Abstract

Thermal modifications induced in corneal stroma were investigated with the use of fluorescence microscopy. Tissue samples were heated in a water bath at temperatures in the 35–90°C range. Fluorescence images of the structural modifications induced were acquired after staining with Indocyanine Green (ICG). Discrete Fourier Transform (DFT) and entropy analyses of each image made it possible to characterize the thermally-induced phase transitions in the stroma, and to indicate a threshold value for high thermal damage. The procedure could be proposed as the basis for a real-time controlling system for surgical techniques based on induced thermal effects.

© 2007 Optical Society of America

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References

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  1. R. Brinkmann, N. Koop, G. Geerling, J. Kampmeier, S. Borcherding, K. Kamm, R. Birngruber, "Diode laser thermokeratoplasty: application strategy and dosimetry," J. Cataract Refract. Surg. 24, 1195-207 (1998).
    [PubMed]
  2. F. Rossi, R. Pini, L. Menabuoni, R. Mencucci, U. Menchini, S. Ambrosini, G. Vannelli, "Experimental study on the healing process following laser welding of the cornea," J. Biomed. Opt. 10, 024004 (2005).
    [CrossRef] [PubMed]
  3. K. Suthamjariya and R. Rox Anderson, "Laser in Dermatology," in Biomedical Photonics Handbook, T. Vo-Dinh, Ed., (CRC Press 2003), pp. 40/1-40/40.
  4. A. L. Wallace, R. M. Hollinshead, and C. B. Franck, "The scientific basis of thermal capsular shrinkage," J. Shoulder Elbow Surg. 9, 354-360 (2000).
    [CrossRef] [PubMed]
  5. J. Kampmeier, B. Radt, R. Birngruber, and R. Brinkmann, "Thermal and biomechanical parameters of porcine cornea," Cornea 19, 355-363 (2000).
    [CrossRef] [PubMed]
  6. C. A. Miles, T. V. Burjanadze, and A. J. Bailey, "The kinetics of the thermal denaturation of collagen in unrestrained rat tail tendon determined by differential scanning calorimetry," J. Mol. Biol. 245, 437-446 (1995).
    [CrossRef] [PubMed]
  7. F. Flandin, C. Buffevant, and D. Herbage, "A differential scanning calorimetry analysis of the age-related changes in the thermal stability of rat skin collagen," Biochim. Biophys. Acta 791, 205-211 (1984).
    [CrossRef] [PubMed]
  8. P. Kronick, B. Maleeff, and R. Carroll, "The locations of collagens with different thermal stabilities in fibrils of bovine reticular dermis," Connect. Tissue Res. 18, 123-134 (1988).
    [CrossRef] [PubMed]
  9. R. Agah, J. A. Pearce, A. J. Welch, and M. Motamedi, "Rate process model for arterial tissue thermal damage: implications on vessel photocoagulation," Lasers Surg. Med. 15, 176-184 (1994).
    [CrossRef] [PubMed]
  10. A. D. Zweig, B. Meierhofer, O. M. Muller, C. Mischler, V. Romano, M. Frenz, and H. P. Weber, "Lateral thermal damage along pulsed laser incisions," Lasers Surg. Med. 10, 262-274 (1990).
    [CrossRef] [PubMed]
  11. T. Tanaka, S. Furutani-Miura, M. Nakamura, and T. Nishida, "Immunohistochemical study of localization of extracellular matrix after holmium YAG laser irradiation in rat cornea," Jpn. J. Ophthalmol. 44, 482-488 (2000).
    [CrossRef] [PubMed]
  12. S. J. Lin, C. Y. Hsiao, Y. Sun, W. Lo, W. C. Lin, G. J. Jan, S. H. Jee, C. Y. Dong, "Monitoring the thermally induced structural transitions of collagen by use of second-harmonic generation microscopy," Opt. Lett. 30, 622-624 (2005).
