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European Archives of Oto-Rhino-Laryngology

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01-10-2015 | Review Article

Role of near-infrared fluorescence imaging in head and neck cancer surgery: from animal models to humans

Authors: Ihab Atallah, Clément Milet, Jean-Luc Coll, Emile Reyt, Christian Adrien Righini, Amandine Hurbin

Published in: European Archives of Oto-Rhino-Laryngology | Issue 10/2015

Abstract

Complete resection of head and neck cancers with negative surgical margins improves the prognosis of the disease and decreases the recurrence rate. Near-infrared fluorescence-guided surgery of head and neck cancer is a rapidly evolving field that represents an invaluable tool for tumor detection and resection. Here, we present a literature review of the principles of near-infrared fluorescence imaging and its use in head and neck cancer surgery. We discuss important studies in both animal models and humans that have been carried out up to this point. We also outline the important fluorescent molecules and devices used in head and neck fluorescence imaging-guided surgery. Although near-infrared fluorescence-guided surgery for head and neck cancers showed efficacy in animal models, its use in humans is limited by the small number of fluorescent probes that are approved for clinical use. However, it is considered as a novel surgical aid that helps delineate tumor margins preoperatively and could spare patients from the added morbidity that is associated with additional surgery or chemoradiation. In addition, it is a useful tool to detect sentinel lymph nodes as well as metastatic lymph nodes.

Mehanna H, Paleri V, West CM, Nutting C (2011) Head and neck cancer-part 1: epidemiology, presentation, and preservation. Clin Otolaryngol 36(1):65–68. doi:10.1111/j.1749-4486.2010.02231.x PubMedCrossRef

Payakachat N, Ounpraseuth S, Suen JY (2013) Late complications and long-term quality of life for survivors (>5 years) with history of head and neck cancer. Head Neck 35(6):819–825. doi:10.1002/hed.23035 PubMedCrossRef

Swinson B, Jerjes W, El-Maaytah M, Norris P, Hopper C (2006) Optical techniques in diagnosis of head and neck malignancy. Oral Oncol 42(3):221–228. doi:10.1016/j.oraloncology.2005.05.001 PubMedCrossRef

Gioux S, Coutard JG, Berger M, Grateau H, Josserand V, Keramidas M, Righini C, Coll JL, Dinten JM (2012) FluoSTIC: miniaturized fluorescence image-guided surgery system. J Biomed Opt 17(10):106014. doi:10.1117/1.JBO.17.10.106014 PubMedCrossRef

Gioux S, Choi HS, Frangioni JV (2010) Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging 9(5):237–255PubMedCentralPubMed

Svistun E, Alizadeh-Naderi R, El-Naggar A, Jacob R, Gillenwater A, Richards-Kortum R (2004) Vision enhancement system for detection of oral cavity neoplasia based on autofluorescence. Head Neck 26(3):205–215. doi:10.1002/hed.10381 PubMedCrossRef

Poh CF, Ng SP, Williams PM, Zhang L, Laronde DM, Lane P, Macaulay C, Rosin MP (2007) Direct fluorescence visualization of clinically occult high-risk oral premalignant disease using a simple hand-held device. Head Neck 29(1):71–76. doi:10.1002/hed.20468 PubMedCrossRef

Tan NC, Herd MK, Brennan PA, Puxeddu R (2012) The role of narrow band imaging in early detection of head and neck cancer. Br J Oral Maxillofac Surg 50(2):132–136. doi:10.1016/j.bjoms.2010.12.001 PubMedCrossRef

Muto M, Minashi K, Yano T, Saito Y, Oda I, Nonaka S, Omori T, Sugiura H, Goda K, Kaise M, Inoue H, Ishikawa H, Ochiai A, Shimoda T, Watanabe H, Tajiri H, Saito D (2010) Early detection of superficial squamous cell carcinoma in the head and neck region and esophagus by narrow band imaging: a multicenter randomized controlled trial. J Clin Oncol 28(9):1566–1572. doi:10.1200/JCO.2009.25.4680 PubMedCentralPubMedCrossRef

10.

Hori K, Okada H, Kawahara Y, Takenaka R, Shimizu S, Ohno Y, Onoda T, Sirakawa Y, Naomoto Y, Yamamoto K (2011) Lugol-voiding lesions are an important risk factor for a second primary squamous cell carcinoma in patients with esophageal cancer or head and neck cancer. Am J Gastroenterol 106(5):858–866. doi:10.1038/ajg.2010.489 PubMedCrossRef

11.

