Abstract
Shock waves are used to treat musculoskeletal injuries and trigger the body’s mechanisms to initiate healing; however, the cellular and molecular working mechanisms are not fully known. Raman spectroscopy may be a useful tool to provide information on structural changes. Solid collagen type I from rat tail (> 90% pure) was suspended in water and was exposed in vitro to different numbers of shock waves and energy flux densities. Raman spectra were recorded at 2 h, 1 week, and 3 weeks after shock-wave treatment. The spectral analysis indicated that varying the number of shock waves and the energy flux density induced molecular changes in the collagen structure. Varying the energy flux density induced more significant changes than modifying the number of shock waves; however, in most cases, the collagen recovered its original conformation 3 weeks after treatment. A significant decrease in the relative intensities of the conformational bands, which include amide I, amide III, and stretching C–C, was observed at different energy flux densities. In many clinical cases, the natural repair of tissue is improved after shock-wave treatment. Raman spectroscopy revealed that varying the energy flux density of the shock waves applied to rat collagen type I induced strong conformational molecular changes. Approximately 2–3 weeks after shock-wave treatment, a phase of “molecular ordering” tending to a “recovering molecular sequence repair” was observed.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Wess, O.: Physics and technology of shock wave and pressure wave therapy. 9th International Congress of the International Society for Musculoskeletal Shockwave Therapy (ISMST), News Letter, ISMST, vol. 2, pp. 2–12 (2006)
Cleveland, R.O., McAteer, J.A.: The physics of shock-wave lithotripsy. In: Smith, A.D., Badlani, G.H., Preminger, G.M., Kavoussi, L.R. (eds.) Smith’s Textbook of Endourology, pp. 529–558. Wiley, Chichester (2012). https://doi.org/10.1002/9781444345148.ch49
Loske, A.M.: Medical and Biomedical Applications of Shock Waves. Springer, Cham (2017). https://doi.org/10.1007/978-3-319-47570-7
Brañes, J., Contreras, H., Cabello, P., Antonic, V., Guiloff, L., Brañes, M.: Shoulder rotator cuff responses to extracorporeal shockwave therapy: morphological and immunohistochemical analysis. Shoulder Elbow 4, 163–168 (2012). https://doi.org/10.1111/j.1758-5740.2012.00178.x
Sandoval, C., Valenzuela, A., Rojas, C., Brañes, M., Guiloff, L.: Extracorporeal shockwave therapy for atrophic and oligotrophic nonunion of tibia and femur in high energy trauma patients. Case series. Int. J. Surg. Open 9, 36–40 (2017). https://doi.org/10.1016/j.ijso.2017.09.002
Wang, C., Wang, F., Yang, K.: Biological mechanism of musculoskeletal shock waves. Int. Soc. Musculoskelet. Shockwave Ther. News 1, 5–11 (2004)
Wang, C.-J., Chen, H.-S., Chen, C.-E., Yang, K.D.: Treatment of nonunions of long bone fractures with shock waves. Clin. Orthop. Relat. Res. 387, 95–101 (2001). https://doi.org/10.1097/00003086-200106000-00013
Wang, C.-J., Huang, H.-Y., Chen, H.-H., Pai, C.-H., Yang, K.D.: Effect of shock wave therapy on acute fractures of the tibia: A study in a dog model. Clin. Orthop. Relat. Res. 387, 112–118 (2001). https://doi.org/10.1097/00003086-200106000-00015
