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Virtual Journal for Biomedical Optics

| EXPLORING THE INTERFACE OF LIGHT AND BIOMEDICINE

  • Editors: Andrew Dunn and Anthony Durkin
  • Vol. 6, Iss. 1 — Jan. 3, 2011
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Polarized near-infrared autofluorescence imaging combined with near-infrared diffuse reflectance imaging for improving colonic cancer detection

Xiaozhuo Shao, Wei Zheng, and Zhiwei Huang  »View Author Affiliations


Optics Express, Vol. 18, Issue 23, pp. 24293-24300 (2010)
http://dx.doi.org/10.1364/OE.18.024293


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Abstract

We evaluate the diagnostic feasibility of the integrated polarized near-infrared (NIR) autofluorescence (AF) and NIR diffuse reflectance (DR) imaging technique developed for colonic cancer detection. A total of 48 paired colonic tissue specimens (normal vs. cancer) were measured using the integrated NIR DR (850-1100 nm) and NIR AF imaging at the 785 nm laser excitation. The results showed that NIR AF intensities of cancer tissues are significantly lower than those of normal tissues (p<0.001, paired 2-sided Student’s t-test, n = 48). NIR AF imaging under polarization conditions gives a higher diagnostic accuracy (of ~92-94%) compared to non-polarized NIR AF imaging or NIR DR imaging. Further, the ratio imaging of NIR DR to NIR AF with polarization provides the best diagnostic accuracy (of ~96%) among the NIR AF and NIR DR imaging techniques. This work suggests that the integrated NIR AF/DR imaging under polarization condition has the potential to improve the early diagnosis and detection of malignant lesions in the colon.

© 2010 OSA

1. Introduction

2. Materials and methods

2.1 Integrated NIR autofluorescence and NIR diffuse reflectance imaging system

Figure 1
Fig. 1 Schematic of the integrated NIR AF and NIR DR imaging system with polarization developed for tissue measurements: collimator (C); band pass filter (BP); neutral density filter (ND); dichroic mirror (DM); long pass filter (LP); polarizer (P); analyzer (A); lens (L).
shows a schematic diagram of the integrated NIR AF and diffuse reflectance (DR) imaging system developed for tissue measurements. A 785 nm excitation light from a diode laser (maximum output: 300 mW, B&W Tec Inc, Newark, DE) is coupled into a 200 μm fiber and delivered into a collimator (F220SMA-B, Thorlabs, Newton, NJ) coupled with a narrow band-pass (BP) filter (LL01-785-12.5, Semrock Inc. Rochester, NY) for removing interference of fiber background fluorescence and laser noise. Then the filtered laser light is reflected by a dichroic mirror (Reflection: 450-800 nm, Transmission: 800-1400 nm; Semrock Inc., Rochester, NY) and shined onto the tissue specimen with a beam size of 10 mm. The induced AF emission from tissue passes through the dichroic mirror and a 850 nm long-pass filter (FEL0850, Thorlabs, Newton, NJ) and subsequently are collected by an NIR-optimized back-illuminated, deep-depletion charge-coupled device (CCD) detector (512x512 image pixels, 16 µm/pixel, Cascade II: 512, Photometrics, Tuscon, AZ). For the NIR DR imaging, a tungsten halogen light (HL-2000, Ocean Optics Inc., Dunedin, FL) is coupled into a 200 μm fiber and passes through a beam expander integrated with a polarizer to illuminate the tissue directly. The NIR diffuse reflectance photons from the tissue are collected by the CCD after passing through the dichroic mirror and the 850 nm long-pass filter. To acquire the AF and DR images under different polarization conditions, two linear polarizers (Model-10P109AR.16, Newport corporation, Irvine, CA) are placed along the AF and DR illumination light paths, and the parallel and perpendicular polarized AF/DR images can be acquired in tandem by rotating the analyzer positioned in front of the camera lens in the NIR AF/DR imaging system (Fig. 1). With the integrated NIR AF/DR imaging system developed, a set of six images can be acquired for colonic tissues in tandem, i.e., NIR AF image and the corresponding NIR DR image under three different excitation light polarization conditions (i.e., non-polarization; parallel and perpendicular polarization). The system acquires NIR AF images and DR images within the spectral bandwidth of 850-1100 nm, and each NIR AF image was acquired within 5 s with the 785 nm laser light irradiance of 0.15 W/cm2, while each NIR DR image was acquired within 0.01 s with the tungsten light incident power of 0.1 mW on the tissue surface.