Jayaprakash V, Sullivan M, Merzianu M, Rigual NR, Loree TR, Popat SR, Moysich KB, Ramananda S, Johnson T, Marshall JR, Hutson AD, Mang TS, Wilson BC, Gill SR, Frustino J, Bogaards A, Reid ME (2009) Autofluorescence-guided surveillance for oral cancer. Cancer Prev Res (Phila) 2(11):966–974. doi:10.1158/1940-6207.CAPR-09-0062 CrossRef

12.

van Driel PB, van der Vorst JR, Verbeek FP, Oliveira S, Snoeks TJ, Keereweer S, Frangioni JV, van Bergen En Henegouwen PM, Vahrmeijer AL, Lowik CW (2013) Intraoperative fluorescence delineation of head and neck cancer with a fluorescent anti-epidermal growth factor receptor nanobody. Int J Cancer. doi:10.1002/ijc.28601 PubMedCentralPubMed

13.

Gibbs SL (2012) Near infrared fluorescence for image-guided surgery. Quant Imaging Med Surg 2(3):177–187. doi:10.3978/j.issn.2223-4292.2012.09.04.qims-02-03-177 PubMedCentralPubMed

14.

Hussain T, Nguyen QT (2013) Molecular imaging for cancer diagnosis and surgery. Adv Drug Deliv Rev. doi:10.1016/j.addr.2013.09.007 PubMedCentralPubMed

15.

Bredell MG (2010) Sentinel lymph node mapping by indocyanin green fluorescence imaging in oropharyngeal cancer—preliminary experience. Head Neck Oncol 2:31. doi:10.1186/1758-3284-2-31 PubMedCentralPubMedCrossRef

16.

Nakamura Y, Fujisawa Y, Maruyama H, Furuta J, Kawachi Y, Otsuka F (2013) Improvement of the sentinel lymph node detection rate of cervical sentinel lymph node biopsy using real-time fluorescence navigation with indocyanine green in head and neck skin cancer. J Dermatol 40(6):453–457. doi:10.1111/1346-8138.12158 PubMedCrossRef

17.

van der Vorst JR, Schaafsma BE, Verbeek FP, Keereweer S, Jansen JC, van der Velden LA, Langeveld AP, Hutteman M, Lowik CW, van de Velde CJ, Frangioni JV, Vahrmeijer AL (2013) Near-infrared fluorescence sentinel lymph node mapping of the oral cavity in head and neck cancer patients. Oral Oncol 49(1):15–19. doi:10.1016/j.oraloncology.2012.07.017 PubMedCentralPubMedCrossRef

18.

Gleysteen JP, Duncan RD, Magnuson JS, Skipper JB, Zinn K, Rosenthal EL (2007) Fluorescently labeled cetuximab to evaluate head and neck cancer response to treatment. Cancer Biol Ther 6(8):1181–1185 (pii):4379PubMedCrossRef

19.

Gleysteen JP, Newman JR, Chhieng D, Frost A, Zinn KR, Rosenthal EL (2008) Fluorescent labeled anti-EGFR antibody for identification of regional and distant metastasis in a preclinical xenograft model. Head Neck 30(6):782–789. doi:10.1002/hed.20782 PubMedCentralPubMedCrossRef

20.

Yang K, Zhao C, Cao YA, Tang H, Bai YL, Huang H, Zhao CR, Chen R, Zhao D (2012) In vivo and in situ imaging of head and neck squamous cell carcinoma using near-infrared fluorescent quantum dot probes conjugated with epidermal growth factor receptor monoclonal antibodies in mice. Oncol Rep 27(6):1925–1931. doi:10.3892/or.2012.1705 PubMed

21.

Huang H, Bai YL, Yang K, Tang H, Wang YW (2013) Optical imaging of head and neck squamous cell carcinoma in vivo using arginine-glycine-aspartic acid peptide conjugated near-infrared quantum dots. Onco Targets Ther 6:1779–1787. doi:10.2147/OTT.S53901ott-6-1779 PubMedCentralPubMed

22.

Oliveira S, van Dongen GA, Stigter-van Walsum M, Roovers RC, Stam JC, Mali W, van Diest PJ, van Bergen en Henegouwen PM (2012) Rapid visualization of human tumor xenografts through optical imaging with a near-infrared fluorescent anti-epidermal growth factor receptor nanobody. Mol Imaging 11(1):33–46PubMed

23.

Keereweer S, Kerrebijn JD, Mol IM, Mieog JS, Van Driel PB, Baatenburg de Jong RJ, Vahrmeijer AL, Lowik CW (2012) Optical imaging of oral squamous cell carcinoma and cervical lymph node metastasis. Head Neck 34(7):1002–1008. doi:10.1002/hed.21861 PubMedCrossRef

24.

