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Molecular Imaging and Biology
Published in: Molecular Imaging and Biology 2/2019

01-04-2019 | Review Article

Fluorescence Guidance in Surgical Oncology: Challenges, Opportunities, and Translation

Published in: Molecular Imaging and Biology | Issue 2/2019

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Abstract

Surgical resection continues to function as the primary treatment option for most solid tumors. However, the detection of cancerous tissue remains predominantly subjective and reliant on the expertise of the surgeon. Surgery that is guided by fluorescence imaging has shown clinical relevance as a new approach to detecting the primary tumor, tumor margins, and metastatic lymph nodes. It is a technique to reduce recurrence and increase the possibility of a curative resection. While significant progress has been made in developing this emerging technology as a tool to assist the surgeon, further improvements are still necessary. Refining imaging agents and tumor targeting strategies to be a precise and reliable surgical strategy is essential in order to translate this technology into patient care settings. This review seeks to provide a comprehensive update on the most recent progress of fluorescence-guided surgery and its translation into the clinic. By highlighting the current status and recent developments of fluorescence image-guided surgery in the field of surgical oncology, we aim to offer insight into the challenges and opportunities that require further investigation.
Literature
1.
Stewart B, Wild C (2014) World cancer report 2014. International Agency for Research on Cancer
2.
3.
4.
5.
Keating J, Tchou J, Okusanya O, Fisher C, Batiste R, Jiang J, Kennedy G, Nie S, Singhal S (2016) Identification of breast cancer margins using intraoperative near-infrared imaging. J Surg Oncol 113:508–514CrossRefPubMed
6.
Madajewski B, Judy BF, Mouchli A, Kapoor V, Holt D, Wang MD, Nie S, Singhal S (2012) Intraoperative near-infrared imaging of surgical wounds after tumor resections can detect residual disease. Clin Cancer Res 18:5741–5751CrossRefPubMedPubMedCentral
7.
8.
Witkowski ER, Smith JK, Tseng JF (2013) Outcomes following resection of pancreatic cancer. J Surg Oncol 107:97–103CrossRefPubMed
9.
Shaib Y, Davila J, Naumann C, El-Serag H (2007) The impact of curative intent surgery on the survival of pancreatic Cancer patients: a U.S. population-based study. Am J Gastroenterol 102:1377–1382CrossRefPubMed
10.
11.
Tamburrino D, Partelli S, Crippa S, Manzoni A, Maurizi A, Falconi M (2014) Selection criteria in resectable pancreatic cancer: a biological and morphological approach. World J Gastroenterol 20:11210–11215CrossRefPubMedPubMedCentral
12.
13.
14.
Sehouli J, Grabowski JP (2017) Surgery for recurrent ovarian cancer: options and limits. Best Pract Res Clin Obstet Gynaecol 41:88–95CrossRefPubMed
15.
Liberale G, Vankerckhove S, Gomez Caldon M et al (2016) Fluorescence imaging after indocyanine green injection for detection of peritoneal metastases in patients undergoing cytoreductive surgery for peritoneal carcinomatosis from colorectal cancer: a pilot study. Ann Surg 264:1110–1115CrossRefPubMed
16.
Hoogstins CE, Weixler B, Boogerd LS et al (2017) In search for optimal targets for intraoperative fluorescence imaging of peritoneal metastasis from colorectal cancer. Biomark Cancer 9:1179299X1772825CrossRef
17.
18.
Gibbs-Strauss SL, Nasr K, Fish KM, Khullar O, Ashitate Y, Siclovan TM, Johnson BF, Barnhardt NE, Tan Hehir CA, Frangioni JV (2011) Nerve-highlighting fluorescent contrast agents for image-guided surgery. Mol Imaging 10:91–101CrossRefPubMed
19.
Hussain T, Mastrodimos MB, Raju SC, Glasgow HL, Whitney M, Friedman B, Moore JD, Kleinfeld D, Steinbach P, Messer K, Pu M, Tsien RY, Nguyen QT (2015) Fluorescently labeled peptide increases identification of degenerated facial nerve branches during surgery and improves functional outcome. PLoS One 10:e0119600CrossRefPubMedPubMedCentral
20.
Hussain T, Nguyen LT, Whitney M, Hasselmann J, Nguyen QT (2016) Improved facial nerve identification during parotidectomy with fluorescently labeled peptide. Laryngoscope 126:2711–2717CrossRefPubMedPubMedCentral
21.
Whitney MA, Crisp JL, Nguyen LT, Friedman B, Gross LA, Steinbach P, Tsien RY, Nguyen QT (2011) Fluorescent peptides highlight peripheral nerves during surgery in mice. Nat Biotechnol 29:352–356CrossRefPubMedPubMedCentral
22.
He K, Zhou J, Yang F, Chi C, Li H, Mao Y, Hui B, Wang K, Tian J, Wang J (2018) Near-infrared intraoperative imaging of thoracic sympathetic nerves: from preclinical study to clinical trial. Theranostics 8:304–313CrossRefPubMedPubMedCentral
23.
Hong G, Antaris AL, Dai H (2017) Near-infrared fluorophores for biomedical imaging. Nat Biomed Eng 1:10CrossRef
24.
Ferraro N, Barbarite E, Albert TR, Berchmans E, Shah AH, Bregy A, Ivan ME, Brown T, Komotar RJ (2016) The role of 5-aminolevulinic acid in brain tumor surgery: a systematic review. Neurosurg Rev 39:545–555CrossRefPubMed
25.
Zhao S, Wu J, Wang C, Liu H, Dong X, Shi C, Shi C, Liu Y, Teng L, Han D, Chen X, Yang G, Wang L, Shen C, Li H (2013) Intraoperative fluorescence-guided resection of high-grade malignant gliomas using 5-aminolevulinic acid–induced porphyrins: a systematic review and meta-analysis of prospective studies. PLoS One 8:e63682CrossRefPubMedPubMedCentral
26.
