Abstract

The assessment of the muscle invasion of bladder cancer typically plays a crucial role in therapeutic decision-making and has significant impacts on the recurrence rate and survival rate. Although histopathology is sufficiently accurate and usually served as the gold standard for bladder cancer diagnosis, it is invasive, time-consuming, and requires intensive sample preparation by a well-trained pathologist to achieve an optimal diagnosis. Therefore, a fast and noninvasive method to accurately identify non-muscle-invasive bladder cancer (NMIBC) and muscle-invasive bladder cancer (MIBC) is in demand. In this study, the SERS technique combined with the PLS-LDA method based on a small amount of blood serum samples is employed to distinguish healthy volunteers, NMIBC, and MIBC patients. According to the results, the overall diagnostic accuracy is 93.3%. The diagnostic accuracies are 97.8% and 93.2% for healthy versus bladder cancer groups and NMIBC versus MIBC groups, respectively. Therefore, the proposed method has demonstrated excellent performance on accurately identifying muscle invasion of bladder cancer, which can assist timely diagnosis and proper treatment for bladder cancer patients.

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

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2019 (1)

S. Zhu, X. Cui, W. Xu, S. Chen, and W. Qian, “Weighted Spectral Reconstruction Method for Discrimination of Bacteria Species with Low Signal-to-Noise Ratio Raman Measurements,” RSC Advances 9(17), 9500–9508 (2019).
[Crossref]

2018 (4)

S. Chen, L. Kong, W. Xu, X. Cui, and Q. Liu, “A Fast Fluorescence Background Suppression Method for Raman Spectroscopy Based on Stepwise Spectral Reconstruction,” IEEE Access 6, 67709–67717 (2018).
[Crossref]

Y. Zhang, X. Ping, Q. Zeng, L. Li, L. Lin, S. Li, Z. Liu, C. Su, M. Qi, and Z. Guo, “Classifying low-grade and high-grade bladder cancer using label-free serum surface-enhanced Raman spectroscopy and support vector machine,” Laser Phys. 28(3), 035603 (2018).
[Crossref]

F. Bray, J. Ferlay, I. Soerjomataram, R. L. Siegel, L. A. Torre, and A. Jemal, “Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries,” CA Cancer J. Clin. 68(6), 394–424 (2018).
[Crossref] [PubMed]

L. Xue, B. Yan, Y. Li, Y. Tan, X. Luo, and M. Wang, “Surface-enhanced Raman spectroscopy of blood serum based on gold nanoparticles for tumor stages detection and histologic grades classification of oral squamous cell carcinoma,” Int. J. Nanomedicine 13, 4977–4986 (2018).
[Crossref] [PubMed]

2017 (3)

S. Antoni, J. Ferlay, I. Soerjomataram, A. Znaor, A. Jemal, and F. Bray, “Bladder Cancer Incidence and Mortality: A Global Overview and Recent Trends,” Eur. Urol. 71(1), 96–108 (2017).
[Crossref] [PubMed]

P. Mariappan, V. Lavin, C. Q. Phua, S. A. A. Khan, R. Donat, and G. Smith, “Predicting grade and stage at cystoscopy in newly presenting bladder cancers-a prospective double-blind clinical study,” Urology 109, 134–139 (2017).
[Crossref] [PubMed]

S. Chen, C. Zhu, C. Hoe-Kong Chui, G. Sheoran, B. K. Tan, and Q. Liu, “Spectral diffuse reflectance and autofluorescence imaging can perform early prediction of blood vessel occlusion in skin flaps,” J. Biophotonics 10(12), 1665–1675 (2017).
[Crossref] [PubMed]

2015 (2)

S. Li, L. Li, Q. Zeng, Y. Zhang, Z. Guo, Z. Liu, M. Jin, C. Su, L. Lin, J. Xu, and S. Liu, “Characterization and noninvasive diagnosis of bladder cancer with serum surface enhanced Raman spectroscopy and genetic algorithms,” Sci. Rep. 5(1), 9582 (2015).
[Crossref] [PubMed]

K. Kong, C. Kendall, N. Stone, and I. Notingher, “Raman spectroscopy for medical diagnostics--From in-vitro biofluid assays to in-vivo cancer detection,” Adv. Drug Deliv. Rev. 89, 121–134 (2015).
[Crossref] [PubMed]

2014 (4)

