Does radiocolloid remain the gold standard in melanomas? New sentinel lymph node localization techniques
Abstract
Melanoma is one of the most aggressive types of cancer, which makes accurate staging crucial for determining appropriate treatment. In melanoma patients, lymph node status is the most significant predictor of survival. Sentinel lymph node biopsy (SLNB) is a minimally invasive technique that provides essential information for staging, prognosis, and identifying patients who require further treatment. SLNB involves using a radioactive tracer (Technetium-99) and lymphatic mapping with a vital blue dye, such as isosulfan blue, methylene blue, or patent blue. This procedure helps patients avoid unnecessary complete lymph node dissection (CLND) when pathological examination reveals no melanoma metastases. This review summarizes various techniques for sentinel lymph nodes (SLNs) mapping and explores emerging approaches, including indocyanine green (ICG), magnetic tracers, and 18F-fluorodeoxyglucose positron emission tomography/computed tomography (18F-FDG PET/CT).
Keywords: sentinel lymph node biopsymelanomaradiotracerindocyanine greensuperparamagnetic iron oxide
References
- Ahmed B, Qadir MI, Ghafoor S. Malignant Melanoma: Skin Cancer-Diagnosis, Prevention, and Treatment. Crit Rev Eukaryot Gene Expr. 2020; 30(4): 291–297.
- Balch CM, Gershenwald JE, Soong SJ, et al. Multivariate analysis of prognostic factors among 2,313 patients with stage III melanoma: comparison of nodal micrometastases versus macrometastases. J Clin Oncol. 2010; 28(14): 2452–2459.
- Lee KK, Vetto JT, Mehrany K, et al. Sentinel lymph node biopsy. Clin Dermatol. 2004; 22(3): 234–239.
- Wright FC, Souter LH, Kellett S, et al. Melanoma Disease Site Group. Primary excision margins, sentinel lymph node biopsy, and completion lymph node dissection in cutaneous melanoma: a clinical practice guideline. Curr Oncol. 2019; 26(4): e541–e550.
- GARCELON GG. Salivary gland tumors: management and results. AMA Arch Surg. 1959; 78(1): 12–16.
- Lyman GH, Giuliano AE, Somerfield MR, et al. American Society of Clinical Oncology. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005; 23(30): 7703–7720.
- Keilholz U, Ascierto PA, Dummer R, et al. ESMO consensus conference recommendations on the management of locoregional melanoma: under the auspices of the ESMO Guidelines Committee. Ann Oncol. 2020; 31(11): 1449–1461.
- Reintgen DS, Cox EB, McCarty KS, et al. Efficacy of elective lymph node dissection in patients with intermediate thickness primary melanoma. Ann Surg. 1983; 198(3): 379–385.
- Drepper H, Köhler CO, Bastian B, et al. Benefit of elective lymph node dissection in subgroups of melanoma patients. Results of a multicenter study of 3616 patients. Cancer. 1993; 72(3): 741–749, doi: 10.1002/1097-0142(19930801)72:3<741::aid-cncr2820720318>3.0.co;2-w.
- Crowley N. The Case Against Elective Lymphadenectomy. Surg Oncol Clin N Am. 1992; 1(2): 223–246.
- Wrone DA, Tanabe KK, Cosimi AB, et al. Lymphedema after sentinel lymph node biopsy for cutaneous melanoma: a report of 5 cases. Arch Dermatol. 2000; 136(4): 511–514.
- Morton DL, Wen DR, Wong JH, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg. 1992; 127(4): 392–399.
- Cascinelli N, Morabito A, Santinami M, et al. Immediate or delayed dissection of regional nodes in patients with melanoma of the trunk: a randomised trial. Lancet. 1998; 351(9105): 793–796.
- Morton D, Thompson J, Cochran A, et al. Sentinel-Node Biopsy or Nodal Observation in Melanoma. N Engl J Med. 2006; 355(13): 1307–1317.
- Han D, Han G, Duque MT, et al. Sentinel Lymph Node Biopsy Is Prognostic in Thickest Melanoma Cases and Should Be Performed for Thick Melanomas. Ann Surg Oncol. 2021; 28(2): 1007–1016.
