Abstract

Raman spectroscopy has been widely demonstrated for tissue characterization and disease discrimination, however current implementations with either 785 or 830 nm near-infrared (NIR) excitation have been ineffectual in tissues with intense autofluorescence such as the liver. Here we report the use of a dispersive 1064 nm Raman system using a low-noise Indium-Gallium-Arsenide (InGaAs) array to discriminate highly autofluorescent bulk tissue ex vivo specimens from healthy liver, adenocarcinoma, and hepatocellular carcinoma (N = 5 per group). The resulting spectra have been combined with a multivariate discrimination algorithm, sparse multinomial logistic regression (SMLR), to predict class membership of healthy and diseased tissues, and spectral bands selected for robust classification have been extracted. A quantitative metric called feature importance is defined based on classification outputs and is used to guide the association of spectral features with biological indicators of healthy and diseased liver tissue. Spectral bands with high feature importance for healthy and liver tumor specimens include retinol, heme, biliverdin, or quinones (1595 cm−1); lactic acid (838 cm−1); collagen (873 cm−1); and nucleic acids (1485 cm−1). Classification performance in both binary (normal versus tumor, 100% sensitivity and 89% specificity) and three-group cases (classification accuracy: normal 89%, adenocarcinoma 74%, hepatocellular carcinoma 64%) indicates the potential for accurately separating healthy and cancerous tissues and suggests implications for utilizing Raman techniques during surgical guidance in liver resection.

© 2015 Optical Society of America

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2015 (1)

M. C. Gaggini, R. S. Navarro, A. R. Stefanini, R. S. Sano, and L. Silveira., “Correlation between METAVIR scores and Raman spectroscopy in liver lesions induced by hepatitis C virus: a preliminary study,” Lasers Med. Sci. 30(4), 1347–1355 (2015).
[Crossref] [PubMed]

2014 (1)

2013 (3)

A. Rethy, T. Langø, and R. Mårvik, “Laparoscopic ultrasound for hepatocellular carcinoma and colorectal liver metastasis: an overview,” Surg. Laparosc. Endosc. Percutan. Tech. 23(2), 135–144 (2013).
[Crossref] [PubMed]

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

2012 (1)

H. Lui, J. Zhao, D. McLean, and H. Zeng, “Real-time Raman Spectroscopy for In Vivo Skin Cancer Diagnosis,” Cancer Res. 72(10), 2491–2500 (2012).
[Crossref] [PubMed]

2011 (6)

H. Q. Wang, N. Y. Huang, J. H. Zhao, H. Lui, M. Korbelik, and H. S. Zeng, “Depth-resolved in vivo micro-Raman spectroscopy of a murine skin tumor model reveals cancer-specific spectral biomarkers,” J. Raman Spectrosc. 42(2), 160–166 (2011).
[Crossref]

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

J. Bruix, M. Sherman, and American Association for the Study of Liver Diseases, “Management of hepatocellular carcinoma: an update,” Hepatology 53(3), 1020–1022 (2011).
[Crossref] [PubMed]

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

N. Huang, M. Short, J. Zhao, H. Wang, H. Lui, M. Korbelik, and H. Zeng, “Full range characterization of the Raman spectra of organs in a murine model,” Opt. Express 19(23), 22892–22909 (2011).
[Crossref] [PubMed]

2010 (2)

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

2009 (2)

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

2008 (2)

P. S. Hammon, S. Makeig, H. Poizner, E. Todorov, and V. R. de Sa, “Predicting reaching targets from human EEG,” IEEE Signal Proc. Mag. 25(1), 69–77 (2008).
[Crossref]

C. A. Lieber, S. K. Majumder, D. L. Ellis, D. D. Billheimer, and A. Mahadevan-Jansen, “In vivo nonmelanoma skin cancer diagnosis using Raman microspectroscopy,” Lasers Surg. Med. 40(7), 461–467 (2008).
[Crossref] [PubMed]

2007 (2)

N. Stone, R. Baker, K. Rogers, A. W. Parker, and P. Matousek, “Subsurface probing of calcifications with spatially offset Raman spectroscopy (SORS): future possibilities for the diagnosis of breast cancer,” Analyst (Lond.) 132(9), 899–905 (2007).
[Crossref] [PubMed]