Fabricius EM, Wildner GP, Kruse-Boitschenko U, Hoffmeister B, Goodman SL, Raguse JD (2011) Immunohistochemical analysis of integrins alphavbeta3, alphavbeta5 and alpha5beta1, and their ligands, fibrinogen, fibronectin, osteopontin and vitronectin, in frozen sections of human oral head and neck squamous cell carcinomas. Exp Ther Med 2(1):9–19. doi:10.3892/etm.2010.171etm-02-01-0009 PubMedCentralPubMed

25.

Beer AJ, Grosu AL, Carlsen J, Kolk A, Sarbia M, Stangier I, Watzlowik P, Wester HJ, Haubner R, Schwaiger M (2007) [18F]galacto-RGD positron emission tomography for imaging of alphavbeta3 expression on the neovasculature in patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 13(22 Pt 1):6610–6616. doi:10.1158/1078-0432.CCR-07-0528 PubMedCrossRef

26.

Li P, Liu F, Sun L, Zhao Z, Ding X, Shang D, Xu Z, Sun C (2011) Chemokine receptor 7 promotes cell migration and adhesion in metastatic squamous cell carcinoma of the head and neck by activating integrin alphavbeta3. Int J Mol Med 27(5):679–687. doi:10.3892/ijmm.2011.628 PubMed

27.

Jin ZH, Josserand V, Razkin J, Garanger E, Boturyn D, Favrot MC, Dumy P, Coll JL (2006) Noninvasive optical imaging of ovarian metastases using Cy5-labeled RAFT-c(-RGDfK-)4. Mol Imaging 5(3):188–197PubMed

28.

Jin ZH, Josserand V, Foillard S, Boturyn D, Dumy P, Favrot MC, Coll JL (2007) In vivo optical imaging of integrin alphaV-beta3 in mice using multivalent or monovalent cRGD targeting vectors. Mol Cancer 6:41. doi:10.1186/1476-4598-6-41 PubMedCentralPubMedCrossRef

29.

Sancey L, Ardisson V, Riou LM, Ahmadi M, Marti-Batlle D, Boturyn D, Dumy P, Fagret D, Ghezzi C, Vuillez JP (2007) In vivo imaging of tumour angiogenesis in mice with the alpha(v)beta (3) integrin-targeted tracer 99mTc-RAFT-RGD. Eur J Nucl Med Mol Imaging 34(12):2037–2047. doi:10.1007/s00259-007-0497-z PubMedCrossRef

30.

Garanger E, Boturyn D, Jin Z, Dumy P, Favrot MC, Coll JL (2005) New multifunctional molecular conjugate vector for targeting, imaging, and therapy of tumors. Mol Ther 12(6):1168–1175. doi:10.1016/j.ymthe.2005.06.095 PubMedCrossRef

31.

Wenk CH, Ponce F, Guillermet S, Tenaud C, Boturyn D, Dumy P, Watrelot-Virieux D, Carozzo C, Josserand V, Coll JL (2013) Near-infrared optical guided surgery of highly infiltrative fibrosarcomas in cats using an anti-alphavss3 integrin molecular probe. Cancer Lett 334(2):188–195. doi:10.1016/j.canlet.2012.10.041 PubMedCrossRef

32.

Keramidas M, Josserand V, Righini CA, Wenk C, Faure C, Coll JL (2010) Intraoperative near-infrared image-guided surgery for peritoneal carcinomatosis in a preclinical experimental model. Br J Surg 97(5):737–743. doi:10.1002/bjs.6986 PubMedCrossRef

33.

Xie BW, Mol IM, Keereweer S, van Beek ER, Que I, Snoeks TJ, Chan A, Kaijzel EL, Lowik CW (2012) Dual-wavelength imaging of tumor progression by activatable and targeting near-infrared fluorescent probes in a bioluminescent breast cancer model. PLoS One 7(2):e31875. doi:10.1371/journal.pone.0031875PONE-D-11-16502 PubMedCentralPubMedCrossRef

34.

Withrow KP, Newman JR, Skipper JB, Gleysteen JP, Magnuson JS, Zinn K, Rosenthal EL (2008) Assessment of bevacizumab conjugated to Cy5.5 for detection of head and neck cancer xenografts. Technol Cancer Res Treat 7(1):61–66PubMedCrossRef

35.

Shan L, Hao Y, Wang S, Korotcov A, Zhang R, Wang T, Califano J, Gu X, Sridhar R, Bhujwalla ZM, Wang PC (2008) Visualizing head and neck tumors in vivo using near-infrared fluorescent transferrin conjugate. Mol Imaging 7(1):42–49PubMed

36.

Keereweer S, Sterenborg HJ, Kerrebijn JD, Van Driel PB, Baatenburg de Jong RJ, Lowik CW (2012) Image-guided surgery in head and neck cancer: current practice and future directions of optical imaging. Head Neck 34(1):120–126. doi:10.1002/hed.21625 PubMedCrossRef

37.

