Fluorescence-guided surgery with live molecular navigation-a new cutting edge

Nature Reviews Cancer

Volumn 13, Issue 9, 2013, Pages 653-662

  Nguyen, Quyen T ^a   Tsien, Roger Y ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER SURGERY; FLUORESCENCE GUIDED SURGERY; HEALTH CARE COST; HUMAN; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SURGICAL TECHNIQUE;

FLUORESCENCE; FLUORESCENT DYES; HUMANS; MOLECULAR IMAGING; NEOPLASM, RESIDUAL; NEOPLASMS; OPTICAL IMAGING; PATIENT SELECTION;

EID: 84883192924     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc3566     Document Type: Review

References (74)

1. National Cancer Institute. Previous version: SEER cancer statistics review, 1975-2005 [online], http://seer.cancer.gov/csr/1975-2005 (2008).
2. Haque, R., Contreras, R., McNicoll, M. P., Eckberg, E. C. & Petitti, D. B. Surgical margins and survival after head and neck cancer surgery. BMC Ear Nose Throat Disord. 16, 2 (2006).
3. Singletary, S. Surgical margins in patients with early-stage breast cancer treated with breast conservation therapy. Am. J. Surg. 184, 383-393 (2002).
4. Meric, F. et al. Positive surgical margins and ipsilateral breast tumor recurrence predict disease-specific survival after breast-conserving therapy. Cancer 97, 926-933 (2003).
5. Snijder, R., de la Riviere, A., Elbers, H. & van den Bosch, J. Survival in resected stage I lung cancer with residual tumor at the bronchial resection margin. Ann. Thorac. Surg. 65, 212-216 (1998).
6. Nagtegaal, I. D. & Quirke, P. What is the role for the circumferential margin in the modern treatment of rectal cancer J. Clin. Oncol. 26, 303-312 (2008).
7. Dotan, Z. et al. Positive surgical margins in soft tissue following radical cystectomy for bladder cancer and cancer specific survival. J. Urol. 178, 2308-2312 (2007).
8. Wieder, J. A. & Soloway, M. S. Incidence, etiology, location, prevention and treatment of positive surgical margins after radical prostatectomy for prostate cancer. J. Urol. 160, 299-315 (1998).
9. Kumar, A., Puri, R., Gadgil, P. V. & Jatoi, I. Sentinel lymph node biopsy in primary breast cancer: window to management of the axilla. World J. Surg. 36, 1453-1459 (2012).
10. Wong, S. L. et al. Sentinel lymph node biopsy for melanoma: American Society of Clinical Oncology and Society of Surgical Oncology joint clinical practice guideline. J. Clin. Oncol. 30, 2912-2918 (2012).
11. Hutteman, M. et al. Randomized, double-blind comparison of indocyanine green with or without albumin premixing for near-infrared fluorescence imaging of sentinel lymph nodes in breast cancer patients. Breast Cancer Res. Treat. 127, 163-170 (2011).
12. van der Vorst, J. R. et al. Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99m technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients. Ann. Surg. Oncol. 19, 4104-4111 (2012).
13. Emerson, D. K. et al. A receptor-targeted fluorescent radiopharmaceutical for multireporter sentinel lymph node imaging. Radiology 265, 186-193 (2012).
14. Joseph, M., Phillips, M., Farrell, T. M. & Rupp, C. C. Can residents safely and efficiently be taught single incision laparoscopic cholecystectomy J. Surg. Educ. 69, 468-472 (2012).
15. Kandil, E. H., Noureldine, S. I., Yao, L. & Slakey, D. P. Robotic transaxillary thyroidectomy: an examination of the first one hundred cases. J. Am. Coll. Surg. 214, 558-564 (2012).
16. Lee, J. C., Jang, H. D. & Shin, B. J. Learning curve and clinical outcomes of minimally invasive transforaminal lumbar interbody fusion: our experience in 86 consecutive cases. Spine 37, 1548-1557 (2012).
17. Pappo, I. et al. Diagnostic performance of a novel device for real-time margin assessment in lumpectomy specimens. J. Surg. Res. 160, 277-281 (2010).
18. Rivera, R. J., Holmes, D. R. & Tafra, L. Analysis of the impact of intraoperative margin assessment with adjunctive use of MarginProbe versus standard of care on tissue volume removed. Int. J. Surg. Oncol. 2012, 868623 (2012).
19. Dotan, Z. A. et al. Detection of prostate cancer by radio-frequency near-field spectroscopy in radical prostatectomy ex vivo specimens. Prostate Cancer Prostatic Dis. 16, 73-78 (2012).
20. Pavlova, I. et al. Multiphoton microscopy and microspectroscopy for diagnostics of inflammatory and neoplastic lung. J. Biomed. Opt. 17, 036014 (2012).