2.2. Colonic tissue specimens

3. Results and discussion

To compare the diagnostic performance of NIR AF imaging under different polarization conditions, NIR AF intensities are calculated from the relatively homogenous regions (~2 x 2 mm2) on the normal and cancer NIR AF images, respectively. We apply the threshold value of 1 as a decision line for the normal to tumor NIR AF intensity ratio algorithm for differentiation between normal and tumor tissues (i.e., NIR AF ratio of >1 classified as normal, whereas NIR AF ratio of 1 ≤ classified as tumor). Figure 3(a)
Fig. 3 Pair-wise comparison of NIR AF intensities of all 48 paired (normal vs cancer) colonic tissues under the three different polarization conditions: (a) non-polarization, (b) parallel polarization, and (c) perpendicular polarization.
3(c) shows the pair-wise comparison of NIR AF intensities of all 48 paired (normal vs cancer) colonic tissues under the three polarization conditions (i.e., (a) non-polarization, (b) parallel and (c) perpendicular polarization). NIR AF intensities of cancer tissue are significantly lower than those of normal tissue with the p-values of 3.5E-4, 3.2E-8 and 5.8E-9, respectively, under the non-polarization, parallel and perpendicular polarization light excitation conditions (paired 2-sided Student’s t-test, n = 48). Based on the NIR AF intensity ratio of normal to cancer tissues (Inormal/Icancer), the diagnostic accuracies of 79.2% (38/48), 91.7% (44/48) and 93.8% (45/48), respectively, can be achieved by using the NIR AF imaging under the non-polarization, parallel and perpendicular polarization light excitation. Hence, the polarized NIR AF imaging was able to enhance the contrast between normal and cancer colonic tissue (Figs. 2 and 3) with a higher diagnostic accuracy (of ~92-94%) compared to the non-polarized AF imaging (accuracy of ~79%).

To explore the possible reason that the polarized NIR AF imaging performs better than the non-polarized NIR AF imaging technique for colonic cancer detection, we have also studied NIR AF polarization properties of normal and cancer colonic tissue by calculating the polarization ratio values (Ratio = (Ipar-Iper)/(Ipar + Iper)) in NIR AF images [Fig. 4(a)
Fig. 4 (a) The processed polarization ratio image ((Ipar-Iper)/(Ipar + Iper), where Ipar and Iper are the NIR AF intensities of normal and cancer tissues under the parallel and perpendicular polarization conditions. (b) Polarized ratio values along the line across normal and cancer colonic tissue as indicated on the polarization ratio image in Fig. 4(a).
]. It is observed that the polarization ratio values of cancer colonic tissue are in the range of 0.0001 to 0.01, while the polarization ratio values of normal tissue are much higher, ranging from 0.012 to 0.075 as shown in Fig. 4(b). Similar to the polarized reflectance imaging [23

23. S. L. Jacques, J. R. Roman, and K. Lee, “Imaging superficial tissues with polarized light,” Lasers Surg. Med. 26(2), 119–129 (2000). [CrossRef] [PubMed]

], the parallel-polarized NIR AF imaging contains the information mainly from the surface or shallower layer of the tissue, whereas the perpendicular-polarized NIR AF imaging reveals the information predominantly from deeper areas of the tissue [23

23. S. L. Jacques, J. R. Roman, and K. Lee, “Imaging superficial tissues with polarized light,” Lasers Surg. Med. 26(2), 119–129 (2000). [CrossRef] [PubMed]

,24

24. X. Wang and L. V. Wang, “Propagation of polarized light in birefringent turbid media: a Monte Carlo study,” J. Biomed. Opt. 7(3), 279–290 (2002). [CrossRef] [PubMed]

]. A much reduced polarization ratio of cancer tissue reflects that much more multiple light scatterings may occur in deeper regions of tissue due to the disorganized structures of tissue in colonic adenocarcinoma, resulting in a larger contribution of the perpendicular polarized light component as compared to the normal tissue. As such, the polarized NIR AF imaging technique has the ability to selectively probe the AF light photons that arise from the subsurface or deep areas of tissue for improving cancer diagnosis and characterization.

