Skip to main content
Top
Published in: BMC Medical Imaging 1/2020

Open Access 01-12-2020 | Digital Volume Tomography | Research article

Sentinel lymph node mapping using ICG fluorescence and cone beam CT – a feasibility study in a rabbit model of oral cancer

Authors: Nidal Muhanna, Harley H. L. Chan, Catriona M. Douglas, Michael J. Daly, Atul Jaidka, Donovan Eu, Jonathan Bernstein, Jason L. Townson, Jonathan C. Irish

Published in: BMC Medical Imaging | Issue 1/2020

Login to get access

Abstract

Background

Current sentinel lymph node biopsy (SLNB) techniques, including use of radioisotopes, have disadvantages including the use of a radioactive tracer. Indocyanine green (ICG) based near-infrared (NIR) fluorescence imaging and cone beam CT (CBCT) have advantages for intraoperative use. However, limited literature exists regarding their use in head and neck cancer SLNB.

Methods

This was a prospective, non-randomized study using a rabbit oral cavity VX2 squamous cell carcinoma model (n = 10) which develops lymph node metastasis. Pre-operatively, images were acquired by MicroCT. During surgery, CBCT and NIR fluorescence imaging of ICG was used to map and guide the SLNB resection.

Results

Intraoperative use of ICG to guide fluorescence resection resulted in identification of all lymph nodes identified by pre-operative CT. CBCT was useful for near real time intraoperative imaging and 3D reconstruction.