21. Pierce, M. C. et al. Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia. Cancer Prev. Res. 5, 801-809 (2012).
22. Gurtner, G. C. et al. Intraoperative laser angiography using the SPY system: review of the literature and recommendations for use. Ann. Surg. Innov. Res. 7, 1 (2013).
23. Kuroda, K. et al. Intra-arterial injection fluorescein videoangiography in aneurysm surgery. Neurosurgery 72, 141-150 (2012).
24. Shin, D., Vigneswaran, N., Gillenwater, A. & Richards-Kortum, R. Advances in fluorescence imaging techniques to detect oral cancer and its precursors. Future Oncol. 6, 1143-1154 (2010).
25. Foersch, S. et al. Confocal laser endomicroscopy for diagnosis and histomorphologic imaging of brain tumors in vivo. PLoS ONE 7, e41760 (2012).
26. Vila, P. M. et al. Discrimination of benign and neoplastic mucosa with a High-Resolution Microendoscope (HRME) in head and neck cancer. Ann. Surg. Oncol. 19, 3534-3539 (2012).
27. Barker, F. G. et al. Survival and functional status after resection of recurrent glioblastoma multiforme. Neurosurgery 42, 709-720 (1998).
28. Swindle, P. et al. Do margins matter The prognostic significance of positive surgical margins in radical prostatectomy specimens. J. Urol. 179, S47-S51 (2008).
29. Warner, J. N. et al. Impact of margin status at 37 months after robot assisted radical prostatectomy. Can. J. Urol. 18, 6043-6049 (2011).
30. Chalfin, H. J. et al. Impact of surgical margin status on prostate-cancer-specific mortality. BJU Int. 110, 1684-1689 (2012).
31. Pleijhuis, R. G. et al. Obtaining adequate surgical margins in breast-conserving therapy for patients with early-stage breast cancer: current modalities and future directions. Ann. Surg. Oncol. 16, 2717-2730 (2009).
32. Atkins, J. et al. Positive margin rates following breast-conserving surgery for stage I-III breast cancer: palpable versus nonpalpable tumors. J. Surg. Res. 177, 109-115 (2012).
33. Cutter, J. L. et al. Topical application of activity-based probes for visualization of brain tumor tissue. PLoS ONE 7, e33060 (2012).
34. Verdoes, M. et al. A nonpeptidic cathepsin S activity-based probe for noninvasive optical imaging of tumor-associated macrophages. Chem. Biol. 19, 619-628 (2012).
35. Sheth, R. A. et al. Improved detection of ovarian cancer metastases by intraoperative quantitative fluorescence protease imaging in a pre-clinical model. Gynecol. Oncol. 112, 616-622 (2009).
36. Nguyen, Q. T. et al. Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival. Proc. Natl Acad. Sci. USA 107, 4317-4322 (2010).
37. Jiang, T. et al. Tumor imaging by means of proteolytic activation of cell-penetrating peptides. Proc. Natl Acad. Sci. USA 101, 17867-17872 (2004).
38. Olson, E. S. et al. In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer. Integr. Biol. 1, 382-393 (2009).
39. Aguilera, T. A., Olson, E. S., Timmers, M. M., Jiang, T. & Tsien, R. Y. Systemic in vivo distribution of activatable cell penetrating peptides is superior to that of cell penetrating peptides. Integr. Biol. 1, 371-381 (2009).
40. Savariar, E. N. et al. Real-time in vivo molecular detection of primary tumors and metastases with ratiometric activatable cell-penetrating peptides. Cancer Res. 73, 855-864 (2013).
41. Nakajima, T. et al. Targeted, activatable, in vivo fluorescence imaging of prostate-specific membrane antigen (PSMA) positive tumors using the quenched humanized J591 antibody-indocyanine green (ICG) conjugate. Bioconjug. Chem. 22, 1700-1705 (2011).
42. Tran Cao, H. S. et al. Tumor-specific fluorescence antibody imaging enables accurate staging laparoscopy in an orthotopic model of pancreatic cancer. Hepatogastroenterology 59, 1994-1999 (2012).
43. McElroy, M. et al. Imaging of primary and metastatic pancreatic cancer using a fluorophore-conjugated anti-CA19-9 antibody for surgical navigation. World J. Surg. 32, 1057-1066 (2008).
44. Hall, M. A. et al. Comparison of mAbs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: quantitative small-animal PET/CT and NIRF. J. Nucl. Med. 53, 1427-1437 (2012).
45. Rosbach, K. J., Williams, M. D., Gillenwater, A. M. & Richards-Kortum, R. R. Optical molecular imaging of multiple biomarkers of epithelial neoplasia: epidermal growth factor receptor expression and metabolic activity in oral mucosa. Transl Oncol. 5, 160-171 (2012).
