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Virtual Journal for Biomedical Optics

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  • Editor: Gregory W. Faris
  • Vol. 2, Iss. 10 — Oct. 31, 2007
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Monitoring thermally-induced phase transitions in porcine cornea with the use of fluorescence micro-imaging analysis

F. Rossi, P. Matteini, I. Bruno, P. Nesi, and R. Pini  »View Author Affiliations


Optics Express, Vol. 15, Issue 18, pp. 11178-11184 (2007)
http://dx.doi.org/10.1364/OE.15.011178


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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

1. Introduction

Thermal therapies are increasingly used in clinical practice for the treatment of diseases and injuries. Heat-induced effects have been exploited in ophthalmology for refractive surgery [1

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

] and for the closure of corneal wounds [2

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

]; in dermatology, for skin rejuvenation and resurfacing or for the treatment of cutaneous vascular lesions [3

3. K. Suthamjariya and R. Rox AndersonT. Vo-Dinh, Ed., (CRC Press2003), pp. 40/1–40/40.

]; in orthopedics, for the thermal treatment of shoulder instability [4

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]

]. The heating devices employed are based principally on the use of laser irradiation, radiofrequency electrical current, or microwaves. The main problem to solve, independently of applications and devices, is the control of the heating effect induced, during both the surgical treatment and the healing. In fact, monitoring thermally-induced structural modifications in connective tissues is of utmost importance in verifying the efficacy of the procedure and in preventing undesirable thermal damage to the surrounding tissues.

Structural changes in connective tissue resulting from therapeutic thermal treatments are primarily imputable to fibrillar collagen, the most common type of collagen in these tissues. This protein has a crystalline triple-helical tertiary structure that is transformed into an amorphous random coil configuration upon heating. Several techniques have been employed to characterize thermal modifications of collagen tissue. Calorimetric studies have typically been conducted using Differential Scanning Calorimetry (DSC). This method makes it possible to characterize the thermodynamic behavior of many connective tissues, which then show substantial improvement compared to the use of other previously-adopted approaches [5

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

8

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]

]. On the other hand, histological techniques (e.g. histological staining and immuno-fluorescent labeling) remain the most commonly-used imaging platform, due to their relative ease of use [9

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]

11

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]

]. Transmission Electron Microscopy (TEM) is used when high resolution is required [9

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]

, 11

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]

], but it involves high costs as well as complex protocols for specimen processing. Although DSC and the afore-mentioned microscopy techniques may be very useful when used on tissue ex vivo, they are unsuitable for monitoring heat-induced changes in vivo. Recently, Second Harmonic Generation (SHG) microscopy has been proposed as an alternative approach, as it is capable of furnishing accurate thermal responses without the need for histological or labeling protocols [12

12. S.J. Lin, C.Y. Hsiao, Y. Sun, W. Lo, W.C. Lin, G.J. Jan, S.H. Jee, and 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]

14

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]

]. Furthermore, this technique has the potential to be developed into an effective imaging tool for in vivo characterization. However, two main factors of SHG make the technique intrinsically unsuitable for tissue phase-transition characterization: firstly, the analysis has to be limited to fibrillar collagen, as it is the only component possessing nonlinear optical properties [15

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]

]; secondly, the signal rapidly decreases with an increase in the temperature, and is therefore ineffective in accurately detecting changes beyond the main peak of collagen denaturation [14

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]

].