Conclusions

This pre-clinical study further demonstrates the technical feasibility, limitations and advantages of intraoperative NIR-guided ICG imaging for SLN identification as a complementary method during head and neck surgery.
Literature
1.
go back to reference Dik EA, et al. Watchful waiting of the neck in early stage oral cancer is unfavourable for patients with occult nodal disease. Int J Oral Maxillofac Surg. 2016;45(8):945–50.CrossRef Dik EA, et al. Watchful waiting of the neck in early stage oral cancer is unfavourable for patients with occult nodal disease. Int J Oral Maxillofac Surg. 2016;45(8):945–50.CrossRef
2.
go back to reference Schilling C, et al. Sentinel lymph node biopsy for oral squamous cell carcinoma. Where are we now? Br J Oral Maxillofac Surg. 2017;55(8):757–62.CrossRef Schilling C, et al. Sentinel lymph node biopsy for oral squamous cell carcinoma. Where are we now? Br J Oral Maxillofac Surg. 2017;55(8):757–62.CrossRef
3.
go back to reference Abu-Ghanem S, et al. Elective neck dissection vs observation in early-stage squamous cell carcinoma of the Oral tongue with no clinically apparent lymph node metastasis in the neck: a systematic review and meta-analysis. JAMA Otolaryngol Head Neck Surg. 2016;142(9):857–65.CrossRef Abu-Ghanem S, et al. Elective neck dissection vs observation in early-stage squamous cell carcinoma of the Oral tongue with no clinically apparent lymph node metastasis in the neck: a systematic review and meta-analysis. JAMA Otolaryngol Head Neck Surg. 2016;142(9):857–65.CrossRef
4.
go back to reference Tardelli E, et al. Sentinel lymph node biopsy in cutaneous melanoma: standard and new technical procedures and clinical advances. A systematic review of the literature. Clin Nucl Med. 2016;41(12):e498–507.CrossRef Tardelli E, et al. Sentinel lymph node biopsy in cutaneous melanoma: standard and new technical procedures and clinical advances. A systematic review of the literature. Clin Nucl Med. 2016;41(12):e498–507.CrossRef
5.
go back to reference El Hage Chehade H, et al. Is sentinel lymph node biopsy a viable alternative to complete axillary dissection following neoadjuvant chemotherapy in women with node-positive breast cancer at diagnosis? An updated meta-analysis involving 3,398 patients. Am J Surg. 2016;212(5):969–81.CrossRef El Hage Chehade H, et al. Is sentinel lymph node biopsy a viable alternative to complete axillary dissection following neoadjuvant chemotherapy in women with node-positive breast cancer at diagnosis? An updated meta-analysis involving 3,398 patients. Am J Surg. 2016;212(5):969–81.CrossRef
6.
go back to reference Network NCC. NCCN clinical practice guidelines in oncology (NCCN guideline):head and neck cancers; 2018. Network NCC. NCCN clinical practice guidelines in oncology (NCCN guideline):head and neck cancers; 2018.
7.
go back to reference Schaafsma BE, et al. The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol. 2011;104(3):323–32.CrossRef Schaafsma BE, et al. The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol. 2011;104(3):323–32.CrossRef
8.
go back to reference Bredell MG. Sentinel lymph node mapping by indocyanin green fluorescence imaging in oropharyngeal cancer - preliminary experience. Head Neck Oncol. 2010;2:31.CrossRef Bredell MG. Sentinel lymph node mapping by indocyanin green fluorescence imaging in oropharyngeal cancer - preliminary experience. Head Neck Oncol. 2010;2:31.CrossRef
9.
go back to reference van den Berg NS, et al. Concomitant radio- and fluorescence-guided sentinel lymph node biopsy in squamous cell carcinoma of the oral cavity using ICG-(99m)Tc-nanocolloid. Eur J Nucl Med Mol Imaging. 2012;39(7):1128–36.CrossRef van den Berg NS, et al. Concomitant radio- and fluorescence-guided sentinel lymph node biopsy in squamous cell carcinoma of the oral cavity using ICG-(99m)Tc-nanocolloid. Eur J Nucl Med Mol Imaging. 2012;39(7):1128–36.CrossRef
10.
go back to reference KleinJan GH, et al. The best of both worlds: a hybrid approach for optimal pre- and intraoperative identification of sentinel lymph nodes. Eur J Nucl Med Mol Imaging. 2018;45(11):1915–25. KleinJan GH, et al. The best of both worlds: a hybrid approach for optimal pre- and intraoperative identification of sentinel lymph nodes. Eur J Nucl Med Mol Imaging. 2018;45(11):1915–25.
11.
go back to reference Chand M, et al. Furthering precision in sentinel node navigational surgery for Oral Cancer: a novel triple targeting system. J Fluoresc. 2018;28(2):483-486. Chand M, et al. Furthering precision in sentinel node navigational surgery for Oral Cancer: a novel triple targeting system. J Fluoresc. 2018;28(2):483-486.