S. Chen, X. Lin, C. Yuen, S. Padmanabhan, R. W. Beuerman, and Q. Liu, “Recovery of Raman spectra with low signal-to-noise ratio using Wiener estimation,” Opt. Express 22(10), 12102–12114 (2014).
[Crossref] [PubMed]

L. T. Kerr, K. Domijan, I. Cullen, and B. M. Hennelly, “Applications of Raman spectroscopy to the urinary bladder for cancer diagnostics,” Photonics Lasers Med. 3(3), 193–224 (2014).
[Crossref]

F. Ye, L. Wang, M. Castillo-Martin, R. McBride, M. D. Galsky, J. Zhu, P. Boffetta, D. Y. Zhang, and C. Cordon-Cardo, “Biomarkers for bladder cancer management: present and future,” Am. J. Clin. Exp. Urol. 2(1), 1–14 (2014).
[PubMed]

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
[Crossref] [PubMed]

2013 (5)

S. J. Dawson, D. W. Y. Tsui, M. Murtaza, H. Biggs, O. M. Rueda, S. F. Chin, M. J. Dunning, D. Gale, T. Forshew, B. Mahler-Araujo, S. Rajan, S. Humphray, J. Becq, D. Halsall, M. Wallis, D. Bentley, C. Caldas, and N. Rosenfeld, “Analysis of Circulating tumor DNA to monitor metastatic breast cancer,” N. Engl. J. Med. 368(13), 1199–1209 (2013).
[Crossref] [PubMed]

K. Dettmer, F. C. Vogl, A. P. Ritter, W. Zhu, N. Nürnberger, M. Kreutz, P. J. Oefner, W. Gronwald, and E. Gottfried, “Distinct metabolic differences between various human cancer and primary cells,” Electrophoresis 34(19), 2836–2847 (2013).
[Crossref] [PubMed]

P. Tripathi, B. S. Somashekar, M. Ponnusamy, A. Gursky, S. Dailey, P. Kunju, C. T. Lee, A. M. Chinnaiyan, T. M. Rajendiran, and A. Ramamoorthy, “HR-MAS NMR tissue metabolomic signatures cross-validated by mass spectrometry distinguish bladder cancer from benign disease,” J. Proteome Res. 12(7), 3519–3528 (2013).
[Crossref] [PubMed]

M. Takeuchi, S. Sasaki, T. Naiki, N. Kawai, K. Kohri, M. Hara, and Y. Shibamoto, “MR imaging of urinary bladder cancer for T-staging: a review and a pictorial essay of diffusion-weighted imaging,” J. Magn. Reson. Imaging 38(6), 1299–1309 (2013).
[Crossref] [PubMed]

N. Lawrentschuk, S. T. Lee, and A. M. Scott, “Current role of PET, CT, MR for invasive bladder cancer,” Curr. Urol. Rep. 14(2), 84–89 (2013).
[Crossref] [PubMed]

2012 (3)

D. Cialla, A. März, R. Böhme, F. Theil, K. Weber, M. Schmitt, and J. Popp, “Surface-enhanced Raman spectroscopy (SERS): progress and trends,” Anal. Bioanal. Chem. 403(1), 27–54 (2012).
[Crossref] [PubMed]

B. J. Altman and C. V. Dang, “Normal and cancer cell metabolism: lymphocytes and lymphoma,” FEBS J. 279(15), 2598–2609 (2012).
[Crossref] [PubMed]

H. Song, J. S. Peng, Y. Dong-Sheng, Z. L. Yang, H. L. Liu, Y. K. Zeng, X. P. Shi, and B. Y. Lu, “Serum metabolic profiling of human gastric cancer based on gas chromatography/mass spectrometry,” Braz. J. Med. Biol. Res. 45(1), 78–85 (2012).
[Crossref] [PubMed]

2011 (2)

J. Lin, R. Chen, S. Feng, J. Pan, Y. Li, G. Chen, M. Cheng, Z. Huang, Y. Yu, and H. Zeng, “A novel blood plasma analysis technique combining membrane electrophoresis with silver nanoparticle-based SERS spectroscopy for potential applications in noninvasive cancer detection,” Nanomedicine (Lond.) 7(5), 655–663 (2011).
[Crossref] [PubMed]