Hadjipanayis CG, Widhalm G, Stummer W (2015) What is the surgical benefit of utilizing 5-aminolevulinic acid for fluorescence-guided surgery of malignant gliomas? Neurosurgery 77:663–673CrossRefPubMed
27.
Moiyadi A, Syed P, Srivastava S (2014) Fluorescence-guided surgery of malignant gliomas based on 5-aminolevulinic acid: paradigm shifts but not a panacea. Nat Rev Cancer 14:146–146CrossRefPubMed
28.
Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ (2000) Fluorescence-guided resection of glioblastoma multiforme utilizing 5-ALA-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 93:1003–1013CrossRefPubMed
29.
Stummer W, Tonn J-C, Goetz C, Ullrich W, Stepp H, Bink A, Pietsch T, Pichlmeier U (2014) 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 20CrossRefPubMed
30.
Thevarajah S, Huston TL, Simmons RM (2005) A comparison of the adverse reactions associated with isosulfan blue versus methylene blue dye in sentinel lymph node biopsy for breast cancer. Am J Surg 189:236–239CrossRefPubMed
31.
Kidd SA, Lancaster PAL, Anderson JC et al (1996) Fetal death after exposure to methylene blue dye during mid-trimester amniocentesis in twin pregnancy. Prenat Diagn 16:39–47CrossRefPubMed
32.
Zhang RR, Schroeder AB, Grudzinski JJ, Rosenthal EL, Warram JM, Pinchuk AN, Eliceiri KW, Kuo JS, Weichert JP (2017) Beyond the margins: real-time detection of cancer using targeted fluorophores. Nat Rev Clin Oncol 14:347–364CrossRefPubMedPubMedCentral
33.
Verbeek FPR, van der Vorst JR, Schaafsma BE, Swijnenburg RJ, Gaarenstroom KN, Elzevier HW, van de Velde CJH, Frangioni JV, Vahrmeijer AL (2013) Intraoperative near infrared fluorescence guided identification of the ureters using low dose methylene blue: a first in human experience. J Urol 190:574–579CrossRefPubMedPubMedCentral
34.
Dip FD, Moreira Grecco AD, Nguyen D, Sarotto L, Perrins S, Rosenthal RJ (2015) Ureter identification using methylene blue and fluorescein. In: Fluorescence imaging for surgeons. Springer International Publishing, Cham, pp 327–332
35.
Seif C, Martínez Portillo FJ, Osmonov DK, Böhler G, van der Horst C, Leissner J, Hohenfellner R, Juenemann KP, Braun PM (2004) Methylene blue staining for nerve-sparing operative procedures: an animal model. Urology 63:1205–1208CrossRefPubMed
36.
Osorio JA, Breshears JD, Arnaout O, Simon NG, Hastings-Robinson AM, Aleshi P, Kliot M (2015) Ultrasound-guided percutaneous injection of methylene blue to identify nerve pathology and guide surgery. Neurosurg Focus 39:E2CrossRefPubMed
37.
Candell L, Campbell MJ, Shen WT, Gosnell JE, Clark OH, Duh QY (2014) Ultrasound-guided methylene blue dye injection for parathyroid localization in the reoperative neck. World J Surg 38:88–91CrossRefPubMed
38.
Kir G, Alimoglu O, Sarbay BC, Bas G (2014) Ex vivo intra-arterial methylene blue injection in the operation theater may improve the detection of lymph node metastases in colorectal cancer. Pathol Res Pract 210:818–821CrossRefPubMed
39.
Tummers QRJG, Schepers A, Hamming JF, Kievit J, Frangioni JV, van de Velde CJH, Vahrmeijer AL (2015) Intraoperative guidance in parathyroid surgery using near-infrared fluorescence imaging and low-dose methylene blue. Surgery 158:1323–1330CrossRefPubMed
40.
van der Vorst JR, Schaafsma BE, Verbeek FPR, Swijnenburg RJ, Tummers QRJG, Hutteman M, Hamming JF, Kievit J, Frangioni JV, van de Velde CJH, Vahrmeijer AL (2014) Intraoperative near-infrared fluorescence imaging of parathyroid adenomas with use of low-dose methylene blue. Head Neck 36:853–858CrossRefPubMed
41.
van der Vorst JR, Vahrmeijer AL, Hutteman M, Bosse T, Smit VT, van de Velde C, Frangioni JV, Bonsing BA (2012) Near-infrared fluorescence imaging of a solitary fibrous tumor of the pancreas using methylene blue. World J Gastrointest Surg 4:180–184CrossRefPubMedPubMedCentral
42.
Chu M, Wan Y (2009) Sentinel lymph node mapping using near-infrared fluorescent methylene blue. J Biosci Bioeng 107:455–459CrossRefPubMed
43.
Schaafsma BE, Mieog JSD, Hutteman M, van der Vorst JR, Kuppen PJK, Löwik CWGM, Frangioni JV, van de Velde CJH, Vahrmeijer AL (2011) The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol 104:323–332CrossRefPubMedPubMedCentral
44.
Marshall MV, Rasmussen JC, Tan I-C, Aldrich MB, Adams KE, Wang X, Fife CE, Maus EA, Smith LA, Sevick-Muraca EM (2010) Near-infrared fluorescence imaging in humans with Indocyanine green: a review and update. Open Surg Oncol J 2:12–25CrossRefPubMedPubMedCentral
45.
Namikawa T, Sato T, Hanazaki K (2015) Recent advances in near-infrared fluorescence-guided imaging surgery using indocyanine green. Surg Today 45:1467–1474CrossRefPubMed
46.
Pitsinis V, Provenzano E, Kaklamanis L, Wishart GC, Benson JR (2015) Indocyanine green fluorescence mapping for sentinel lymph node biopsy in early breast cancer. Surg Oncol 24:375–379CrossRefPubMed
47.