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

2006 (1)

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

2005 (1)

B. Krishnapuram, L. Carin, M. A. T. Figueiredo, and A. J. Hartemink, “Sparse multinomial logistic regression: Fast algorithms and generalization bounds,” IEEE Trans. Pattern Anal. Mach. Intell. 27(6), 957–968 (2005).
[Crossref] [PubMed]

2004 (1)

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

2003 (1)

2002 (1)

1998 (1)

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

1997 (1)

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

1996 (3)

R. Manoharan, Y. Wang, and M. S. Feld, “Histochemical analysis of biological tissues using Raman spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 52(2), 215–249 (1996).
[Crossref]

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]

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

1995 (1)

C. J. Frank, R. L. McCreery, and D. C. Redd, “Raman spectroscopy of normal and diseased human breast tissues,” Anal. Chem. 67(5), 777–783 (1995).
[Crossref] [PubMed]

1994 (2)

C. J. Frank, D. C. Redd, T. S. Gansler, and R. L. McCreery, “Characterization of human breast biopsy specimens with near-IR Raman spectroscopy,” Anal. Chem. 66(3), 319–326 (1994).
[Crossref] [PubMed]

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

1991 (1)

G. Cassanas, M. Morssli, E. Fabregue, and L. Bardet, “Vibrational-spectra of lactic-acid and lactates,” J. Raman Spectrosc. 22(7), 409–413 (1991).
[Crossref]

1990 (1)

J. Goral and V. Zichy, “Fourier-Transform Raman Studies of Materials and Compounds of Biological Importance,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 46(2), 253–275 (1990).
[Crossref]

1976 (1)

V. J. C. Lin and J. L. Koenig, “Raman Studies of Bovine Serum Albumin,” Biopolymers 15(1), 203–218 (1976).
[Crossref] [PubMed]

Adar, F.

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

Auner, G.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Baek, S. J.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Baker, R.

N. Stone, R. Baker, K. Rogers, A. W. Parker, and P. Matousek, “Subsurface probing of calcifications with spatially offset Raman spectroscopy (SORS): future possibilities for the diagnosis of breast cancer,” Analyst (Lond.) 132(9), 899–905 (2007).
[Crossref] [PubMed]

Bao, P.

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

Baranska, M.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Bardet, L.

G. Cassanas, M. Morssli, E. Fabregue, and L. Bardet, “Vibrational-spectra of lactic-acid and lactates,” J. Raman Spectrosc. 22(7), 409–413 (1991).
[Crossref]

Bauer, M.

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

Bergholt, M. S.

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

Billheimer, D. D.

C. A. Lieber, S. K. Majumder, D. L. Ellis, D. D. Billheimer, and A. Mahadevan-Jansen, “In vivo nonmelanoma skin cancer diagnosis using Raman microspectroscopy,” Lasers Surg. Med. 40(7), 461–467 (2008).
[Crossref] [PubMed]

Bourquain, H.

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

Bruix, J.

J. Bruix, M. Sherman, and American Association for the Study of Liver Diseases, “Management of hepatocellular carcinoma: an update,” Hepatology 53(3), 1020–1022 (2011).
[Crossref] [PubMed]

Budach, W.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Campbell, W. B.

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

Cao, A.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Carin, L.

B. Krishnapuram, L. Carin, M. A. T. Figueiredo, and A. J. Hartemink, “Sparse multinomial logistic regression: Fast algorithms and generalization bounds,” IEEE Trans. Pattern Anal. Mach. Intell. 27(6), 957–968 (2005).
[Crossref] [PubMed]

Cassanas, G.

G. Cassanas, M. Morssli, E. Fabregue, and L. Bardet, “Vibrational-spectra of lactic-acid and lactates,” J. Raman Spectrosc. 22(7), 409–413 (1991).
[Crossref]

Chen, C. C.

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

Chlopicki, S.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Chruszcz-Lipska, K.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Clements, L.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Crowe, J. P.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Dasari, R. R.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

de Matos Granja, N.

