Abstract

Raman spectroscopy (RS) has shown great potential in noninvasive cancer screening. Statistically based algorithms, such as principal component analysis, are commonly employed to provide tissue classification; however, they are difficult to relate to the chemical and morphological basis of the spectroscopic features and underlying disease. As a result, we propose the first Raman biophysical model applied to in vivo skin cancer screening data. We expand upon previous models by utilizing in situ skin constituents as the building blocks, and validate the model using previous clinical screening data collected from a Raman optical fiber probe. We built an 830nm confocal Raman microscope integrated with a confocal laser-scanning microscope. Raman imaging was performed on skin sections spanning various disease states, and multivariate curve resolution (MCR) analysis was used to resolve the Raman spectra of individual in situ skin constituents. The basis spectra of the most relevant skin constituents were combined linearly to fit in vivo human skin spectra. Our results suggest collagen, elastin, keratin, cell nucleus, triolein, ceramide, melanin and water are the most important model components. We make available for download (see supplemental information) a database of Raman spectra for these eight components for others to use as a reference. Our model reveals the biochemical and structural makeup of normal, nonmelanoma and melanoma skin cancers, and precancers and paves the way for future development of this approach to noninvasive skin cancer diagnosis.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  44. W.-C. Shih, K. L. Bechtel, and M. S. Feld, “Intrinsic Raman spectroscopy for quantitative biological spectroscopy part I: theory and simulations,” Opt. Express 16(17), 12726–12736 (2008).
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2016 (1)

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” Cancer J. Clin. 66(1), 7–30 (2016).
[Crossref] [PubMed]

2015 (2)

R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
[Crossref] [PubMed]

J. Jaumot, A. de Juan, and R. Tauler, “MCR-ALS GUI 2.0: new features and applications,” Chemom. Intell. Lab. Syst. 140, 1–12 (2015).
[Crossref]

2014 (3)

M. Sharma, E. Marple, J. Reichenberg, and J. W. Tunnell, “Design and characterization of a novel multimodal fiber-optic probe and spectroscopy system for skin cancer applications,” Rev. Sci. Instrum. 85(8), 083101 (2014).
[Crossref] [PubMed]

P. Olczyk, Ł. Mencner, and K. Komosinska-Vassev, “The role of the extracellular matrix components in cutaneous wound healing,” BioMed Res. Int. 2014, 747584 (2014).
[Crossref] [PubMed]

L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
[Crossref] [PubMed]

2013 (3)

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
[Crossref] [PubMed]

N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
[Crossref] [PubMed]

D. Zhang, P. Wang, M. N. Slipchenko, D. Ben-Amotz, A. M. Weiner, and J.-X. Cheng, “Quantitative vibrational imaging by hyperspectral stimulated Raman scattering microscopy and multivariate curve resolution analysis,” Anal. Chem. 85(1), 98–106 (2013).
[Crossref] [PubMed]

2012 (3)

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]

B. Bodanese, F. L. Silveira, R. A. Zângaro, M. T. T. Pacheco, C. A. Pasqualucci, and L. Silveira., “Discrimination of basal cell carcinoma and melanoma from normal skin biopsies in vitro through Raman spectroscopy and principal component analysis,” Photomed. Laser Surg. 30(7), 381–387 (2012).
[Crossref] [PubMed]

L. Silveira, F. L. Silveira, B. Bodanese, R. A. Zângaro, and M. T. T. Pacheco, “Discriminating model for diagnosis of basal cell carcinoma and melanoma in vitro based on the Raman spectra of selected biochemicals,” J. Biomed. Opt. 17(7), 077003 (2012).
[Crossref] [PubMed]

2009 (3)

N. D. Magee, J. S. Villaumie, E. T. Marple, M. Ennis, J. S. Elborn, and J. J. McGarvey, “Ex vivo diagnosis of lung cancer using a Raman miniprobe,” J. Phys. Chem. B 113(23), 8137–8141 (2009).
[Crossref] [PubMed]

A. Pappas, “Epidermal surface lipids,” Dermatoendocrinol 1(2), 72–76 (2009).
[Crossref] [PubMed]

P. Vítek, K. Osterrothová, and J. Jehlička, “Beta-carotene—a possible biomarker in the Martian evaporitic environment: Raman micro-spectroscopic study,” Planet. Space Sci. 57(4), 454–459 (2009).
[Crossref]

2008 (3)

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]

W.-C. Shih, K. L. Bechtel, and M. S. Feld, “Intrinsic Raman spectroscopy for quantitative biological spectroscopy part I: theory and simulations,” Opt. Express 16(17), 12726–12736 (2008).
[Crossref] [PubMed]

