Abstract

We report a multimodal optical approach using both Raman spectroscopy and optical coherence tomography (OCT) in tandem to discriminate between colonic adenocarcinoma and normal colon. Although both of these non-invasive techniques are capable of discriminating between normal and tumour tissues, they are unable individually to provide both the high specificity and high sensitivity required for disease diagnosis. We combine the chemical information derived from Raman spectroscopy with the texture parameters extracted from OCT images. The sensitivity obtained using Raman spectroscopy and OCT individually was 89% and 78% respectively and the specificity was 77% and 74% respectively. Combining the information derived using the two techniques increased both sensitivity and specificity to 94% demonstrating that combining complementary optical information enhances diagnostic accuracy. These data demonstrate that multimodal optical analysis has the potential to achieve accurate non-invasive cancer diagnosis.

© 2013 OSA

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N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt.17(7), 071305 (2012).
[CrossRef] [PubMed]

2011

M. Bhattacharjee, P. C. Ashok, K. D. Rao, S. K. Majumder, Y. Verma, and P. K. Gupta, “Binary tissue classification studies on resected human breast tissues using optical coherence tomography images,” J Innovat. Opt. Health Sci.4(01), 59–66 (2011).
[CrossRef]

C. Scalfi-Happ, M. Udart, C. Hauser, and A. Rück, “Investigation of lipid bodies in a colon carcinoma cell line by confocal Raman microscopy,” Med. Laser Appl.26(4), 152–157 (2011).
[CrossRef]

2009

J. W. Evans, R. J. Zawadzki, R. Liu, J. W. Chan, S. M. Lane, and J. S. Werner, “Optical coherence tomography and Raman spectroscopy of the ex-vivo retina,” J Biophotonics2(6-7), 398–406 (2009).
[CrossRef] [PubMed]

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

2008

E. Widjaja, W. Zheng, and Z. W. Huang, “Classification of colonic tissues using near-infrared Raman spectroscopy and support vector machines,” Int. J. Oncol.32(3), 653–662 (2008).
[PubMed]

C. A. Patil, N. Bosschaart, M. D. Keller, T. G. van Leeuwen, and A. Mahadevan-Jansen, “Combined Raman spectroscopy and optical coherence tomography device for tissue characterization,” Opt. Lett.33(10), 1135–1137 (2008).
[CrossRef] [PubMed]

2007

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

2004

S. A. Boppart, “Optical coherence tomography - Principles applications and advances,” Minerva Biotecnol16, 211–237 (2004).

N. Stone, C. Kendall, J. Smith, P. Crow, and H. Barr, “Raman spectroscopy for identification of epithelial cancers,” Faraday Discuss.126, 141–157, discussion 169–183 (2004).
[CrossRef] [PubMed]

2003

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys.66(2), 239–303 (2003).
[CrossRef]

K. W. Gossage, T. S. Tkaczyk, J. J. Rodriguez, and J. K. Barton, “Texture analysis of optical coherence tomography images: feasibility for tissue classification,” J. Biomed. Opt.8(3), 570–575 (2003).
[CrossRef] [PubMed]

R. Leitgeb, C. Hitzenberger, and A. Fercher, “Performance of fourier domain vs. time domain optical coherence tomography,” Opt. Express11(8), 889–894 (2003).
[CrossRef] [PubMed]

C. A. Lieber and A. Mahadevan-Jansen, “Automated method for subtraction of fluorescence from biological Raman spectra,” Appl. Spectrosc.57(11), 1363–1367 (2003).
[CrossRef] [PubMed]

1999

1996

A. Mahadevan-Jansen and R. R. Richards-Kortum, “Raman spectroscopy for the detection of cancers and precancers,” J. Biomed. Opt.1(1), 31–70 (1996).
[CrossRef] [PubMed]

1995

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun.117(1-2), 43–48 (1995).
[CrossRef]

Andrade, P. O.

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

Ashok, P. C.