    [CrossRef] [PubMed]
  13. T. Theodossiou, G. S. Rapti, V. Hovhannisyan, E. Georgiou, K. Politopoulos, and D. Yova, "Thermally induced irreversible conformational changes in collagen probed by optical second harmonic generation and laser-induced fluorescence," Lasers Med. Sci. 17, 34-41 (2002).
    [CrossRef] [PubMed]
  14. M. G. Lin, T. L. Yang, C. T. Chiang, H. C. Kao, J. N. Lee, W. Lo, S. H. Jee, Y. F. Chen, C. Y. Dong, and S. J. Lin, "Evaluation of dermal thermal damage by multiphoton autofluorescence and second-harmonic-generation microscopy," J. Biomed. Opt. 11, 064006 (2006).
    [CrossRef]
  15. G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, "3-dimensional imaging of collagen using second harmonic generation," J. Struct. Biol. 141, 53-62 (2003).
    [CrossRef] [PubMed]
  16. H. Y. Tan, S. W. Teng, W. Lo, W. C. Lin, S. J. Lin, S. H. Jee, and C. Y. Dong, "Characterizing the thermally induced structural changes to intact porcine eye, part 1: second harmonic generation imaging of cornea stroma," J. Biomed. Opt. 10, 054019 (2005).
    [CrossRef] [PubMed]
  17. G. Wollensak, E. Spoerl, and T. Seiler, "Stress-strain measurements of human and porcine corneas after riboflavin-ultraviolet-A-induced cross-linking," J. Cataract Refract. Surg. 29, 1780-1785 (2003)
    [CrossRef] [PubMed]
  18. M. L. J. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, "Light- absorbing properties, stability, and spectral stabilization of indocyanine green," J. Appl. Physiol. 40, 575-583 (1976).
    [PubMed]
  19. L.-P. Kamolza, H. Andel, W. Haslik, A. Donner, W. Winter, G. Meissl, and M. Frey, "Indocyanine green video angiographies help to identify burns requiring operation," Burns 29, 785-791 (2003).
    [CrossRef]
  20. L. A. Yannuzzi, M. D. Ober, J. S. Slakter, R. F. Spaide, Y L. Fisher, R.W. Flower, R. Rosen, "Ophthalmic fundus imaging: today and beyond," Am. J. Ophthalmol. 137, 511-524 (2004).
    [CrossRef] [PubMed]
  21. G. P. Holley, A. Alam, A. Kiri, and H. F. Edelhauser, "Effect of indocyanine green intraocular stain on human and rabbit corneal endothelial structure and viability. An in vitro study," J. Cataract Refract. Surg. 28, 1027-1033 (2002).
    [CrossRef] [PubMed]
  22. T. John, "Use of indocyanine green in deep lamellar endothelial keratoplasty," J. Cataract Refract. Surg. 29, 437-443 (2003).
    [CrossRef] [PubMed]
  23. L. Menabuoni, R. Pini, F. Rossi, I. Lenzetti, S. H. Yoo, and J.-M. Parel, "Laser-assisted corneal welding in cataract surgery: a retrospective study," J. Cataract Refract. Surg. (to be published).
  24. K. M. McNally-Heintzelman, "Laser Tissue Welding," in Biomedical Photonics Handbook, T. Vo-Dinh, ed., (CRC Press, 2003), Chap. 39, pp. 1-45.
  25. A. J. Welch and M. Van Germert, Optical-thermal response of laser-irradiated tissue (Plenum Press, 1995).
  26. A. Jain, Fundamentals of digital image processing (Prentice-Hall, 1989)
  27. M. N. Asiyo-Vogel, R. Brinkmann, H. Notbohm, R. Eggers, H. Lubatschowski, H. Laqua, and A. Vogel, "Histologic analysis of thermal effects of laser thermokeratoplasty and corneal ablation using Sirius-red polarization microscopy," J. Cataract Refract. Surg. 23, 515-26 (1997).
    [PubMed]