Cárcamo, J.J., Aliaga, A.E., Clavijo, E., Brañes, M., Campos-Vallette, M.M.: Raman and surface-enhanced Raman scattering in the study of human rotator cuff tissues after shock wave treatment. J. Raman Spectrosc. 43, 248–254 (2012). https://doi.org/10.1002/jrs.3019
Albert, J.-D., Meadeb, J., Guggenbuhl, P., Marin, F., Benkalfate, T., Thomazeau, H., Chalès, G.: High-energy extracorporeal shock-wave therapy for calcifying tendinitis of the rotator cuff: a randomised trial. J. Bone Joint Surg. Br. 89, 335–341 (2007). https://doi.org/10.1302/0301-620X.89B3.18249
Daecke, W., Kusnierczak, D., Loew, M.: Long-term effects of extracorporeal shockwave therapy in chronic calcific tendinitis of the shoulder. J. Shoulder Elb. Surg. 11, 476–480 (2002). https://doi.org/10.1067/mse.2002.126614
Furia, J.P.: High-energy extracorporeal shock wave therapy as a treatment for insertional Achilles tendinopathy. Am. J. Sports Med. 34, 733–740 (2006). https://doi.org/10.1177/0363546505281810
Ji, H.M., Kim, H.J., Han, S.J.: Extracorporeal shock wave therapy in myofascial pain syndrome of upper trapezius. Ann. Rehabil. Med. 36, 675–680 (2012). https://doi.org/10.5535/arm.2012.36.5.675
Yalcin, E., Keskin Akca, A., Selcuk, B., Kurtaran, A., Akyuz, M.: Effects of extracorporeal shock wave therapy on symptomatic heel spurs: a correlation between clinical outcome and radiologic changes. Rheumatol. Int. 32, 343–347 (2012). https://doi.org/10.1007/s00296-010-1622-z
Schaden, W., Thiele, R., Kölpl, C., Pusch, A.: Extracorporeal shock wave therapy (ESWT) in skin lesions. Int. Soc. Musculoskelet. Shockwave Ther. News 2, 13–14 (2006)
Weil Jr., L.S., Roukis, T.S., Weil Sr., L.S., Borrelli, A.H.: Extracorporeal shock wave therapy for the treatment of chronic plantar fasciitis: Indications, protocol, intermediate results, and a comparison of results to fasciotomy. J. Foot Ankle Surg. 41, 166–172 (2002). https://doi.org/10.1016/S1067-2516(02)80066-7
Cheing, G.L., Chang, H.: Extracorporeal shock wave therapy. J. Orthop. Sports Phys. 33, 337–343 (2003). https://doi.org/10.2519/jospt.2003.33.6.337
Lin, S.-Y., Li, M.-J., Cheng, W.-T.: FT-IR and Raman vibrational microspectroscopies used for spectral biodiagnosis of human tissues. J. Spectrosc. 21, 1–30 (2007). https://doi.org/10.1155/2007/278765
Bonifacio, A., Sergo, V.: Effects of sample orientation in Raman microspectroscopy of collagen fibers and their impact on the interpretation of the amide III band. Vib. Spectrosc. 53, 314–317 (2010). https://doi.org/10.1016/j.vibspec.2010.04.004
Janko, M., Davydovskaya, P., Bauer, M., Zink, A., Stark, R.W.: Anisotropic Raman scattering in collagen bundles. Opt. Lett. 35, 2765–2767 (2010). https://doi.org/10.1364/OL.35.002765
Frushour, B.G., Koenig, J.L.: Raman scattering of collagen, gelatin, and elastin. Biopolymers 14, 379–391 (1975). https://doi.org/10.1002/bip.1975.360140211
Campos-Vallette, M.M., Rey-Lafon, M.: Vibrational spectra and rotational isomerism in short chain n-perfluoroalkanes. J. Mol. Struct. 101, 23–45 (1983). https://doi.org/10.1016/0022-2860(83)85041-8
Spiro, T.G., Gaber, B.P.: Laser Raman scattering as a probe of protein structure. Ann. Rev. Biochem. 46, 553–572 (1977). https://doi.org/10.1146/annurev.bi.46.070177.003005
