Stimulated Raman scattering microscopy for rapid brain tumor histology

Yifan Yang; Lingchao Chen; Minbiao Ji

doi:10.1142/s1793545817300105

[1] G. Husmann, P. Kaatsch, A. Katalinic, J. Bertz, J. Haberland et al., “Krebs in Deutschland 2005/2006,” Robert Koch-Institut und die Gesellschaft der epidemiologischen Kreberegister in Deutschland e.V., (2010).

[2] P. Kremer, F. Mahmoudreza, R. Ding, M. Pritsch, S. Zoubaa et al., “Intraoperative fluorescence staining of malignant brain tumors using 5-aminofluorescein-labeled albumin,” Neurosurgery 64, S53-S61 (2009).

[3] K. Petrecca, M. C. Guiot, V. Panet-Raymond, L. Souhami “Failure pattern following complete resection plus radiotherapy and temozolomide is at the resection margin in patients with glioblastoma,” J. Neurooncol. 111, 19-23 (2013).

[4] N. Sanai, M. Y. Polley, M. W. McDermott, A. T. Parsa and M. S. Berger, “An extent of resection threshold for newly diagnosed glioblastomas,” J. Neurosurg. 115, 3-8 (2011).

[5] W. Stummer, J. C. Tonn, H. M. Mehdorn, U. Nestler, K. Franz et al., “Counterbalancing risks and gains from extended resections in malignant glioma surgery: A supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study Clinical article,” J. Neurosurg. 114, 613-623 (2011).

[6] I. F. Talos, K. H. Zou, L. Ohno-Machado, J. G. Bhagwat, R. Kikinis et al., “Supratentorial low-grade glioma resectability: Statistical predictive analysis based on anatomic MR features and tumor characteristics,” Radiology 239, 506-513 (2006).

[7] L. Eisenhardt and H. Cushing, “Diagnosis of intracranial tumors by supravital technique,” Am. J. Pathol. 6, 541-U531 (1930).

[8] D. D. Langleben and G. M. Segall, “PET in differentiation of recurrent brain tumor from radiation injury,” J. Nucl. Med. 41, 1861-1867 (2000).

[9] M. C. Preul, R. Leblanc, Z. Caramanos, R. Kasrai, S. Narayanan et al., “Magnetic resonance spectroscopy guided brain tumor resection: Differentiation between recurrent glioma and radiation change in two diagnostically difficult cases,” Can. J. Neurol. Sci. 25, 13-22 (1998).

[10] W. Chen, “Clinical applications of PET in brain tumors,” J. Nucl. Med. 48, 1468-1481 (2007).

[11] Y. L. Ge, M. Law and R. I. Grossman, Applications of diffusion tensor MR imaging in multiple sclerosis, White Matter in Cognitive Neuroscience: Advances in Diffusion Tensor Imaging and Its Applications, J. L. UlmerL. ParsonsM. MoseleyJ. Gabrieli, Eds., p. 202, New York, Acad Sciences, New York (2005).

[12] M. H. T. Reinges, H. H. Nguyen, T. Krings, B. O. Hutter, V. Rohde et al., “Course of brain shift during microsurgical resection of supratentorial cerebral lesions: Limits of conventional neuronavigation,” Acta Neurochir. 146, 369-377 (2004).

[13] M. Makary, E. A. Chiocca, N. Erminy, M. Antor, S. D. Bergese et al., “Clinical and economic outcomes of low-field intraoperative MRI-guided tumor resection neurosurgery,” J. Mag. Reson. Imaging 34, 1022-1030 (2011).

[14] C. Ewelt, F. W. Floeth, J. Felsberg, H. J. Steiger, M. Sabel et al., “Finding the anaplastic focus in diffuse gliomas: The value of Gd-DTPA MRI. enhanced, FET-PET, and intraoperative, ALA-derived tissue fluorescence,” Clin. Neurol. Neurosurg. 113, 541-547 (2011).

[15] J. Regelsberger, F. Lohmann, K. Helmke and M. Westphal, “Ultrasound-guided surgery of deep seated brain lesions,” Eur. J. Ultrasound 12, 115-121 (2000).

[16] H. Bohringer, E. Lankenau, F. Stellmacher, E. Reusche, G. Huttmann et al., “Imaging of human brain tumor tissue by near-infrared laser coherence tomography,” Acta Neurochir. 151, 507-517 (2009).