One notes that tissue NIR AF image acquired depends on not only the tissue status (e.g., tissue surface structures, physiology or histopathology status, etc.), but also the measurement conditions (e.g., light excitation-tissue-collection configurations with respect to the tissue surface, illumination light power variation, etc.) [25

25. J. Y. Qu, J. Hua, and Z. Huang, “Correction of geometrical effects on fluorescence imaging of tissue,” Opt. Commun. 176, 319–326 (2000). [CrossRef]

]. To eliminate the geometrical effects on NIR AF measurements such as the variations of the light source-tissue distance, the varying angles for the incident light and tissue fluorescence collections, and the irregularities of the tissue surface which are naturally encountered in practical tissue fluorescence imaging, we have also measured the NIR DR images from normal and cancer tissue serving as background image to normalize the NIR AF image for correcting the artifacts of NIR AF image non-uniformity. Figure 5
Fig. 5 NIR DR images of colonic tissues acquired using a white light source under different polarization illumination: (a) non-polarization, (b) parallel polarization, and (c) perpendicular polarization.
shows the NIR DR images of normal and cancer colonic tissue acquired under the three polarization conditions, which give no significance differences in NIR DR intensities between normal and cancer tissue (p-values of 0.20, 0.28 and 0.17, respectively for the non-polarization, parallel and perpendicular polarization conditions, paired 2-sided Student’s t-test, n = 48).

However, when normalize the NIR DR images [Figs. 5(a)5(c)] to the corresponding NIR AF images [Figs. 2(a)2(c)], much enhanced differences in NIR ratio imaging between normal and cancer tissue can be observed clearly in Figs. 6(a)
Fig. 6 Ratio imaging of the NIR DR image to the NIR AF image of colonic tissues under different polarization conditions: (a) non-polarization, (b) parallel polarization, (c) perpendicular polarization. (d) Comparison of ratio intensity profiles along the lines as indicated on the ratio images in (a-c). Note that the ratio intensity profiles under parallel and perpendicular polarization have been magnified by 3 times in Fig. 6(d) for better visualization.
6(c) [with the p-values of 5.0E-5, 2.5E-9 and 7.8E-10, respectively under the non-polarization, parallel and perpendicular polarization conditions (paired 2-sided Student’s t-test, n = 48)], and the NIR DR/NIR AF ratio values of cancer tissue can be ~2.8-fold larger than those of normal tissue [Fig. 6(d)]. The diagnostic accuracies of 83.3% (40/48), 93.8% (45/48) and 95.8% (46/48), respectively, can also be achieved by using the NIR DR/NIR AF ratio imaging under the non-polarization, parallel and perpendicular polarization conditions. Therefore, with the ability of correcting the geometrical effects on NIR AF measurements, the NIR DR/NIR AF ratio imaging technique can further improve the diagnostic accuracy (of ~94 to 96%) for colonic cancer detection, and may also have potential to be used for assisting in delineating the margins of tumors for surgical operation. One notes that the NIR laser light and the white light are incident onto the tissue surface with different angles in the current NIR AF and NIR DR imaging system (Fig. 1), resulting in the intensity gradient changes across the tissue surfaces (Figs. 5 and 6). With further optimizations of the integrated NIR AF/NIR DR imaging system using a collinear-illumination configuration (i.e., the white light is coupled into the same optical path of the NIR laser light in the NIR imaging system), the NIR DR/NIR AF ratio imaging technique can totally remove the tissue surface geometric effects for better tissue diagnosis and characterization. On top of these, due to heterogeneous properties of biological tissues, there are certain regions are with common intensities in both normal and cancer tissues. Hence, further investigations on correlating the NIR AF/DR images with the exact histological mapping of tissues are required to fully evaluate the detection power of the integrated NIR AF/NIR DR imaging technique.