G. Wang, R. J. Lipert, M. Jain, S. Kaur, S. Chakraboty, M. P. Torres, S. K. Batra, R. E. Brand, and M. D. Porter, “Detection of the potential pancreatic cancer marker MUC4 in serum using surface-enhanced Raman scattering,” Anal. Chem. 83(7), 2554–2561 (2011).
[Crossref] [PubMed]

2010 (1)

S. Feng, R. Chen, J. Lin, J. Pan, G. Chen, Y. Li, M. Cheng, Z. Huang, J. Chen, and H. Zeng, “Nasopharyngeal cancer detection based on blood plasma surface-enhanced Raman spectroscopy and multivariate analysis,” Biosens. Bioelectron. 25(11), 2414–2419 (2010).
[Crossref] [PubMed]

2009 (5)

M. Si, Y. Kang, and Z. Zhang, “Surface-enhanced Raman scattering (SERS) spectra of chloramphenicol in Ag colloids prepared by microwave heating method,” J. Raman Spec. 40(9), 1319–1323 (2009).
[Crossref]

A. C. Goh and S. P. Lerner, “Application of new technology in bladder cancer diagnosis and treatment,” World J. Urol. 27(3), 301–307 (2009).
[Crossref] [PubMed]

B. W. G. van Rhijn, M. Burger, Y. Lotan, E. Solsona, C. G. Stief, R. J. Sylvester, J. A. Witjes, and A. R. Zlotta, “Recurrence and progression of disease in non-muscle-invasive bladder cancer: from epidemiology to treatment strategy,” Eur. Urol. 56(3), 430–442 (2009).
[Crossref] [PubMed]

H. W. Han, X. L. Yan, R. X. Dong, G. Ban, and K. Li, “Analysis of serum from type ii diabetes mellitus and diabetic complication using surface-enhanced Raman spectra (SERS),” Appl. Phys. B 94(4), 667–672 (2009).
[Crossref]

A. Hirayama, K. Kami, M. Sugimoto, M. Sugawara, N. Toki, H. Onozuka, T. Kinoshita, N. Saito, A. Ochiai, M. Tomita, H. Esumi, and T. Soga, “Quantitative metabolome profiling of colon and stomach cancer microenvironment by capillary electrophoresis time-of-flight mass spectrometry,” Cancer Res. 69(11), 4918–4925 (2009).
[Crossref] [PubMed]

2007 (3)

J. D. Gelder, K. D. Gussem, P. Vandenabeele, and L. Moens, “Reference database of Raman spectra of biological molecules,” J. Raman Spectrosc. 38(9), 1133–1147 (2007).
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J. A. Menendez and R. Lupu, “Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis,” Nat. Rev. Cancer 7(10), 763–777 (2007).
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E. C. Le Ru, E. Blackie, M. Meyer, and P. G. Etchegoin, “Surface Enhanced Raman Scattering Enhancement Factors: A Comprehensive Study,” J. Phys. Chem. C 111(37), 13794–13803 (2007).
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2006 (3)

K. Liu and S. F. Wu, “Silver colloid synthesized by microwave method and applied in Surface Enhanced Raman Scattering,” J. Light Scattering 14(7), 332–335 (2006).

T. Fawcett, “An introduction to roc analysis,” Pattern Recognit. Lett. 27(8), 861–874 (2006).
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F. P. Kuhajda, “Fatty Acid Synthase and Cancer: New Application of an Old Pathway,” Cancer Res. 66(12), 5977–5980 (2006).
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2005 (2)

Z. Kirkali, T. Chan, M. Manoharan, F. Algaba, C. Busch, L. Cheng, L. Kiemeney, M. Kriegmair, R. Montironi, W. M. Murphy, I. A. Sesterhenn, M. Tachibana, and J. Weider, “Bladder cancer: epidemiology, staging and grading, and diagnosis,” Urology 66(6Suppl 1), 4–34 (2005).
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A. Tekes, I. Kamel, K. Imam, G. Szarf, M. Schoenberg, K. Nasir, R. Thompson, and D. Bluemke, “Dynamic MRI of bladder cancer: evaluation of staging accuracy,” AJR Am. J. Roentgenol. 184(1), 121–127 (2005).
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2004 (3)