2006 (1)

M. G. Lin, T. L. Yang, C. T. Chiang, H. C. Kao, J. N. Lee, W. Lo, S. H. Jee, Y. F. Chen, C. Y. Dong, and S. J. Lin, "Evaluation of dermal thermal damage by multiphoton autofluorescence and second-harmonic-generation microscopy," J. Biomed. Opt. 11, 064006 (2006).
[CrossRef]

2005 (3)

S. J. Lin, C. Y. Hsiao, Y. Sun, W. Lo, W. C. Lin, G. J. Jan, S. H. Jee, C. Y. Dong, "Monitoring the thermally induced structural transitions of collagen by use of second-harmonic generation microscopy," Opt. Lett. 30, 622-624 (2005).
[CrossRef] [PubMed]

H. Y. Tan, S. W. Teng, W. Lo, W. C. Lin, S. J. Lin, S. H. Jee, and C. Y. Dong, "Characterizing the thermally induced structural changes to intact porcine eye, part 1: second harmonic generation imaging of cornea stroma," J. Biomed. Opt. 10, 054019 (2005).
[CrossRef] [PubMed]

F. Rossi, R. Pini, L. Menabuoni, R. Mencucci, U. Menchini, S. Ambrosini, G. Vannelli, "Experimental study on the healing process following laser welding of the cornea," J. Biomed. Opt. 10, 024004 (2005).
[CrossRef] [PubMed]

2004 (1)

L. A. Yannuzzi, M. D. Ober, J. S. Slakter, R. F. Spaide, Y L. Fisher, R.W. Flower, R. Rosen, "Ophthalmic fundus imaging: today and beyond," Am. J. Ophthalmol. 137, 511-524 (2004).
[CrossRef] [PubMed]

2003 (4)

T. John, "Use of indocyanine green in deep lamellar endothelial keratoplasty," J. Cataract Refract. Surg. 29, 437-443 (2003).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, "Stress-strain measurements of human and porcine corneas after riboflavin-ultraviolet-A-induced cross-linking," J. Cataract Refract. Surg. 29, 1780-1785 (2003)
[CrossRef] [PubMed]

L.-P. Kamolza, H. Andel, W. Haslik, A. Donner, W. Winter, G. Meissl, and M. Frey, "Indocyanine green video angiographies help to identify burns requiring operation," Burns 29, 785-791 (2003).
[CrossRef]

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, "3-dimensional imaging of collagen using second harmonic generation," J. Struct. Biol. 141, 53-62 (2003).
[CrossRef] [PubMed]

2002 (2)

T. Theodossiou, G. S. Rapti, V. Hovhannisyan, E. Georgiou, K. Politopoulos, and D. Yova, "Thermally induced irreversible conformational changes in collagen probed by optical second harmonic generation and laser-induced fluorescence," Lasers Med. Sci. 17, 34-41 (2002).
[CrossRef] [PubMed]

G. P. Holley, A. Alam, A. Kiri, and H. F. Edelhauser, "Effect of indocyanine green intraocular stain on human and rabbit corneal endothelial structure and viability. An in vitro study," J. Cataract Refract. Surg. 28, 1027-1033 (2002).
[CrossRef] [PubMed]

2000 (3)

T. Tanaka, S. Furutani-Miura, M. Nakamura, and T. Nishida, "Immunohistochemical study of localization of extracellular matrix after holmium YAG laser irradiation in rat cornea," Jpn. J. Ophthalmol. 44, 482-488 (2000).
[CrossRef] [PubMed]

A. L. Wallace, R. M. Hollinshead, and C. B. Franck, "The scientific basis of thermal capsular shrinkage," J. Shoulder Elbow Surg. 9, 354-360 (2000).
[CrossRef] [PubMed]

J. Kampmeier, B. Radt, R. Birngruber, and R. Brinkmann, "Thermal and biomechanical parameters of porcine cornea," Cornea 19, 355-363 (2000).
[CrossRef] [PubMed]

1998 (1)

R. Brinkmann, N. Koop, G. Geerling, J. Kampmeier, S. Borcherding, K. Kamm, R. Birngruber, "Diode laser thermokeratoplasty: application strategy and dosimetry," J. Cataract Refract. Surg. 24, 1195-207 (1998).
[PubMed]

1997 (1)

M. N. Asiyo-Vogel, R. Brinkmann, H. Notbohm, R. Eggers, H. Lubatschowski, H. Laqua, and A. Vogel, "Histologic analysis of thermal effects of laser thermokeratoplasty and corneal ablation using Sirius-red polarization microscopy," J. Cataract Refract. Surg. 23, 515-26 (1997).
[PubMed]

1995 (1)

C. A. Miles, T. V. Burjanadze, and A. J. Bailey, "The kinetics of the thermal denaturation of collagen in unrestrained rat tail tendon determined by differential scanning calorimetry," J. Mol. Biol. 245, 437-446 (1995).
[CrossRef] [PubMed]

1994 (1)

R. Agah, J. A. Pearce, A. J. Welch, and M. Motamedi, "Rate process model for arterial tissue thermal damage: implications on vessel photocoagulation," Lasers Surg. Med. 15, 176-184 (1994).
[CrossRef] [PubMed]

1990 (1)

A. D. Zweig, B. Meierhofer, O. M. Muller, C. Mischler, V. Romano, M. Frenz, and H. P. Weber, "Lateral thermal damage along pulsed laser incisions," Lasers Surg. Med. 10, 262-274 (1990).
[CrossRef] [PubMed]