In this paper we present an imaging system for monitoring thermally-induced phase transitions in connective tissues. The procedure is based on the use of fluorescence micro-imaging analysis of ICG-stained tissues. Our study was performed on porcine corneas, because this kind of connective tissue has a very regular structure and its thermal and biomechanical parameters are well-known [5

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

, 16

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

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]

]. Corneal collagen is regularly arranged in fibers that are organized into lamellae, i.e. in planes running parallel to the corneal surface. ICG has the advantage of staining the tissue homogeneously and un-specifically, thus providing a bright fluorescence emission from the entire structure of the sample. ICG was chosen because its photophysical properties are well-known [18

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]

], and because of its low toxicity and use in common practice in medical diagnostics and surgery [19

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]

22

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

]. Specifically, it has been proposed as a photosensitizer in several applications of laser welding techniques [23

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

24. K.M. McNally-HeintzelmanVo-Dinh Ted. (CRC Press, 2003), Chap. 39, pp. 1–45.

]. The procedure is based on a thermal process that induces immediate fusion of a wound wall. If simple analysis of the stained tissue during treatment has to be performed, it will be possible to characterize the phase transitions of the tissue. The proposed technique could thus be useful as an alternative, low-cost micro-imaging analysis for controlling thermal structural modifications in connective tissues.

2. Materials and methods

2.1. Heat bath treatment

Sixty-three freshly-enucleated, intact porcine eyes were used (mean age of the animals: 9–11 months). The entire corneas were extracted, and their transparency and integrity were controlled prior to being used in the tests. The samples were stored in BSS at room temperature for less then 6 hours. Each sample was then immersed in a water bath for five minutes. This treatment time ensured that thermal equilibrium was reached [25

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

]. A heating immersion circulator (mod. ED, Julabo Labortechnik GmbH, Seelbach, Germany) with ±0.03 °C temperature stability and a reading error of ±0.1 °C was used to heat the water bath. The temperature values studied were in the range of interest for medical applications: namely, the values 35, 40, 45, 47, 50, 53, 55, 56, 57, 58, 59, 60, 61, 62, 63, 66, 68, 71, 74, 77, 90°C were tested. Three different corneas were heated at each temperature, in order to give statistical significance to the study. After immersion in the water bath, the samples were stored in formalin until micro-imaging was performed.

2.2. Image acquisition

Cornea samples were sliced in 200-µm-thick cross-sections, which were stained with a 0.5% (w/w) water solution of Indocyanine Green (IC-GREEN, Akorn, Buffalo Grove, IL) over a 4- minute period. The slices were briefly rinsed in water and then mounted on microscope glass slides. All measurements were performed using an inverted epifluorescence microscope (Diaphot Nikon, Tokyo, Japan) equipped with a high-pressure mercury lamp (HBO 100 W, Osram, Augsberg, Germany) as the light source. The excitation wavelengths were selected using 10-nm bandwidth interference filters (436FS10-25, Andover Corporation, Salem, NH, USA) coupled to a dichroic mirror (ND510 Diaphot Nikon). Fluorescence images were acquired using a slow-scan cooled CCD camera (Chroma CX260, DTA, Cascina, Italy) equipped with a 512×512 pixel detector (KAF261E, Kodak, Heidelberg, Germany). The thermally-induced modifications to the corneal specimens were evaluated using fluorescence images acquired with a NIR long wave pass filter (800FH90-25, Andover Corporation).

2.3. Micro-imaging analysis

Two grey levels images showing a 400×400 µm tissue area were acquired from each cornea sample, in order to visualize both the anterior and posterior corneal stroma. The two techniques were then applied, by means of a commercial software image processing tool (Matlab® 7.1, the Mathworks, Natick, MA, USA). The 2D DFT of each image was computed with the proper software function. The DFT is usually defined for a discrete function f(m,n) that is nonzero only over the finite region 0≤mM-1 and 0≤nN-1. The two-dimensional MxN DFT and inverse MxN DFT relationships are given by:

F(p,q)=m=0M1n=0N1f(m,n)ej(2πM)pmej(2πN)qnp=0,1,,M1q=0,1,,N1
f(m,n)=1MNp=0M1q=0N1F(p,q)ej(2πM)pmej(2πN)qnm=0,1,,M1n=0,1,,N1
(1)

The values F(p,q) are the DFT coefficients of f(m,n). The resulting image spectrum was then shifted so as the zero-frequency component F(0,0), corresponding to the image average brightness, is displayed in the center of the frequency distribution image.