M. Bhattacharjee, P. C. Ashok, K. D. Rao, S. K. Majumder, Y. Verma, and P. K. Gupta, “Binary tissue classification studies on resected human breast tissues using optical coherence tomography images,” J Innovat. Opt. Health Sci.4(01), 59–66 (2011).
[CrossRef]

Backman, V. M.

Barr, H.

N. Stone, C. Kendall, J. Smith, P. Crow, and H. Barr, “Raman spectroscopy for identification of epithelial cancers,” Faraday Discuss.126, 141–157, discussion 169–183 (2004).
[CrossRef] [PubMed]

Barton, J. K.

K. W. Gossage, T. S. Tkaczyk, J. J. Rodriguez, and J. K. Barton, “Texture analysis of optical coherence tomography images: feasibility for tissue classification,” J. Biomed. Opt.8(3), 570–575 (2003).
[CrossRef] [PubMed]

Bhattacharjee, M.

M. Bhattacharjee, P. C. Ashok, K. D. Rao, S. K. Majumder, Y. Verma, and P. K. Gupta, “Binary tissue classification studies on resected human breast tissues using optical coherence tomography images,” J Innovat. Opt. Health Sci.4(01), 59–66 (2011).
[CrossRef]

Bitar, R. A.

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

Boppart, S. A.

S. A. Boppart, “Optical coherence tomography - Principles applications and advances,” Minerva Biotecnol16, 211–237 (2004).

Bosschaart, N.

Brennan, J. F.

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Brown, C. T. A.

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt.17(7), 071305 (2012).
[CrossRef] [PubMed]

Bruno, P. M.

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

Chan, J. W.

J. W. Evans, R. J. Zawadzki, R. Liu, J. W. Chan, S. M. Lane, and J. S. Werner, “Optical coherence tomography and Raman spectroscopy of the ex-vivo retina,” J Biophotonics2(6-7), 398–406 (2009).
[CrossRef] [PubMed]

Crow, P.

N. Stone, C. Kendall, J. Smith, P. Crow, and H. Barr, “Raman spectroscopy for identification of epithelial cancers,” Faraday Discuss.126, 141–157, discussion 169–183 (2004).
[CrossRef] [PubMed]

Dasari, R.

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Dholakia, K.

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt.17(7), 071305 (2012).
[CrossRef] [PubMed]

Drexler, W.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys.66(2), 239–303 (2003).
[CrossRef]

El-Zaiat, S. Y.

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun.117(1-2), 43–48 (1995).
[CrossRef]

Evans, J. W.

J. W. Evans, R. J. Zawadzki, R. Liu, J. W. Chan, S. M. Lane, and J. S. Werner, “Optical coherence tomography and Raman spectroscopy of the ex-vivo retina,” J Biophotonics2(6-7), 398–406 (2009).
[CrossRef] [PubMed]

Feld, M. S.

G. Zonios, L. T. Perelman, V. M. Backman, R. Manoharan, M. Fitzmaurice, J. Van Dam, and M. S. Feld, “Diffuse reflectance spectroscopy of human adenomatous colon polyps in vivo,” Appl. Opt.38(31), 6628–6637 (1999).
[CrossRef] [PubMed]

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Fercher, A.

Fercher, A. F.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys.66(2), 239–303 (2003).
[CrossRef]

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun.117(1-2), 43–48 (1995).
[CrossRef]

Fitzmaurice, M.

Ghita, A.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Giardini, M. E.

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt.17(7), 071305 (2012).
[CrossRef] [PubMed]

Gossage, K. W.

K. W. Gossage, T. S. Tkaczyk, J. J. Rodriguez, and J. K. Barton, “Texture analysis of optical coherence tomography images: feasibility for tissue classification,” J. Biomed. Opt.8(3), 570–575 (2003).
[CrossRef] [PubMed]

Gupta, P. K.

M. Bhattacharjee, P. C. Ashok, K. D. Rao, S. K. Majumder, Y. Verma, and P. K. Gupta, “Binary tissue classification studies on resected human breast tissues using optical coherence tomography images,” J Innovat. Opt. Health Sci.4(01), 59–66 (2011).
[CrossRef]

Hauser, C.