J. Zhao, H. Lui, D. I. McLean, and H. Zeng, “Integrated real-time Raman system for clinical in vivo skin analysis,” Skin Res. Technol. 14(4), 484–492 (2008).
[Crossref] [PubMed]

2007 (2)

N. Stone, M. C. Hart Prieto, P. Crow, J. Uff, and A. W. Ritchie, “The use of Raman spectroscopy to provide an estimation of the gross biochemistry associated with urological pathologies,” Anal. Bioanal. Chem. 387(5), 1657–1668 (2007).
[Crossref] [PubMed]

Z. Movasaghi, S. Rehman, and I. U. Rehman, “Raman spectroscopy of biological tissues,” Appl. Spectrosc. Rev. 42(5), 493–541 (2007).
[Crossref]

2006 (2)

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]

P. R. T. Jess, V. Garcés-Chávez, D. Smith, M. Mazilu, L. Paterson, A. Riches, C. S. Herrington, W. Sibbett, and K. Dholakia, “Dual beam fibre trap for Raman micro-spectroscopy of single cells,” Opt. Express 14(12), 5779–5791 (2006).
[Crossref] [PubMed]

2005 (2)

P. Crow, A. Molckovsky, N. Stone, J. Uff, B. Wilson, and L.-M. WongKeeSong, “Assessment of fiberoptic near-infrared raman spectroscopy for diagnosis of bladder and prostate cancer,” Urology 65(6), 1126–1130 (2005).
[Crossref] [PubMed]

A. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
[Crossref] [PubMed]

2004 (3)

Z. Huang, H. Lui, X. K. Chen, A. Alajlan, D. I. McLean, and H. Zeng, “Raman spectroscopy of in vivo cutaneous melanin,” J. Biomed. Opt. 9(6), 1198–1205 (2004).
[Crossref] [PubMed]

D. R. English, C. Del Mar, and R. C. Burton, “Factors influencing the number needed to excise: excision rates of pigmented lesions by general practitioners,” Med. J. Aust. 180(1), 16–19 (2004).
[PubMed]

J. T. Motz, M. Hunter, L. H. Galindo, J. A. Gardecki, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Optical fiber probe for biomedical Raman spectroscopy,” Appl. Opt. 43(3), 542–554 (2004).
[Crossref] [PubMed]

2003 (2)

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]

P. J. Caspers, G. W. Lucassen, and G. J. Puppels, “Combined in vivo confocal Raman spectroscopy and confocal microscopy of human skin,” Biophys. J. 85(1), 572–580 (2003).
[Crossref] [PubMed]

2002 (2)

K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
[Crossref]

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
[Crossref] [PubMed]

2001 (3)

J. Chen and X. Z. Wang, “A new approach to near-infrared spectral data analysis using independent component analysis,” J. Chem. Inf. Comput. Sci. 41(4), 992–1001 (2001).
[Crossref] [PubMed]

H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
[Crossref] [PubMed]

P. J. Caspers, G. W. Lucassen, E. A. Carter, H. A. Bruining, and G. J. Puppels, “In vivo confocal Raman microspectroscopy of the skin: noninvasive determination of molecular concentration profiles,” J. Invest. Dermatol. 116(3), 434–442 (2001).
[Crossref] [PubMed]

1998 (2)

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, M. F. Mitchell, N. Ramanujam, U. Utzinger, and R. Richards-Kortum, “Development of a fiber optic probe to measure NIR Raman spectra of cervical tissue in vivo,” Photochem. Photobiol. 68(3), 427–431 (1998).
[Crossref] [PubMed]

1995 (1)

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104(6), 946–952 (1995).
[Crossref] [PubMed]

1992 (3)

D. T. Downing, “Lipid and protein structures in the permeability barrier of mammalian epidermis,” J. Lipid Res. 33(3), 301–313 (1992).
[PubMed]

R. Manoharan, J. J. Baraga, M. S. Feld, and R. P. Rava, “Quantitative Histochemical Analysis of Human Artery Using Raman Spectroscopy,” J. Photochem. Photobiol. B 16(2), 211–233 (1992).
[Crossref] [PubMed]

W. Windig and D. Stephenson, “Self-modeling mixture analysis of second-derivative near-infrared spectral data using the SIMPLISMA approach,” Anal. Chem. 64(22), 2735–2742 (1992).
[Crossref]

1984 (1)

S. Wold, A. Ruhe, H. Wold, and I. Dunn, WJ, “The collinearity problem in linear regression. The partial least squares (PLS) approach to generalized inverses,” SIAM J. Sci. Statist. Comput. 5(3), 735–743 (1984).
[Crossref]

Alajlan, A.