Sugie T, Kassim KA, Takeuchi M, Hashimoto T, Yamagami K, Masai Y, Toi M (2010) A novel method for sentinel lymph node biopsy by indocyanine green fluorescence technique in breast cancer. Cancers (Basel) 2:713–720CrossRef
48.
Vahrmeijer AL, Hutteman M, van der Vorst JR, van de Velde CJH, Frangioni JV (2013) Image-guided cancer surgery using near-infrared fluorescence. Nat Rev Clin Oncol 10:507–518CrossRefPubMedPubMedCentral
49.
Hill TK, Abdulahad A, Kelkar SS, Marini FC, Long TE, Provenzale JM, Mohs AM (2015) Indocyanine green-loaded nanoparticles for image-guided tumor surgery. Bioconjug Chem 26:294–303CrossRefPubMedPubMedCentral
50.
Kraft JC, Ho RJY (2014) Interactions of Indocyanine green and lipid in enhancing near-infrared fluorescence properties: the basis for near-infrared imaging in Vivo. Biochemistry 53:1275–1283CrossRefPubMed
51.
Moore LS, Rosenthal EL, Chung TK, de Boer E, Patel N, Prince AC, Korb ML, Walsh EM, Young ES, Stevens TM, Withrow KP, Morlandt AB, Richman JS, Carroll WR, Zinn KR, Warram JM (2017) Characterizing the utility and limitations of repurposing an open-field optical imaging device for fluorescence-guided surgery in head and neck Cancer patients. J Nucl Med 58:246–251CrossRefPubMedPubMedCentral
52.
Korb ML, Hartman YE, Kovar J et al (2014) Use of monoclonal antibody-IRDye800CW bioconjugates in the resection of breast cancer HHS public access. J Surg Res 111:119–128CrossRef
53.
Rosenthal EL, Warram JM, de Boer E, Chung TK, Korb ML, Brandwein-Gensler M, Strong TV, Schmalbach CE, Morlandt AB, Agarwal G, Hartman YE, Carroll WR, Richman JS, Clemons LK, Nabell LM, Zinn KR (2015) Safety and tumor specificity of cetuximab-IRDye800 for surgical navigation in head and neck cancer. Clin Cancer Res 21:3658–3666CrossRefPubMedPubMedCentral
54.
Tansi FL, Rüger R, Rabenhold M, et al (2015) Fluorescence-quenching of a liposomal-encapsulated near-infrared fluorophore as a tool for in vivo optical imaging. J Vis Exp e52136
55.
Lisy M-R, Goermar A, Thomas C, Pauli J, Resch-Genger U, Kaiser WA, Hilger I (2008) In vivo near-infrared fluorescence imaging of carcinoembryonic antigen–expressing tumor cells in mice. Radiology 247:779–787CrossRefPubMed
56.
Pauli J, Brehm R, Spieles M, Kaiser WA, Hilger I, Resch-Genger U (2010) Novel fluorophores as building blocks for optical probes for in vivo near infrared fluorescence (NIRF) imaging. J Fluoresc 20:681–693CrossRefPubMed
57.
Luo S, Zhang E, Su Y, Cheng T, Shi C (2011) A review of NIR dyes in cancer targeting and imaging. Biomaterials 32:7127–7138CrossRefPubMed
58.
Pansare VJ, Hejazi S, Faenza WJ, Prud’homme RK (2012) Review of long-wavelength optical and NIR imaging materials: contrast agents, fluorophores, and multifunctional nano carriers. Chem Mater 24:812–827CrossRefPubMedPubMedCentral
59.
60.
Moore GE, Peyton WT, French LA, Walker WW (1948) The clinical use of fluorescein in neurosurgery. J Neurosurg 5:392–398CrossRefPubMed
61.
Dilek O, Ihsan A, Tulay H (2011) Anaphylactic reaction after fluorescein sodium administration during intracranial surgery. J Clin Neurosci 18:430–431CrossRefPubMed
62.
Tanahashi S, Iida H, Dohi S (1995) An anaphylactoid reaction after administration of fluorescein sodium during neurosurgery. Can J Anaesth 42:181–185
63.
64.
Ji X, Peng F, Zhong Y, Su Y, He Y (2014) Fluorescent quantum dots: synthesis, biomedical optical imaging, and biosafety assessment. Colloids Surfaces B Biointerfaces 124:132–139CrossRefPubMed
65.
66.
Hill TK, Mohs AM (2016) Image-guided tumor surgery: will there be a role for fluorescent nanoparticles? Wiley Interdiscip Rev Nanomed Nanobiotechnol 8:498–511CrossRefPubMed
67.
Gioux S, Kianzad V, Ciocan R, Gupta S, Oketokoun R, Frangioni JV (2009) High-power, computer-controlled, light-emitting diode-based light sources for fluorescence imaging and image-guided surgery. Mol Imaging 8:156–165CrossRefPubMed
68.
Gioux S, Choi HS, Frangioni JV (2010) Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging 9:237–255CrossRefPubMed
69.
DSouza AV, Lin H, Henderson ER, Samkoe KS, Pogue BW (2016) Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging. J Biomed Opt 21:80901CrossRefPubMed
70.
Zhu B, Sevick-Muraca EM (2015) A review of performance of near-infrared fluorescence imaging devices used in clinical studies. Br J Radiol 88:20140547CrossRefPubMed
71.
Matsumura Y, Maeda H, Jain RK et al (1986) A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res 46:6387–6392PubMed
72.
Bertrand N, Wu J, Xu X, Kamaly N, Farokhzad OC (2014) Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv Drug Deliv Rev 66:2–25CrossRefPubMed
73.
Maeda H, Tsukigawa K, Fang J (2016) A retrospective 30 years after discovery of the enhanced permeability and retention effect of solid tumors: next-generation chemotherapeutics and photodynamic therapy-problems, solutions, and prospects. Microcirculation 23:173–182CrossRefPubMed
74.