12.
go back to reference Park YM, et al. Endoscopic sentinel lymph node biopsy using indocyanine green-neomannosyl human serum albumin. Laryngoscope. 2018;128(4):E135–40.CrossRef Park YM, et al. Endoscopic sentinel lymph node biopsy using indocyanine green-neomannosyl human serum albumin. Laryngoscope. 2018;128(4):E135–40.CrossRef
13.
go back to reference Den RB, et al. Daily image guidance with cone-beam computed tomography for head-and-neck cancer intensity-modulated radiotherapy: a prospective study. Int J Radiat Oncol Biol Phys. 2010;76(5):1353–9.CrossRef Den RB, et al. Daily image guidance with cone-beam computed tomography for head-and-neck cancer intensity-modulated radiotherapy: a prospective study. Int J Radiat Oncol Biol Phys. 2010;76(5):1353–9.CrossRef
14.
go back to reference Kagadis GC, et al. Emerging technologies for image guidance and device navigation in interventional radiology. Med Phys. 2012;39(9):5768–81.CrossRef Kagadis GC, et al. Emerging technologies for image guidance and device navigation in interventional radiology. Med Phys. 2012;39(9):5768–81.CrossRef
15.
go back to reference Muhanna N, et al. The image-guided operating room-utility and impact on surgeon's performance in the head and neck surgery. Head Neck. 2019;41(9):3372–82. Muhanna N, et al. The image-guided operating room-utility and impact on surgeon's performance in the head and neck surgery. Head Neck. 2019;41(9):3372–82.
16.
go back to reference King E, et al. Intraoperative cone-beam CT for head and neck surgery: feasibility of clinical implementation using a prototype mobile C-arm. Head Neck. 2013;35(7):959–67.CrossRef King E, et al. Intraoperative cone-beam CT for head and neck surgery: feasibility of clinical implementation using a prototype mobile C-arm. Head Neck. 2013;35(7):959–67.CrossRef
17.
go back to reference Muhanna N, Douglas CM, Daly MJ, Chan HHL, Weersink R, Townson J, Monteiro E, Yu E, Weimer E, Kucharczyk W, Jaffray DA, Irish JC, de Almeida JR. Evaluating an Image-Guided Operating Room with Cone Beam CT for Skull Base Surgery. J Neurol Surg B. 2020. Muhanna N, Douglas CM, Daly MJ, Chan HHL, Weersink R, Townson J, Monteiro E, Yu E, Weimer E, Kucharczyk W, Jaffray DA, Irish JC, de Almeida JR. Evaluating an Image-Guided Operating Room with Cone Beam CT for Skull Base Surgery. J Neurol Surg B. 2020.
18.
go back to reference Lin LM, et al. VX2-induced rabbit buccal carcinoma: a potential cancer model for human buccal mucosa squamous cell carcinoma. Oral Oncol. 2009;45(11):e196–203.CrossRef Lin LM, et al. VX2-induced rabbit buccal carcinoma: a potential cancer model for human buccal mucosa squamous cell carcinoma. Oral Oncol. 2009;45(11):e196–203.CrossRef
19.
go back to reference Kalender WA, Kyriakou Y. Flat-detector computed tomography (FD-CT). Eur Radiol. 2007;17(11):2767–79.CrossRef Kalender WA, Kyriakou Y. Flat-detector computed tomography (FD-CT). Eur Radiol. 2007;17(11):2767–79.CrossRef
20.
go back to reference Shaye DA, Tollefson TT, Strong EB. Use of intraoperative computed tomography for maxillofacial reconstructive surgery. JAMA Facial Plast Surg. 2015;17(2):113–9.CrossRef Shaye DA, Tollefson TT, Strong EB. Use of intraoperative computed tomography for maxillofacial reconstructive surgery. JAMA Facial Plast Surg. 2015;17(2):113–9.CrossRef
21.
go back to reference Schwartz DL, et al. Adaptive radiotherapy for head-and-neck cancer: initial clinical outcomes from a prospective trial. Int J Radiat Oncol Biol Phys. 2012;83(3):986–93.CrossRef Schwartz DL, et al. Adaptive radiotherapy for head-and-neck cancer: initial clinical outcomes from a prospective trial. Int J Radiat Oncol Biol Phys. 2012;83(3):986–93.CrossRef
22.
go back to reference Lechuga L, Weidlich GA. Cone Beam CT vs. Fan Beam CT: A Comparison of Image Quality and Dose Delivered Between Two Differing CT Imaging Modalities. Cureus. 2016;8(9):e778.PubMedPubMedCentral Lechuga L, Weidlich GA. Cone Beam CT vs. Fan Beam CT: A Comparison of Image Quality and Dose Delivered Between Two Differing CT Imaging Modalities. Cureus. 2016;8(9):e778.PubMedPubMedCentral
23.
go back to reference Pfister DG, et al. Head and neck cancers, version 1.2015. J Natl Compr Cancer Netw. 2015;13(7):847–55 quiz 856.CrossRef Pfister DG, et al. Head and neck cancers, version 1.2015. J Natl Compr Cancer Netw. 2015;13(7):847–55 quiz 856.CrossRef
24.