Z. Huang, H. Lui, X. K. Chen, A. Alajlan, D. I. McLean, and H. Zeng, “Raman spectroscopy of in vivo cutaneous melanin,” J. Biomed. Opt. 9(6), 1198–1205 (2004).
[Crossref] [PubMed]

Anderson, R. R.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104(6), 946–952 (1995).
[Crossref] [PubMed]

Baraga, J. J.

R. Manoharan, J. J. Baraga, M. S. Feld, and R. P. Rava, “Quantitative Histochemical Analysis of Human Artery Using Raman Spectroscopy,” J. Photochem. Photobiol. B 16(2), 211–233 (1992).
[Crossref] [PubMed]

Barman, I.

R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
[Crossref] [PubMed]

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
[Crossref] [PubMed]

Bechtel, K. L.

Ben-Amotz, D.

D. Zhang, P. Wang, M. N. Slipchenko, D. Ben-Amotz, A. M. Weiner, and J.-X. Cheng, “Quantitative vibrational imaging by hyperspectral stimulated Raman scattering microscopy and multivariate curve resolution analysis,” Anal. Chem. 85(1), 98–106 (2013).
[Crossref] [PubMed]

Bergner, N.

N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
[Crossref] [PubMed]

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).
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Bodanese, B.

B. Bodanese, F. L. Silveira, R. A. Zângaro, M. T. T. Pacheco, C. A. Pasqualucci, and L. Silveira., “Discrimination of basal cell carcinoma and melanoma from normal skin biopsies in vitro through Raman spectroscopy and principal component analysis,” Photomed. Laser Surg. 30(7), 381–387 (2012).
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L. Silveira, F. L. Silveira, B. Bodanese, R. A. Zângaro, and M. T. T. Pacheco, “Discriminating model for diagnosis of basal cell carcinoma and melanoma in vitro based on the Raman spectra of selected biochemicals,” J. Biomed. Opt. 17(7), 077003 (2012).
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Bruining, H. A.

P. J. Caspers, G. W. Lucassen, E. A. Carter, H. A. Bruining, and G. J. Puppels, “In vivo confocal Raman microspectroscopy of the skin: noninvasive determination of molecular concentration profiles,” J. Invest. Dermatol. 116(3), 434–442 (2001).
[Crossref] [PubMed]

Bruschke, A. V.

H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
[Crossref] [PubMed]

Burton, R. C.

D. R. English, C. Del Mar, and R. C. Burton, “Factors influencing the number needed to excise: excision rates of pigmented lesions by general practitioners,” Med. J. Aust. 180(1), 16–19 (2004).
[PubMed]

Buschman, H. P.

H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
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Carter, E. A.

P. J. Caspers, G. W. Lucassen, E. A. Carter, H. A. Bruining, and G. J. Puppels, “In vivo confocal Raman microspectroscopy of the skin: noninvasive determination of molecular concentration profiles,” J. Invest. Dermatol. 116(3), 434–442 (2001).
[Crossref] [PubMed]

Caspers, P. J.

P. J. Caspers, G. W. Lucassen, and G. J. Puppels, “Combined in vivo confocal Raman spectroscopy and confocal microscopy of human skin,” Biophys. J. 85(1), 572–580 (2003).
[Crossref] [PubMed]

P. J. Caspers, G. W. Lucassen, E. A. Carter, H. A. Bruining, and G. J. Puppels, “In vivo confocal Raman microspectroscopy of the skin: noninvasive determination of molecular concentration profiles,” J. Invest. Dermatol. 116(3), 434–442 (2001).
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J. Chen and X. Z. Wang, “A new approach to near-infrared spectral data analysis using independent component analysis,” J. Chem. Inf. Comput. Sci. 41(4), 992–1001 (2001).
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Chen, X. K.

Z. Huang, H. Lui, X. K. Chen, A. Alajlan, D. I. McLean, and H. Zeng, “Raman spectroscopy of in vivo cutaneous melanin,” J. Biomed. Opt. 9(6), 1198–1205 (2004).
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Cheng, J.-X.

D. Zhang, P. Wang, M. N. Slipchenko, D. Ben-Amotz, A. M. Weiner, and J.-X. Cheng, “Quantitative vibrational imaging by hyperspectral stimulated Raman scattering microscopy and multivariate curve resolution analysis,” Anal. Chem. 85(1), 98–106 (2013).
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Crow, P.

N. Stone, M. C. Hart Prieto, P. Crow, J. Uff, and A. W. Ritchie, “The use of Raman spectroscopy to provide an estimation of the gross biochemistry associated with urological pathologies,” Anal. Bioanal. Chem. 387(5), 1657–1668 (2007).
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P. Crow, A. Molckovsky, N. Stone, J. Uff, B. Wilson, and L.-M. WongKeeSong, “Assessment of fiberoptic near-infrared raman spectroscopy for diagnosis of bladder and prostate cancer,” Urology 65(6), 1126–1130 (2005).
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Crowe, J.

A. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
[Crossref] [PubMed]

K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
[Crossref]

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.

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
[Crossref] [PubMed]

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. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
[Crossref] [PubMed]

J. T. Motz, M. Hunter, L. H. Galindo, J. A. Gardecki, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Optical fiber probe for biomedical Raman spectroscopy,” Appl. Opt. 43(3), 542–554 (2004).
[Crossref] [PubMed]

K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
[Crossref]

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
[Crossref] [PubMed]

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J. Jaumot, A. de Juan, and R. Tauler, “MCR-ALS GUI 2.0: new features and applications,” Chemom. Intell. Lab. Syst. 140, 1–12 (2015).
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H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
[Crossref] [PubMed]

Del Mar, C.

D. R. English, C. Del Mar, and R. C. Burton, “Factors influencing the number needed to excise: excision rates of pigmented lesions by general practitioners,” Med. J. Aust. 180(1), 16–19 (2004).
[PubMed]

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Dingari, N. C.

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
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N. D. Magee, J. S. Villaumie, E. T. Marple, M. Ennis, J. S. Elborn, and J. J. McGarvey, “Ex vivo diagnosis of lung cancer using a Raman miniprobe,” J. Phys. Chem. B 113(23), 8137–8141 (2009).
[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]

English, D. R.

D. R. English, C. Del Mar, and R. C. Burton, “Factors influencing the number needed to excise: excision rates of pigmented lesions by general practitioners,” Med. J. Aust. 180(1), 16–19 (2004).
[PubMed]

Ennis, M.

N. D. Magee, J. S. Villaumie, E. T. Marple, M. Ennis, J. S. Elborn, and J. J. McGarvey, “Ex vivo diagnosis of lung cancer using a Raman miniprobe,” J. Phys. Chem. B 113(23), 8137–8141 (2009).
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Esterowitz, D.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104(6), 946–952 (1995).
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Feld, M. S.

W.-C. Shih, K. L. Bechtel, and M. S. Feld, “Intrinsic Raman spectroscopy for quantitative biological spectroscopy part I: theory and simulations,” Opt. Express 16(17), 12726–12736 (2008).
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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. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
[Crossref] [PubMed]

J. T. Motz, M. Hunter, L. H. Galindo, J. A. Gardecki, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Optical fiber probe for biomedical Raman spectroscopy,” Appl. Opt. 43(3), 542–554 (2004).
[Crossref] [PubMed]

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
[Crossref] [PubMed]

K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
[Crossref]

H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
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R. Manoharan, J. J. Baraga, M. S. Feld, and R. P. Rava, “Quantitative Histochemical Analysis of Human Artery Using Raman Spectroscopy,” J. Photochem. Photobiol. B 16(2), 211–233 (1992).
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Fitzmaurice, M.

R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
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I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
[Crossref] [PubMed]

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. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
[Crossref] [PubMed]

K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
[Crossref]

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
[Crossref] [PubMed]

H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
[Crossref] [PubMed]

Galindo, L. H.

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
[Crossref] [PubMed]

J. T. Motz, M. Hunter, L. H. Galindo, J. A. Gardecki, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Optical fiber probe for biomedical Raman spectroscopy,” Appl. Opt. 43(3), 542–554 (2004).
[Crossref] [PubMed]

Garcés-Chávez, V.

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]

J. T. Motz, M. Hunter, L. H. Galindo, J. A. Gardecki, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Optical fiber probe for biomedical Raman spectroscopy,” Appl. Opt. 43(3), 542–554 (2004).
[Crossref] [PubMed]

Geiger, K. D.

N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
[Crossref] [PubMed]

Grossman, M.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104(6), 946–952 (1995).
[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]

A. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
[Crossref] [PubMed]

K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
[Crossref]

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
[Crossref] [PubMed]

Hart Prieto, M. C.

N. Stone, M. C. Hart Prieto, P. Crow, J. Uff, and A. W. Ritchie, “The use of Raman spectroscopy to provide an estimation of the gross biochemistry associated with urological pathologies,” Anal. Bioanal. Chem. 387(5), 1657–1668 (2007).
[Crossref] [PubMed]

Herrington, C. S.

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]

Huang, Z.

Z. Huang, H. Lui, X. K. Chen, A. Alajlan, D. I. McLean, and H. Zeng, “Raman spectroscopy of in vivo cutaneous melanin,” J. Biomed. Opt. 9(6), 1198–1205 (2004).
[Crossref] [PubMed]

Hunter, M.

Jaumot, J.

J. Jaumot, A. de Juan, and R. Tauler, “MCR-ALS GUI 2.0: new features and applications,” Chemom. Intell. Lab. Syst. 140, 1–12 (2015).
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Jehlicka, J.

