Abstract

We report on the use of line-scan hyperspectral Raman microscopy in combination with multivariate statistical analyses for identifying and classifying single cells isolated from clinical samples of human thyroid nodules based on their intrinsic Raman spectral signatures. A total of 248 hyperspectral Raman images of single cells from benign thyroid (n = 127) and classic variant of papillary carcinoma (n = 121) nodules were collected. Spectral differences attributed to phenylalanine, tryptophan, proteins, lipids, and nucleic acids were identified for benign and papillary carcinoma cells. Using principal component analysis and linear discriminant analysis, cells were identified with 97% diagnostic accuracy. In addition, preliminary data of cells from follicular adenoma (n = 20), follicular carcinoma (n = 25), and follicular variant of papillary carcinoma (n = 18) nodules suggest the feasibility of further discrimination of subtypes. Our findings indicate that hyperspectral Raman microscopy can potentially be developed into an objective approach for analyzing single cells from fine needle aspiration (FNA) biopsies to enable the minimally invasive diagnosis of “indeterminate” thyroid nodules and other challenging cases.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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    [Crossref] [PubMed]
  22. A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
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    [Crossref]

2019 (1)

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

2018 (1)

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2018,” CA Cancer J. Clin. 68(1), 7–30 (2018).
[Crossref] [PubMed]

2017 (4)

E. S. Cibas and S. Z. Ali, “The 2017 Bethesda System for Reporting Thyroid Cytopathology,” Thyroid 27(11), 1341–1346 (2017).
[Crossref] [PubMed]

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

2016 (2)

I. W. Schie and J. W. Chan, “Estimation of spectra sample size for characterizing single cells using micro-Raman spectroscopy,” J. Raman Spectrosc. 47(4), 384–390 (2016).
[Crossref]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

2015 (3)

T. Huser and J. Chan, “Raman spectroscopy for physiological investigations of tissues and cells,” Adv. Drug Deliv. Rev. 89, 57–70 (2015).
[Crossref] [PubMed]

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

2014 (2)

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

I. W. Schie, L. Alber, A. L. Gryshuk, and J. W. Chan, “Investigating drug induced changes in single, living lymphocytes based on Raman micro-spectroscopy,” Analyst (Lond.) 139(11), 2726–2733 (2014).
[Crossref] [PubMed]

2013 (1)

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

2012 (1)

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

2011 (2)

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

2010 (1)

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

2009 (2)

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

2004 (1)

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

2003 (1)

1985 (1)

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

Akaike, M.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Alber, L.

I. W. Schie, L. Alber, A. L. Gryshuk, and J. W. Chan, “Investigating drug induced changes in single, living lymphocytes based on Raman micro-spectroscopy,” Analyst (Lond.) 139(11), 2726–2733 (2014).
[Crossref] [PubMed]

Alexander, E. K.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Ali, S. Z.

E. S. Cibas and S. Z. Ali, “The 2017 Bethesda System for Reporting Thyroid Cytopathology,” Thyroid 27(11), 1341–1346 (2017).
[Crossref] [PubMed]

Angell, T. E.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Arisawa, E. A. L.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Attwood, K.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Balachandar, S.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Baloch, Z.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Bando, E.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Barletta, J. A.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Bergholt, M. S.

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Bernet, V.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Bitar, R. A.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Bongiovanni, M.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Bowers, J.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

Brandão, L. G.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Cao, B.

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Caricato, M.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Carty, S. E.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Cernea, C. R.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Chan, J.

T. Huser and J. Chan, “Raman spectroscopy for physiological investigations of tissues and cells,” Adv. Drug Deliv. Rev. 89, 57–70 (2015).
[Crossref] [PubMed]

Chan, J. W.