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

de Sa, V. R.

P. S. Hammon, S. Makeig, H. Poizner, E. Todorov, and V. R. de Sa, “Predicting reaching targets from human EEG,” IEEE Signal Proc. Mag. 25(1), 69–77 (2008).
[Crossref]

Diderhoshan, M. A.

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

Dippel, B.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

Donfack, P.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Edwin, B.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Ellis, D. L.

C. A. Lieber, S. K. Majumder, D. L. Ellis, D. D. Billheimer, and A. Mahadevan-Jansen, “In vivo nonmelanoma skin cancer diagnosis using Raman microspectroscopy,” Lasers Surg. Med. 40(7), 461–467 (2008).
[Crossref] [PubMed]

Enejder, A. M.

Fabregue, E.

G. Cassanas, M. Morssli, E. Fabregue, and L. Bardet, “Vibrational-spectra of lactic-acid and lactates,” J. Raman Spectrosc. 22(7), 409–413 (1991).
[Crossref]

Feld, M. S.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

A. M. Enejder, T. W. Koo, J. Oh, M. Hunter, S. Sasic, M. S. Feld, and G. L. Horowitz, “Blood analysis by Raman spectroscopy,” Opt. Lett. 27(22), 2004–2006 (2002).
[Crossref] [PubMed]

R. Manoharan, Y. Wang, and M. S. Feld, “Histochemical analysis of biological tissues using Raman spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 52(2), 215–249 (1996).
[Crossref]

Fendel, S.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

Figueiredo, M. A. T.

B. Krishnapuram, L. Carin, M. A. T. Figueiredo, and A. J. Hartemink, “Sparse multinomial logistic regression: Fast algorithms and generalization bounds,” IEEE Trans. Pattern Anal. Mach. Intell. 27(6), 957–968 (2005).
[Crossref] [PubMed]

Fitzmaurice, M.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Fosse, E.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Frank, C. J.

C. J. Frank, R. L. McCreery, and D. C. Redd, “Raman spectroscopy of normal and diseased human breast tissues,” Anal. Chem. 67(5), 777–783 (1995).
[Crossref] [PubMed]

C. J. Frank, D. C. Redd, T. S. Gansler, and R. L. McCreery, “Characterization of human breast biopsy specimens with near-IR Raman spectroscopy,” Anal. Chem. 66(3), 319–326 (1994).
[Crossref] [PubMed]

Fung, A.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Gaggini, M. C.

M. C. Gaggini, R. S. Navarro, A. R. Stefanini, R. S. Sano, and L. Silveira., “Correlation between METAVIR scores and Raman spectroscopy in liver lesions induced by hepatitis C virus: a preliminary study,” Lasers Med. Sci. 30(4), 1347–1355 (2015).
[Crossref] [PubMed]

Galloway, R. L.

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

Gansler, T. S.

C. J. Frank, D. C. Redd, T. S. Gansler, and R. L. McCreery, “Characterization of human breast biopsy specimens with near-IR Raman spectroscopy,” Anal. Chem. 66(3), 319–326 (1994).
[Crossref] [PubMed]

Gardecki, J. A.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Goral, J.

J. Goral and V. Zichy, “Fourier-Transform Raman Studies of Materials and Compounds of Biological Importance,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 46(2), 253–275 (1990).
[Crossref]

Haddad, D.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Haka, A. S.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Hammon, P. S.

P. S. Hammon, S. Makeig, H. Poizner, E. Todorov, and V. R. de Sa, “Predicting reaching targets from human EEG,” IEEE Signal Proc. Mag. 25(1), 69–77 (2008).
[Crossref]

Hartemink, A. J.

B. Krishnapuram, L. Carin, M. A. T. Figueiredo, and A. J. Hartemink, “Sparse multinomial logistic regression: Fast algorithms and generalization bounds,” IEEE Trans. Pattern Anal. Mach. Intell. 27(6), 957–968 (2005).
[Crossref] [PubMed]

Hawi, S. R.

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

Heizmann, O.

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

Herline, A. J.

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

Hicks, D.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Ho, K. Y.

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

Hoffmann, A.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Horowitz, G. L.