M. I. Toma, M. G. Friedrich, S. H. Hautmann, K. T. Jäkel, A. Erbersdobler, A. Hellstern, and H. Huland, “Comparison of the ImmunoCyt test and urinary cytology with other urine tests in the detection and surveillance of bladder cancer,” World J. Urol. 22(2), 145–149 (2004).
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B. P. Schrier, M. P. Hollander, B. W. van Rhijn, L. A. Kiemeney, and J. A. Witjes, “Prognosis of muscle-invasive bladder cancer: difference between primary and progressive tumours and implications for therapy,” Eur. Urol. 45(3), 292–296 (2004).
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W. Dröge, “Autophagy and aging--importance of amino acid levels,” Mech. Ageing Dev. 125(3), 161–168 (2004).
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2000 (1)

A. D. MacVicar, “Bladder cancer staging,” BJU Int. 86(Suppl 1), 111–122 (2000).
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1997 (1)

S. Nie and S. R. Emory, “Probing Single Molecules and Single Nanoparticles by Surface-Enhanced Raman Scattering,” Science 275(5303), 1102–1106 (1997).
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1995 (1)

G. S. Wasserman and H. Mohsen, “Computer intensive statistical methods: validation, model selection and bootstrap,” J. Qual. Technol. 27(3), 268–270 (1995).
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1989 (2)

M. S. Soloway, “Diagnosis and management of superficial bladder cancer,” Semin. Surg. Oncol. 5(4), 247–254 (1989).
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J. E. Husband, J. F. Olliff, M. P. Williams, C. W. Heron, and G. R. Cherryman, “Bladder cancer: staging with CT and MR imaging,” Radiology 173(2), 435–440 (1989).
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1988 (2)

J. O. Salo, L. Kivisaari, and T. Lehtonen, “Comparison of magnetic resonance imaging with computed tomography and intravesical ultrasound in staging bladder cancer,” Urol. Radiol. 10(4), 167–172 (1988).
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J. M. Argilés and J. Azcón-Bieto, “The metabolic environment of cancer,” Mol. Cell. Biochem. 81(1), 3–17 (1988).
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1984 (1)

N. P. DeFelippo, R. P. Fortunato, H. Z. Mellins, and J. P. Richie, “Intravenous urography: important adjunct for diagnosis of bladder tumours,” Br. J. Urol. 56(5), 502–505 (1984).
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1982 (1)

P. C. Lee and D. Meisel, “Adsorption and Surface-Enhanced Raman of Dyes on Silver and God Sols,” J. Phys. Chem. 86(17), 3391–3395 (1982).
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Agrawal, N.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
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Alani, R. M.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
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Algaba, F.

Z. Kirkali, T. Chan, M. Manoharan, F. Algaba, C. Busch, L. Cheng, L. Kiemeney, M. Kriegmair, R. Montironi, W. M. Murphy, I. A. Sesterhenn, M. Tachibana, and J. Weider, “Bladder cancer: epidemiology, staging and grading, and diagnosis,” Urology 66(6Suppl 1), 4–34 (2005).
[Crossref] [PubMed]

Allen, P. J.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
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Altman, B. J.

B. J. Altman and C. V. Dang, “Normal and cancer cell metabolism: lymphocytes and lymphoma,” FEBS J. 279(15), 2598–2609 (2012).
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Antonarakis, E. S.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
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Antoni, S.

S. Antoni, J. Ferlay, I. Soerjomataram, A. Znaor, A. Jemal, and F. Bray, “Bladder Cancer Incidence and Mortality: A Global Overview and Recent Trends,” Eur. Urol. 71(1), 96–108 (2017).
[Crossref] [PubMed]

Argilés, J. M.

J. M. Argilés and J. Azcón-Bieto, “The metabolic environment of cancer,” Mol. Cell. Biochem. 81(1), 3–17 (1988).
[Crossref] [PubMed]

Azad, N. S.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
[Crossref] [PubMed]

Azcón-Bieto, J.

J. M. Argilés and J. Azcón-Bieto, “The metabolic environment of cancer,” Mol. Cell. Biochem. 81(1), 3–17 (1988).
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Ban, G.

H. W. Han, X. L. Yan, R. X. Dong, G. Ban, and K. Li, “Analysis of serum from type ii diabetes mellitus and diabetic complication using surface-enhanced Raman spectra (SERS),” Appl. Phys. B 94(4), 667–672 (2009).
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Bardelli, A.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
[Crossref] [PubMed]

Bartlett, B. R.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
[Crossref] [PubMed]

Batra, S. K.