4. Conclusions

In summary, we found that under the 785 nm laser excitation, NIR AF emission from colonic tissue can be detected and imaged by the sensitive NIR imaging system. Significant differences in AF intensity are observed between normal and cancer colonic tissue, indicating the feasibility of NIR AF imaging technique for colonic cancer detection. The ratio imaging of NIR DR to NIR AF under polarization condition further improves the colonic cancer diagnosis and characterization. We anticipate that with further miniaturization of the current NIR excitation and imaging system coupled with an endoscope, the integrated NIR AF and NIR DR imaging with polarization excitation technique developed in this work may have the potential to be a clinically useful tool for in vivo diagnosis and detection of colonic cancer during colonoscopic examination.

Acknowledgments

This research was supported by the Biomedical Research Council, the National Medical Research Council, and the Faculty Research Fund from the National University of Singapore.

References and links

1.

A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, and M. J. Thun, “Cancer statistics, 2009,” CA Cancer J. Clin. 59(4), 225–249 (2009). [CrossRef] [PubMed]

2.

W. Du, J. T. L. Mah, J. Lee, R. Sankila, R. Sankaranarayanan, and K. S. Chia, “Incidence and survival of mucinous adenocarcinoma of the colorectum: a population-based study from an Asian country,” Dis. Colon Rectum 47(1), 78–85 (2004). [CrossRef] [PubMed]

3.

R. M. Soetikno, T. Kaltenbach, R. V. Rouse, W. Park, A. Maheshwari, T. Sato, S. Matsui, and S. Friedland, “Prevalence of nonpolypoid (flat and depressed) colorectal neoplasms in asymptomatic and symptomatic adults,” JAMA 299(9), 1027–1035 (2008). [CrossRef] [PubMed]

4.

R. Kiesslich, A. Hoffman, and M. F. Neurath, “Colonoscopy, tumors, and inflammatory bowel disease - new diagnostic methods,” Endoscopy 38(1), 5–10 (2006). [CrossRef] [PubMed]

5.

A. L. McCallum, J. T. Jenkins, D. Gillen, and R. G. Molloy, “Evaluation of autofluorescence colonoscopy for the detection and diagnosis of colonic polyps,” Gastrointest. Endosc. 68(2), 283–290 (2008). [CrossRef] [PubMed]

6.

G. J. E. Brown and B. P. Saunders, “Advances in colonic imaging: technical improvements in colonoscopy,” Eur. J. Gastroenterol. Hepatol. 17(8), 785–792 (2005). [CrossRef] [PubMed]

7.

S. Anandasabapathy, “Endoscopic imaging: emerging optical techniques for the detection of colorectal neoplasia,” Curr. Opin. Gastroenterol. 24(1), 64–69 (2008). [CrossRef]

8.

T. D. Wang and G. Triadafilopoulos, “Autofluorescence imaging: have we finally seen the light?” Gastrointest. Endosc. 61(6), 686–688 (2005). [CrossRef] [PubMed]

9.

J. Hung, S. Lam, J. C. LeRiche, and B. Palcic, “Autofluorescence of normal and malignant bronchial tissue,” Lasers Surg. Med. 11(2), 99–105 (1991). [CrossRef] [PubMed]

10.

D. Roblyer, R. Richards-Kortum, K. Sokolov, A. K. El-Naggar, M. D. Williams, C. Kurachi, and A. M. Gillenwater, “Multispectral optical imaging device for in vivo detection of oral neoplasia,” J. Biomed. Opt. 13(2), 024019 (2008). [CrossRef] [PubMed]

11.