Hu, J. M.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Huang, N.

Huang, N. Y.

H. Q. Wang, N. Y. Huang, J. H. Zhao, H. Lui, M. Korbelik, and H. S. Zeng, “Depth-resolved in vivo micro-Raman spectroscopy of a murine skin tumor model reveals cancer-specific spectral biomarkers,” J. Raman Spectrosc. 42(2), 160–166 (2011).
[Crossref]

Huang, Z. W.

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

Hunter, M.

Jarnagin, W.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Jasztal, A.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Kajdacsy-Balla, A.

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

Kan, L.

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

Kanter, E. M.

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

Kazaryan, A. M.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Keller, M. D.

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

Keller, S.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Kelley, M. C.

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

Kettelhack, C.

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

Klein, M. D.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Kochan, K.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Koenig, J. L.

V. J. C. Lin and J. L. Koenig, “Raman Studies of Bovine Serum Albumin,” Biopolymers 15(1), 203–218 (1976).
[Crossref] [PubMed]

Koo, T. W.

Korbelik, M.

N. Huang, M. Short, J. Zhao, H. Wang, H. Lui, M. Korbelik, and H. Zeng, “Full range characterization of the Raman spectra of organs in a murine model,” Opt. Express 19(23), 22892–22909 (2011).
[Crossref] [PubMed]

H. Q. Wang, N. Y. Huang, J. H. Zhao, H. Lui, M. Korbelik, and H. S. Zeng, “Depth-resolved in vivo micro-Raman spectroscopy of a murine skin tumor model reveals cancer-specific spectral biomarkers,” J. Raman Spectrosc. 42(2), 160–166 (2011).
[Crossref]

Krafft, C.

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

Krishnapuram, B.

B. Krishnapuram, L. Carin, M. A. T. Figueiredo, and A. J. Hartemink, “Sparse multinomial logistic regression: Fast algorithms and generalization bounds,” IEEE Trans. Pattern Anal. Mach. Intell. 27(6), 957–968 (2005).
[Crossref] [PubMed]

Langenburg, S. E.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Langø, T.

A. Rethy, T. Langø, and R. Mårvik, “Laparoscopic ultrasound for hepatocellular carcinoma and colorectal liver metastasis: an overview,” Surg. Laparosc. Endosc. Percutan. Tech. 23(2), 135–144 (2013).
[Crossref] [PubMed]

Lieber, C. A.

Lin, V. J. C.

V. J. C. Lin and J. L. Koenig, “Raman Studies of Bovine Serum Albumin,” Biopolymers 15(1), 203–218 (1976).
[Crossref] [PubMed]

Lochte, T.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

Lorincz, A.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Lui, H.

H. Lui, J. Zhao, D. McLean, and H. Zeng, “Real-time Raman Spectroscopy for In Vivo Skin Cancer Diagnosis,” Cancer Res. 72(10), 2491–2500 (2012).
[Crossref] [PubMed]

H. Q. Wang, N. Y. Huang, J. H. Zhao, H. Lui, M. Korbelik, and H. S. Zeng, “Depth-resolved in vivo micro-Raman spectroscopy of a murine skin tumor model reveals cancer-specific spectral biomarkers,” J. Raman Spectrosc. 42(2), 160–166 (2011).
[Crossref]

N. Huang, M. Short, J. Zhao, H. Wang, H. Lui, M. Korbelik, and H. Zeng, “Full range characterization of the Raman spectra of organs in a murine model,” Opt. Express 19(23), 22892–22909 (2011).
[Crossref] [PubMed]

Lyons, J.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Mahadevan-Jansen, A.

C. A. Patil, I. J. Pence, C. A. Lieber, and A. Mahadevan-Jansen, “1064 nm dispersive Raman spectroscopy of tissues with strong near-infrared autofluorescence,” Opt. Lett. 39(2), 303–306 (2014).
[Crossref] [PubMed]

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

C. A. Lieber, S. K. Majumder, D. L. Ellis, D. D. Billheimer, and A. Mahadevan-Jansen, “In vivo nonmelanoma skin cancer diagnosis using Raman microspectroscopy,” Lasers Surg. Med. 40(7), 461–467 (2008).
[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]

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

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]

Majumder, S.