G. Wang, R. J. Lipert, M. Jain, S. Kaur, S. Chakraboty, M. P. Torres, S. K. Batra, R. E. Brand, and M. D. Porter, “Detection of the potential pancreatic cancer marker MUC4 in serum using surface-enhanced Raman scattering,” Anal. Chem. 83(7), 2554–2561 (2011).
[Crossref] [PubMed]

Becq, J.

S. J. Dawson, D. W. Y. Tsui, M. Murtaza, H. Biggs, O. M. Rueda, S. F. Chin, M. J. Dunning, D. Gale, T. Forshew, B. Mahler-Araujo, S. Rajan, S. Humphray, J. Becq, D. Halsall, M. Wallis, D. Bentley, C. Caldas, and N. Rosenfeld, “Analysis of Circulating tumor DNA to monitor metastatic breast cancer,” N. Engl. J. Med. 368(13), 1199–1209 (2013).
[Crossref] [PubMed]

Bentley, D.

S. J. Dawson, D. W. Y. Tsui, M. Murtaza, H. Biggs, O. M. Rueda, S. F. Chin, M. J. Dunning, D. Gale, T. Forshew, B. Mahler-Araujo, S. Rajan, S. Humphray, J. Becq, D. Halsall, M. Wallis, D. Bentley, C. Caldas, and N. Rosenfeld, “Analysis of Circulating tumor DNA to monitor metastatic breast cancer,” N. Engl. J. Med. 368(13), 1199–1209 (2013).
[Crossref] [PubMed]

Bettegowda, C.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
[Crossref] [PubMed]

Beuerman, R. W.

Biggs, H.

S. J. Dawson, D. W. Y. Tsui, M. Murtaza, H. Biggs, O. M. Rueda, S. F. Chin, M. J. Dunning, D. Gale, T. Forshew, B. Mahler-Araujo, S. Rajan, S. Humphray, J. Becq, D. Halsall, M. Wallis, D. Bentley, C. Caldas, and N. Rosenfeld, “Analysis of Circulating tumor DNA to monitor metastatic breast cancer,” N. Engl. J. Med. 368(13), 1199–1209 (2013).
[Crossref] [PubMed]

Blackie, E.

E. C. Le Ru, E. Blackie, M. Meyer, and P. G. Etchegoin, “Surface Enhanced Raman Scattering Enhancement Factors: A Comprehensive Study,” J. Phys. Chem. C 111(37), 13794–13803 (2007).
[Crossref]

Bluemke, D.

A. Tekes, I. Kamel, K. Imam, G. Szarf, M. Schoenberg, K. Nasir, R. Thompson, and D. Bluemke, “Dynamic MRI of bladder cancer: evaluation of staging accuracy,” AJR Am. J. Roentgenol. 184(1), 121–127 (2005).
[Crossref] [PubMed]

Boffetta, P.

F. Ye, L. Wang, M. Castillo-Martin, R. McBride, M. D. Galsky, J. Zhu, P. Boffetta, D. Y. Zhang, and C. Cordon-Cardo, “Biomarkers for bladder cancer management: present and future,” Am. J. Clin. Exp. Urol. 2(1), 1–14 (2014).
[PubMed]

Böhme, R.

D. Cialla, A. März, R. Böhme, F. Theil, K. Weber, M. Schmitt, and J. Popp, “Surface-enhanced Raman spectroscopy (SERS): progress and trends,” Anal. Bioanal. Chem. 403(1), 27–54 (2012).
[Crossref] [PubMed]

Brand, R. E.

G. Wang, R. J. Lipert, M. Jain, S. Kaur, S. Chakraboty, M. P. Torres, S. K. Batra, R. E. Brand, and M. D. Porter, “Detection of the potential pancreatic cancer marker MUC4 in serum using surface-enhanced Raman scattering,” Anal. Chem. 83(7), 2554–2561 (2011).
[Crossref] [PubMed]

Bray, F.

F. Bray, J. Ferlay, I. Soerjomataram, R. L. Siegel, L. A. Torre, and A. Jemal, “Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries,” CA Cancer J. Clin. 68(6), 394–424 (2018).
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S. Antoni, J. Ferlay, I. Soerjomataram, A. Znaor, A. Jemal, and F. Bray, “Bladder Cancer Incidence and Mortality: A Global Overview and Recent Trends,” Eur. Urol. 71(1), 96–108 (2017).
[Crossref] [PubMed]

Brem, H.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
[Crossref] [PubMed]

Burger, M.