go back to reference Heuveling DA, et al. Feasibility of intraoperative detection of sentinel lymph nodes with 89-zirconium-labelled nanocolloidal albumin PET-CT and a handheld high-energy gamma probe. EJNMMI Res. 2018;8(1):15.CrossRef Heuveling DA, et al. Feasibility of intraoperative detection of sentinel lymph nodes with 89-zirconium-labelled nanocolloidal albumin PET-CT and a handheld high-energy gamma probe. EJNMMI Res. 2018;8(1):15.CrossRef
25.
go back to reference Pezier T, et al. Sentinel lymph node biopsy for T1/T2 oral cavity squamous cell carcinoma--a prospective case series. Ann Surg Oncol. 2012;19(11):3528–33.CrossRef Pezier T, et al. Sentinel lymph node biopsy for T1/T2 oral cavity squamous cell carcinoma--a prospective case series. Ann Surg Oncol. 2012;19(11):3528–33.CrossRef
26.
go back to reference He K, et al. Comparison between the indocyanine green fluorescence and blue dye methods for sentinel lymph node biopsy using novel fluorescence image-guided resection equipment in different types of hospitals. Transl Res. 2016;178:74–80.CrossRef He K, et al. Comparison between the indocyanine green fluorescence and blue dye methods for sentinel lymph node biopsy using novel fluorescence image-guided resection equipment in different types of hospitals. Transl Res. 2016;178:74–80.CrossRef
27.
go back to reference Agrawal A, et al. [(99m)Tc] Tilmanocept accurately detects sentinel lymph nodes and predicts node pathology status in patients with Oral squamous cell carcinoma of the head and neck: results of a phase III multi-institutional trial. Ann Surg Oncol. 2015;22(11):3708–15.CrossRef Agrawal A, et al. [(99m)Tc] Tilmanocept accurately detects sentinel lymph nodes and predicts node pathology status in patients with Oral squamous cell carcinoma of the head and neck: results of a phase III multi-institutional trial. Ann Surg Oncol. 2015;22(11):3708–15.CrossRef
28.
go back to reference Civantos FJ, et al. Sentinel lymph node biopsy accurately stages the regional lymph nodes for T1-T2 oral squamous cell carcinomas: results of a prospective multi-institutional trial. J Clin Oncol. 2010;28(8):1395–400.CrossRef Civantos FJ, et al. Sentinel lymph node biopsy accurately stages the regional lymph nodes for T1-T2 oral squamous cell carcinomas: results of a prospective multi-institutional trial. J Clin Oncol. 2010;28(8):1395–400.CrossRef
29.
go back to reference Morton DL, et al. Sentinel node biopsy for early-stage melanoma: accuracy and morbidity in MSLT-I, an international multicenter trial. Ann Surg. 2005;242(3):302–11 discussion 311-3.PubMedPubMedCentral Morton DL, et al. Sentinel node biopsy for early-stage melanoma: accuracy and morbidity in MSLT-I, an international multicenter trial. Ann Surg. 2005;242(3):302–11 discussion 311-3.PubMedPubMedCentral
30.
go back to reference van der Vorst JR, et al. Near-infrared fluorescence sentinel lymph node mapping of the oral cavity in head and neck cancer patients. Oral Oncol. 2013;49(1):15–9.CrossRef van der Vorst JR, et al. Near-infrared fluorescence sentinel lymph node mapping of the oral cavity in head and neck cancer patients. Oral Oncol. 2013;49(1):15–9.CrossRef
31.
go back to reference Mieog JS, et al. Toward optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol. 2011;18(9):2483–91.CrossRef Mieog JS, et al. Toward optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol. 2011;18(9):2483–91.CrossRef
32.
go back to reference Speich R, et al. Anaphylactoid reactions after indocyanine-green administration. Ann Intern Med. 1988;109(4):345–6.CrossRef Speich R, et al. Anaphylactoid reactions after indocyanine-green administration. Ann Intern Med. 1988;109(4):345–6.CrossRef
33.
go back to reference Langhans L, et al. Evaluation of sentinel lymph node size and shape as a predictor of occult metastasis in patients with squamous cell carcinoma of the oral cavity. Eur Arch Otorhinolaryngol. 2013;270(1):249–54.CrossRef Langhans L, et al. Evaluation of sentinel lymph node size and shape as a predictor of occult metastasis in patients with squamous cell carcinoma of the oral cavity. Eur Arch Otorhinolaryngol. 2013;270(1):249–54.CrossRef
Metadata
Title
Sentinel lymph node mapping using ICG fluorescence and cone beam CT – a feasibility study in a rabbit model of oral cancer
Authors
Nidal Muhanna
Harley H. L. Chan
Catriona M. Douglas
Michael J. Daly
Atul Jaidka
Donovan Eu
Jonathan Bernstein
Jason L. Townson
Jonathan C. Irish
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Medical Imaging / Issue 1/2020
Electronic ISSN: 1471-2342
DOI
https://doi.org/10.1186/s12880-020-00507-x

Other articles of this Issue 1/2020

BMC Medical Imaging 1/2020 Go to the issue