- Bello DM, Faries MB. The Landmark Series: MSLT-1, MSLT-2 and DeCOG (Management of Lymph Nodes). Ann Surg Oncol. 2020; 27(1): 15–21.
- Rychlik A, Zalewski K. Tracers and corresponding detection devices: technetium colloids, blue dyes & NIR fluorescence. Chin Clin Oncol. 2021; 10(2): 16.
- Lee A, Kim HJ, Kim E, et al. Complications and outcomes following inguinal lymphadenectomy for malignant melanoma in an Asian population. Korean J Clin Oncol. 2020; 16(2): 71–78.
- Moody JA, Ali RF, Carbone AC, et al. Complications of sentinel lymph node biopsy for melanoma - A systematic review of the literature. Eur J Surg Oncol. 2017; 43(2): 270–277.
- Guo RQ, Xiang Xi, Wang LY, et al. Percutaneous contrast-enhanced ultrasound for localization and qualitative diagnosis of sentinel lymph nodes in cutaneous malignant melanoma of lower extremities: a preliminary study. Quant Imaging Med Surg. 2022; 12(1): 366–375.
- McGregor A, Kim S, Norwich-Cavanaugh A, et al. Clinical Value of Single-photon Emission Computed Tomography Combined With Computed Tomography for Sentinel Lymph Node Identification in Melanoma. Ann Plast Surg. 2019; 82(4S Suppl 3): S192–S194.
- Rutkowski P, Wysocki P, Kozak K, et al. Expert recommendations on diagnostic-therapeutic management of melanoma patients. Oncol Clin Pract. 2022; 18(6): 357–392.
- Berger DMS, van den Berg NS, van der Noort V, et al. Technologic (R)Evolution Leads to Detection of More Sentinel Nodes in Patients with Melanoma in the Head and Neck Region. J Nucl Med. 2021; 62(10): 1357–1362.
- Sondak VK, King DW, Zager JS, et al. Combined analysis of phase III trials evaluating [⁹⁹mTc]tilmanocept and vital blue dye for identification of sentinel lymph nodes in clinically node-negative cutaneous melanoma. Ann Surg Oncol. 2013; 20(2): 680–688.
- Lese I, Constantinescu MA, Leckenby JI, et al. Transcutaneous sentinel lymph node detection in cutaneous melanoma with indocyanine green and near-infrared fluorescence: A diagnostic sensitivity study. Medicine (Baltimore). 2022; 101(36): e30424.
- Thompson JF, London K, Uren RF, et al. Same-day or next-day sentinel node biopsy after lymphoscintigraphy for melanoma using Tc-labelled antimony sulphide colloid. Br J Surg. 2020; 107(13): 1773–1779.
- Upadhyaya SN, Knackstedt RW, Ko JS, et al. The Use and Technique of Sentinel Node Biopsy for Skin Cancer. Plast Reconstr Surg. 2022; 149(5): 995e–9951008e.
- Peek MCl, Charalampoudis P, Anninga B, et al. Blue dye for identification of sentinel nodes in breast cancer and malignant melanoma: a systematic review and meta-analysis. Future Oncol. 2017; 13(5): 455–467.
- Mariani G, Erba P, Manca G, et al. Radioguided sentinel lymph node biopsy in patients with malignant cutaneous melanoma: the nuclear medicine contribution. J Surg Oncol. 2004; 85(3): 141–151.
- Gennari R, Bartolomei M, Testori A, et al. Sentinel node localization in primary melanoma: preoperative dynamic lymphoscintigraphy, intraoperative gamma probe, and vital dye guidance. Surgery. 2000; 127(1): 19–25.
- Kim TH, Kim HJ, Seo JW, et al. Efficacy and clinical significance of omitting blue dye injection during sentinel lymph node biopsy before Mohs micrographic surgery for malignant melanoma of the lower extremities. Br J Dermatol. 2020; 182(2): 427–433.
- Leong SPL, Kim J, Ross M, et al. A phase 2 study of (99m)Tc-tilmanocept in the detection of sentinel lymph nodes in melanoma and breast cancer. Ann Surg Oncol. 2011; 18(4): 961–969.