I. W. Schie and J. W. Chan, “Estimation of spectra sample size for characterizing single cells using micro-Raman spectroscopy,” J. Raman Spectrosc. 47(4), 384–390 (2016).
[Crossref]

I. W. Schie, L. Alber, A. L. Gryshuk, and J. W. Chan, “Investigating drug induced changes in single, living lymphocytes based on Raman micro-spectroscopy,” Analyst (Lond.) 139(11), 2726–2733 (2014).
[Crossref] [PubMed]

Chandra, D.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
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Chen, A.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
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Chen, G. N.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
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Chen, R.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
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X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
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Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
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M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
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E. S. Cibas and S. Z. Ali, “The 2017 Bethesda System for Reporting Thyroid Cytopathology,” Thyroid 27(11), 1341–1346 (2017).
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N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Crescenzi, A.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
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Crucitti, P.

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
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da Costa, R. B.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
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L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
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de Azevedo Canevari, R.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
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L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
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Fahey, T. J.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Feng, S. Y.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Ferris, R. L.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

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A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

Fosca, M.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Friguglietti, C. U. M.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Ganly, I.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Garg, M.

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
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A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

Gniadecka, M.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Gniadecki, R.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Gochi, A.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Gould, M. N.

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
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Gowda, G. A. N.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
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Graziani, V.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
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Gryshuk, A. L.

I. W. Schie, L. Alber, A. L. Gryshuk, and J. W. Chan, “Investigating drug induced changes in single, living lymphocytes based on Raman micro-spectroscopy,” Analyst (Lond.) 139(11), 2726–2733 (2014).
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Hammoud, Z.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
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Hansen, L. K.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Harris, A. T.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

Hercogova, J.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Higashiyama, M.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

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A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

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R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
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M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
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R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Horimoto, K.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
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M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
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Huang, Z. F.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

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T. Huser and J. Chan, “Raman spectroscopy for physiological investigations of tissues and cells,” Adv. Drug Deliv. Rev. 89, 57–70 (2015).
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Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
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Imaizumi, A.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Imamura, F.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Ishikawa, T.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
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Jemal, A.

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Jones, M. P.

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

Kebebew, E.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Kim, M. I.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Kimura, H.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Kirkham, J.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

Kopecky, K. J.

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

Krane, J. F.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Kulcsar, M. A. V.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Kumar, R.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Kuzmin, A. N.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Kwong, N.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Larsen, P. R.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Li, C.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Li, Z. F.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Lieber, C. A.

Lin, D.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Lin, J. Q.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Lin, K.

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Liu, L.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

Liu, N. R.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Liu, X.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Lyng, F. M.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Mahadevan-Jansen, A.

Malkin, A.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Marqusee, E.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Martin, A. A.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Martin-Hirsch, D. P.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

Martinho, H. S.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Meade, A. D.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Medeiros Neto, L. P.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Medici, M.

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

Mello, E. S.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Miller, K. D.

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2018,” CA Cancer J. Clin. 68(1), 7–30 (2018).
[Crossref] [PubMed]

Miller, R. C.

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

Mitsushima, T.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Miura, T.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Miyagi, Y.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Miyano, H.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Moriyama, M.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Nakamura, N.

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

Nielsen, O. F.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

O’Dea, D.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

O’Malley, J.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Okamoto, N.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Onetti Muda, A.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Oshita, F.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Pan, J. J.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Patel, K. N.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Pereira, M. A.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Philipsen, P. A.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Pliss, A.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Pozzilli, P.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Prasad, P. N.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Raftery, D.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

Rau, J. V.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Rennie, A.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

Rocchia, M.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Rossen, K.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Santos, A. B. O.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Santos, L. D.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Saruki, N.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Schie, I. W.

I. W. Schie and J. W. Chan, “Estimation of spectra sample size for characterizing single cells using micro-Raman spectroscopy,” J. Raman Spectrosc. 47(4), 384–390 (2016).
[Crossref]

I. W. Schie, L. Alber, A. L. Gryshuk, and J. W. Chan, “Investigating drug induced changes in single, living lymphocytes based on Raman micro-spectroscopy,” Analyst (Lond.) 139(11), 2726–2733 (2014).
[Crossref] [PubMed]

Shaha, A.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Shen, J.