46. Urano, Y. et al. Rapid cancer detection by topically spraying a -glutamyltranspeptidase-activated fluorescent probe. Sci. Transl Med. 3, 110ra119 (2011).
47. van Dam, G. M. et al. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor- targeting: first in-human results. Nature Med. 17, 1315-1319 (2011).
48. Stummer, W. et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 7, 392-401 (2006).
49. Stummer, W. et al. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J. Neurosurg. 93, 1003-1013 (2000).
50. Kalli, K. R. et al. Folate receptor as a tumor target in epithelial ovarian cancer. Gynecol. Oncol. 108, 619-626 (2008).
51. Schafer, C. et al. Glutamyl transferase expression in higher-grade astrocytic glioma. Acta Oncol. 40, 529-535 (2001).
52. Floeth, F. W. et al. Comparison of 18F-FET PET and 5-ALA fluorescence in cerebral gliomas. Eur. J. Nucl. Med. Mol. Imaging 38, 731-741 (2011).
53. Sun, C. et al. Tumor-targeted drug delivery and MRI contrast enhancement by chlorotoxin-conjugated iron oxide nanoparticles. Nanomed. 3, 495-505 (2008).
54. Sun, C. et al. In vivo MRI detection of gliomas by chlorotoxin-conjugated superparamagnetic nanoprobes. Small 4, 372-379 (2008).
55. Olson, E. S. et al. Activatable cell penetrating peptides linked to nanoparticles as dual probes for in vivo fluorescence and MR imaging of proteases. Proc. Natl Acad. Sci. USA 107, 4311-4316 (2010).
56. Gibbs-Strauss, S. L. et al. Nerve-highlighting fluorescent contrast agents for image-guided surgery. Mol. Imaging 10, 91-101 (2011).
57. Whitney, M. et al. Fluorescent peptides highlight peripheral nerves during surgery in mice. Nature Biotech. 29, 352-356 (2011).
58. Sturm, M. B. et al. Targeted imaging of esophageal neoplasia with a fluorescently labeled peptide: first-in-human results. Sci. Transl Med. 5, 184ra61 (2013).
59. Blum, G., von Degenfeld, G., Merchant, M. J., Blau, H. M. & Bogyo, M. Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes. Nature Chem. Biol. 3, 668-677 (2007).
60. Figueiredo, J. L., Alencar, H., Weissleder, R. & Mahmood, U. Near infrared thoracoscopy of tumoral protease activity for improved detection of peripheral lung cancer. Int. J. Cancer 118, 2672-2677 (2006).
61. Kelly, K., Alencar, H., Funovics, M., Mahmood, U. & Weissleder, R. Detection of invasive colon cancer using a novel, targeted, library-derived fluorescent peptide. Cancer Res. 64, 6247-6251 (2004).
62. Veiseh, M. et al. Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res. 67, 6882-6888 (2007).
63. Stroud, M. R., Hansen, S. J. & Olson, J. M. In vivo bio-imaging using chlorotoxin-based conjugates. Curr. Pharm. Des. 17, 4362-4371 (2011).
64. Ye, Y. et al. Near-infrared fluorescent divalent RGD ligand for integrin v3-targeted optical imaging. Bioorg. Med. Chem. Lett. 22, 5405-5409 (2012).
65. Gao, J. et al. A novel clinically translatable fluorescent nanoparticle for targeted molecular imaging of tumors in living subjects. Nano Lett. 12, 281-286 (2012).
66. Zhu, L. et al. Dual-functional, receptor-targeted fluorogenic probe for in vivo imaging of extracellular protease expressions. Bioconjugate Chem. 22, 1001-1005 (2011).
67. Wu, A. P. et al. Improved facial nerve identification with novel fluorescently labeled probe. Laryngoscope 121, 805-810 (2011).
68. Cotero, V. E. et al. Intraoperative fluorescence imaging of peripheral and central nerves through a myelin-selective contrast agent. Mol. Imaging Biol. 14, 708-717 (2012).
69. Tsien, R. Y. & Harootunian, A. T. Practical design criteria for a dynamic ratio imaging system. Cell Calcium 11, 93-109 (1990).
70. Orosco, R. K., Tsien, R. Y. & Nguyen, Q. T. Fluorescence imaging in surgery. IEEE Rev. Biomed. Eng. 6, 178-187 (2013).
71. Taruttis, A. & Ntziachristos, V. Translational optical imaging. Am. J. Roentgenol. 199, 263-271 (2012).
72. Nunn, A. D. The cost of developing imaging agents for routine clinical use. Invest. Radiol. 41, 206-212 (2006).
73. Mitsunaga, M. et al. Fluorescence endoscopic detection of murine colitis-associated colon cancer by topically applied enzymatically rapid-activatable probe. Gut 62, 1179-1186 (2013).
74. Ashitate, Y. et al. Simultaneous assessment of luminal integrity and vascular perfusion of the gastrointestinal tract using dual-channel near-infrared fluorescence. Mol. Imaging 11, 301-308 (2012).