- Gesuelli GC, Sartelli M, Berbellini A, et al. [Sentinel lymph node identification in the staging of cutaneous melanoma. Blue dye vs. radioguided localization]. Minerva Chir. 2000; 55(7-8): 513–516.
- Gipponi M, Di Somma C, Peressini A, et al. Sentinel lymph node biopsy in patients with Stage I/II melanoma: Clinical experience and literature review. J Surg Oncol. 2004; 85(3): 133–140.
- Landi G, Polverelli M, Moscatelli G, et al. Sentinel lymph node biopsy in patients with primary cutaneous melanoma: study of 455 cases. J Eur Acad Dermatol Venereol. 2000; 14(1): 35–45.
- Karakousis CP, Grigoropoulos P. Sentinel node biopsy before and after wide excision of the primary melanoma. Ann Surg Oncol. 1999; 6(8): 785–789.
- Morton DL, Thompson JF, Essner R, et al. Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: a multicenter trial. Multicenter Selective Lymphadenectomy Trial Group. Ann Surg. 1999; 230(4): 453–63; discussion 463.
- Bostick P, Essner R, Sarantou T, et al. Intraoperative lymphatic mapping for early-stage melanoma of the head and neck. Am J Surg. 1997; 174(5): 536–539.
- Gesuelli GC, Berbellini A, Brianzoni E, et al. THE SENTINEL NODE IN CUTANEOUS MELANOMA. Ann Ital Chir. 2000; 71(2): 169–176.
- Faries M, Thompson J, Cochran A, et al. Completion Dissection or Observation for Sentinel-Node Metastasis in Melanoma. N Engl J Med. 2017; 376(23): 2211–2222.
- Nejc D, Wrzesień M, Piekarski J, et al. Sentinel node biopsy in skin melanoma patients--measurements of absorbed doses of radiation to the hands of medical staff. J Surg Oncol. 2006; 93(5): 355–361.
- Brănişteanu DE, Cozmin M, Porumb-Andrese E, et al. Sentinel Lymph Node Biopsy in Cutaneous Melanoma, a Clinical Point of View. Medicina (Kaunas). 2022; 58(11).
- Cimmino VM, Brown AC, Szocik JF, et al. Allergic reactions to isosulfan blue during sentinel node biopsy--a common event. Surgery. 2001; 130(3): 439–442.
- Keller B, Yawalkar N, Pichler C, et al. Hypersensitivity reaction against patent blue during sentinel lymph node removal in three melanoma patients. Am J Surg. 2007; 193(1): 122–124.
- Dewachter P, Mouton-Faivre C, Tréchot P, et al. Severe anaphylactic shock with methylene blue instillation. Anesth Analg. 2005; 101(1): 149–50, table of contents.
- Rzymski P, Wozniak J, Opala T, et al. Anaphylactic reaction to methylene blue dye after laparoscopic chromopertubation. Int J Gynaecol Obstet. 2003; 81(1): 71–72.
- Albo D, Wayne JD, Hunt KK, et al. Anaphylactic reactions to isosulfan blue dye during sentinel lymph node biopsy for breast cancer. Am J Surg. 2001; 182(4): 393–398.
- Olson MT, Ly QP, Mohs AM. Fluorescence Guidance in Surgical Oncology: Challenges, Opportunities, and Translation. Mol Imaging Biol. 2019; 21(2): 200–218.
- Srivastava A, Goyal A, Seenu V, et al. Evaluation of New Tracers in the Identification of Sentinel Lymph Node in Patients with Early Breast Cancer. Indian J Nucl Med. 2023; 38(1): 91–95.
- Pandit-Taskar N, Dauer LT, Montgomery L, et al. Organ and fetal absorbed dose estimates from 99mTc-sulfur colloid lymphoscintigraphy and sentinel node localization in breast cancer patients. J Nucl Med. 2006; 47(7): 1202–1208.
- Andtbacka RHI, Donaldson MR, Bowles TL, et al. Sentinel lymph node biopsy for melanoma in pregnant women. Ann Surg Oncol. 2013; 20(2): 689–696.