The same image source was processed by applying the edge function, based on Canny filter, to perform edge detection and extract the spatial distribution of the lamellar planes. The entropy was then evaluated. For an image with L grey levels, entropy E is a scalar value, defined as:

E=k=0L1P(gk)log(P(gk))
(2)

where: P(gk) is the histogram value of the k-th grey level gk. A new parameter was defined as the entropy inverse: it was indicated as the Disorganization Parameter (DP=1/E), and it was used to characterize heat-induced phase transitions in the stroma.

3. Results

We acquired six fluorescence images for each temperature value. The results are shown in Fig. 1. A regular horizontal pattern of lamellar sheets was observed at temperatures in the 35° to 47°C range. At higher values (50 to 61°C), the horizontal patterns showed increasing amplitude, while undulations were evident. Above 62°C, the patterns had a random distribution in space and a considerably increasing thickness. This behavior was evidenced by the plot of the logarithm of the DFT absolute value: the DFT distribution was prevalently along the vertical axis until the temperatures were below 62°C. When a temperature of more then 63°C was induced in the tissue, the DFT distribution was uniform and the plot of its absolute value assumed a circular form. The intensity entropy was calculated for each image, and the resulting DP was plotted. The results are shown in Fig. 2, where the calculated mean DP value and the standard error of the mean are reported for each temperature. Five relative maximum peaks are present, corresponding to the temperature values of 45°C, 53°C, 57°C, ~66°C and ~75°C.

4. Discussion

Micro-imaging analysis of ICG stained corneas evidenced the thermal structural phase transitions with the use of a simple image processing procedure. The DFT spatial distribution enabled us to characterize a threshold temperature that corresponded to 63°C in the case of corneal tissue. In the 35 to 62°C range, stromal lamellae orientations were preserved, even if an increasing thickness was observed.

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.

The method described here could be proposed as a control system, especially in those surgical procedures in which ICG staining of the tissue is also part of the treatment protocol. For example, it could be used in laser welding of the cornea: this surgical technique is currently performed as a substitute for or support to conventional suturing [23

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).

]. Corneal tissue fusion is accomplished after staining the wound edges with an ICG solution, which acts as a photo-enhancing chromophore, and then irradiating with a low-power diode laser emitting at 810 nm. In this case, the simple method that we have set up could be useful in monitoring the photothermal effect induced in corneal tissue. Its extension to in vivo real-time applications could be carried out by means of an association with confocal microscopy.

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].

5. Conclusion

We have described a procedure for characterizing phase transitions in corneal tissue with the use of a low cost apparatus and the simple implementation of an image-processing algorithm. The system has been found to be extremely precise in detecting thermally-induced morphological modifications in the corneal stroma. It could, therefore, be used as the basis for a control methodology during surgical procedures based on heating treatments in connective tissues.

References and links

1.

R. Brinkmann, N. Koop, G. Geerling, J. Kampmeier, S. Borcherding, K. Kamm, and 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, and 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 AndersonT. Vo-Dinh, Ed., (CRC Press2003), 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, and 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, and 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-HeintzelmanVo-Dinh Ted. (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]

OCIS Codes
(100.2960) Image processing : Image analysis
(120.6810) Instrumentation, measurement, and metrology : Thermal effects
(170.2520) Medical optics and biotechnology : Fluorescence microscopy

ToC Category:
Medical Optics and Biotechnology

History
Original Manuscript: June 4, 2007
Revised Manuscript: July 25, 2007
Manuscript Accepted: July 25, 2007
Published: August 21, 2007

Virtual Issues
Vol. 2, Iss. 10 Virtual Journal for Biomedical Optics

Citation
F. Rossi, P. Matteini, I. Bruno, P. Nesi, and R. Pini, "Monitoring thermally-induced phase transitions in porcine cornea with the use of fluorescence micro-imaging analysis," Opt. Express 15, 11178-11184 (2007)
http://www.opticsinfobase.org/vjbo/abstract.cfm?URI=oe-15-18-11178


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References

  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]

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