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Siegel, R. L.

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2018,” CA Cancer J. Clin. 68(1), 7–30 (2018).
[Crossref] [PubMed]

Sigurdsson, S.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Smith, D. A.

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

So, J. B. Y.

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Steward, D. L.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Sykiotis, G. P.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Taffon, C.

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Teh, M.

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Teixeira, C. S. B.

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

Tellez Soto, C. A.

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

Tenou, H.

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

Thomsen, H. K.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Tochikubo, O.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Tufano, R. P.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Upile, T.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

Wang, J.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Waqar-Uddin, H.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

Wei, S.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

Wessel, S.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Wheatley, S. R.

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

Wiseman, S. M.

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

Wulf, H. C.

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

Xu, L.

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Yadav, N.

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Yamakado, M.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Yamamoto, H.

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

Yang, X. B. B.

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

Yeoh, K. G.

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Yu, Y.

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Zhang, H.

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Zhang, J.

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

Zhang, X.

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Zhao, T.

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

Zheng, W.

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Ziros, P. G.

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Adv. Drug Deliv. Rev. (1)

T. Huser and J. Chan, “Raman spectroscopy for physiological investigations of tissues and cells,” Adv. Drug Deliv. Rev. 89, 57–70 (2015).
[Crossref] [PubMed]

Analyst (Lond.) (2)

C. S. B. Teixeira, R. A. Bitar, H. S. Martinho, A. B. O. Santos, M. A. V. Kulcsar, C. U. M. Friguglietti, R. B. da Costa, E. A. L. Arisawa, and A. A. Martin, “Thyroid tissue analysis through Raman spectroscopy,” Analyst (Lond.) 134(11), 2361–2370 (2009).
[Crossref] [PubMed]

I. W. Schie, L. Alber, A. L. Gryshuk, and J. W. Chan, “Investigating drug induced changes in single, living lymphocytes based on Raman micro-spectroscopy,” Analyst (Lond.) 139(11), 2726–2733 (2014).
[Crossref] [PubMed]

Appl. Spectrosc. (1)

Biochim. Biophys. Acta (1)

X. Zhang, L. Xu, J. Shen, B. Cao, T. Cheng, T. Zhao, X. Liu, and H. Zhang, “Metabolic signatures of esophageal cancer: NMR-based metabolomics and UHPLC-based focused metabolomics of blood serum,” Biochim. Biophys. Acta 1832(8), 1207–1216 (2013).
[Crossref] [PubMed]

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R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2018,” CA Cancer J. Clin. 68(1), 7–30 (2018).
[Crossref] [PubMed]

Cancer Lett. (1)

J. O’Malley, R. Kumar, A. N. Kuzmin, A. Pliss, N. Yadav, S. Balachandar, J. Wang, K. Attwood, P. N. Prasad, and D. Chandra, “Lipid quantification by Raman microspectroscopy as a potential biomarker in prostate cancer,” Cancer Lett. 397, 52–60 (2017).
[Crossref] [PubMed]

Cytopathology (1)

D. O’Dea, M. Bongiovanni, G. P. Sykiotis, P. G. Ziros, A. D. Meade, F. M. Lyng, and A. Malkin, “Raman spectroscopy for the preoperative diagnosis of thyroid cancer and its subtypes: An in vitro proof-of-concept study,” Cytopathology 30(1), 51–60 (2019).
[Crossref] [PubMed]

Head Neck Oncol. (2)

A. T. Harris, A. Rennie, H. Waqar-Uddin, S. R. Wheatley, S. K. Ghosh, D. P. Martin-Hirsch, S. E. Fisher, A. S. High, J. Kirkham, and T. Upile, “Raman spectroscopy in head and neck cancer,” Head Neck Oncol. 2(1), 26 (2010).
[Crossref] [PubMed]