B. W. G. van Rhijn, M. Burger, Y. Lotan, E. Solsona, C. G. Stief, R. J. Sylvester, J. A. Witjes, and A. R. Zlotta, “Recurrence and progression of disease in non-muscle-invasive bladder cancer: from epidemiology to treatment strategy,” Eur. Urol. 56(3), 430–442 (2009).
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Busch, C.

Z. Kirkali, T. Chan, M. Manoharan, F. Algaba, C. Busch, L. Cheng, L. Kiemeney, M. Kriegmair, R. Montironi, W. M. Murphy, I. A. Sesterhenn, M. Tachibana, and J. Weider, “Bladder cancer: epidemiology, staging and grading, and diagnosis,” Urology 66(6Suppl 1), 4–34 (2005).
[Crossref] [PubMed]

Caldas, C.

S. J. Dawson, D. W. Y. Tsui, M. Murtaza, H. Biggs, O. M. Rueda, S. F. Chin, M. J. Dunning, D. Gale, T. Forshew, B. Mahler-Araujo, S. Rajan, S. Humphray, J. Becq, D. Halsall, M. Wallis, D. Bentley, C. Caldas, and N. Rosenfeld, “Analysis of Circulating tumor DNA to monitor metastatic breast cancer,” N. Engl. J. Med. 368(13), 1199–1209 (2013).
[Crossref] [PubMed]

Cameron, J. L.

C. Bettegowda, M. Sausen, R. J. Leary, I. Kinde, Y. Wang, N. Agrawal, B. R. Bartlett, H. Wang, B. Luber, R. M. Alani, E. S. Antonarakis, N. S. Azad, A. Bardelli, H. Brem, J. L. Cameron, C. C. Lee, L. A. Fecher, G. L. Gallia, P. Gibbs, D. Le, R. L. Giuntoli, M. Goggins, M. D. Hogarty, M. Holdhoff, S. M. Hong, Y. Jiao, H. H. Juhl, J. J. Kim, G. Siravegna, D. A. Laheru, C. Lauricella, M. Lim, E. J. Lipson, S. K. Marie, G. J. Netto, K. S. Oliner, A. Olivi, L. Olsson, G. J. Riggins, A. Sartore-Bianchi, K. Schmidt, M. Shih, S. M. Oba-Shinjo, S. Siena, D. Theodorescu, J. Tie, T. T. Harkins, S. Veronese, T. L. Wang, J. D. Weingart, C. L. Wolfgang, L. D. Wood, D. Xing, R. H. Hruban, J. Wu, P. J. Allen, C. M. Schmidt, M. A. Choti, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, N. Papadopoulos, and L. A. Diaz, “Detection of circulating tumor DNA in early- and late-stage human malignancies,” Sci. Transl. Med. 6(224), 224ra24 (2014).
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Figures (6)

Fig. 1
Fig. 1 The TEM micrograph of the concentrated silver colloid mixed with blood serum (Left) and the UV/visible absorption spectrum of the silver colloid (Right).
Fig. 2
Fig. 2 The comparison of SERS spectrum and spontaneous Raman spectrum of the same blood serum sample, Raman spectrum of silver colloid and Raman spectrum of aluminum foil.
Fig. 3
Fig. 3 (a) The average SERS spectra after fluorescence background removal and normalization from the healthy, NMIBC and MIBC groups, in which the shaded areas represent the standard deviations among each group; (b) the subtracted spectra between different groups.
Fig. 4
Fig. 4 The first twenty PLS components of blood serum SERS spectra: (a) PC 1 to 4 (from left to right); (b) PC 5 to 8 (from left to right); (c) PC 9 to 12 (from left to right); (d) PC 13 to 16 (from left to right); (e) PC 17 to 20 (from left to right).
Fig. 5
Fig. 5 3D scatter plot of PC scores of (a) healthy and bladder cancer groups, (b) NMIBC and MIBC groups; Scatter plot of the linear discriminant scores of (c) healthy and bladder cancer groups, (d) NMIBC and MIBC groups.
Fig. 6
Fig. 6 The ROC curves obtained by using PLS-LDA based classification model between healthy and bladder cancer groups, and between NMIBC and MIBC groups.

Tables (2)

Tables Icon

Table 1 The Assignments of the Raman Peaks with Significant Differences among Healthy, NMIBC and MIBC Groups

Tables Icon

Table 2 The Overall Classification Results of Healthy, NMIBC and MIBC Groups

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