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

Majumder, S. K.

C. A. Lieber, S. K. Majumder, D. L. Ellis, D. D. Billheimer, and A. Mahadevan-Jansen, “In vivo nonmelanoma skin cancer diagnosis using Raman microspectroscopy,” Lasers Surg. Med. 40(7), 461–467 (2008).
[Crossref] [PubMed]

Makeig, S.

P. S. Hammon, S. Makeig, H. Poizner, E. Todorov, and V. R. de Sa, “Predicting reaching targets from human EEG,” IEEE Signal Proc. Mag. 25(1), 69–77 (2008).
[Crossref]

Malpica, A.

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

Manda, P.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Manoharan, R.

R. Manoharan, Y. Wang, and M. S. Feld, “Histochemical analysis of biological tissues using Raman spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 52(2), 215–249 (1996).
[Crossref]

Marangos, I. P.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Mårvik, R.

A. Rethy, T. Langø, and R. Mårvik, “Laparoscopic ultrasound for hepatocellular carcinoma and colorectal liver metastasis: an overview,” Surg. Laparosc. Endosc. Percutan. Tech. 23(2), 135–144 (2013).
[Crossref] [PubMed]

Marzec, K. M.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Maslak, E.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Materny, A.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Mathisen, O.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Matousek, P.

N. Stone, R. Baker, K. Rogers, A. W. Parker, and P. Matousek, “Subsurface probing of calcifications with spatially offset Raman spectroscopy (SORS): future possibilities for the diagnosis of breast cancer,” Analyst (Lond.) 132(9), 899–905 (2007).
[Crossref] [PubMed]

McCreery, R. L.

C. J. Frank, R. L. McCreery, and D. C. Redd, “Raman spectroscopy of normal and diseased human breast tissues,” Anal. Chem. 67(5), 777–783 (1995).
[Crossref] [PubMed]

C. J. Frank, D. C. Redd, T. S. Gansler, and R. L. McCreery, “Characterization of human breast biopsy specimens with near-IR Raman spectroscopy,” Anal. Chem. 66(3), 319–326 (1994).
[Crossref] [PubMed]

McLean, D.

H. Lui, J. Zhao, D. McLean, and H. Zeng, “Real-time Raman Spectroscopy for In Vivo Skin Cancer Diagnosis,” Cancer Res. 72(10), 2491–2500 (2012).
[Crossref] [PubMed]

Metz, K.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Miga, M.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Miljkovic, M.

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

Mitchell, M. F.

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

Morssli, M.

G. Cassanas, M. Morssli, E. Fabregue, and L. Bardet, “Vibrational-spectra of lactic-acid and lactates,” J. Raman Spectrosc. 22(7), 409–413 (1991).
[Crossref]

Murphy, R.

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

Musiolik, H.

K. Kochan, K. M. Marzec, K. Chruszcz-Lipska, A. Jasztal, E. Maslak, H. Musiolik, S. Chłopicki, and M. Baranska, “Pathological changes in the biochemical profile of the liver in atherosclerosis and diabetes assessed by Raman spectroscopy,” Analyst (Lond.) 138(14), 3885–3890 (2013).
[Crossref] [PubMed]

Mycek, M. A.

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

Naik, R.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Naik, V.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Navarro, R. S.

M. C. Gaggini, R. S. Navarro, A. R. Stefanini, R. S. Sano, and L. Silveira., “Correlation between METAVIR scores and Raman spectroscopy in liver lesions induced by hepatitis C virus: a preliminary study,” Lasers Med. Sci. 30(4), 1347–1355 (2015).
[Crossref] [PubMed]

Nazemi, J.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Nithipatikom, K.

S. R. Hawi, W. B. Campbell, A. Kajdacsy-Balla, R. Murphy, F. Adar, and K. Nithipatikom, “Characterization of normal and malignant human hepatocytes by Raman microspectroscopy,” Cancer Lett. 110(1-2), 35–40 (1996).
[Crossref] [PubMed]

Oertli, D.

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

Oh, J.