Kharaishvili G, Simkova D, Bouchalova K, Gachechiladze M, Narsia N, Bouchal J (2014) The role of cancer-associated fibroblasts, solid stress and other microenvironmental factors in tumor progression and therapy resistance. Cancer Cell Int 14:41CrossRefPubMedPubMedCentral
75.
Fang J, Nakamura H, Maeda H (2011) The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv Drug Deliv Rev 63:136–151CrossRefPubMed
76.
77.
Bergers G, Benjamin LE (2003) Angiogenesis: tumorigenesis and the angiogenic switch. Nat Rev Cancer 3:401–410CrossRefPubMed
78.
Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, McDonald DM (2002) Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160:985–1000CrossRefPubMedPubMedCentral
79.
Padera TP, Kadambi A, di Tomaso E, Carreira CM, Brown EB, Boucher Y, Choi NC, Mathisen D, Wain J, Mark EJ, Munn LL, Jain RK (2002) Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296:1883–1886CrossRefPubMed
80.
81.
Maeda H (2012) Macromolecular therapeutics in cancer treatment: the EPR effect and beyond. J Control Release 164:138–144CrossRefPubMed
82.
Nakamura H, Etrych T, Chytil P, Ohkubo M, Fang J, Ulbrich K, Maeda H (2014) Two step mechanisms of tumor selective delivery of N-(2-hydroxypropyl)methacrylamide copolymer conjugated with pirarubicin via an acid-cleavable linkage. J Control Release 174:81–87CrossRefPubMed
83.
Kobayashi H, Watanabe R, Choyke PL (2013) Improving conventional enhanced permeability and retention (EPR) effects; what is the appropriate target? Theranostics 4:81–89CrossRefPubMedPubMedCentral
84.
Nakamura Y, Mochida A, Choyke PL, Kobayashi H (2016) Nanodrug delivery: is the enhanced permeability and retention effect sufficient for curing cancer? Bioconjug Chem 27:2225–2238CrossRefPubMedPubMedCentral
85.
86.
Padera TP, Stoll BR, Tooredman JB, Capen D, Tomaso E, Jain RK (2004) Pathology: cancer cells compress intratumour vessels. Nature 427:695–695CrossRefPubMed
87.
88.
Heldin C-H, Rubin K, Pietras K, Östman A (2004) High interstitial fluid pressure — an obstacle in cancer therapy. Nat Rev Cancer 4:806–813CrossRefPubMed
89.
Baxter LT, Jain’ RK (1989) Transport of fluid and macromolecules in tumors I. Role of interstitial pressure and convection. Microvasc Res 37:77–104CrossRefPubMed
90.
Wu M, Frieboes HB, Chaplain MAJ, McDougall SR, Cristini V, Lowengrub JS (2014) The effect of interstitial pressure on therapeutic agent transport: coupling with the tumor blood and lymphatic vascular systems. J Theor Biol 355:194–207CrossRefPubMedPubMedCentral
91.
Miao L, Lin CM, Huang L (2015) Stromal barriers and strategies for the delivery of nanomedicine to desmoplastic tumors. J Control Release 219:192–204CrossRefPubMedPubMedCentral
92.
93.
Durymanov MO, Rosenkranz AA, Sobolev AS (2015) Current approaches for improving Intratumoral accumulation and distribution of nanomedicines. Theranostics 5:1007–1020CrossRefPubMedPubMedCentral
94.
Ojha T, Pathak V, Shi Y, et al (2017) Pharmacological and physical vessel modulation strategies to improve EPR-mediated drug targeting to tumors. Advanced Drug Delivery Reviews 119:44–60
95.
Yokoi K, Tanei T, Godin B, van de Ven AL, Hanibuchi M, Matsunoki A, Alexander J, Ferrari M (2014) Serum biomarkers for personalization of nanotherapeutics-based therapy in different tumor and organ microenvironments. Cancer Lett 345:48–55CrossRefPubMed
96.
Yokoi K, Kojic M, Milosevic M, Tanei T, Ferrari M, Ziemys A (2014) Capillary-wall collagen as a biophysical marker of nanotherapeutic permeability into the tumor microenvironment. Cancer Res 74:4239–4246CrossRefPubMedPubMedCentral
97.
Bolkestein M, de Blois E, Koelewijn SJ, Eggermont AMM, Grosveld F, de Jong M, Koning GA (2016) Investigation of factors determining the enhanced permeability and retention effect in subcutaneous xenografts. J Nucl Med 57:601–607CrossRefPubMed
98.
Miller J, Wang ST, Orukari I, Prior J, Sudlow G, Su X, Liang K, Tang R, Hillman EMC, Weilbaecher KN, Culver JP, Berezin MY, Achilefu S (2017) Perfusion-based fluorescence imaging method delineates diverse organs and identifies multifocal tumors using generic near infrared molecular probes. J Biophotonics 11:e201700232. https://​doi.​org/​10.​1002/​jbio.​201700232 CrossRef
99.
Srinivasarao M, Galliford CV, Low PS (2015) Principles in the design of ligand-targeted cancer therapeutics and imaging agents. Nat Rev Drug Discov 14:203–219CrossRefPubMed
100.
Choi HS, Gibbs SL, Lee JH, Kim SH, Ashitate Y, Liu F, Hyun H, Park GL, Xie Y, Bae S, Henary M, Frangioni JV (2013) Targeted zwitterionic near-infrared fluorophores for improved optical imaging. Nat Biotechnol 31:148–153CrossRefPubMed
101.
102.
Warram JM, de Boer E, Sorace AG, Chung TK, Kim H, Pleijhuis RG, van Dam GM, Rosenthal EL (2014) Antibody-based imaging strategies for cancer. Cancer Metastasis Rev 33:809–822CrossRefPubMedPubMedCentral
103.
Hiroshima Y, Lwin TM, Murakami T, Mawy AA, Kuniya T, Chishima T, Endo I, Clary BM, Hoffman RM, Bouvet M (2016) Effective fluorescence-guided surgery of liver metastasis using a fluorescent anti-CEA antibody. J Surg Oncol 114:951–958CrossRefPubMedPubMedCentral
104.