[17] N. Sanai, J. Eschbacher, G. Hattendorf, S. W. Coons, M. C. Preul et al., “Intraoperative confocal microscopy for brain tumors: A feasibility analysis in humans,” Neurosurgery 68, 282-290 (2011).

[18] W. Stummer, J. C. Tonn, C. Goetz, W. Ullrich, H. Stepp et al., “5-aminolevulinic acid-derived tumor fluorescence: The diagnostic accuracy of visible fluorescence qualities as corroborated by spectrometry and histology and postoperative imaging,” Neurosurgery 74, 310-319 (2014).

[19] D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman et al., “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. USA 100, 7081-7086 (2003).

[20] S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva et al., “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. USA 108, 5970-5975 (2011).

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

[22] R. Bhargava, “Infrared spectroscopic imaging: The next generation,” Appl. Spectrosc. 66, 1091-1120 (2012).

[23] T. Meyer, N. Bergner, C. Bielecki, C. Krafft, D. Akimov et al., “Nonlinear microscopy, infrared, and Raman microspectroscopy for brain tumor analysis,” J. Biomed. Opt. 16, 021113 (2011).

[24] C. Krafft, L. Shapoval, S. B. Sobottka, G. Schackert and R. Salzer, “Identification of primary tumors of brain metastases by infrared spectroscopic imaging and linear discriminant analysis,” Technol. Cancer Res. Treat. 5, 291-298 (2006).

[25] C. Krafft, S. B. Sobottka, K. D. Geiger, G. Schackert and R. Salzer, “Classification of malignant gliomas by infrared spectroscopic imaging and linear discriminant analysis,” Anal. Bioanal. Chem. 387, 1669-1677 (2007).

[26] T. M. Greve, K. B. Andersen and O. F. Nielsen, “ATR-FTIR, FT-NIR and near-FT-Raman spectroscopic studies of molecular composition in human skin in vivo and pig ear skin in vitro,” Spectroscopy 22, 437-457 (2008).

[27] S. N. Kalkanis, R. E. Kast, M. L. Rosenblum, T. Mikkelsen, S. M. Yurgelevic et al., “Raman spectroscopy to distinguish grey matter, necrosis, and glioblastoma multiforme in frozen tissue sections,” J. Neurooncol. 116, 477-485 (2014).

[28] A. Mizuno, H. Kitajima, K. Kawauchi, S. Muraishi and Y. Ozaki, “Near-infrared Fourier-transform Raman-spectroscopic study of human brain-tissues and tumors,” J. Raman Spectrosc. 25, 25-29 (1994).

[29] M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette et al., “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7, 274ra19 (2015).

[30] H. Karabeber, R. Huang, P. Iacono, J. M. Samii, K. Pitter et al., “Guiding brain tumor resection using surface-enhanced Raman scattering nanoparticles and a hand-held Raman scanner,” ACS Nano 8, 9755-9766 (2014).

[31] C. L. Evans, E. O. Potma, M. Puoris’haag, D. Cote, C. P. Lin et al., “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. USA 102, 16807-16812 (2005).

[32] B. G. Saar, C. W. Freudiger, J. Reichman, C. M. Stanley, G. R. Holtom et al., “Video-rate molecular imaging in vivo with stimulated Raman scattering,” Science 330, 1368-1370 (2010).

[33] A. Zumbusch, G. R. Holtom and X. S. Xie, “Three-dimensional vibrational imaging by coherent anti-Stokes Raman scattering,” Phys. Rev. Lett. 82, 4142-4145 (1999).

[34] J. X. Cheng, A. Volkmer and X. S. Xie, “Theoretical and experimental characterization of coherent anti-Stokes Raman scattering microscopy,” J. Opt. Soc. Am. B 19, 1363-1375 (2002).

[35] J. X. Cheng and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: Instrumentation, theory, and applications,” J. Phys. Chem. B 108, 827-840 (2004).

[36] E. J. Woodbury and W. K. Ng, “Ruby laser operation in the near IR,” Proc. Inst. Radio Eng. 50, 2367 (1962).

[37] A. Owyoung and E. D. Jones, “Stimulated Raman spectroscopy using low-power cw lasers,” Opt. Lett. 1, 152-154 (1977).

[38] E. Ploetz, S. Laimgruber, S. Berner, W. Zinth and P. Gilch, “Femtosecond stimulated Raman microscopy,” Appl. Phys. B 87, 389-393 (2007).