Ondrake, J.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Pahnke, J.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Pandya, A.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Parker, A. W.

N. Stone, R. Baker, K. Rogers, A. W. Parker, and P. Matousek, “Subsurface probing of calcifications with spatially offset Raman spectroscopy (SORS): future possibilities for the diagnosis of breast cancer,” Analyst (Lond.) 132(9), 899–905 (2007).
[Crossref] [PubMed]

Patil, C. A.

Peitgen, H. O.

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

Pence, I. J.

Pheiffer, T.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Ping, J.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Poizner, H.

P. S. Hammon, S. Makeig, H. Poizner, E. Todorov, and V. R. de Sa, “Predicting reaching targets from human EEG,” IEEE Signal Proc. Mag. 25(1), 69–77 (2008).
[Crossref]

Popp, J.

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

Potthast, S.

O. Heizmann, S. Zidowitz, H. Bourquain, S. Potthast, H. O. Peitgen, D. Oertli, and C. Kettelhack, “Assessment of intraoperative liver deformation during hepatic resection: prospective clinical study,” World J. Surg. 34(8), 1887–1893 (2010).
[Crossref] [PubMed]

Rabah, R.

A. Lorincz, D. Haddad, R. Naik, V. Naik, A. Fung, A. Cao, P. Manda, A. Pandya, G. Auner, R. Rabah, S. E. Langenburg, and M. D. Klein, “Raman spectroscopy for neoplastic tissue differentiation: a pilot study,” J. Pediatr. Surg. 39(6), 953–956 (2004).
[Crossref] [PubMed]

Ramanujam, N.

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

Rao, G. G.

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

Recknagel, P.

C. Krafft, M. A. Diderhoshan, P. Recknagel, M. Miljkovic, M. Bauer, and J. Popp, “Crisp and soft multivariate methods visualize individual cell nuclei in Raman images of liver tissue sections,” Vib. Spectrosc. 55(1), 90–100 (2011).
[Crossref]

Redd, D. C.

C. J. Frank, R. L. McCreery, and D. C. Redd, “Raman spectroscopy of normal and diseased human breast tissues,” Anal. Chem. 67(5), 777–783 (1995).
[Crossref] [PubMed]

C. J. Frank, D. C. Redd, T. S. Gansler, and R. L. McCreery, “Characterization of human breast biopsy specimens with near-IR Raman spectroscopy,” Anal. Chem. 66(3), 319–326 (1994).
[Crossref] [PubMed]

Rehlaender, A.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Rethy, A.

A. Rethy, T. Langø, and R. Mårvik, “Laparoscopic ultrasound for hepatocellular carcinoma and colorectal liver metastasis: an overview,” Surg. Laparosc. Endosc. Percutan. Tech. 23(2), 135–144 (2013).
[Crossref] [PubMed]

Richards-Kortum, R.

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

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]

Riedl, M.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

Rogers, K.

N. Stone, R. Baker, K. Rogers, A. W. Parker, and P. Matousek, “Subsurface probing of calcifications with spatially offset Raman spectroscopy (SORS): future possibilities for the diagnosis of breast cancer,” Analyst (Lond.) 132(9), 899–905 (2007).
[Crossref] [PubMed]

Røsok, B. I.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Rosseland, A. R.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Rucker, D.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Ruwe, M.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Sano, R. S.

M. C. Gaggini, R. S. Navarro, A. R. Stefanini, R. S. Sano, and L. Silveira., “Correlation between METAVIR scores and Raman spectroscopy in liver lesions induced by hepatitis C virus: a preliminary study,” Lasers Med. Sci. 30(4), 1347–1355 (2015).
[Crossref] [PubMed]

Sasic, S.

Schrader, B.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Schrader, W.

S. Keller, B. Schrader, A. Hoffmann, W. Schrader, K. Metz, A. Rehlaender, J. Pahnke, M. Ruwe, and W. Budach, “Application of near-Infrared Fourier-Transform Raman-Spectroscopy in medical-research,” J. Raman Spectrosc. 25(7-8), 663–671 (1994).
[Crossref]

Schulte, R.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

Shen, A. G.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Sherman, M.