Lwin TM, Murakami T, Miyake K et al (2018) Tumor-specific labeling of pancreatic cancer using a humanized anti-CEA antibody conjugated to a near-infrared fluorophore. Ann Surg Oncol:1–7
105.
Moore LS, Rosenthal EL, de Boer E, Prince AC, Patel N, Richman JM, Morlandt AB, Carroll WR, Zinn KR, Warram JM (2017) Effects of an unlabeled loading dose on tumor-specific uptake of a fluorescently labeled antibody for optical surgical navigation. Mol Imaging Biol 19:610–616CrossRefPubMedPubMedCentral
106.
107.
Kobayashi H, Choyke PL, Ogawa M (2016) Monoclonal antibody-based optical molecular imaging probes; considerations and caveats in chemistry, biology and pharmacology. Curr Opin Chem Biol 33:32–38CrossRefPubMedPubMedCentral
108.
Mazzocco C, Fracasso G, Germain-Genevois C, Dugot-Senant N, Figini M, Colombatti M, Grenier N, Couillaud F (2016) In vivo imaging of prostate cancer using an anti-PSMA scFv fragment as a probe. Sci Rep 6:23314CrossRefPubMedPubMedCentral
109.
Sonn GA, Behesnilian AS, Jiang ZK, Zettlitz KA, Lepin EJ, Bentolila LA, Knowles SM, Lawrence D, Wu AM, Reiter RE (2016) Fluorescent image-guided surgery with an anti-prostate stem cell antigen (PSCA) diabody enables targeted resection of mouse prostate cancer xenografts in real time. Clin Cancer Res 22:1403–1412CrossRefPubMed
110.
Owens B (2017) Faster, deeper, smaller—the rise of antibody-like scaffolds. Nat Biotechnol 35:602–603CrossRefPubMed
111.
Sexton K, Tichauer K, Samkoe KS, Gunn J, Hoopes PJ, Pogue BW (2013) Fluorescent affibody peptide penetration in glioma margin is superior to full antibody. PLoS One 8:e60390CrossRefPubMedPubMedCentral
112.
de Souza ALR, Marra K, Gunn J, Samkoe KS, Hoopes PJ, Feldwisch J, Paulsen KD, Pogue BW (2017) Fluorescent affibody molecule administered in vivo at a microdose level labels EGFR expressing glioma tumor regions. Mol Imaging Biol 19:41–48CrossRefPubMed
113.
Samkoe KS, Gunn JR, Marra K, Hull SM, Moodie KL, Feldwisch J, Strong TV, Draney DR, Hoopes PJ, Roberts DW, Paulsen K, Pogue BW (2017) Toxicity and pharmacokinetic profile for single-dose injection of ABY-029: a fluorescent anti-EGFR synthetic affibody molecule for human use. Mol Imaging Biol 19:512–521CrossRefPubMedPubMedCentral
114.
115.
Debie P, Vanhoeij M, Poortmans N et al (2017) Improved debulking of peritoneal tumor implants by near-infrared fluorescent nanobody image guidance in an experimental mouse model. Mol Imaging Biol:1–7
116.
117.
Sun X, Li Y, Liu T et al (2017) Peptide-based imaging agents for cancer detection. Adv Drug Deliv Rev 110–111:38–51CrossRefPubMed
118.
Handgraaf HJM, Boonstra MC, Prevoo HAJM, Kuil J, Bordo MW, Boogerd LSF, Sibinga Mulder BG, Sier CFM, Vinkenburg-van Slooten M, Valentijn ARPM, Burggraaf J, van de Velde C, Frangioni JV, Vahrmeijer AL (2017) Real-time near-infrared fluorescence imaging using cRGD-ZW800-1 for intraoperative visualization of multiple cancer types. Oncotarget 8:21054–21066CrossRefPubMed
119.
Sato K, Gorka AP, Nagaya T, Michie MS, Nani RR, Nakamura Y, Coble VL, Vasalatiy OV, Swenson RE, Choyke PL, Schnermann MJ, Kobayashi H (2016) Role of fluorophore charge on the In Vivo optical imaging properties of near-infrared cyanine dye/monoclonal antibody conjugates. Bioconjug Chem 27:404–413CrossRefPubMed
120.
Yin X, Wang M, Wang H, Deng H, He T, Tan Y, Zhu Z, Wu Z, Hu S, Li Z (2017) Evaluation of neurotensin receptor 1 as a potential imaging target in pancreatic ductal adenocarcinoma. Amino Acids 49:1325–1335CrossRefPubMedPubMedCentral
121.
Wyatt LC, Lewis JS, Andreev OA, Reshetnyak YK, Engelman DM (2017) Applications of pHLIP technology for cancer imaging and therapy. Trends Biotechnol 35:653–664CrossRefPubMedPubMedCentral
122.
Golijanin J, Amin A, Moshnikova A, Brito JM, Tran TY, Adochite RC, Andreev GO, Crawford T, Engelman DM, Andreev OA, Reshetnyak YK, Golijanin D (2016) Targeted imaging of urothelium carcinoma in human bladders by an ICG pHLIP peptide ex vivo. Proc Natl Acad Sci U S A 113:11829–11834CrossRefPubMedPubMedCentral
123.
Karabadzhak AG, An M, Yao L, Langenbacher R, Moshnikova A, Adochite RC, Andreev OA, Reshetnyak YK, Engelman DM (2014) pHLIP-FIRE, a cell insertion-triggered fluorescent probe for imaging tumors demonstrates targeted cargo delivery in vivo. ACS Chem Biol 9:2545–2553CrossRefPubMedPubMedCentral
124.
Darmostuk M, Rimpelova S, Gbelcova H, Ruml T (2015) Current approaches in SELEX: an update to aptamer selection technology. Biotechnol Adv 33:1141–1161CrossRefPubMed
125.