D. Pantalone, F. Andreoli, F. Fusi, V. Basile, G. Romano, G. Giustozzi, L. Rigacci, R. Alterini, and M. Monici, “Multispectral imaging autofluorescence microscopy in colonic and gastric cancer metastatic lymph nodes,” Clin. Gastroenterol. Hepatol. 5(2), 230–236 (2007). [CrossRef] [PubMed]

12.

W. R. Kessler, “Autofluorescence colonoscopy: a green light on the long road to “real-time” histology,” Gastrointest. Endosc. 68(2), 291–293 (2008). [CrossRef] [PubMed]

13.

R. Richards-Kortum, R. P. Rava, R. E. Petras, M. Fitzmaurice, M. Sivak, and M. S. Feld, “Spectroscopic diagnosis of colonic dysplasia,” Photochem. Photobiol. 53(6), 777–786 (1991). [PubMed]

14.

K. T. Schomacker, J. K. Frisoli, C. C. Compton, T. J. Flotte, J. M. Richter, N. S. Nishioka, and T. F. Deutsch, “Ultraviolet laser-induced fluorescence of colonic tissue: basic biology and diagnostic potential,” Lasers Surg. Med. 12(1), 63–78 (1992). [CrossRef] [PubMed]

15.

H. Aihara, K. Sumiyama, S. Saito, H. Tajiri, and M. Ikegami, “Numerical analysis of the autofluorescence intensity of neoplastic and non-neoplastic colorectal lesions by using a novel videoendoscopy system,” Gastrointest. Endosc. 69(3 Pt 2), 726–733 (2009). [CrossRef] [PubMed]

16.

X. Han, H. Lui, D. I. McLean, and H. Zeng, “Near-infrared autofluorescence imaging of cutaneous melanins and human skin in vivo,” J. Biomed. Opt. 14(2), 024017 (2009). [CrossRef] [PubMed]

17.

Z. Huang, H. Zeng, I. Hamzavi, A. Alajlan, E. Tan, D. I. McLean, and H. Lui, “Cutaneous melanin exhibiting fluorescence emission under near-infrared light excitation,” J. Biomed. Opt. 11(3), 34010 (2006). [CrossRef] [PubMed]

18.

Z. Huang, H. Lui, D. I. McLean, M. Korbelik, and H. Zeng, “Raman spectroscopy in combination with background near-infrared autofluorescence enhances the in vivo assessment of malignant tissues,” Photochem. Photobiol. 81(5), 1219–1226 (2005). [CrossRef] [PubMed]

19.

E. B. Hanlon, I. Itzkan, R. R. Dasari, M. S. Feld, R. J. Ferrante, A. C. McKee, D. Lathi, and N. W. Kowall, “Near-infrared fluorescence spectroscopy detects Alzheimer’s disease in vitro,” Photochem. Photobiol. 70(2), 236–242 (1999). [PubMed]

20.

Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24(1), 59–63 (2004).

21.

G. I. Zonios, R. M. Cothren, J. T. Arendt, J. Wu, J. Van Dam, J. M. Crawford, R. Manoharan, and M. S. Feld, “Morphological model of human colon tissue fluorescence,” IEEE Trans. Biomed. Eng. 43(2), 113–122 (1996). [CrossRef] [PubMed]

22.

R. Drezek, K. Sokolov, U. Utzinger, I. Boiko, A. Malpica, M. Follen, and R. Richards-Kortum, “Understanding the contributions of NADH and collagen to cervical tissue fluorescence spectra: modeling, measurements, and implications,” J. Biomed. Opt. 6(4), 385–396 (2001). [CrossRef] [PubMed]

23.

S. L. Jacques, J. R. Roman, and K. Lee, “Imaging superficial tissues with polarized light,” Lasers Surg. Med. 26(2), 119–129 (2000). [CrossRef] [PubMed]

24.

X. Wang and L. V. Wang, “Propagation of polarized light in birefringent turbid media: a Monte Carlo study,” J. Biomed. Opt. 7(3), 279–290 (2002). [CrossRef] [PubMed]

25.

