Quantitative molecular phenotyping with topically applied SERS nanoparticles for intraoperative guidance of breast cancer lumpectomy

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Wang, Yu ^a   Kang, Soyoung ^a   Khan, Altaz ^b   Ruttner, Gabriel ^b   Leigh, Steven Y ^a,b   Murray, Melissa ^c   Abeytunge, Sanjee ^c   Peterson, Gary ^c   Rajadhyaksha, Milind ^c   Dintzis, Suzanne ^a   Javid, Sara ^a   Liu, Jonathan T C ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; NANOPARTICLE; TUMOR MARKER;

ANIMAL; BREAST NEOPLASMS; CHEMISTRY; COMPUTER ASSISTED SURGERY; DISEASE MODEL; FEMALE; HUMAN; METABOLISM; MOLECULAR IMAGING; MOUSE; PARTIAL MASTECTOMY; PROCEDURES; RAMAN SPECTROMETRY; SURGICAL MARGIN; XENOGRAFT;

ANIMALS; BIOMARKERS, TUMOR; BREAST NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; HETEROGRAFTS; HUMANS; MARGINS OF EXCISION; MASTECTOMY, SEGMENTAL; MICE; MOLECULAR IMAGING; NANOPARTICLES; RECEPTORS, CELL SURFACE; SPECTRUM ANALYSIS, RAMAN; SURGERY, COMPUTER-ASSISTED;

EID: 84958554836     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21242     Document Type: Article

References (59)