[39] C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom et al., “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322, 1857-1861 (2008).

[40] D. Fu, F. K. Lu, X. Zhang, C. Freudiger, D. R. Pernik et al., “Quantitative chemical imaging with multiplex stimulated Raman scattering microscopy,” J. Am. Chem. Soc. 134, 3623-3626 (2012).

[41] D. A. Orringer, B. Pandian, Y. S. Niknafs, T. C. Hollon, J. Boyle et al., “Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy,” Nat. Biomed. Eng. 1, 0027 (2017).

[42] M. B. Ji, D. A. Orringer, C. W. Freudiger, S. Ramkissoon, X. H. Liu et al., “Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy,” Sci. Transl. Med. 5, 201ra119 (2013).

[43] M. B. Ji, S. Lewis, S. Camelo-Piragua, S. H. Ramkissoon, M. Snuderl et al., “Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy,” Sci. Transl. Med. 7, 309ra163 (2015).

[44] C. W. Freudiger, R. Pfannl, D. A. Orringer, B. G. Saar, M. B. Ji et al., “Multicolored stain-free histopathology with coherent Raman imaging,” Lab. Invest. 92, 1661-1661 (2012).

[45] F. K. Lu, S. Basu, V. Igras, M. P. Hoang, M. Ji et al., “Label-free DNA imaging in vivo with stimulated Raman scattering microscopy,” Proc. Natl. Acad. Sci. USA 112, 11624-11629 (2015).

[46] D. Fu, G. Holtom, C. Freudiger, X. Zhang and X. S. Xie, “Hyperspectral imaging with stimulated Raman scattering by chirped femtosecond lasers,” J. Phys. Chem. B 117, 4634-4640 (2013).

[47] R. He, Z. Liu, Y. Xu, W. Huang, H. Ma et al., “Stimulated Raman scattering microscopy and spectroscopy with a rapid scanning optical delay line,” Opt. Lett. 42, 659-662 (2017).

[48] A. Francis, K. Berry, Y. Chen, B. Figueroa and D. Fu, “Label-free pathology by spectrally sliced femtosecond stimulated Raman scattering (SRS) microscopy,” PLoS One 12, e0178750 (2017).

[49] F.-K. Lu, M. Ji, D. Fu, X. Ni, C. W. Freudiger et al., “Multicolor stimulated Raman scattering microscopy,” Mol. Phys. 110, 1927-1932 (2012).

[50] C. S. Liao, M. N. Slipchenko, P. Wang, J. Li, S. Y. Lee et al., “Microsecond scale vibrational spectroscopic imaging by multiplex stimulated Raman scattering microscopy,” Light Sci. Appl. 4, e265 (2015).

[51] D. Fu, “Quantitative chemical imaging with stimulated Raman scattering microscopy,” Curr. Opin. Chem. Biol. 39, 24-31 (2017).

[52] C. W. Freudiger, W. Yang, G. R. Holtom, N. Peyghambarian, X. S. Xie et al., “Stimulated Raman scattering microscopy with a robust fibre laser source,” Nat. Photonics 8, 153-159 (2014).

[53] L. Zhang, S. Shen, Z. Liu and M. Ji, “Label-free, quantitative imaging of MoS2-nanosheets in live cells with simultaneous stimulated Raman scattering and transient absorption microscopy,” Adv. Biosyst. 1, 1700013-1700020 (2017).

[54] Y. Xu, Q. Liu, R. He, X. Miao and M. Ji, “Imaging laser-triggered drug release from gold nanocages with transient absorption lifetime microscopy,” ACS Appl. Mater. Interfaces 9, 19653-19661 (2017).

[55] C. L. Evans, X. Xu, S. Kesari, X. S. Xie, S. T. C. Wong et al., “Chemically-selective imaging of brain structures with CARS microscopy,” Opt. Express 15, 12076-12087 (2007).

[56] F. K. Lu, D. Calligaris, O. I. Olubiyi, I. Norton, W. Yang et al., “Label-free neurosurgical pathology with stimulated Raman imaging,” Cancer Res. 76, 3451-3462 (2016).

[57] R. He, Y. Xu, L. Zhang, S. Ma, X. Wang et al., “Dual-phase stimulated Raman scattering microscopy for real-time two-color imaging,” Optica 4, 44-47 (2017).