P. Vítek, K. Osterrothová, and J. Jehlička, “Beta-carotene—a possible biomarker in the Martian evaporitic environment: Raman micro-spectroscopic study,” Planet. Space Sci. 57(4), 454–459 (2009).
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R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” Cancer J. Clin. 66(1), 7–30 (2016).
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Jess, P. R. T.

Kirsch, M.

N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
[Crossref] [PubMed]

Klein, N.

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
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P. Olczyk, Ł. Mencner, and K. Komosinska-Vassev, “The role of the extracellular matrix components in cutaneous wound healing,” BioMed Res. Int. 2014, 747584 (2014).
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Krafft, C.

N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
[Crossref] [PubMed]

Kramer, J. R.

J. T. Motz, M. Hunter, L. H. Galindo, J. A. Gardecki, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Optical fiber probe for biomedical Raman spectroscopy,” Appl. Opt. 43(3), 542–554 (2004).
[Crossref] [PubMed]

H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
[Crossref] [PubMed]

Lieber, C. A.

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).
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L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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Liu, W.

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
[Crossref] [PubMed]

Lucassen, G. W.

P. J. Caspers, G. W. Lucassen, and G. J. Puppels, “Combined in vivo confocal Raman spectroscopy and confocal microscopy of human skin,” Biophys. J. 85(1), 572–580 (2003).
[Crossref] [PubMed]

P. J. Caspers, G. W. Lucassen, E. A. Carter, H. A. Bruining, and G. J. Puppels, “In vivo confocal Raman microspectroscopy of the skin: noninvasive determination of molecular concentration profiles,” J. Invest. Dermatol. 116(3), 434–442 (2001).
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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).
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J. Zhao, H. Lui, D. I. McLean, and H. Zeng, “Integrated real-time Raman system for clinical in vivo skin analysis,” Skin Res. Technol. 14(4), 484–492 (2008).
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Z. Huang, H. Lui, X. K. Chen, A. Alajlan, D. I. McLean, and H. Zeng, “Raman spectroscopy of in vivo cutaneous melanin,” J. Biomed. Opt. 9(6), 1198–1205 (2004).
[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]

Magee, N. D.

N. D. Magee, J. S. Villaumie, E. T. Marple, M. Ennis, J. S. Elborn, and J. J. McGarvey, “Ex vivo diagnosis of lung cancer using a Raman miniprobe,” J. Phys. Chem. B 113(23), 8137–8141 (2009).
[Crossref] [PubMed]

Mahadevan-Jansen, A.

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).
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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).
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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).
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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).
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R. Manoharan, J. J. Baraga, M. S. Feld, and R. P. Rava, “Quantitative Histochemical Analysis of Human Artery Using Raman Spectroscopy,” J. Photochem. Photobiol. B 16(2), 211–233 (1992).
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L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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M. Sharma, E. Marple, J. Reichenberg, and J. W. Tunnell, “Design and characterization of a novel multimodal fiber-optic probe and spectroscopy system for skin cancer applications,” Rev. Sci. Instrum. 85(8), 083101 (2014).
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N. D. Magee, J. S. Villaumie, E. T. Marple, M. Ennis, J. S. Elborn, and J. J. McGarvey, “Ex vivo diagnosis of lung cancer using a Raman miniprobe,” J. Phys. Chem. B 113(23), 8137–8141 (2009).
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Mazilu, M.

McGarvey, J. J.

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R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
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N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
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P. Olczyk, Ł. Mencner, and K. Komosinska-Vassev, “The role of the extracellular matrix components in cutaneous wound healing,” BioMed Res. Int. 2014, 747584 (2014).
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L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” Cancer J. Clin. 66(1), 7–30 (2016).
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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).
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A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, U. Utzinger, and R. Richards-Kortum, “Development of a fiber optic probe to measure NIR Raman spectra of cervical tissue in vivo,” Photochem. Photobiol. 68(3), 427–431 (1998).
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P. Crow, A. Molckovsky, N. Stone, J. Uff, B. Wilson, and L.-M. WongKeeSong, “Assessment of fiberoptic near-infrared raman spectroscopy for diagnosis of bladder and prostate cancer,” Urology 65(6), 1126–1130 (2005).
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H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
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K. E. Shafer-Peltier, A. S. Haka, M. Fitzmaurice, J. Crowe, J. Myles, R. R. Dasari, and M. S. Feld, “Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo,” J. Raman Spectrosc. 33(7), 552–563 (2002).
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L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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P. Vítek, K. Osterrothová, and J. Jehlička, “Beta-carotene—a possible biomarker in the Martian evaporitic environment: Raman micro-spectroscopic study,” Planet. Space Sci. 57(4), 454–459 (2009).
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B. Bodanese, F. L. Silveira, R. A. Zângaro, M. T. T. Pacheco, C. A. Pasqualucci, and L. Silveira., “Discrimination of basal cell carcinoma and melanoma from normal skin biopsies in vitro through Raman spectroscopy and principal component analysis,” Photomed. Laser Surg. 30(7), 381–387 (2012).
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Plecha, D.