Yokoyama J, Fujimaki M, Ohba S, Anzai T, Yoshii R, Ito S, Kojima M, Ikeda K (2013) A feasibility study of NIR fluorescent image-guided surgery in head and neck cancer based on the assessment of optimum surgical time as revealed through dynamic imaging. Onco Targets Ther 6:325–330. doi:10.2147/OTT.S42006ott-6-325 PubMedCentralPubMedCrossRef

38.

Sharkey FE, Fogh J (1984) Considerations in the use of nude mice for cancer research. Cancer Metastasis Rev 3(4):341–360PubMedCrossRef

39.

Kim S (2009) Animal models of cancer in the head and neck region. Clin Exp Otorhinolaryngol 2(2):55–60. doi:10.3342/ceo.2009.2.2.55 PubMedCentralPubMedCrossRef

40.

Lu SL, Herrington H, Wang XJ (2006) Mouse models for human head and neck squamous cell carcinomas. Head Neck 28(10):945–954. doi:10.1002/hed.20397 PubMedCrossRef

41.

Cabanillas R, Secades P, Rodrigo JP, Astudillo A, Suarez C, Chiara MD (2005) Orthotopic murine model of head and neck squamous cell carcinoma. Acta Otorrinolaringol Esp 56(3):89–95PubMedCrossRef

42.

Heath CH, Deep NL, Sweeny L, Zinn KR, Rosenthal EL (2012) Use of panitumumab-IRDye800 to image microscopic head and neck cancer in an orthotopic surgical model. Ann Surg Oncol 19(12):3879–3887. doi:10.1245/s10434-012-2435-y PubMedCentralPubMedCrossRef

43.

Day KE, Sweeny L, Kulbersh B, Zinn KR, Rosenthal EL (2013) Preclinical comparison of near-infrared-labeled cetuximab and panitumumab for optical imaging of head and neck squamous cell carcinoma. Mol Imaging Biol 15(6):722–729. doi:10.1007/s11307-013-0652-9 PubMedCentralPubMedCrossRef

44.

Keereweer S, Mol IM, Kerrebijn JD, Van Driel PB, Xie B, Baatenburg de Jong RJ, Vahrmeijer AL, Lowik CW (2012) Targeting integrins and enhanced permeability and retention (EPR) effect for optical imaging of oral cancer. J Surg Oncol 105(7):714–718. doi:10.1002/jso.22102 PubMedCrossRef

45.

Rosenthal EL, Kulbersh BD, King T, Chaudhuri TR, Zinn KR (2007) Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts. Mol Cancer Ther 6(4):1230–1238. doi:10.1158/1535-7163.MCT-06-0741 PubMedCrossRef

46.

Brouwer OR, Klop WM, Buckle T, Vermeeren L, van den Brekel MW, Balm AJ, Nieweg OE, Valdes Olmos RA, van Leeuwen FW (2012) Feasibility of sentinel node biopsy in head and neck melanoma using a hybrid radioactive and fluorescent tracer. Ann Surg Oncol 19(6):1988–1994. doi:10.1245/s10434-011-2180-7 PubMedCentralPubMedCrossRef

47.

Ohnishi S, Lomnes SJ, Laurence RG, Gogbashian A, Mariani G, Frangioni JV (2005) Organic alternatives to quantum dots for intraoperative near-infrared fluorescent sentinel lymph node mapping. Mol Imaging 4(3):172–181PubMed

48.

Sandanaraj BS, Gremlich HU, Kneuer R, Dawson J, Wacha S (2010) Fluorescent nanoprobes as a biomarker for increased vascular permeability: implications in diagnosis and treatment of cancer and inflammation. Bioconjug Chem 21(1):93–101. doi:10.1021/bc900311h PubMedCrossRef

49.

Maeda H (2010) Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects. Bioconjug Chem 21(5):797–802. doi:10.1021/bc100070g PubMedCrossRef

Title: Role of near-infrared fluorescence imaging in head and neck cancer surgery: from animal models to humans
Authors: Ihab Atallah
Clément Milet
Jean-Luc Coll
Emile Reyt
Christian Adrien Righini
Amandine Hurbin
Publication date: 01-10-2015
Publisher: Springer Berlin Heidelberg
Published in: European Archives of Oto-Rhino-Laryngology / Issue 10/2015
Print ISSN: 0937-4477
Electronic ISSN: 1434-4726
DOI: https://doi.org/10.1007/s00405-014-3224-y

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Role of near-infrared fluorescence imaging in head and neck cancer surgery: from animal models to humans

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

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