J. Bruix, M. Sherman, and American Association for the Study of Liver Diseases, “Management of hepatocellular carcinoma: an update,” Hepatology 53(3), 1020–1022 (2011).
[Crossref] [PubMed]

Short, M.

Silveira, L.

M. C. Gaggini, R. S. Navarro, A. R. Stefanini, R. S. Sano, and L. Silveira., “Correlation between METAVIR scores and Raman spectroscopy in liver lesions induced by hepatitis C virus: a preliminary study,” Lasers Med. Sci. 30(4), 1347–1355 (2015).
[Crossref] [PubMed]

Simpson, A.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Sinha, T. K.

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

So, J. B. Y.

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

Stefanini, A. R.

M. C. Gaggini, R. S. Navarro, A. R. Stefanini, R. S. Sano, and L. Silveira., “Correlation between METAVIR scores and Raman spectroscopy in liver lesions induced by hepatitis C virus: a preliminary study,” Lasers Med. Sci. 30(4), 1347–1355 (2015).
[Crossref] [PubMed]

Stone, N.

N. Stone, R. Baker, K. Rogers, A. W. Parker, and P. Matousek, “Subsurface probing of calcifications with spatially offset Raman spectroscopy (SORS): future possibilities for the diagnosis of breast cancer,” Analyst (Lond.) 132(9), 899–905 (2007).
[Crossref] [PubMed]

Tatsch, E.

B. Schrader, B. Dippel, S. Fendel, S. Keller, T. Lochte, M. Riedl, R. Schulte, and E. Tatsch, “NIR FT Raman spectroscopy - A new tool in medical diagnostics,” J. Mol. Struct. 408, 23–31 (1997).
[Crossref]

Teh, M.

M. S. Bergholt, W. Zheng, L. Kan, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. W. Huang, “On-line image-guided Raman endoscopy for in vivo diagnosis of gastric cancer,” J. Gastroenterol. Hepatol. 26, 192 (2011).

Thomsen, S.

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

Todorov, E.

P. S. Hammon, S. Makeig, H. Poizner, E. Todorov, and V. R. de Sa, “Predicting reaching targets from human EEG,” IEEE Signal Proc. Mag. 25(1), 69–77 (2008).
[Crossref]

Utzinger, U.

A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, A. Malpica, S. Thomsen, U. Utzinger, and R. Richards-Kortum, “Near-infrared Raman spectroscopy for in vitro detection of cervical precancers,” Photochem. Photobiol. 68(1), 123–132 (1998).
[Crossref] [PubMed]

Vargis, E.

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

Villanger, O.

A. M. Kazaryan, I. P. Marangos, B. I. Røsok, A. R. Rosseland, O. Villanger, E. Fosse, O. Mathisen, and B. Edwin, “Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome,” Ann. Surg. 252(6), 1005–1012 (2010).
[Crossref] [PubMed]

Volynskaya, Z.

A. S. Haka, Z. Volynskaya, J. A. Gardecki, J. Nazemi, J. Lyons, D. Hicks, M. Fitzmaurice, R. R. Dasari, J. P. Crowe, and M. S. Feld, “In vivo margin assessment during partial mastectomy breast surgery using raman spectroscopy,” Cancer Res. 66(6), 3317–3322 (2006).
[Crossref] [PubMed]

Wang, H.

N. Huang, M. Short, J. Zhao, H. Wang, H. Lui, M. Korbelik, and H. Zeng, “Full range characterization of the Raman spectra of organs in a murine model,” Opt. Express 19(23), 22892–22909 (2011).
[Crossref] [PubMed]

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Wang, H. Q.

H. Q. Wang, N. Y. Huang, J. H. Zhao, H. Lui, M. Korbelik, and H. S. Zeng, “Depth-resolved in vivo micro-Raman spectroscopy of a murine skin tumor model reveals cancer-specific spectral biomarkers,” J. Raman Spectrosc. 42(2), 160–166 (2011).
[Crossref]

Wang, Y.

R. Manoharan, Y. Wang, and M. S. Feld, “Histochemical analysis of biological tissues using Raman spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 52(2), 215–249 (1996).
[Crossref]

Warmath, J. R.