C. Scalfi-Happ, M. Udart, C. Hauser, and A. Rück, “Investigation of lipid bodies in a colon carcinoma cell line by confocal Raman microscopy,” Med. Laser Appl.26(4), 152–157 (2011).
[CrossRef]

Hitzenberger, C.

Hitzenberger, C. K.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys.66(2), 239–303 (2003).
[CrossRef]

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun.117(1-2), 43–48 (1995).
[CrossRef]

Huang, Z. W.

E. Widjaja, W. Zheng, and Z. W. Huang, “Classification of colonic tissues using near-infrared Raman spectroscopy and support vector machines,” Int. J. Oncol.32(3), 653–662 (2008).
[PubMed]

Kamp, G.

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun.117(1-2), 43–48 (1995).
[CrossRef]

Keller, M. D.

Kendall, C.

N. Stone, C. Kendall, J. Smith, P. Crow, and H. Barr, “Raman spectroscopy for identification of epithelial cancers,” Faraday Discuss.126, 141–157, discussion 169–183 (2004).
[CrossRef] [PubMed]

Koloydenko, A. A.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Krstajic, N.

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt.17(7), 071305 (2012).
[CrossRef] [PubMed]

Lane, S. M.

J. W. Evans, R. J. Zawadzki, R. Liu, J. W. Chan, S. M. Lane, and J. S. Werner, “Optical coherence tomography and Raman spectroscopy of the ex-vivo retina,” J Biophotonics2(6-7), 398–406 (2009).
[CrossRef] [PubMed]

Larraona-Puy, M.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Lasser, T.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys.66(2), 239–303 (2003).
[CrossRef]

Leach, I. H.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Leitgeb, R.

Lieber, C. A.

Liu, R.

J. W. Evans, R. J. Zawadzki, R. Liu, J. W. Chan, S. M. Lane, and J. S. Werner, “Optical coherence tomography and Raman spectroscopy of the ex-vivo retina,” J Biophotonics2(6-7), 398–406 (2009).
[CrossRef] [PubMed]

Mahadevan-Jansen, A.

Majumder, S. K.

M. Bhattacharjee, P. C. Ashok, K. D. Rao, S. K. Majumder, Y. Verma, and P. K. Gupta, “Binary tissue classification studies on resected human breast tissues using optical coherence tomography images,” J Innovat. Opt. Health Sci.4(01), 59–66 (2011).
[CrossRef]

Manoharan, R.

G. Zonios, L. T. Perelman, V. M. Backman, R. Manoharan, M. Fitzmaurice, J. Van Dam, and M. S. Feld, “Diffuse reflectance spectroscopy of human adenomatous colon polyps in vivo,” Appl. Opt.38(31), 6628–6637 (1999).
[CrossRef] [PubMed]

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Martin, A. A.

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

Martinho, H.

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

Notingher, I.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Orensteincarndona, J.

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Patil, C. A.

Perelman, L. T.

Perkins, W.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Rao, K. D.

M. Bhattacharjee, P. C. Ashok, K. D. Rao, S. K. Majumder, Y. Verma, and P. K. Gupta, “Binary tissue classification studies on resected human breast tissues using optical coherence tomography images,” J Innovat. Opt. Health Sci.4(01), 59–66 (2011).
[CrossRef]

Richards-Kortum, R. R.

A. Mahadevan-Jansen and R. R. Richards-Kortum, “Raman spectroscopy for the detection of cancers and precancers,” J. Biomed. Opt.1(1), 31–70 (1996).
[CrossRef] [PubMed]

Rodriguez, J. J.

K. W. Gossage, T. S. Tkaczyk, J. J. Rodriguez, and J. K. Barton, “Texture analysis of optical coherence tomography images: feasibility for tissue classification,” J. Biomed. Opt.8(3), 570–575 (2003).
[CrossRef] [PubMed]

Romer, T. J.

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Rück, A.