I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
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Popp, J.

N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
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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).
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R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
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Rava, R. P.

R. Manoharan, J. J. Baraga, M. S. Feld, and R. P. Rava, “Quantitative Histochemical Analysis of Human Artery Using Raman Spectroscopy,” J. Photochem. Photobiol. B 16(2), 211–233 (1992).
[Crossref] [PubMed]

Rehman, I. U.

Z. Movasaghi, S. Rehman, and I. U. Rehman, “Raman spectroscopy of biological tissues,” Appl. Spectrosc. Rev. 42(5), 493–541 (2007).
[Crossref]

Rehman, S.

Z. Movasaghi, S. Rehman, and I. U. Rehman, “Raman spectroscopy of biological tissues,” Appl. Spectrosc. Rev. 42(5), 493–541 (2007).
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M. Sharma, E. Marple, J. Reichenberg, and J. W. Tunnell, “Design and characterization of a novel multimodal fiber-optic probe and spectroscopy system for skin cancer applications,” Rev. Sci. Instrum. 85(8), 083101 (2014).
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L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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A. Mahadevan-Jansen, M. F. Mitchell, N. Ramanujam, U. Utzinger, and R. Richards-Kortum, “Development of a fiber optic probe to measure NIR Raman spectra of cervical tissue in vivo,” Photochem. Photobiol. 68(3), 427–431 (1998).
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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).
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Ritchie, A. W.

N. Stone, M. C. Hart Prieto, P. Crow, J. Uff, and A. W. Ritchie, “The use of Raman spectroscopy to provide an estimation of the gross biochemistry associated with urological pathologies,” Anal. Bioanal. Chem. 387(5), 1657–1668 (2007).
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L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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[Crossref] [PubMed]

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R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
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N. Bergner, A. Medyukhina, K. D. Geiger, M. Kirsch, G. Schackert, C. Krafft, and J. Popp, “Hyperspectral unmixing of Raman micro-images for assessment of morphological and chemical parameters in non-dried brain tumor specimens,” Anal. Bioanal. Chem. 405(27), 8719–8728 (2013).
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A. S. Haka, K. E. Shafer-Peltier, M. Fitzmaurice, J. Crowe, R. R. Dasari, and M. S. Feld, “Diagnosing breast cancer by using Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(35), 12371–12376 (2005).
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[Crossref]

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
[Crossref] [PubMed]

Sharma, M.

M. Sharma, E. Marple, J. Reichenberg, and J. W. Tunnell, “Design and characterization of a novel multimodal fiber-optic probe and spectroscopy system for skin cancer applications,” Rev. Sci. Instrum. 85(8), 083101 (2014).
[Crossref] [PubMed]

Shih, W.-C.

Sibbett, W.

Siegel, R. L.

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” Cancer J. Clin. 66(1), 7–30 (2016).
[Crossref] [PubMed]

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B. Bodanese, F. L. Silveira, R. A. Zângaro, M. T. T. Pacheco, C. A. Pasqualucci, and L. Silveira., “Discrimination of basal cell carcinoma and melanoma from normal skin biopsies in vitro through Raman spectroscopy and principal component analysis,” Photomed. Laser Surg. 30(7), 381–387 (2012).
[Crossref] [PubMed]

L. Silveira, F. L. Silveira, B. Bodanese, R. A. Zângaro, and M. T. T. Pacheco, “Discriminating model for diagnosis of basal cell carcinoma and melanoma in vitro based on the Raman spectra of selected biochemicals,” J. Biomed. Opt. 17(7), 077003 (2012).
[Crossref] [PubMed]

Silveira, L.

B. Bodanese, F. L. Silveira, R. A. Zângaro, M. T. T. Pacheco, C. A. Pasqualucci, and L. Silveira., “Discrimination of basal cell carcinoma and melanoma from normal skin biopsies in vitro through Raman spectroscopy and principal component analysis,” Photomed. Laser Surg. 30(7), 381–387 (2012).
[Crossref] [PubMed]

L. Silveira, F. L. Silveira, B. Bodanese, R. A. Zângaro, and M. T. T. Pacheco, “Discriminating model for diagnosis of basal cell carcinoma and melanoma in vitro based on the Raman spectra of selected biochemicals,” J. Biomed. Opt. 17(7), 077003 (2012).
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D. Zhang, P. Wang, M. N. Slipchenko, D. Ben-Amotz, A. M. Weiner, and J.-X. Cheng, “Quantitative vibrational imaging by hyperspectral stimulated Raman scattering microscopy and multivariate curve resolution analysis,” Anal. Chem. 85(1), 98–106 (2013).
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Soares, J. S.