Hori S, Herrera A, Rossi J, Zhou J (2018) Current advances in aptamers for cancer diagnosis and therapy. Cancers (Basel) 10:9CrossRef
126.
Huang YF, Chang HT, Tan W (2008) Cancer cell targeting using multiple aptamers conjugated on nanorods. Anal Chem 80:567–572CrossRefPubMed
127.
Tang J, Huang N, Zhang X, Zhou T, Tan Y, Pi J, Pi L, Cheng S, Zheng H, Cheng Y (2017) Aptamer-conjugated PEGylated quantum dots targeting epidermal growth factor receptor variant III for fluorescence imaging of glioma. Int J Nanomedicine 12:3899–3911CrossRefPubMedPubMedCentral
128.
Tan J, Yang N, Zhong L, Tan J, Hu Z, Zhao Q, Gong W, Zhang Z, Zheng R, Lai Z, Li Y, Zhou C, Zhang G, Zheng D, Zhang Y, Wu S, Jiang X, Zhong J, Huang Y, Zhou S, Zhao Y (2017) A new theranostic system based on endoglin aptamer conjugated fluorescent silica nanoparticles. Theranostics 7:4862–4876CrossRefPubMedPubMedCentral
129.
Bazak R, Houri M, El Achy S et al (2015) Cancer active targeting by nanoparticles: a comprehensive review of literature. J Cancer Res Clin Oncol 141:769–784CrossRefPubMed
130.
Duman FD, Erkisa M, Khodadust R, Ari F, Ulukaya E, Acar HY (2017) Folic acid-conjugated cationic Ag2S quantum dots for optical imaging and selective doxorubicin delivery to HeLa cells. Nanomedicine 12:2319–2333CrossRefPubMed
131.
Predina JD, Newton AD, Connolly C, Dunbar A, Baldassari M, Deshpande C, Cantu E III, Stadanlick J, Kularatne SA, Low PS, Singhal S (2018) Identification of a folate receptor-targeted near-infrared molecular contrast agent to localize pulmonary adenocarcinomas. Mol Ther 26:390–403CrossRefPubMed
132.
Hoogstins CES, Tummers QRJG, Gaarenstroom KN, de Kroon CD, Trimbos JBMZ, Bosse T, Smit VTHBM, Vuyk J, van de Velde CJH, Cohen AF, Low PS, Burggraaf J, Vahrmeijer AL (2016) A novel tumor-specific agent for intraoperative near-infrared fluorescence imaging: a translational study in healthy volunteers and patients with ovarian cancer. Clin Cancer Res 22:2929–2938CrossRefPubMed
133.
Keating JJ, Runge JJ, Singhal S, Nims S, Venegas O, Durham AC, Swain G, Nie S, Low PS, Holt DE (2017) Intraoperative near-infrared fluorescence imaging targeting folate receptors identifies lung cancer in a large-animal model. Cancer 123:1051–1060CrossRefPubMed
134.
Zhu M, Sheng Z, Jia Y, Hu D, Liu X, Xia X, Liu C, Wang P, Wang X, Zheng H (2017) Indocyanine green-holo-transferrin nanoassemblies for tumor-targeted dual-modal imaging and photothermal therapy of glioma. ACS Appl Mater Interfaces 9:39249–39258CrossRefPubMed
135.
Mochida A, Ogata F, Nagaya T, Choyke PL, Kobayashi H (2018) Activatable fluorescent probes in fluorescence-guided surgery: practical considerations. Bioorg Med Chem 26:925–930CrossRefPubMed
136.
Kobayashi H, Choyke PL (2011) Target-cancer-cell-specific activatable fluorescence imaging probes: rational design and in vivo applications. Acc Chem Res 44:83–90CrossRefPubMed
137.
Chinen AB, Guan CM, Ferrer JR, Barnaby SN, Merkel TJ, Mirkin CA (2015) Nanoparticle probes for the detection of cancer biomarkers, cells, and tissues by fluorescence. Chem Rev 115:10530–10574CrossRefPubMedPubMedCentral
138.
Choi HS, Liu W, Liu F, Nasr K, Misra P, Bawendi MG, Frangioni JV (2010) Design considerations for tumour-targeted nanoparticles. Nat Nanotechnol 5:42–47CrossRefPubMed
139.
Chi C, Zhang Q, Mao Y, Kou D, Qiu J, Ye J, Wang J, Wang Z, du Y, Tian J (2015) Increased precision of orthotopic and metastatic breast cancer surgery guided by matrix metalloproteinase-activatable near-infrared fluorescence probes. Sci Rep 5:14197CrossRefPubMedPubMedCentral
140.
Alley SC, Okeley NM, Senter PD (2010) Antibody–drug conjugates: targeted drug delivery for cancer. Curr Opin Chem Biol 14:529–537CrossRefPubMed
141.
Matsuzaki S, Serada S, Hiramatsu K, Nojima S, Matsuzaki S, Ueda Y, Ohkawara T, Mabuchi S, Fujimoto M, Morii E, Yoshino K, Kimura T, Naka T (2018) Anti-glypican-1 antibody-drug conjugate exhibits potent preclinical antitumor activity against glypican-1 positive uterine cervical cancer. Int J Cancer 142:1056–1066CrossRefPubMed
142.
Su C-Y, Chen M, Chen L-C, Ho YS, Ho HO, Lin SY, Chuang KH, Sheu MT (2018) Bispecific antibodies (anti-mPEG/anti-HER2) for active tumor targeting of docetaxel (DTX)-loaded mPEGylated nanocarriers to enhance the chemotherapeutic efficacy of HER2-overexpressing tumors. Drug Deliv 25:1066–1079CrossRefPubMedPubMedCentral
143.
144.
Huang R, Li J, Kebebe D, Wu Y, Zhang B, Liu Z (2018) Cell penetrating peptides functionalized gambogic acid-nanostructured lipid carrier for cancer treatment. Drug Deliv 25:757–765CrossRefPubMedPubMedCentral
145.