1988 (1)

P. Kronick, B. Maleeff, and R. Carroll, "The locations of collagens with different thermal stabilities in fibrils of bovine reticular dermis," Connect. Tissue Res. 18, 123-134 (1988).
[CrossRef] [PubMed]

1984 (1)

F. Flandin, C. Buffevant, and D. Herbage, "A differential scanning calorimetry analysis of the age-related changes in the thermal stability of rat skin collagen," Biochim. Biophys. Acta 791, 205-211 (1984).
[CrossRef] [PubMed]

1976 (1)

M. L. J. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, "Light- absorbing properties, stability, and spectral stabilization of indocyanine green," J. Appl. Physiol. 40, 575-583 (1976).
[PubMed]

Am. J. Ophthalmol. (1)

L. A. Yannuzzi, M. D. Ober, J. S. Slakter, R. F. Spaide, Y L. Fisher, R.W. Flower, R. Rosen, "Ophthalmic fundus imaging: today and beyond," Am. J. Ophthalmol. 137, 511-524 (2004).
[CrossRef] [PubMed]

Biochim. Biophys. Acta (1)

F. Flandin, C. Buffevant, and D. Herbage, "A differential scanning calorimetry analysis of the age-related changes in the thermal stability of rat skin collagen," Biochim. Biophys. Acta 791, 205-211 (1984).
[CrossRef] [PubMed]

Burns (1)

L.-P. Kamolza, H. Andel, W. Haslik, A. Donner, W. Winter, G. Meissl, and M. Frey, "Indocyanine green video angiographies help to identify burns requiring operation," Burns 29, 785-791 (2003).
[CrossRef]

Connect. Tissue Res. (1)

P. Kronick, B. Maleeff, and R. Carroll, "The locations of collagens with different thermal stabilities in fibrils of bovine reticular dermis," Connect. Tissue Res. 18, 123-134 (1988).
[CrossRef] [PubMed]

Cornea (1)

J. Kampmeier, B. Radt, R. Birngruber, and R. Brinkmann, "Thermal and biomechanical parameters of porcine cornea," Cornea 19, 355-363 (2000).
[CrossRef] [PubMed]

J. Appl. Physiol. (1)

M. L. J. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, "Light- absorbing properties, stability, and spectral stabilization of indocyanine green," J. Appl. Physiol. 40, 575-583 (1976).
[PubMed]

J. Biomed. Opt. (3)

M. G. Lin, T. L. Yang, C. T. Chiang, H. C. Kao, J. N. Lee, W. Lo, S. H. Jee, Y. F. Chen, C. Y. Dong, and S. J. Lin, "Evaluation of dermal thermal damage by multiphoton autofluorescence and second-harmonic-generation microscopy," J. Biomed. Opt. 11, 064006 (2006).
[CrossRef]

H. Y. Tan, S. W. Teng, W. Lo, W. C. Lin, S. J. Lin, S. H. Jee, and C. Y. Dong, "Characterizing the thermally induced structural changes to intact porcine eye, part 1: second harmonic generation imaging of cornea stroma," J. Biomed. Opt. 10, 054019 (2005).
[CrossRef] [PubMed]

F. Rossi, R. Pini, L. Menabuoni, R. Mencucci, U. Menchini, S. Ambrosini, G. Vannelli, "Experimental study on the healing process following laser welding of the cornea," J. Biomed. Opt. 10, 024004 (2005).
[CrossRef] [PubMed]

J. Cataract Refract. Surg. (6)

R. Brinkmann, N. Koop, G. Geerling, J. Kampmeier, S. Borcherding, K. Kamm, R. Birngruber, "Diode laser thermokeratoplasty: application strategy and dosimetry," J. Cataract Refract. Surg. 24, 1195-207 (1998).
[PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, "Stress-strain measurements of human and porcine corneas after riboflavin-ultraviolet-A-induced cross-linking," J. Cataract Refract. Surg. 29, 1780-1785 (2003)
[CrossRef] [PubMed]

M. N. Asiyo-Vogel, R. Brinkmann, H. Notbohm, R. Eggers, H. Lubatschowski, H. Laqua, and A. Vogel, "Histologic analysis of thermal effects of laser thermokeratoplasty and corneal ablation using Sirius-red polarization microscopy," J. Cataract Refract. Surg. 23, 515-26 (1997).
[PubMed]

G. P. Holley, A. Alam, A. Kiri, and H. F. Edelhauser, "Effect of indocyanine green intraocular stain on human and rabbit corneal endothelial structure and viability. An in vitro study," J. Cataract Refract. Surg. 28, 1027-1033 (2002).
[CrossRef] [PubMed]

T. John, "Use of indocyanine green in deep lamellar endothelial keratoplasty," J. Cataract Refract. Surg. 29, 437-443 (2003).
[CrossRef] [PubMed]

L. Menabuoni, R. Pini, F. Rossi, I. Lenzetti, S. H. Yoo, and J.-M. Parel, "Laser-assisted corneal welding in cataract surgery: a retrospective study," J. Cataract Refract. Surg. (to be published).