R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
[Crossref] [PubMed]

Spegazzini, N.

R. Sathyavathi, A. Saha, J. S. Soares, N. Spegazzini, S. McGee, R. Rao Dasari, M. Fitzmaurice, and I. Barman, “Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy,” Sci. Rep. 5(1), 9907 (2015).
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N. Stone, M. C. Hart Prieto, P. Crow, J. Uff, and A. W. Ritchie, “The use of Raman spectroscopy to provide an estimation of the gross biochemistry associated with urological pathologies,” Anal. Bioanal. Chem. 387(5), 1657–1668 (2007).
[Crossref] [PubMed]

P. Crow, A. Molckovsky, N. Stone, J. Uff, B. Wilson, and L.-M. WongKeeSong, “Assessment of fiberoptic near-infrared raman spectroscopy for diagnosis of bladder and prostate cancer,” Urology 65(6), 1126–1130 (2005).
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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).
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Tunnell, J. W.

L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
[Crossref] [PubMed]

M. Sharma, E. Marple, J. Reichenberg, and J. W. Tunnell, “Design and characterization of a novel multimodal fiber-optic probe and spectroscopy system for skin cancer applications,” Rev. Sci. Instrum. 85(8), 083101 (2014).
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N. Stone, M. C. Hart Prieto, P. Crow, J. Uff, and A. W. Ritchie, “The use of Raman spectroscopy to provide an estimation of the gross biochemistry associated with urological pathologies,” Anal. Bioanal. Chem. 387(5), 1657–1668 (2007).
[Crossref] [PubMed]

P. Crow, A. Molckovsky, N. Stone, J. Uff, B. Wilson, and L.-M. WongKeeSong, “Assessment of fiberoptic near-infrared raman spectroscopy for diagnosis of bladder and prostate cancer,” Urology 65(6), 1126–1130 (2005).
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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).
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H. P. Buschman, G. Deinum, J. T. Motz, M. Fitzmaurice, J. R. Kramer, A. van der Laarse, A. V. Bruschke, and M. S. Feld, “Raman microspectroscopy of human coronary atherosclerosis: biochemical assessment of cellular and extracellular morphologic structures in situ,” Cardiovasc. Pathol. 10(2), 69–82 (2001).
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N. D. Magee, J. S. Villaumie, E. T. Marple, M. Ennis, J. S. Elborn, and J. J. McGarvey, “Ex vivo diagnosis of lung cancer using a Raman miniprobe,” J. Phys. Chem. B 113(23), 8137–8141 (2009).
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P. Vítek, K. Osterrothová, and J. Jehlička, “Beta-carotene—a possible biomarker in the Martian evaporitic environment: Raman micro-spectroscopic study,” Planet. Space Sci. 57(4), 454–459 (2009).
[Crossref]

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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, P.

D. Zhang, P. Wang, M. N. Slipchenko, D. Ben-Amotz, A. M. Weiner, and J.-X. Cheng, “Quantitative vibrational imaging by hyperspectral stimulated Raman scattering microscopy and multivariate curve resolution analysis,” Anal. Chem. 85(1), 98–106 (2013).
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W. Windig and D. Stephenson, “Self-modeling mixture analysis of second-derivative near-infrared spectral data using the SIMPLISMA approach,” Anal. Chem. 64(22), 2735–2742 (1992).
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P. Olczyk, Ł. Mencner, and K. Komosinska-Vassev, “The role of the extracellular matrix components in cutaneous wound healing,” BioMed Res. Int. 2014, 747584 (2014).
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I. Barman, N. C. Dingari, A. Saha, S. McGee, L. H. Galindo, W. Liu, D. Plecha, N. Klein, R. R. Dasari, and M. Fitzmaurice, “Application of Raman spectroscopy to identify microcalcifications and underlying breast lesions at stereotactic core needle biopsy,” Cancer Res. 73(11), 3206–3215 (2013).
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J. Biomed. Opt. (3)

L. Lim, B. Nichols, M. R. Migden, N. Rajaram, J. S. Reichenberg, M. K. Markey, M. I. Ross, and J. W. Tunnell, “Clinical study of noninvasive in vivo melanoma and nonmelanoma skin cancers using multimodal spectral diagnosis,” J. Biomed. Opt. 19(11), 117003 (2014).
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L. Silveira, F. L. Silveira, B. Bodanese, R. A. Zângaro, and M. T. T. Pacheco, “Discriminating model for diagnosis of basal cell carcinoma and melanoma in vitro based on the Raman spectra of selected biochemicals,” J. Biomed. Opt. 17(7), 077003 (2012).
[Crossref] [PubMed]

