{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T18:44:46Z","timestamp":1790707486897,"version":"4.1.0"},"reference-count":40,"publisher":"MDPI AG","issue":"23","license":[{"start":{"date-parts":[[2024,11,22]],"date-time":"2024-11-22T00:00:00Z","timestamp":1732233600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Objectives: To assess the efficacy of magnetic resonance (MR) lymphography with gadobutrol contrast for sentinel lymph node (SLN) mapping in early-stage oral squamous cell carcinoma (OSCC). Methods: This pilot study compared the identification of SLNs by MR lymphography using a gadolinium-based contrast agent (gadobutrol) to conventional [99mTc]Tc-nanocolloid lymphoscintigraphy (including single-photon emission computed tomography\/computed tomography (SPECT\/CT)) in 10 early-stage OSCC patients undergoing SLN biopsy. The patients initially underwent conventional lymphoscintigraphy following the peritumoral administration of indocyanine green [99mTc]Tc-nanocolloid (120 megabecquerel; ~0.5 mL). Subsequently, 0.5\u20131.0 mL gadobutrol was peritumorally injected, and MR imaging was acquired for 30 min. The following day, the identified SLNs were harvested and subjected to a histopathological assessment. The MR lymphography and [99mTc]Tc-nanocolloid lymphoscintigraphy results were evaluated and compared with respect to those of the SLN identification. The reference standard consisted of a histopathological evaluation of the harvested SLNs, complementary neck dissection specimens, and follow-up data. Results: The MR lymphography detected 16 out of 27 SLNs identified by [99mTc]Tc-nanocolloid lymphoscintigraphy, revealing an additional SLN that did not harbor metastasis. MR lymphography failed to identify any SLNs in one patient. Of the seven histopathologically positive SLNs detected by [99mTc]Tc-nanocolloid lymphoscintigraphy, three were identified by MR lymphography. All patients remained disease-free after a median follow-up of 16 months. Compared to [99mTc]Tc-nanocolloid lymphoscintigraphy, MR lymphography using gadobutrol achieved an SLN identification rate of 59%, a sensitivity of 75%, and a negative predictive value of 86%. Conclusions: MR lymphography using gadobutrol demonstrates limited reliability for SLN mapping in early-stage OSCC.<\/jats:p>","DOI":"10.3390\/jcm13237052","type":"journal-article","created":{"date-parts":[[2024,11,22]],"date-time":"2024-11-22T06:41:48Z","timestamp":1732257708000},"page":"7052","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Sentinel Lymph Node Detection in Early-Stage Oral Squamous Cell Carcinoma Using Magnetic Resonance Lymphography: A Pilot Study"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9359-8205","authenticated-orcid":false,"given":"Dominique N. V.","family":"Donders","sequence":"first","affiliation":[{"name":"Department of Head and Neck Surgical Oncology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8518-4659","authenticated-orcid":false,"given":"Rutger","family":"Mahieu","sequence":"additional","affiliation":[{"name":"Department of Head and Neck Surgical Oncology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roosmarijn S.","family":"Tellman","sequence":"additional","affiliation":[{"name":"Department of Head and Neck Surgical Oncology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0205-3459","authenticated-orcid":false,"given":"Marielle E. P.","family":"Philippens","sequence":"additional","affiliation":[{"name":"Department of Radiotherapy, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert J. J.","family":"van Es","sequence":"additional","affiliation":[{"name":"Department of Head and Neck Surgical Oncology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ellen M.","family":"Van Cann","sequence":"additional","affiliation":[{"name":"Department of Head and Neck Surgical Oncology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0365-3667","authenticated-orcid":false,"given":"Gerben E.","family":"Breimer","sequence":"additional","affiliation":[{"name":"Department of Pathology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7128-5814","authenticated-orcid":false,"given":"Remco","family":"de Bree","sequence":"additional","affiliation":[{"name":"Department of Head and Neck Surgical Oncology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6270-9483","authenticated-orcid":false,"given":"Bart","family":"de Keizer","sequence":"additional","affiliation":[{"name":"Department of Radiology and Nuclear Medicine, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,11,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"4010","DOI":"10.1200\/JCO.20.01661","article-title":"Equivalence Randomized Trial to Compare Treatment on the Basis of Sentinel Node Biopsy Versus Neck Node Dissection in Operable T1-T2N0 Oral and Oropharyngeal Cancer","volume":"38","author":"Garrel","year":"2020","journal-title":"J. Clin. Oncol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1200\/JCO.20.03637","article-title":"Neck Dissections Based on Sentinel Lymph Node Navigation Versus Elective Neck Dissections in Early