A. T. Harris, M. Garg, X. B. B. Yang, S. E. Fisher, J. Kirkham, D. A. Smith, D. P. Martin-Hirsch, and A. S. High, “Raman spectroscopy and advanced mathematical modelling in the discrimination of human thyroid cell lines,” Head Neck Oncol. 1(1), 38 (2009).
[Crossref] [PubMed]

J. Clin. Endocrinol. Metab. (1)

N. Kwong, M. Medici, T. E. Angell, X. Liu, E. Marqusee, E. S. Cibas, J. F. Krane, J. A. Barletta, M. I. Kim, P. R. Larsen, and E. K. Alexander, “The Influence of Patient Age on Thyroid Nodule Formation, Multinodularity, and Thyroid Cancer Risk,” J. Clin. Endocrinol. Metab. 100(12), 4434–4440 (2015).
[Crossref] [PubMed]

J. Invest. Dermatol. (1)

M. Gniadecka, P. A. Philipsen, S. Sigurdsson, S. Wessel, O. F. Nielsen, D. H. Christensen, J. Hercogova, K. Rossen, H. K. Thomsen, R. Gniadecki, L. K. Hansen, and H. C. Wulf, “Melanoma diagnosis by Raman spectroscopy and neural networks: structure alterations in proteins and lipids in intact cancer tissue,” J. Invest. Dermatol. 122(2), 443–449 (2004).
[Crossref] [PubMed]

J. Radiat. Res. (Tokyo) (1)

R. C. Miller, T. Hiraoka, N. Nakamura, H. Tenou, K. J. Kopecky, M. P. Jones, and M. N. Gould, “In vitro culture of human thyroid cells; methods and application to radiation biology,” J. Radiat. Res. (Tokyo) 26(3), 269–282 (1985).
[Crossref] [PubMed]

J. Raman Spectrosc. (1)

I. W. Schie and J. W. Chan, “Estimation of spectra sample size for characterizing single cells using micro-Raman spectroscopy,” J. Raman Spectrosc. 47(4), 384–390 (2016).
[Crossref]

Laser Phys. Lett. (1)

Z. F. Li, C. Li, D. Lin, Z. F. Huang, J. J. Pan, G. N. Chen, J. Q. Lin, N. R. Liu, Y. Yu, S. Y. Feng, and R. Chen, “Surface-enhanced Raman spectroscopy for differentiation between benign and malignant thyroid tissues,” Laser Phys. Lett. 11(4), 045602 (2014).
[Crossref]

Photodiagn. Photodyn. Ther. (1)

L. P. Medeiros Neto, L. F. das Chagas E Silva de Carvalho, L. D. Santos, C. A. Tellez Soto, R. de Azevedo Canevari, A. B. de Oliveira Santos, E. S. Mello, M. A. Pereira, C. R. Cernea, L. G. Brandão, and A. A. Martin, “Micro-Raman spectroscopic study of thyroid tissues,” Photodiagn. Photodyn. Ther. 17, 164–172 (2017).
[Crossref] [PubMed]

PLoS One (2)

Y. Miyagi, M. Higashiyama, A. Gochi, M. Akaike, T. Ishikawa, T. Miura, N. Saruki, E. Bando, H. Kimura, F. Imamura, M. Moriyama, I. Ikeda, A. Chiba, F. Oshita, A. Imaizumi, H. Yamamoto, H. Miyano, K. Horimoto, O. Tochikubo, T. Mitsushima, M. Yamakado, and N. Okamoto, “Plasma Free Amino Acid Profiling of Five Types of Cancer Patients and Its Application for Early Detection,” PLoS One 6(9), e24143 (2011).
[Crossref] [PubMed]

J. Zhang, J. Bowers, L. Liu, S. Wei, G. A. N. Gowda, Z. Hammoud, and D. Raftery, “Esophageal Cancer Metabolite Biomarkers Detected by LC-MS and NMR Methods,” PLoS One 7(1), e30181 (2012).
[Crossref] [PubMed]

Sci. Rep. (2)