Z. Huang, H. Lui, X. K. Chen, A. Alajlan, D. I. McLean, and H. Zeng, “Raman spectroscopy of in vivo cutaneous melanin,” J. Biomed. Opt. 9(6), 1198–1205 (2004).
[Crossref] [PubMed]

J. Cell. Biochem. Suppl. (1)

K. E. Shafer-Peltier, A. S. Haka, J. T. Motz, M. Fitzmaurice, R. R. Dasari, and M. S. Feld, “Model-based biological Raman spectral imaging,” J. Cell. Biochem. Suppl. 87(S39), 125–137 (2002).
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M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104(6), 946–952 (1995).
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Supplementary Material (1)

NameDescription
» Data File 1: CSV (107 KB)      Basis spectra of eight Raman active components

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Figures (9)

Fig. 1
Fig. 1 Schematic of confocal Raman and confocal laser-scanning microscope used for skin measurements. The flip mirror and CMOS camera were used for bright-field imaging. ISO, isolator; D1, D2: dichroic mirror; P1 – P3: pinhole; L1 – L6, lens; GM, galvanometer mirror; FM, flip mirror.
Fig. 2
Fig. 2 Extracting cellular components from a BCC lesion. Raman images of nucleus (a) and cytoplasm (b) and Raman substrate (c) are compared with bright-field image (d), CLSM image (e) and histopathology image (f). The boxes on (e) and (f) mark the location of Raman imaging. The contrast of the CLSM image was provided by the relative difference in refractive index of cells and the surrounding stroma. Plots on the right show Raman spectra of in situ nucleus, synthetic DNA and their difference spectrum. Also in situ cytoplasm, synthetic actin and their difference spectrum. Scale bar: 10 μm.
Fig. 3
Fig. 3 Extracting the epidermal component from a normal skin section. Raman images of in situ keratin (a) and Raman substrate (b) are compared with bright-field image (c) and histopathology image (d). Plots on the right show Raman spectra of in situ, synthetic keratin and their difference spectrum. Scale bar:10 μm.
Fig. 4
Fig. 4 Extracting dermal components from a BCC skin section. In situ collagen (a) and elastin (b) are resolved from the image. The dye used by the dermatologist to mark the orientation of the tissue was also detected (c). Raman images are compared with the bright-field image (d), CLSM image (e) and histopathology image (f). The box on (e) marks the location of Raman imaging. The arrow in (f) points to a thin blue-gray elastic fiber. Plots on the right displays Raman spectrum of in situ collagen, synthetic collagen and the difference spectrum. Also Raman spectrum of in situ elastin, synthetic elastin, and their difference spectrum. Scale bar: 10 μm.
Fig. 5
Fig. 5 Extracting lipids within a hair follicle from a SCC skin section. In situ ceramide (a), triolein (b) and Raman substrate (c) are resolved from the image. Raman images are compared with the bright-field image (d), CLSM image (e) and histopathology image (f). Some lipids in (f) were lost during the staining processing. The box on (e) and (f) marks the location of Raman imaging. Difference spectrum between in situ ceramide and palmitic acid and difference spectrum between in situ ceramide and triolein are also shown. Scale bar: 10 μm.
Fig. 6
Fig. 6 Extracting melanin from a MM skin section. Raman image of melanin (d) are compared with bright field image (a) CLSM image (b) and histopathology image (c). Basis spectra of melanin and beta carotene are shown on the right. Scale bar: 50 μm.
Fig. 7
Fig. 7 Basis Raman spectra of water, calcium hydroxyapatite (CaH), hemoglobin (Hb), hair follicle (HF) and keratin pearl (KP) collected in situ are displayed. The difference spectrum between HF and KP is also shown.
Fig. 8
Fig. 8 Basis spectra used in the biophysical model of skin. Model components include collagen (a), elastin (b), triolein (c), nucleus (d), keratin (e), ceramide (f), melanin (g), water (h). See Data File 1 for underlying values.
Fig. 9
Fig. 9 Model fitting results for in vivo human skin spectra categorized as Normal, BCC, SCC, AK, PL and MM. Mean Raman tissue spectra (solid lines), model fits (dotted lines), residuals are plotted on the same scale. Fit coefficients in percentage are listed on the right. The arrow indicates the most characteristic changes for each lesion type.

Tables (2)

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Table 1 Collinearity measurement for candidate model componentsa

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Table 2 Peak positions of main Raman bands in the Raman active components (Refs. 2, 9, 19, 31, 33, 38)

Equations (3)

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D=C S T +E
X=cs+e
R= x T y ( x T x )( y T y )

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