- Pham Dang N, Cassier S, Mulliez A, et al. Eight Years' Experience of Sentinel Lymph Node Biopsy in Melanoma Using Lymphoscintigraphy and Gamma Probe Detection After Radiocolloid Mapping. Dermatol Surg. 2017; 43(2): 287–292.
- Anninga B, White SH, Moncrieff M, et al. MELAMAG Multicentre Trialists Group. Magnetic Technique for Sentinel Lymph Node Biopsy in Melanoma: The MELAMAG Trial. Ann Surg Oncol. 2016; 23(6): 2070–2078.
- Wagner JD, Park HM, Coleman JJ, et al. Cervical sentinel lymph node biopsy for melanomas of the head and neck and upper thorax. Arch Otolaryngol Head Neck Surg. 2000; 126(3): 313–321.
- Niebling MG, Pleijhuis RG, Bastiaannet E, et al. A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping. Eur J Surg Oncol. 2016; 42(4): 466–473.
- Knackstedt RW, Couto RA, Gastman B. Indocyanine green fluorescence imaging with lymphoscintigraphy for sentinel node biopsy in head and neck melanoma. J Surg Res. 2018; 228: 77–83.
- Couto RA, Lamaris GA, Knackstedt R, et al. Determining the False-Negative Rate Using Fluorescence Image-Assisted Sentinel Lymph Node Biopsy in Cutaneous Melanoma. Ann Plast Surg. 2018; 80(1): 54–58.
- Knackstedt R, Gastman BR. Indocyanine Green Fluorescence Imaging with Lymphoscintigraphy Improves the Accuracy of Sentinel Lymph Node Biopsy in Melanoma. Plast Reconstr Surg. 2021; 148(1): 83e–93e.
- Stoffels I, Dissemond J, Pöppel T, et al. Intraoperative Fluorescence Imaging for Sentinel Lymph Node Detection: Prospective Clinical Trial to Compare the Usefulness of Indocyanine Green vs Technetium Tc 99m for Identification of Sentinel Lymph Nodes. JAMA Surg. 2015; 150(7): 617–623.
- Houpeau JL, Chauvet MP, Guillemin F, et al. Sentinel lymph node identification using superparamagnetic iron oxide particles versus radioisotope: The French Sentimag feasibility trial. J Surg Oncol. 2016; 113(5): 501–507.
- Mirzaei N, Katsarelias D, Zaar P, et al. Sentinel lymph node localization and staging with a low-dose of superparamagnetic iron oxide (SPIO) enhanced MRI and magnetometer in patients with cutaneous melanoma of the extremity - The MAGMEN feasibility study. Eur J Surg Oncol. 2022; 48(2): 326–332.
- Piñero-Madrona A, Nicolás-Ruiz F, Rull-Ortuño R, et al. Correlation between ferromagnetic and isotopic tracers for sentinel lymph node detection in cutaneous melanoma: IMINEM study. J Surg Oncol. 2021; 123(2): 654–659.
- Schaarschmidt BM, Grueneisen J, Stebner V, et al. Can integrated 18F-FDG PET/MR replace sentinel lymph node resection in malignant melanoma? Eur J Nucl Med Mol Imaging. 2018; 45(12): 2093–2102.
- Wagner JD, Schauwecker D, Davidson D, et al. Prospective study of fluorodeoxyglucose-positron emission tomography imaging of lymph node basins in melanoma patients undergoing sentinel node biopsy. J Clin Oncol. 1999; 17(5): 1508–1515.
- Wagner JD, Schauwecker D, Davidson D, et al. Inefficacy of F-18 fluorodeoxy-D-glucose-positron emission tomography scans for initial evaluation in early-stage cutaneous melanoma. Cancer. 2005; 104(3): 570–579.
- Zamani-Siahkali N, Mirshahvalad SA, Pirich C, et al. Diagnostic Performance of [F]F-FDG Positron Emission Tomography (PET) in Non-Ophthalmic Malignant Melanoma: A Systematic Review and Meta-Analysis of More Than 10,000 Melanoma Patients. Cancers (Basel). 2024; 16(1).