Tu, A.T.: Laser Raman scattering as a probe of protein structure. In: Clark, R.J.H., Hester, R.E. (eds.) Advances in Infrared and Raman Spectroscopy, vol. 13, pp. 47–112. Wiley, London (1986)
Fratzl, P.: Collagen: Structure and mechanics, an introduction. In: Fratzl, P. (ed.) Collagen: Structure and Mechanics, pp. 1–13. Springer, Boston (2008). https://doi.org/10.1007/978-0-387-73906-9_1
Shoulders, M.D., Raines, R.T.: Collagen structure and stability. Ann. Rev. Biochem. 78, 929–958 (2009). https://doi.org/10.1146/annurev.biochem.77.032207.120833
Brinckmann, J.: Collagens at a glance. In: Brinckmann, J., Notbohm, H., Mueller, P.K. (eds.) Collagen: Primer in Structure, Processing and Assembly. Topics in Current Chemistry, vol. 247, pp. 1–6. Springer, Heidelberg (2005). https://doi.org/10.1007/b103817
Bank, R.A., TeKoppele, J.M., Oostingh, G., Hazleman, B.L., Riley, G.P.: Lysylhydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann. Rheum. Dis. 58, 35–41 (1999). https://doi.org/10.1136/ard.58.1.35
Bernard, C.: Tejido conectivo. In: Geneser, F. (ed.) Histología, Sobre Bases Moleculares, pp. 197–225. Editorial Médica Panamericana, Madrid (2000)
Aragno, I., Odetti, P., Altamura, F., Cavalleri, O., Rolandi, R.: Structure of rat tail tendon collagen examined by atomic force microscope. Experientia 51, 1063–1067 (1995). https://doi.org/10.1007/BF01946917
Revenko, I., Sommer, F., Minh, D.T., Garrone, R., Franc, J.-M.: Atomic force microscopy study of the collagen fibre structure. Biol. Cell 80, 67–69 (1994). https://doi.org/10.1016/0248-4900(94)90019-1
Taatjes, D.J., Quinn, A.S., Bovill, E.G.: Imaging of collagen type III in fluid by atomic force microscopy. Microsc. Res. Tech. 44, 347–352 (1999). https://doi.org/10.1002/(SICI)1097-0029(19990301)44:5%3C347::AID-JEMT5%3E3.0.CO;2-2
Gullekson, C., Lucas, L., Hewitt, K., Kreplak, L.: Surface-sensitive Raman spectroscopy of collagen I fibrils. Biophys. J. 100, 1837–1845 (2011). https://doi.org/10.1016/j.bpj.2011.02.026
Cárcamo, J.J., Aliaga, A.E., Clavijo, R.E., Brañes, M.R., Campos-Vallette, M.M.: Raman study of the shock wave effect on collagens. Spectrochim. Acta A 86, 360–365 (2012). https://doi.org/10.1016/j.saa.2011.10.049
Perez, C., Chen, H., Matula, T.J., Karzova, M., Khokhlova, V.A.: Acoustic field characterization of the Duolith: Measurements and modeling of a clinical shock wave therapy device. J. Acoust. Soc. Am. 134, 1663–1674 (2013). https://doi.org/10.1121/1.4812885
Aliaga, A.E., Osorio-Román, I., Leyton, P., Garrido, C., Cárcamo, J., Caniulef, C., Célis, F., Díaz, F.G., Clavijo, E., Gómez-Jeria, J.S., Campos-Vallette, M.M.: Surface-enhanced Raman scattering study of l-tryptophan. J. Raman Spectrosc. 40, 164–169 (2009). https://doi.org/10.1002/jrs.2099
Aliaga, A.E., Osorio-Roman, I., Garrido, C., Leyton, P., Cárcamo, J., Clavijo, E., Gómez-Jeria, J.S., Díaz, F.G., Campos-Vallette, M.M.: Surface enhanced Raman scattering study of l-lysine. Vib. Spectrosc. 50, 131–135 (2009). https://doi.org/10.1016/j.vibspec.2008.09.018
Diaz Fleming, G., Finnerty, J.J., Campos-Vallette, M., Célis, F., Aliaga, A.E., Fredes, C., Koch, R.: Experimental and theoretical Raman and surface-enhanced Raman scattering study of cysteine. J. Raman Spectrosc. 40, 632–638 (2009). https://doi.org/10.1002/jrs.2175