J. Y. Qu, J. Hua, and Z. Huang, “Correction of geometrical effects on fluorescence imaging of tissue,” Opt. Commun. 176, 319–326 (2000). [CrossRef]

OCIS Codes
(170.0110) Medical optics and biotechnology : Imaging systems
(170.3890) Medical optics and biotechnology : Medical optics instrumentation
(170.4580) Medical optics and biotechnology : Optical diagnostics for medicine

ToC Category:
Medical Optics and Biotechnology

History
Original Manuscript: August 9, 2010
Revised Manuscript: September 13, 2010
Manuscript Accepted: October 24, 2010
Published: November 5, 2010

Virtual Issues
Vol. 6, Iss. 1 Virtual Journal for Biomedical Optics

Citation
Xiaozhuo Shao, Wei Zheng, and Zhiwei Huang, "Polarized near-infrared autofluorescence imaging combined with near-infrared diffuse reflectance imaging for improving colonic cancer detection," Opt. Express 18, 24293-24300 (2010)
http://www.opticsinfobase.org/vjbo/abstract.cfm?URI=oe-18-23-24293


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References

  1. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, and M. J. Thun, “Cancer statistics, 2009,” CA Cancer J. Clin. 59(4), 225–249 (2009). [CrossRef] [PubMed]
  2. W. Du, J. T. L. Mah, J. Lee, R. Sankila, R. Sankaranarayanan, and K. S. Chia, “Incidence and survival of mucinous adenocarcinoma of the colorectum: a population-based study from an Asian country,” Dis. Colon Rectum 47(1), 78–85 (2004). [CrossRef] [PubMed]
  3. R. M. Soetikno, T. Kaltenbach, R. V. Rouse, W. Park, A. Maheshwari, T. Sato, S. Matsui, and S. Friedland, “Prevalence of nonpolypoid (flat and depressed) colorectal neoplasms in asymptomatic and symptomatic adults,” JAMA 299(9), 1027–1035 (2008). [CrossRef] [PubMed]
  4. R. Kiesslich, A. Hoffman, and M. F. Neurath, “Colonoscopy, tumors, and inflammatory bowel disease - new diagnostic methods,” Endoscopy 38(1), 5–10 (2006). [CrossRef] [PubMed]
  5. A. L. McCallum, J. T. Jenkins, D. Gillen, and R. G. Molloy, “Evaluation of autofluorescence colonoscopy for the detection and diagnosis of colonic polyps,” Gastrointest. Endosc. 68(2), 283–290 (2008). [CrossRef] [PubMed]
  6. G. J. E. Brown and B. P. Saunders, “Advances in colonic imaging: technical improvements in colonoscopy,” Eur. J. Gastroenterol. Hepatol. 17(8), 785–792 (2005). [CrossRef] [PubMed]
  7. S. Anandasabapathy, “Endoscopic imaging: emerging optical techniques for the detection of colorectal neoplasia,” Curr. Opin. Gastroenterol. 24(1), 64–69 (2008). [CrossRef]
  8. T. D. Wang and G. Triadafilopoulos, “Autofluorescence imaging: have we finally seen the light?” Gastrointest. Endosc. 61(6), 686–688 (2005). [CrossRef] [PubMed]
  9. J. Hung, S. Lam, J. C. LeRiche, and B. Palcic, “Autofluorescence of normal and malignant bronchial tissue,” Lasers Surg. Med. 11(2), 99–105 (1991). [CrossRef] [PubMed]
  10. D. Roblyer, R. Richards-Kortum, K. Sokolov, A. K. El-Naggar, M. D. Williams, C. Kurachi, and A. M. Gillenwater, “Multispectral optical imaging device for in vivo detection of oral neoplasia,” J. Biomed. Opt. 13(2), 024019 (2008). [CrossRef] [PubMed]