J. Mol. Biol. (1)

C. A. Miles, T. V. Burjanadze, and A. J. Bailey, "The kinetics of the thermal denaturation of collagen in unrestrained rat tail tendon determined by differential scanning calorimetry," J. Mol. Biol. 245, 437-446 (1995).
[CrossRef] [PubMed]

J. Shoulder Elbow Surg. (1)

A. L. Wallace, R. M. Hollinshead, and C. B. Franck, "The scientific basis of thermal capsular shrinkage," J. Shoulder Elbow Surg. 9, 354-360 (2000).
[CrossRef] [PubMed]

J. Struct. Biol. (1)

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, "3-dimensional imaging of collagen using second harmonic generation," J. Struct. Biol. 141, 53-62 (2003).
[CrossRef] [PubMed]

Jpn. J. Ophthalmol. (1)

T. Tanaka, S. Furutani-Miura, M. Nakamura, and T. Nishida, "Immunohistochemical study of localization of extracellular matrix after holmium YAG laser irradiation in rat cornea," Jpn. J. Ophthalmol. 44, 482-488 (2000).
[CrossRef] [PubMed]

Lasers Med. Sci. (1)

T. Theodossiou, G. S. Rapti, V. Hovhannisyan, E. Georgiou, K. Politopoulos, and D. Yova, "Thermally induced irreversible conformational changes in collagen probed by optical second harmonic generation and laser-induced fluorescence," Lasers Med. Sci. 17, 34-41 (2002).
[CrossRef] [PubMed]

Lasers Surg. Med. (2)

R. Agah, J. A. Pearce, A. J. Welch, and M. Motamedi, "Rate process model for arterial tissue thermal damage: implications on vessel photocoagulation," Lasers Surg. Med. 15, 176-184 (1994).
[CrossRef] [PubMed]

A. D. Zweig, B. Meierhofer, O. M. Muller, C. Mischler, V. Romano, M. Frenz, and H. P. Weber, "Lateral thermal damage along pulsed laser incisions," Lasers Surg. Med. 10, 262-274 (1990).
[CrossRef] [PubMed]

Opt. Lett. (1)

Other (4)

K. Suthamjariya and R. Rox Anderson, "Laser in Dermatology," in Biomedical Photonics Handbook, T. Vo-Dinh, Ed., (CRC Press 2003), pp. 40/1-40/40.

K. M. McNally-Heintzelman, "Laser Tissue Welding," in Biomedical Photonics Handbook, T. Vo-Dinh, ed., (CRC Press, 2003), Chap. 39, pp. 1-45.

A. J. Welch and M. Van Germert, Optical-thermal response of laser-irradiated tissue (Plenum Press, 1995).

A. Jain, Fundamentals of digital image processing (Prentice-Hall, 1989)

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Figures (2)

Fig. 1.
Fig. 1.

Fluorescence micro-images of cornea samples heated in a water-bath at different temperatures. The logarithm of the absolute value of the DFT is also shown to the right of each image. The images correspond to an area of 400×400 µm.

Fig. 2.
Fig. 2.

Plot of the Disorganization Parameter (DP) vs. temperature. Peaks are in correspondence with the principal phase transition temperatures of corneal tissue [5, 16].

Equations (3)

Equations on this page are rendered with MathJax. Learn more.

F ( p , q ) = m = 0 M 1 n = 0 N 1 f ( m , n ) e j ( 2 π M ) pm e j ( 2 π N ) qn p = 0 , 1 , , M 1 q = 0 , 1 , , N 1
f ( m , n ) = 1 MN p = 0 M 1 q = 0 N 1 F ( p , q ) e j ( 2 π M ) pm e j ( 2 π N ) qn m = 0 , 1 , , M 1 n = 0 , 1 , , N 1
E = k = 0 L 1 P ( g k ) log ( P ( g k ) )

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