Cárcamo, J.J., Aliaga, A.E., Clavijo, E., Garrido, C., Gómez-Jeria, J.S., Campos-Vallette, M.M.: Proline and hydroxyproline deposited on silver nanoparticles. A Raman, SERS and theoretical study. J. Raman Spectrosc. 43, 750–755 (2012). https://doi.org/10.1002/jrs.3092
De Gelder, J., De Gussem, K., Vandenabeele, P., Moens, L.: Reference database of Raman spectra of biological molecules. J. Raman Spectrosc. 38, 1133–1147 (2007). https://doi.org/10.1002/jrs.1734
Xu, J., Stangel, I., Butler, I.S., Gilson, D.F.R.: An FT-Raman spectroscopic investigation of dentin and collagen surfaces modified by 2-hydroxyethylmethacrylate. J. Dent. Res. 76, 596–601 (1997). https://doi.org/10.1177/00220345970760011101
Lyng, F.M., Faoláin, E.Ó., Conroy, J., Meade, A.D., Knief, P., Duffy, B., Hunter, M.B., Byrne, J.M., Kelehan, P., Byrne, H.J.: Vibrational spectroscopy for cervical cancer pathology, from biochemical analysis to diagnostic tool. Exp. Mol. Pathol. 82, 121–129 (2007). https://doi.org/10.1016/j.yexmp.2007.01.001
Cheng, W.T., Liu, M.T., Liu, H.N., Lin, S.Y.: Micro-Raman spectroscopy used to identify and grade human skin pilomatrixoma. Microsc. Res. Tech. 68, 75–79 (2005). https://doi.org/10.1002/jemt.20229
Herlinger, A.W., Long, T.V.: Laser-Raman and infrared spectra of amino acids and their metal complexes. III. Proline and bisprolinato complexes. J. Am. Chem. Soc. 92, 6481–6486 (1970). https://doi.org/10.1021/ja00725a016
Wolpert, M., Hellwig, P.: Infrared spectra and molar absorption coefficients of the 20 alpha amino acids in aqueous solutions in the spectral range from 1800 to 500 cm−1. Spectrochim. Acta A 64, 987–1001 (2006). https://doi.org/10.1016/j.saa.2005.08.025
Rainey, J.K., Goh, M.C.: A statistically derived parameterization for the collagen triple-helix. Protein Sci. 11, 2748–2754 (2002). https://doi.org/10.1110/ps.0218502
Gunn, J.S., Ehrlich, H.P.: Evidence that translocation of collagen fibril segments plays a role in early intrinsic tendon repair. Plast. Reconstr. Surg. 129, 300e–306e (2012). https://doi.org/10.1097/PRS.0b013e31823aeb5a
Hazard, S.W., Myers, R.L., Ehrlich, H.P.: Demonstrating collagen tendon fibril segments involvement in intrinsic tendon repair. Exp. Mol. Pathol. 91, 660–663 (2011). https://doi.org/10.1016/j.yexmp.2011.08.002
Svensson, R.B., Herchenhan, A., Starborg, T., Larsen, M., Kadler, K.E., Qvortrup, K., Magnusson, S.P.: Evidence of structurally continuous collagen fibrils in tendons. Acta Biomater. 50, 293–301 (2017). https://doi.org/10.1016/j.actbio.2017.01.006
Acknowledgements
Ricardo Aroca and Francisco Fernández are acknowledged for revision of the manuscript. This work was financially supported by the “Fondo Nacional de Desarrollo Científico y Tecnológico” (FONDECYT) of Chile (Project No. 11140262).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict interest.
Additional information
Communicated by S. H. R. Hosano and A. Higgins.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cárcamo-Vega, J.J., Brañes, M.R., Loske, A.M. et al. The influence of the number of shock waves and the energy flux density on the Raman spectrum of collagen type I from rat. Shock Waves 30, 201–214 (2020). https://doi.org/10.1007/s00193-019-00920-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00193-019-00920-4