  11. D. Pantalone, F. Andreoli, F. Fusi, V. Basile, G. Romano, G. Giustozzi, L. Rigacci, R. Alterini, and M. Monici, “Multispectral imaging autofluorescence microscopy in colonic and gastric cancer metastatic lymph nodes,” Clin. Gastroenterol. Hepatol. 5(2), 230–236 (2007). [CrossRef] [PubMed]
  12. W. R. Kessler, “Autofluorescence colonoscopy: a green light on the long road to “real-time” histology,” Gastrointest. Endosc. 68(2), 291–293 (2008). [CrossRef] [PubMed]
  13. R. Richards-Kortum, R. P. Rava, R. E. Petras, M. Fitzmaurice, M. Sivak, and M. S. Feld, “Spectroscopic diagnosis of colonic dysplasia,” Photochem. Photobiol. 53(6), 777–786 (1991). [PubMed]
  14. K. T. Schomacker, J. K. Frisoli, C. C. Compton, T. J. Flotte, J. M. Richter, N. S. Nishioka, and T. F. Deutsch, “Ultraviolet laser-induced fluorescence of colonic tissue: basic biology and diagnostic potential,” Lasers Surg. Med. 12(1), 63–78 (1992). [CrossRef] [PubMed]
  15. H. Aihara, K. Sumiyama, S. Saito, H. Tajiri, and M. Ikegami, “Numerical analysis of the autofluorescence intensity of neoplastic and non-neoplastic colorectal lesions by using a novel videoendoscopy system,” Gastrointest. Endosc. 69(3 Pt 2), 726–733 (2009). [CrossRef] [PubMed]
  16. X. Han, H. Lui, D. I. McLean, and H. Zeng, “Near-infrared autofluorescence imaging of cutaneous melanins and human skin in vivo,” J. Biomed. Opt. 14(2), 024017 (2009). [CrossRef] [PubMed]
  17. Z. Huang, H. Zeng, I. Hamzavi, A. Alajlan, E. Tan, D. I. McLean, and H. Lui, “Cutaneous melanin exhibiting fluorescence emission under near-infrared light excitation,” J. Biomed. Opt. 11(3), 34010 (2006). [CrossRef] [PubMed]
  18. Z. Huang, H. Lui, D. I. McLean, M. Korbelik, and H. Zeng, “Raman spectroscopy in combination with background near-infrared autofluorescence enhances the in vivo assessment of malignant tissues,” Photochem. Photobiol. 81(5), 1219–1226 (2005). [CrossRef] [PubMed]
  19. E. B. Hanlon, I. Itzkan, R. R. Dasari, M. S. Feld, R. J. Ferrante, A. C. McKee, D. Lathi, and N. W. Kowall, “Near-infrared fluorescence spectroscopy detects Alzheimer’s disease in vitro,” Photochem. Photobiol. 70(2), 236–242 (1999). [PubMed]
  20. Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24(1), 59–63 (2004).
  21. G. I. Zonios, R. M. Cothren, J. T. Arendt, J. Wu, J. Van Dam, J. M. Crawford, R. Manoharan, and M. S. Feld, “Morphological model of human colon tissue fluorescence,” IEEE Trans. Biomed. Eng. 43(2), 113–122 (1996). [CrossRef] [PubMed]
  22. R. Drezek, K. Sokolov, U. Utzinger, I. Boiko, A. Malpica, M. Follen, and R. Richards-Kortum, “Understanding the contributions of NADH and collagen to cervical tissue fluorescence spectra: modeling, measurements, and implications,” J. Biomed. Opt. 6(4), 385–396 (2001). [CrossRef] [PubMed]
  23. S. L. Jacques, J. R. Roman, and K. Lee, “Imaging superficial tissues with polarized light,” Lasers Surg. Med. 26(2), 119–129 (2000). [CrossRef] [PubMed]
  24. X. Wang and L. V. Wang, “Propagation of polarized light in birefringent turbid media: a Monte Carlo study,” J. Biomed. Opt. 7(3), 279–290 (2002). [CrossRef] [PubMed]
  25. J. Y. Qu, J. Hua, and Z. Huang, “Correction of geometrical effects on fluorescence imaging of tissue,” Opt. Commun. 176, 319–326 (2000). [CrossRef]

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