBiochem Mol Biol 2002, 277:10931-10937.
57. Wang X.T., Liu P.Y., Tang J.B. Tendon healing invitro: modification of tenocytes with exogenous vascular endothelial growth factor gene increases expression of transforming growth factor beta but minimally affects expression of collagen genes. JHand Surg Am 2005, 30:222-229.
58. Zhu H.J., Burgess A.W. Regulation of transforming growth factor-beta signaling. Mol Cell Biol Res Commun 2001, 4:321-330.
59. Zimpfer D., Aharinejad S., Holfeld J., Thomas A., Dumfarth J., Rosenhek R., Czerny M., Schaden W., Gmeiner M., Wolner E., Grimm M. Direct epicardial shock wave therapy improves ventricular function and induces angiogenesis in ischemic heart failure. JThorac Cardiovasc Surg 2009, 137:963-970.