P. Bao, T. K. Sinha, C. C. Chen, J. R. Warmath, R. L. Galloway, and A. J. Herline, “A prototype ultrasound-guided laparoscopic radiofrequency ablation system,” Surg. Endosc. 21(1), 74–79 (2007).
[Crossref] [PubMed]

Wilson, R. H.

M. D. Keller, E. Vargis, N. de Matos Granja, R. H. Wilson, M. A. Mycek, M. C. Kelley, and A. Mahadevan-Jansen, “Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation,” J. Biomed. Opt. 16(7), 077006 (2011).
[Crossref] [PubMed]

Woeste, E.

E. M. Kanter, E. Vargis, S. Majumder, M. D. Keller, E. Woeste, G. G. Rao, and A. Mahadevan-Jansen, “Application of Raman spectroscopy for cervical dysplasia diagnosis,” J. Biophotonics 2(1-2), 81–90 (2009).
[Crossref] [PubMed]

Wu, Y.

D. Rucker, Y. Wu, L. Clements, J. Ondrake, T. Pheiffer, A. Simpson, W. Jarnagin, and M. Miga, “A mechanics-based non-rigid registration method for liver surgery using sparse intraoperative data,” IEEE Trans. Med. Imaging 33, 147–158 (2013).
[PubMed]

Xie, W.

A. G. Shen, B. J. Zhang, J. Ping, W. Xie, P. Donfack, S. J. Baek, X. D. Zhou, H. Wang, A. Materny, and J. M. Hu, “In vivo study on the protection of indole-3-carbinol (13C) against the mouse acute alcoholic liver injury by micro-Raman spectroscopy,” J. Raman Spectrosc. 40(5), 550–555 (2009).
[Crossref]

Yeoh, K. G.

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Figures (6)

Fig. 1
Fig. 1 Schematic of co-aligned Raman spectroscopic systems. The 785 nm system utilized beam shaping optics to best match the excitation parameters of the 1064 nm system.
Fig. 2
Fig. 2 Raman spectra (mean +/− standard deviation) of adenocarcinoma samples for both 785 nm and 1064 nm excitation systems. The strong and variable autofluorescent background present at 785 nm excitation overwhelms modest Raman signal from each spectrum. Spectral trends are representative of all classes measured.
Fig. 3
Fig. 3 Mean +/− standard deviation Raman spectra collected with 1064 nm dispersive system for healthy liver, secondary colorectal metastatic adenocarcinoma, and primary hepatocellular carcinoma samples. All spectra are corrected for wavelength-dependent spectral response and background subtracted using a modified polynomial fitting algorithm previously described. Spectral features utilized during SMLR classification are encoded with graded bands indicating the importance greater than the 0.25 threshold value.
Fig. 4
Fig. 4 The magnitude of SMLR feature weights and corresponding cross-validation frequencies for tumor samples from binary classifier. The non-linear association between these metrics holds for all tissue classes for both binary and three class discrimination tests. Frequently chosen features have a large range of weights suggesting a combination of these values will emphasize informative features with a higher feature importance value.
Fig. 5
Fig. 5 Binary posterior probability of class membership as predicted by SMLR algorithm. Resulting classification yields 90.3% classification accuracy (104/108 spectra), with 100% sensitivity and 89.2% specificity for discriminating healthy (circles) and tumor samples (squares). Thresholds for >50% (dashed) and >80% (dotted) probability for class membership yield identical results.
Fig. 6
Fig. 6 Three class prediction of posterior probability of class membership from SMLR algorithm. Resulting classification yields 78.3% classification accuracy with healthy control (circles, 33/37 spectra), adenocarcinoma (squares, 26/35 spectra), and hepatocellular carcinoma (triangles, 23/36 spectra) samples correctly distinguished. Again, thresholds are indicated for >50% (dashed) and >80% (dotted) probability for class membership and demonstrate spectral heterogeneity manifested in the falloff in classification accuracy.

Tables (1)

Tables Icon

Table 1 Key SMLR classifier spectral bands, feature importance, and assignments.

Metrics