- Horn J, Lock-Andersen J, Sjøstrand H, et al. Routine use of FDG-PET scans in melanoma patients with positive sentinel node biopsy. Eur J Nucl Med Mol Imaging. 2006; 33(8): 887–892.
- de Carvalho CE, Capuzzo R, Crovador C, et al. Near Infrared (NIR) Fluorescence is Not a Substitute for Lymphoscintigraphy and Gamma Probe for Melanoma Sentinel Node Detection: Results from a Prospective Trial. Ann Surg Oncol. 2020; 27(8): 2906–2912.
- Cloyd JM, Wapnir IL, Read BM, et al. Indocyanine green and fluorescence lymphangiography for sentinel lymph node identification in cutaneous melanoma. J Surg Oncol. 2014; 110(7): 888–892.
- Morrison S, Han D. Re-evaluation of Sentinel Lymph Node Biopsy for Melanoma. Curr Treat Options Oncol. 2021; 22(3): 22.
- Fujiwara M, Mizukami T, Suzuki A, et al. Sentinel lymph node detection in skin cancer patients using real-time fluorescence navigation with indocyanine green: preliminary experience. J Plast Reconstr Aesthet Surg. 2009; 62(10): e373–e378.
- Beniey M, Tran A, Boulva K. Mapping sentinel lymph nodes in cutaneous melanoma: a vast array of perioperative imaging modalities. Melanoma Res. 2021; 31(2): 108–118.
- Ballardini B, Santoro L, Sangalli C, et al. The indocyanine green method is equivalent to the ⁹⁹mTc-labeled radiotracer method for identifying the sentinel node in breast cancer: a concordance and validation study. Eur J Surg Oncol. 2013; 39(12): 1332–1336.
- Schaafsma BE, Mieog JS, Hutteman M, 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): 323–332.
- Pameijer CR, Leung A, Neves RI, et al. Indocyanine green and fluorescence lymphangiography for sentinel node identification in patients with melanoma. Am J Surg. 2018; 216(3): 558–561.
- Hersi AF, Eriksson S, Ramos J, et al. A combined, totally magnetic technique with a magnetic marker for non-palpable tumour localization and superparamagnetic iron oxide nanoparticles for sentinel lymph node detection in breast cancer surgery. Eur J Surg Oncol. 2019; 45(4): 544–549.
- Piñero-Madrona A, Torró-Richart JA, de León-Carrillo JM, et al. Grupo de Estudios Senológicos de la Sociedad Española de Patologia Mamaria (SESPM). Superparamagnetic iron oxide as a tracer for sentinel node biopsy in breast cancer: A comparative non-inferiority study. Eur J Surg Oncol. 2015; 41(8): 991–997.
- Man V, Wong TT, Co M, et al. Sentinel Lymph Node Biopsy in Early Breast Cancer: Magnetic Tracer as the Only Localizing Agent. World J Surg. 2019; 43(8): 1991–1996.
- Alvarado MD, Mittendorf EA, Teshome M, et al. SentimagIC: A Non-inferiority Trial Comparing Superparamagnetic Iron Oxide Versus Technetium-99m and Blue Dye in the Detection of Axillary Sentinel Nodes in Patients with Early-Stage Breast Cancer. Ann Surg Oncol. 2019; 26(11): 3510–3516.
- Karakatsanis A, Christiansen PM, Fischer L, et al. The Nordic SentiMag trial: a comparison of super paramagnetic iron oxide (SPIO) nanoparticles versus Tc(99) and patent blue in the detection of sentinel node (SN) in patients with breast cancer and a meta-analysis of earlier studies. Breast Cancer Res Treat. 2016; 157(2): 281–294.
- Karakatsanis A, Daskalakis K, Stålberg P, et al. Superparamagnetic iron oxide nanoparticles as the sole method for sentinel node biopsy detection in patients with breast cancer. Br J Surg. 2017; 104(12): 1675–1685.
- Health C for D and R. Magtrace and Sentimag Magnetic Localization System - P160053/S002. FDA. Published online December 22, 2022. https://www.fda.gov/medical-devices/recently-approved-devices/magtrace-and-sentimag-magnetic-localization-system-p160053s002 (28.03.2024).