J. V. Rau, M. Fosca, V. Graziani, C. Taffon, M. Rocchia, M. Caricato, P. Pozzilli, A. Onetti Muda, and A. Crescenzi, “Proof-of-concept Raman spectroscopy study aimed to differentiate thyroid follicular patterned lesions,” Sci. Rep. 7(1), 14970 (2017).
[Crossref] [PubMed]

J. V. Rau, V. Graziani, M. Fosca, C. Taffon, M. Rocchia, P. Crucitti, P. Pozzilli, A. Onetti Muda, M. Caricato, and A. Crescenzi, “RAMAN spectroscopy imaging improves the diagnosis of papillary thyroid carcinoma,” Sci. Rep. 6(1), 35117 (2016).
[Crossref] [PubMed]

Technol. Cancer Res. Treat. (1)

M. S. Bergholt, W. Zheng, K. Lin, K. Y. Ho, M. Teh, K. G. Yeoh, J. B. Y. So, and Z. Huang, “In Vivo Diagnosis of Esophageal Cancer Using Image-Guided Raman Endoscopy and Biomolecular Modeling,” Technol. Cancer Res. Treat. 10(2), 103–112 (2011).
[Crossref] [PubMed]

Thyroid (2)

E. S. Cibas and S. Z. Ali, “The 2017 Bethesda System for Reporting Thyroid Cytopathology,” Thyroid 27(11), 1341–1346 (2017).
[Crossref] [PubMed]

R. L. Ferris, Z. Baloch, V. Bernet, A. Chen, T. J. Fahey, I. Ganly, S. P. Hodak, E. Kebebew, K. N. Patel, A. Shaha, D. L. Steward, R. P. Tufano, S. M. Wiseman, and S. E. Carty, “American Thyroid Association Statement on Surgical Application of Molecular Profiling for Thyroid Nodules: Current Impact on Perioperative Decision Making,” Thyroid 25(7), 760–768 (2015).
[Crossref] [PubMed]

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Figures (6)

Fig. 1
Fig. 1 Brightfield and Raman images of (a-f) papillary thyroid carcinoma cell and (g-l) benign follicular cell for select Raman bands.
Fig. 2
Fig. 2 Average Raman spectra of (a) 127 benign (blue line) and (b) 121 PTC classic variant (red line) cells. The gray shadows represent ± 1 standard deviations (SD) over the average values. (c) The difference spectrum (benign – CVPTC) highlights the peaks that are associated with benign cells (blue shade) and CVPTC cells (red shade).
Fig. 3
Fig. 3 (a) 3D PCA score plot of all individual Raman spectra for benign (blue circles) and CVPTC (red diamonds) cells. (b) Offset plot of the first three PCs coefficients.
Fig. 4
Fig. 4 (a) 2D and (b) 3D PCA-LDA score plots of benign (blue) and papillary carcinoma (red) cells with 95% interval confidence covariance error ellipses/ellipsoids.
Fig. 5
Fig. 5 Average Raman spectra of (a) 20 FTA (green line), (b) 20 FTC (magenta line) and (c) 18 FVPTC (dark gray line) cells. The light gray shadows represent ± 1 standard deviations (SD) over the average values.
Fig. 6
Fig. 6 (a)-(b) 2D and (c)-(d) 3D PCA-LDA score plot from 20 FTA (green plot), 25 FTC (magenta plot), 18 FVPTC (dark gray plot) and 121 CVPTC (red plot) cells.(e)-(f) Confusion matrices.

Tables (4)

Tables Icon

Table 1 Clinical thyroid tissue samples

Tables Icon

Table 2 Raman band positions and assignments [7,9,11,15]. (Note: ν: stretching vibration; νs: symmetrical stretching vibration; δ: bending vibration).

Tables Icon

Table 3 Confusion matrix of all representative Raman spectra for 127 benign and 121 papillary carcinoma cells.

Tables Icon

Table 4 Performance of the statistical (PCA-LDA with leave-N-out cross validation) analysis in discriminating thyroid cells.

Metrics