Deshpande P, Jhaveri A, Pattni B, Biswas S, Torchilin V (2018) Transferrin and octaarginine modified dual-functional liposomes with improved cancer cell targeting and enhanced intracellular delivery for the treatment of ovarian cancer. Drug Deliv 25:517–532CrossRefPubMedPubMedCentral
146.
Alibolandi M, Ramezani M, Abnous K, Hadizadeh F (2016) AS1411 aptamer-decorated biodegradable polyethylene glycol–poly(lactic-co-glycolic acid) nanopolymersomes for the targeted delivery of gemcitabine to non–small cell lung cancer in vitro. J Pharm Sci 105:1741–1750CrossRefPubMed
147.
148.
Rijpkema M, Oyen WJ, Bos D, Franssen GM, Goldenberg DM, Boerman OC (2014) SPECT- and fluorescence image-guided surgery using a dual-labeled carcinoembryonic antigen-targeting antibody. J Nucl Med 55:1519–1524CrossRefPubMed
149.
Zhang X-S, Xuan Y, Yang X-Q, Cheng K, Zhang RY, Li C, Tan F, Cao YC, Song XL, An J, Hou XL, Zhao YD (2018) A multifunctional targeting probe with dual-mode imaging and photothermal therapy used in vivo. J Nanobiotechnology 16:42CrossRefPubMedPubMedCentral
150.
Yang H-M, Park CW, Park S, Kim J-D (2018) Cross-linked magnetic nanoparticles with a biocompatible amide bond for cancer-targeted dual optical/magnetic resonance imaging. Colloids Surf B Biointerfaces 161:183–191CrossRefPubMed
151.
Kommidi H, Guo H, Nurili F, Vedvyas Y, Jin MM, McClure TD, Ehdaie B, Sayman HB, Akin O, Aras O, Ting R (2018) 18F-positron emitting/trimethine cyanine-fluorescent contrast for image-guided prostate cancer management. J Med Chem 61:4256–4262CrossRefPubMedPubMedCentral
152.
Wang X, Yan J, Pan D, et al (2018) Polyphenol-poloxamer self-assembled supramolecular nanoparticles for tumor NIRF/PET imaging. Adv Healthc Mater 15:1701505
153.
Chi C, Du Y, Ye J et al (2014) Intraoperative imaging-guided cancer surgery: from current fluorescence molecular imaging methods to future multi-modality imaging technology. Theranostics 4:1072–1084CrossRefPubMedPubMedCentral
154.
Hausner SH, Bauer N, Hu LY, Knight LM, Sutcliffe JL (2015) The effect of bi-terminal PEGylation of an integrin αvβ6-targeted 18F peptide on pharmacokinetics and tumor uptake. J Nucl Med 56:784–790CrossRefPubMed
155.
Han Z, Li Y, Roelle S, Zhou Z, Liu Y, Sabatelle R, DeSanto A, Yu X, Zhu H, Magi-Galluzzi C, Lu ZR (2017) Targeted contrast agent specific to an oncoprotein in tumor microenvironment with the potential for detection and risk stratification of prostate cancer with MRI. Bioconjug Chem 28:1031–1040CrossRefPubMedPubMedCentral
156.
Rosenthal EL, Warram JM, Bland KI, Zinn KR (2015) The status of contemporary image-guided modalities in oncologic surgery. Ann Surg 261:46–55CrossRefPubMed
157.
Kim MJ, Kim CS, Park YS et al (2016) The efficacy of intraoperative frozen section analysis during breast-conserving surgery for patients with ductal carcinoma in situ. Breast Cancer (Auckl) 10:205–210
158.
Ko S, Chun YK, Kang SS, Hur MH (2017) The usefulness of intraoperative circumferential frozen-section analysis of lumpectomy margins in breast-conserving surgery. J Breast Cancer 20:176–182CrossRefPubMedPubMedCentral
159.
Pleijhuis RG, Graafland M, de Vries J, Bart J, de Jong JS, van Dam GM (2009) Obtaining adequate surgical margins in breast-conserving therapy for patients with early-stage breast cancer: current modalities and future directions. Ann Surg Oncol 16:2717–2730CrossRefPubMedPubMedCentral
160.
Petropoulou T, Kapoula A, Mastoraki A et al (2017) Imprint cytology versus frozen section analysis for intraoperative assessment of sentinel lymph node in breast cancer. Breast Cancer (Dove Med Press) 9:325–330
161.
Barth CW, Schaefer JM, Rossi VM, Davis SC, Gibbs SL (2017) Optimizing fresh specimen staining for rapid identification of tumor biomarkers during surgery. Theranostics 7:4722–4734CrossRefPubMedPubMedCentral
162.
Hutteman M, Choi HS, Mieog JSD, van der Vorst JR, Ashitate Y, Kuppen PJK, van Groningen MC, Löwik CWGM, Smit VTHBM, van de Velde CJH, Frangioni JV, Vahrmeijer AL (2011) Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light. Ann Surg Oncol 18:1006–1014CrossRefPubMed
163.
Cutter JL, Cohen NT, Wang J, Sloan AE, Cohen AR, Panneerselvam A, Schluchter M, Blum G, Bogyo M, Basilion JP (2012) Topical application of activity-based probes for visualization of brain tumor tissue. PLoS One 7:e33060CrossRefPubMedPubMedCentral
164.
Tipirneni KE, Warram JM, Moore LS, Prince AC, de Boer E, Jani AH, Wapnir IL, Liao JC, Bouvet M, Behnke NK, Hawn MT, Poultsides GA, Vahrmeijer AL, Carroll WR, Zinn KR, Rosenthal E (2017) Oncologic procedures amenable to fluorescence-guided surgery. Ann Surg 266:36–47CrossRefPubMed
165.
Tummers WS, Warram JM, Tipirneni KE et al (2017) Regulatory aspects of optical methods and exogenous targets for cancer detection. Cancer Res 77:2197 LP–2192206CrossRef
166.