1. Fisher, B. et al. Twenty-Year Follow-up of a Randomized Trial Comparing Total Mastectomy, Lumpectomy, and Lumpectomy plus Irradiation for the Treatment of Invasive Breast Cancer. New Engl. J. Med. 347, 1233-1241 (2002).
2. DeSantis, C., Ma, J., Bryan, L., Jemal, A. Breast cancer statistics, 2013. CA-Cancer J. Clin. 64, 52-62 (2014).
3. Waljee, J. F., Hu, E. S., Newman, L. A., Alderman, A. K. Predictors of re-excision among women undergoing breast-conserving surgery for cancer. Ann. Surg. Oncol. 15, 1297-1303 (2008).
4. Jeevan, R. et al. Reoperation rates after breast conserving surgery for breast cancer among women in England: retrospective study of hospital episode statistics. Brit. Med. J. 345 (2012).
5. Moran, M. S. et al. Society of Surgical Oncology-American Society for Radiation Oncology consensus guideline on margins for breastconserving surgery with whole-breast irradiation in stages I and II invasive breast cancer. Int. J. Radiat. Oncol. 88, 553-564 (2014).
6. Barakat, F., Sulaiman, I., Sughayer, M. Reliability of frozen section in breast sentinel lymph node examination. Breast Cancer 21, 576-582 (2014).
7. Cabioglu, N. et al. Role for intraoperative margin assessment in patients undergoing breast-conserving surgery. Ann. Surg. Oncol. 14, 1458-1471 (2007).
8. van Dam, G. M. et al. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results. Nat. Med. 17, 1315-1319 (2011).
9. Yang, D. J., Kim, E. E., Inoue, T. Targeted molecular imaging in oncology. Ann. Nucl. Med. 20, 1-11 (2006).
10. Vahrmeijer, A. L., Hutteman, M., van der Vorst, J. R., van de Velde, C. J. H., Frangioni, J. V. Image-guided cancer surgery using near-infrared fluorescence. Nat. Rev. Clin. Oncol. 10, 507-518 (2013).
11. Weissleder, R., Pittet, M. J. Imaging in the era of molecular oncology. Nature 452, 580-589 (2008).
12. Gerlinger, M. et al. Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing. New Engl. J. Med. 366, 883-892 (2012).
13. Longo, D. L. Tumor heterogeneity and personalized medicine. New Engl. J. Med. 366, 956-957 (2012).
14. Wang, Y. Q., Yan, B., Chen, L. X. SERS Tags: Novel Optical Nanoprobes for Bioanalysis. Chem. Rev. 113, 1391-1428 (2013).
15. Zavaleta, C. L. et al. A Raman-based endoscopic strategy for multiplexed molecular imaging. P. Natl. Acad. Sci. USA 110, E2288-E2297 (2013).
16. Leigh, S. Y., Som, M., Liu, J. T. C. Method for Assessing the Reliability of Molecular Diagnostics Based on Multiplexed SERSCoded Nanoparticles. PLoS ONE 8, e62084 (2013).
17. Wang, Y. W. et al. Rapid ratiometric biomarker detection with topically applied SERS nanoparticles. Technology 02, 118-132 (2014).
18. Qian, X. et al. In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags. Nat. Biotechnol. 26, 83-90 (2007).
19. Maiti, K. K. et al. Multiplex targeted in vivo cancer detection using sensitive near-infrared SERS nanotags. Nano Today 7, 85-93 (2012).
20. Zavaleta, C. L. et al. Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy. P. Natl. Acad. Sci. USA 106, 13511-13516 (2009).
21. Bohndiek, S. E. et al. A small animal Raman instrument for rapid, wide-area, spectroscopic imaging. P. Natl. Acad. Sci. USA 110, 12408-12413 (2013).
22. Mohs, A. M. et al. Hand-held spectroscopic device for in vivo and intraoperative tumor detection: contrast enhancement, detection sensitivity, and tissue penetration. Anal. chem. 82, 9058-9065 (2010).
23. McVeigh, P. Z., Mallia, R. J., Veilleux, I., Wilson, B. C. Widefield quantitative multiplex surface enhanced Raman scattering imaging in vivo. J. Biomed. Opt. 18, 046011 (2013).
24. Garai, E. et al. High-sensitivity, real-time, ratiometric imaging of surface-enhanced Raman scattering nanoparticles with a clinically translatable Raman endoscope device. J. Biomed. Opt. 18, 096008-096013 (2013).
25. Harmsen, S. et al. Surface-enhanced resonance Raman scattering nanostars for high-precision cancer imaging. Sci. Transl. Med. 7, 271-277 (2015).
26. Tichauer, K. M. et al. Microscopic lymph node tumor burden quantified by macroscopic dual-tracer molecular imaging. Nat. Med. 20, 1348-1353 (2014).
27. Jokerst, J. V., Miao, Z., Zavaleta, C., Cheng, Z., Gambhir, S. S. Affibody-Functionalized Gold-Silica Nanoparticles for Raman Molecular Imaging of the Epidermal Growth Factor Receptor. Small 7, 625-633 (2011).
28. Tichauer, K. M. et al. In vivo quantification of tumor receptor binding potential with dual-reporter molecular imaging. Mol. Imag. Biol. 14, 584-592 (2012).
29. Liu, J. T. C. et al. Quantifying Cell-Surface Biomarker Expression in Thick Tissues with Ratiometric Three-Dimensional Microscopy. Biophys. J. 96, 2405-2414 (2009).
30. Wang, Y. W. et al. Comprehensive spectral endoscopy of topically applied SERS nanoparticles in the rat esophagus. Biomed. Opt. Express 5, 2883-2895 (2014).