C. Scalfi-Happ, M. Udart, C. Hauser, and A. Rück, “Investigation of lipid bodies in a colon carcinoma cell line by confocal Raman microscopy,” Med. Laser Appl.26(4), 152–157 (2011).
[CrossRef]

Salenius, J.

M. S. Feld, R. Manoharan, J. Salenius, J. Orensteincarndona, T. J. Romer, J. F. Brennan, R. Dasari, and Y. Wang, “Detection and characterization of human tissue lesions with near infrared Raman spectroscopy,” P Soc Photo-Opt Ins 2388, 99–104 (1995).

Santo, A. M.

P. O. Andrade, R. A. Bitar, K. Yassoyama, H. Martinho, A. M. Santo, P. M. Bruno, and A. A. Martin, “Study of normal colorectal tissue by FT-Raman spectroscopy,” Anal. Bioanal. Chem.387(5), 1643–1648 (2007).
[CrossRef] [PubMed]

Scalfi-Happ, C.

C. Scalfi-Happ, M. Udart, C. Hauser, and A. Rück, “Investigation of lipid bodies in a colon carcinoma cell line by confocal Raman microscopy,” Med. Laser Appl.26(4), 152–157 (2011).
[CrossRef]

Smith, J.

N. Stone, C. Kendall, J. Smith, P. Crow, and H. Barr, “Raman spectroscopy for identification of epithelial cancers,” Faraday Discuss.126, 141–157, discussion 169–183 (2004).
[CrossRef] [PubMed]

Stone, N.

N. Stone, C. Kendall, J. Smith, P. Crow, and H. Barr, “Raman spectroscopy for identification of epithelial cancers,” Faraday Discuss.126, 141–157, discussion 169–183 (2004).
[CrossRef] [PubMed]

Tkaczyk, T. S.

K. W. Gossage, T. S. Tkaczyk, J. J. Rodriguez, and J. K. Barton, “Texture analysis of optical coherence tomography images: feasibility for tissue classification,” J. Biomed. Opt.8(3), 570–575 (2003).
[CrossRef] [PubMed]

Udart, M.

C. Scalfi-Happ, M. Udart, C. Hauser, and A. Rück, “Investigation of lipid bodies in a colon carcinoma cell line by confocal Raman microscopy,” Med. Laser Appl.26(4), 152–157 (2011).
[CrossRef]

Van Dam, J.

van Leeuwen, T. G.

Varma, S.

M. Larraona-Puy, A. Ghita, A. Zoladek, W. Perkins, S. Varma, I. H. Leach, A. A. Koloydenko, H. Williams, and I. Notingher, “Development of Raman microspectroscopy for automated detection and imaging of basal cell carcinoma,” J. Biomed. Opt.14(5), 054031 (2009).
[CrossRef] [PubMed]

Verma, Y.

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Figures (5)

Fig. 1
Fig. 1

Representative histological images from (a) normal, (b) tumour (adenocarcinoma) and (c) mixed normal and tumour tissue samples. In (c), tumour can be seen at the top left, and normal tissue at the bottom right.

Fig. 2
Fig. 2

Comparison of Raman signature between normal and tumour tissues. The solid lines show mean spectra for each category and the dotted lines show the standard deviations. The vertical bars highlight the Raman bands that show significant differences in student’s t test with significance level p < 0.001

Fig. 3
Fig. 3

Typical OCT images from normal and tumour tissues.

Fig. 4
Fig. 4

Flow chart of the data analysis performed using multi-modal data

Fig. 5
Fig. 5

Cluster plot showing principal components from each data set [a] PC1 vs. PC2 clusterplot showing support vectors in the Raman data. [b] PC1 vs. PC2 clusterplot showing support vectors in the OCT data. [c] PC1 of Raman data vs. PC1 of OCT data clusterplot showing support vectors for the combined data set. [d] PC1 of Raman data vs. PC1 of OCT data clusterplot of the combined data set where the data points corresponding to the “mix” samples are also plotted.

Tables (1)

Tables Icon

Table 1 Comparison of sensitivity and specificity of the classifier with data acquired from each modality.

Metrics