- Ghilli M, Carretta E, Di Filippo F, et al. The superparamagnetic iron oxide tracer: a valid alternative in sentinel node biopsy for breast cancer treatment. Eur J Cancer Care (Engl). 2017; 26(4).
- Yılmaz H, Orhan E, Şahin E, et al. Efficacy of positron emission tomography and computed tomography in clinical staging of cutaneous malignant melanoma. Dermatol Ther. 2020; 33(3): e13304.
- Jiménez-Requena F, Delgado-Bolton RC, Fernández-Pérez C, et al. Meta-analysis of the performance of (18)F-FDG PET in cutaneous melanoma. Eur J Nucl Med Mol Imaging. 2010; 37(2): 284–300.
- Tanaka E, Choi HS, Fujii H, et al. Image-guided oncologic surgery using invisible light: completed pre-clinical development for sentinel lymph node mapping. Ann Surg Oncol. 2006; 13(12): 1671–1681.
- Uhara H, Yamazaki N, Takata M, et al. Applicability of radiocolloids, blue dyes and fluorescent indocyanine green to sentinel node biopsy in melanoma. J Dermatol. 2012; 39(4): 336–338.
- Fadel MG, Rauf S, Mohamed HS, et al. The Use of Indocyanine Green and Near-Infrared Fluorescence Imaging Versus Blue Dye in Sentinel Lymph Node Biopsy in Cutaneous Melanoma: A Retrospective, Cohort Study. Ann Surg Oncol. 2023; 30(7): 4333–4340.
- Cousins A, Thompson SK, Wedding AB, et al. Clinical relevance of novel imaging technologies for sentinel lymph node identification and staging. Biotechnol Adv. 2014; 32(2): 269–279.
- Thill M, Kurylcio A, Welter R, et al. The Central-European SentiMag study: sentinel lymph node biopsy with superparamagnetic iron oxide (SPIO) vs. radioisotope. Breast. 2014; 23(2): 175–179.
- Rubio IT, Diaz-Botero S, Esgueva A, et al. The superparamagnetic iron oxide is equivalent to the Tc99 radiotracer method for identifying the sentinel lymph node in breast cancer. Eur J Surg Oncol. 2015; 41(1): 46–51.
- Douek M, Klaase J, Monypenny I, et al. SentiMAG Trialists Group. Sentinel node biopsy using a magnetic tracer versus standard technique: the SentiMAG Multicentre Trial. Ann Surg Oncol. 2014; 21(4): 1237–1245.
- Dellavedova L, Florimonte L, Carletto M, et al. Missing sentinel lymph node in cutaneous melanoma. Indian J Nucl Med. 2015; 30(2): 158–161.
- Jansen L, Koops HS, Nieweg OE, et al. Sentinel node biopsy for melanoma in the head and neck region. Head Neck. 2000; 22(1): 27–33, doi: 10.1002/(sici)1097-0347(200001)22:1<27::aid-hed5>3.0.co;2-z.
- de Rosa N, Lyman GH, Silbermins D, et al. Sentinel node biopsy for head and neck melanoma: a systematic review. Otolaryngol Head Neck Surg. 2011; 145(3): 375–382.
- Passmore-Webb B, Gurney B, Yuen HM, et al. Sentinel lymph node biopsy for melanoma of the head and neck: a multicentre study to examine safety, efficacy, and prognostic value. Br J Oral Maxillofac Surg. 2019; 57(9): 891–897.
- Kwak JJ, Kesner AL, Gleisner A, et al. Utility of Quantitative SPECT/CT Lymphoscintigraphy in Guiding Sentinel Lymph Node Biopsy in Head and Neck Melanoma. Ann Surg Oncol. 2020; 27(5): 1432–1438.
- Oliver JR, Karadaghy OA, Fassas SN, et al. Machine learning directed sentinel lymph node biopsy in cutaneous head and neck melanoma. Head Neck. 2022; 44(4): 975–988.
- Zhang Y, Liu C, Wang Z, et al. Sentinel lymph node biopsy in head and neck cutaneous melanomas: A PRISMA-compliant systematic review and meta-analysis. Medicine (Baltimore). 2021; 100(5): e24284.