31. Wang, Y. W., Kang, S., Khan, A., Bao, P. Q., Liu, J. T. C. In vivo multiplexed molecular imaging of esophageal cancer via spectral endoscopy of topically applied SERS nanoparticles. Biomed. Opt. Express 6, 3714-3723 (2015).
32. Jacques, S. L. Optical properties of biological tissues: a review. Phys. Med. Biol. 58, R37 (2013).
33. Ntziachristos, V., Ripoll, J., Wang, L. V., Weissleder, R. Looking and listening to light: the evolution of whole-body photonic imaging. Nat. Biotechnol. 23, 313-320 (2005).
34. Renshaw, S. Immunohistochemistry. (Scion Publishing Ltd, 2007).
35. Iqbal, N., Iqbal, N. Human Epidermal Growth Factor Receptor 2 (HER2) in Cancers: Overexpression and Therapeutic Implications. Mol. Biol. Int. 2014, 9 (2014).
36. Schmidt, M., Hynes, N. E., Groner, B., Wels, W. A bivalent single-chain antibody-toxin specific for ErbB-2 and the EGF receptor. Int. J. Cancer 65, 538-546 (1996).
37. Sinha, L. et al. Quantification of the binding potential of cell-surface receptors in fresh excised specimens via dual-probe modeling of SERS nanoparticles. Sci. Rep. 5, 8582 (2015).
38. Nayak, A., Bhuiya, T. A. Utility of cytokeratin 5/6 and high-molecular-weight keratin in evaluation of cauterized surgical margins in excised specimens of breast ductal carcinoma in situ. Ann. Diagn. Pathol. 15, 243-249 (2011).
39. Garai, E. et al. A Real-Time Clinical Endoscopic System for Intraluminal, Multiplexed Imaging of Surface-Enhanced Raman Scattering Nanoparticles. PLoS ONE 10, e0123185 (2015).
40. Abeytunge, S. et al. Confocal microscopy with strip mosaicing for rapid imaging over large areas of excised tissue. J. Biomed. Opt. 18, 61227 (2013).
41. Gareau, D. S. et al. Confocal mosaicing microscopy in skin excisions: a demonstration of rapid surgical pathology. J. Microsc. 233, 149-159 (2009).
42. Bydlon, T. M. et al. Advancing optical imaging for breast margin assessment: an analysis of excisional time, cautery, and patent blue dye on underlying sources of contrast. PLoS One 7, e51418 (2012).
43. Sharma, V. et al. Auto-fluorescence lifetime and light reflectance spectroscopy for breast cancer diagnosis: potential tools for intraoperative margin detection. Biomed. Opt. Express 3, 1825-1840 (2012).
44. Nichols, B. S. et al. A Quantitative Diffuse Reflectance Imaging (QDRI) System for Comprehensive Surveillance of the Morphological Landscape in Breast Tumor Margins. PLoS One 10, e0127525 (2015).
45. Lo, J. Y. et al. Wavelength Optimization for Quantitative Spectral Imaging of Breast Tumor Margins. PLoS ONE 8, e61767 (2013).
46. Brown, J. Q. et al. Optical spectral surveillance of breast tissue landscapes for detection of residual disease in breast tumor margins. PLoS One 8, e69906 (2013).
47. Keller, M. D. et al. Development of a spatially offset Raman spectroscopy probe for breast tumor surgical margin evaluation. J. Biomed. Opt. 16, 077006 (2011).
48. Liu, C. H. et al. Resonance Raman and Raman spectroscopy for breast cancer detection. Technol. Cancer Res. Treat. 12, 371-382 (2013).
49. Kong, K. et al. Diagnosis of tumors during tissue-conserving surgery with integrated autofluorescence and Raman scattering microscopy. P. Natl. Acad. Sci. USA 110, 15189-15194 (2013).
50. Valdes, E. K., Boolbol, S. K., Cohen, J. M., Feldman, S. M. Intra-operative touch preparation cytology; does it have a role in reexcision lumpectomy? Ann. Surg. Oncol. 14, 1045-1050 (2007).
51. Saarela, A. O., Paloneva, T. K., Rissanen, T. J., Kiviniemi, H. O. Determinants of positive histologic margins and residual tumor after lumpectomy for early breast cancer: a prospective study with special reference to touch preparation cytology. J. Surg. Oncol. 66, 248-253 (1997).
52. Jorns, J. M. et al. Intraoperative frozen section analysis of margins in breast conserving surgery significantly decreases reoperative rates: one-year experience at an ambulatory surgical center. Am. J. Clin. Pathol. 138, 657-669 (2012).
53. Cutter, J. L. et al. Topical Application of Activity-based Probes for Visualization of Brain Tumor Tissue. PLoS ONE 7, e33060 (2012).
54. Wang, D. et al. Microscopic Delineation of Medulloblastoma Margins in a Transgenic Mouse Model Using a Topically Applied VEGFR-1 Probe. Transl. Oncol. 5, 408-414 (2012).
55. Snuderl, M. et al. Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors. Brain Pathol. 23, 73-81 (2013).
56. Yates, L. R. et al. Subclonal diversification of primary breast cancer revealed by multiregion sequencing. Nat. Med. 21, 751-759 (2015).
57. Zardavas, D., Irrthum, A., Swanton, C., Piccart, M. Clinical management of breast cancer heterogeneity. Nat. Rev. Clin. Oncol. 12, 381-394 (2015).
58. Doering, W. E., Piotti, M. E., Natan, M. J., Freeman, R. G. SERS as a Foundation for Nanoscale, Optically Detected Biological Labels. Adv. Mater. 19, 3100-3108 (2007).
59. Van de Sompel, D., Garai, E., Zavaleta, C., Gambhir, S. S. A Hybrid Least Squares and Principal Component Analysis Algorithm for Raman Spectroscopy. PLoS ONE 7, e38850 (2012).