Mondal SB, Gao S, Zhu N et al (2015) Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping. Sci Rep 5:12117CrossRefPubMed
167.
Mondal SB, Gao S, Zhu N, Habimana-Griffin LM, Akers WJ, Liang R, Gruev V, Margenthaler J, Achilefu S (2017) Optical see-through cancer vision goggles enable direct patient visualization and real-time fluorescence-guided oncologic surgery. Ann Surg Oncol 24:1897–1903CrossRefPubMedPubMedCentral
168.
Boogerd LSF, Hoogstins CES, Schaap DP, Kusters M, Handgraaf HJM, van der Valk MJM, Hilling DE, Holman FA, Peeters KCMJ, Mieog JSD, van de Velde CJH, Farina-Sarasqueta A, van Lijnschoten I, Framery B, Pèlegrin A, Gutowski M, Nienhuijs SW, de Hingh IHJT, Nieuwenhuijzen GAP, Rutten HJT, Cailler F, Burggraaf J, Vahrmeijer AL (2018) Safety and effectiveness of SGM-101, a fluorescent antibody targeting carcinoembryonic antigen, for intraoperative detection of colorectal cancer: a dose-escalation pilot study. Lancet Gastroenterol Hepatol 3:181–191CrossRefPubMed
169.
Payne WM, Hill TK, Svechkarev D, Holmes MB, Sajja BR, Mohs AM (2017) Multimodal imaging nanoparticles derived from hyaluronic acid for integrated preoperative and intraoperative cancer imaging. Contrast Media Mol Imaging 2017:1–14CrossRef
170.
Gao N, Bozeman EN, Qian W, Wang L, Chen H, Lipowska M, Staley CA, Wang YA, Mao H, Yang L (2017) Tumor penetrating theranostic nanoparticles for enhancement of targeted and image-guided drug delivery into peritoneal tumors following intraperitoneal delivery. Theranostics 7:1689–1704CrossRefPubMedPubMedCentral
171.
Biffi S, Petrizza L, Garrovo C, Rampazzo E, Andolfi L, Giustetto P, Nikolov I, Kurdi G, Danailov MB, Zauli G, Secchiero P, Prodi L (2016) Multimodal near-infrared-emitting PluS silica nanoparticles with fluorescent, photoacoustic, and photothermal capabilities. Int J Nanomedicine 11:4865–4874CrossRefPubMedPubMedCentral
172.
Lu Z, Pham TT, Rajkumar V, Yu Z, Pedley RB, Årstad E, Maher J, Yan R (2018) A dual reporter iodinated labeling reagent for cancer positron emission tomography imaging and fluorescence-guided surgery. J Med Chem 61:1636–1645CrossRefPubMedPubMedCentral
173.
Nagaya T, Nakamura Y, Sato K, Harada T, Choyke PL, Hodge JW, Schlom J, Kobayashi H (2017) Near infrared photoimmunotherapy with avelumab, an anti-programmed death-ligand 1 (PD-L1) antibody. Oncotarget 8:8807–8817CrossRefPubMed
174.
Maruoka Y, Nagaya T, Nakamura Y, Sato K, Ogata F, Okuyama S, Choyke PL, Kobayashi H (2017) Evaluation of early therapeutic effects after near-infrared Photoimmunotherapy (NIR-PIT) using luciferase–luciferin photon-counting and fluorescence imaging. Mol Pharm 14:4628–4635CrossRefPubMedPubMedCentral
175.
Sun Q, You Q, Wang J, Liu L, Wang Y, Song Y, Cheng Y, Wang S, Tan F, Li N (2018) Theranostic Nanoplatform: triple-modal imaging-guided synergistic cancer therapy based on liposome-conjugated mesoporous silica nanoparticles. ACS Appl Mater Interfaces 10:1963–1975CrossRefPubMed
176.
Li X, Schumann C, Albarqi HA, Lee CJ, Alani AWG, Bracha S, Milovancev M, Taratula O, Taratula O (2018) A tumor-activatable theranostic nanomedicine platform for NIR fluorescence-guided surgery and combinatorial phototherapy. Theranostics 8:767–784CrossRefPubMedPubMedCentral
177.
Sun Y, Ding M, Zeng X, Xiao Y, Wu H, Zhou H, Ding B, Qu C, Hou W, Er-bu AGA, Zhang Y, Cheng Z, Hong X (2017) Novel bright-emission small-molecule NIR-II fluorophores for in vivo tumor imaging and image-guided surgery. Chem Sci 8:3489–3493CrossRefPubMedPubMedCentral
178.
Cheng K, Chen H, Jenkins CH, Zhang G, Zhao W, Zhang Z, Han F, Fung J, Yang M, Jiang Y, Xing L, Cheng Z (2017) Synthesis, characterization, and biomedical applications of a targeted dual-modal near-infrared-II fluorescence and photoacoustic imaging Nanoprobe. ACS Nano 11:12276–12291CrossRefPubMed
179.
Miao W, Kim H, Gujrati V, Kim JY, Jon H, Lee Y, Choi M, Kim J, Lee S, Lee DY, Kang S, Jon S (2016) Photo-decomposable organic nanoparticles for combined tumor optical imaging and multiple phototherapies. Theranostics 6:2367–2379CrossRefPubMedPubMedCentral
180.
Liu L, Ruan Z, Yuan P, Li T, Yan L (2018) Oxygen self-sufficient amphiphilic polypeptide nanoparticles encapsulating BODIPY for potential near infrared imaging-guided photodynamic therapy at low energy. Nanotheranostics 2:59–69CrossRefPubMedPubMedCentral
Metadata
Title
Fluorescence Guidance in Surgical Oncology: Challenges, Opportunities, and Translation
Publication date
01-04-2019
Published in
Molecular Imaging and Biology / Issue 2/2019
Print ISSN: 1536-1632
Electronic ISSN: 1860-2002
DOI
https://doi.org/10.1007/s11307-018-1239-2

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