Prediction of heat-induced collagen shrinkage by use of second harmonic generation microscopy.

Collagen shrinkage associated with denaturation from thermal treatment has a number of important clinical applications. However, individualized treatment is hindered by the lack of reliable noninvasive methods to monitor the process of collagen denaturation. We investigate the serial changes of collagen denaturation from thermal treatment of rat tail tendons at 58 degrees C by use of second harmonic generation (SHG) microscopy. We find that rat tail tendon shrinks progressively from 0 to 9 min of thermal treatment, and remains unchanged in length upon further thermal treatment. The SHG intensity also decreases from 0 to 9 min of thermal treatment and becomes barely detectable from further thermal treatment. Collagen shrinkage and the SHG intensity are well correlated in a linear model. In addition, SHG imaging reveals a tiger-tail-like pattern of collagen denaturation. The bands of denatured collagen progressively widen from increased thermal treatment and completely replace the adjacent bands of normal collagen after 9 min of thermal treatment. Our results show that collagen denaturation in rat tail tendon from thermal treatment is inhomogeneous, and that SHG intensity can be used to predict the degree of thermally induced collagen shrinkage. With additional development, this approach has the potential to be used in biomedical applications.

[1]  J D Humphrey,et al.  Denaturation of collagen via heating: an irreversible rate process. , 2002, Annual review of biomedical engineering.

[2]  C. A. Miles,et al.  The increase in denaturation temperature following cross-linking of collagen is caused by dehydration of the fibres. , 2005, Journal of molecular biology.

[3]  Chen-Yuan Dong,et al.  Monitoring the thermally induced structural transitions of collagen by use of second-harmonic generation microscopy. , 2005, Optics letters.

[4]  Paul Doty,et al.  The Native and Denatured States of Soluble Collagen , 1956 .

[5]  B. Buckingham,et al.  Relationship between the content of lysyl oxidase-dependent cross-links in skin collagen, nonenzymatic glycosylation, and long-term complications in type I diabetes mellitus. , 1990, The Journal of clinical investigation.

[6]  O. Ishikawa,et al.  An increase of mature type skin collagen cross-link, histidinohydroxylysinonorleucine, in the sclerotic skin of morphea. , 2001, Journal of dermatological science.

[7]  R. E. Burge,et al.  The thermal denaturation of collagen in solution and its structural implications , 1959 .

[8]  D. Goldberg,et al.  Full-face nonablative dermal remodeling with a 1320 nm Nd:YAG laser. , 2000, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[9]  E. Tanzi,et al.  Treatment of Facial Rhytides With a Nonablative 1,450‐nm Diode Laser: A Controlled Clinical and Histologic Study , 2003, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[10]  R. Gebker,et al.  Different pattern of collagen cross-links in two sclerotic skin diseases: lipodermatosclerosis and circumscribed scleroderma. , 2001, The Journal of investigative dermatology.

[11]  A M Rubenchik,et al.  Collagen structure and nonlinear susceptibility: Effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity , 2000, Lasers in surgery and medicine.

[12]  F. Savoie,et al.  Laser-assisted capsulorrhaphy for multidirectional instability of the shoulder. , 2001, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[13]  J D Humphrey,et al.  Heat-induced changes in the mechanics of a collagenous tissue: isothermal, isotonic shrinkage. , 1998, Journal of biomechanical engineering.

[14]  J. Bogdanske,et al.  The effect of nonablative laser energy on the ultrastructure of joint capsular collagen. , 1996, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[15]  J D Humphrey,et al.  Heat-induced changes in the mechanics of a collagenous tissue: isothermal free shrinkage. , 1997, Journal of biomechanical engineering.

[16]  J. Fujimoto,et al.  Ultrahigh-resolution ophthalmic optical coherence tomography , 2001, Nature Medicine.

[17]  Beop-Min Kim,et al.  Polarization-dependent optical second-harmonic imaging of a rat-tail tendon. , 2002, Journal of biomedical optics.

[18]  Iris Riemann,et al.  High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution. , 2003, Journal of biomedical optics.

[19]  D J Goldberg,et al.  Nonablative treatment of rhytids with intense pulsed light , 2000, Lasers in surgery and medicine.

[20]  J. Bogdanske,et al.  The Effect of Thermal Heating on the Length and Histologic Properties of the Glenohumeral Joint Capsule , 1997, The American journal of sports medicine.

[21]  E. Manche,et al.  Conductive keratoplasty for the correction of low to moderate hyperopia: U.S. clinical trial 1-year results on 355 eyes. , 2002, Ophthalmology.

[22]  Pulsed Carbon Dioxide Laser Resurfacing of Photoaged Facial Skin , 1996 .

[23]  W. Webb,et al.  Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Bernard Choi,et al.  Reversible dissociation of collagen in tissues. , 2003, The Journal of investigative dermatology.

[25]  B. Tromberg,et al.  Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Bogdanske,et al.  The Effect of Nonablative Laser Energy on Joint Capsular Properties , 1996, The American journal of sports medicine.

[27]  B Zarins,et al.  The Thermal Properties of Bovine Joint Capsule , 1997, The American journal of sports medicine.

[28]  E. Tanzi,et al.  Improvement of Neck and Cheek Laxity With a Nonablative Radiofrequency Device: A Lifting Experience , 2004, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[29]  Brian Seed,et al.  Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation , 2003, Nature Medicine.

[30]  H Hörmann,et al.  Reversible and irreversible denaturation of collagen fibers. , 1971, Biochemistry.

[31]  M. Yamauchi,et al.  Collagen cross-linking in sun-exposed and unexposed sites of aged human skin. , 1991, The Journal of investigative dermatology.

[32]  Chen-Yuan Dong,et al.  Evaluating cutaneous photoaging by use of multiphoton fluorescence and second-harmonic generation microscopy. , 2005, Optics letters.

[33]  R. Rucker,et al.  Cross-linking amino acids in collagen and elastin. , 1978, The American journal of clinical nutrition.

[34]  Leslie M Loew,et al.  Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms , 2003, Nature Biotechnology.

[35]  T. Alster,et al.  Treatment of Facial Rhytides with a High‐Energy Pulsed Carbon Dioxide Laser , 1996, Plastic and reconstructive surgery.

[36]  N. Cox Fitzpatrick's Dermatology in General Medicine. , 2004 .

[37]  M. Markel,et al.  Thermal modification of joint capsuleand ligamentous tissues , 1998 .

[38]  Takeshi Yasui,et al.  Characterization of collagen orientation in human dermis by two-dimensional second-harmonic-generation polarimetry. , 2004, Journal of biomedical optics.

[39]  R. Geronemus,et al.  Multicenter study of noninvasive radiofrequency for periorbital tissue tightening , 2003, Lasers in surgery and medicine.

[40]  K. Khatri,et al.  Comparison of erbium:YAG and carbon dioxide lasers in resurfacing of facial rhytides. , 1999, Archives of dermatology.

[41]  R. Webb,et al.  In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast. , 1995, The Journal of investigative dermatology.

[42]  K Hayashi,et al.  The Effect of Nonablative Laser Energy on Joint Capsular Properties , 1995, The American journal of sports medicine.

[43]  N. Efron,et al.  Correlation of the Appearance of the Keratoconic Cornea In Vivo by Confocal Microscopy and In Vitro by Light Microscopy , 2005, Cornea.

[44]  T. Alster,et al.  Nonablative Laser Skin Resurfacing using a 1540 nm Erbium Glass Laser: A Clinical and Histologic Analysis , 2002, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].