Oral Cancers: A Randomized, Multicenter, and Noninferiority Trial","volume":"39","author":"Hasegawa","year":"2021","journal-title":"J. Clin. Oncol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"105642","DOI":"10.1016\/j.oraloncology.2021.105642","article-title":"Systematic review and meta-analysis of randomized controlled trials comparing elective neck dissection versus sentinel lymph node biopsy in early-stage clinically node-negative oral and\/or oropharyngeal squamous cell carcinoma: Evidence-base for practice and implications for research","volume":"124","author":"Gupta","year":"2022","journal-title":"Oral Oncol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1007\/s00259-017-3613-8","article-title":"The added value of SPECT-CT for the identification of sentinel lymph nodes in early stage oral cancer","volume":"44","author":"Karagozoglu","year":"2017","journal-title":"Eur. J. Nucl. Med. Mol. Imaging"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"den Toom, I.J., Boeve, K., Lobeek, D., Bloemena, E., Donswijk, M.L., de Keizer, B., Klop, W.M.C., Leemans, C.R., Willems, S.M., and Takes, R.P. (2020). Elective Neck Dissection or Sentinel Lymph Node Biopsy in Early Stage Oral Cavity Cancer Patients: The Dutch Experience. Cancers, 12.","DOI":"10.3390\/cancers12071783"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.bjoms.2020.08.057","article-title":"Challenges and outcomes in establishing a sentinel lymph node biopsy service for oral squamous cell carcinoma in a regional district specialist hospital","volume":"59","author":"Bowe","year":"2021","journal-title":"Br. J. Oral Maxillofac. Surg."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Mahieu, R., de Maar, J.S., Nieuwenhuis, E.R., Deckers, R., Moonen, C., Alic, L., Haken, B.T., de Keizer, B., and de Bree, R. (2020). New Developments in Imaging for Sentinel Lymph Node Biopsy in Early-Stage Oral Cavity Squamous Cell Carcinoma. Cancers, 12.","DOI":"10.3390\/cancers12103055"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1245\/s10434-006-9099-4","article-title":"Lymphoseek: A molecular imaging agent for melanoma sentinel lymph node mapping","volume":"14","author":"Wallace","year":"2007","journal-title":"Ann. Surg. Oncol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1002\/jso.20862","article-title":"PET probe-guided surgery","volume":"96","author":"Gulec","year":"2007","journal-title":"J. Surg. Oncol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"507","DOI":"10.3109\/00016489.2015.1010126","article-title":"Sentinel lymph node biopsy using computed tomographic lymphography in patients with early tongue cancer","volume":"135","author":"Honda","year":"2015","journal-title":"Acta Otolaryngol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1002\/hed.25167","article-title":"MR lymphography for sentinel lymph node detection in patients with oral cavity cancer: Preliminary clinical study","volume":"40","author":"Bae","year":"2018","journal-title":"Head Neck"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Li, C., Meng, S., Yang, X., Zhou, D., Wang, J., and Hu, J. (2015). Sentinel lymph node detection using magnetic resonance lymphography with conventional gadolinium contrast agent in breast cancer: A preliminary clinical study. BMC Cancer, 15.","DOI":"10.1186\/s12885-015-1255-4"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Lu, Q., Hua, J., Kassir, M.M., Delproposto, Z., Dai, Y., Sun, J., Haacke, M., and Hu, J. (2013). Imaging lymphatic system in breast cancer patients with magnetic resonance lymphangiography. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0069701"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Brierley, J.D., Gospodarowicz, M., and Wittekind, C. (2017). UICC TNM Classification of Malignant Tumours, Wiley. [8th ed.].","DOI":"10.1002\/9780471420194.tnmc26.pub3"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1102\/1470-7330.2008.0006","article-title":"Ultrasound of malignant cervical lymph nodes","volume":"8","author":"Ahuja","year":"2008","journal-title":"Cancer Imaging"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"5519","DOI":"10.1007\/s00405-023-08138-y","article-title":"The potential of the Crystal Cam handheld gamma-camera for preoperative and intraoperative sentinel lymph node localization in early-stage oral cancer","volume":"280","author":"Mahieu","year":"2023","journal-title":"Eur. Arch. Otorhinolaryngol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3190","DOI":"10.1245\/s10434-009-0726-8","article-title":"Joint practice guidelines for radionuclide lymphoscintigraphy for sentinel node localization in oral\/oropharyngeal squamous cell carcinoma","volume":"16","author":"Alkureishi","year":"2009","journal-title":"Ann. Surg. Oncol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"436","DOI":"10.4103\/0973-029X.190946","article-title":"Detection of cervical lymph node micrometastasis and isolated tumor cells in oral squamous cell carcinoma using immunohistochemistry and serial sectioning","volume":"20","author":"Dhawan","year":"2016","journal-title":"J. Oral Maxillofac. Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2668","DOI":"10.1002\/(SICI)1097-0142(19991215)86:12<2668::AID-CNCR11>3.0.CO;2-R","article-title":"International Union Against Cancer. Classification of isolated tumor cells and micrometastasis","volume":"86","author":"Hermanek","year":"1999","journal-title":"Cancer"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1007\/s00259-018-4235-5","article-title":"The EANM practical guidelines for sentinel lymph node localisation in oral cavity squamous cell carcinoma","volume":"46","author":"Giammarile","year":"2019","journal-title":"Eur. J. Nucl. Med. Mol. Imaging"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1097\/RLU.0b013e31828da362","article-title":"Improved detection of sentinel lymph nodes in SPECT\/CT images acquired using a low- to medium-energy general-purpose collimator","volume":"39","author":"Yoneyama","year":"2014","journal-title":"Clin. Nucl. Med."},{"key":"ref_22","first-page":"90","article-title":"Using the Common Terminology Criteria for Adverse Events (CTCAE\u2014Version 5.0) to Evaluate the Severity of Adverse Events of Anticancer Therapies","volume":"112","author":"Santana","year":"2021","journal-title":"Actas Dermosifiliogr. (Engl Ed)."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1159\/000077232","article-title":"Immunohistochemical studies in the identification of lymph node micrometastases in patients with squamous cell carcinoma of the head and neck","volume":"66","author":"Rinaldo","year":"2004","journal-title":"ORL J. Otorhinolaryngol. Relat. Spec."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2985","DOI":"10.1002\/hed.26784","article-title":"Serial step sections at narrow intervals with immunohistochemistry are required for accurate histological assessment of sentinel lymph node biopsy in oral squamous cell carcinoma","volume":"43","author":"King","year":"2021","journal-title":"Head Neck"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1016\/j.ijrobp.2006.05.045","article-title":"Indirect MR lymphangiography of the head and neck using conventional gadolinium contrast: A pilot study in humans","volume":"66","author":"Loo","year":"2006","journal-title":"Int. J. Radiat. Oncol. Biol. Phys."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1080\/1061186X.2018.1545235","article-title":"Poly(ethylene glycol)-alendronate coated nanoparticles for magnetic resonance imaging of lymph nodes","volume":"27","author":"Bisso","year":"2019","journal-title":"J. Drug Target."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1007\/s11282-020-00442-1","article-title":"Sentinel lymph node mapping of clinically N0 early oral cancer: A diagnostic pitfall on CT lymphography","volume":"37","author":"Sugiyama","year":"2021","journal-title":"Oral Radiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1007\/s00259-018-4028-x","article-title":"The best of both worlds: A hybrid approach for optimal pre- and intraoperative identification of sentinel lymph nodes","volume":"45","author":"KleinJan","year":"2018","journal-title":"Eur. J. Nucl. Med. Mol. Imaging"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1002\/jso.25810","article-title":"Magnetic detection of sentinel nodes in oral squamous cell carcinoma by means of superparamagnetic iron oxide contrast","volume":"121","author":"Hernando","year":"2020","journal-title":"J. Surg. Oncol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"418","DOI":"10.3109\/00016489.2012.744143","article-title":"Superparamagnetic iron oxide-enhanced interstitial magnetic resonance lymphography to detect a sentinel lymph node in tongue cancer patients","volume":"133","author":"Mizokami","year":"2013","journal-title":"Acta Otolaryngol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1007\/s00259-006-0223-2","article-title":"Multimodal fusion imaging ensemble for targeted sentinel lymph node management: Initial results of an innovative promising approach for anatomically difficult lymphatic drainage in different tumour entities","volume":"34","author":"Maza","year":"2007","journal-title":"Eur. J. Nucl. Med. Mol. Imaging"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1007\/s00247-016-3599-6","article-title":"Safety of gadobutrol in more than 1,000 pediatric patients: Subanalysis of the GARDIAN study, a global multicenter prospective non-interventional study","volume":"46","author":"Glutig","year":"2016","journal-title":"Pediatr. Radiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1148\/radiology.162.1.3786748","article-title":"Low-osmolality contrast media: Premises and promises","volume":"162","author":"McClennan","year":"1987","journal-title":"Radiology"},{"key":"ref_34","first-page":"216","article-title":"Contrast agent design","volume":"24","year":"1969","journal-title":"Some aspects on the synthesis of water soluble contrast agents of low osmolality. J. Theor. Biol."},{"key":"ref_35","first-page":"100696","article-title":"Personalized neck irradiation guided by sentinel lymph node biopsy in patients with squamous cell carcinoma of the oropharynx, larynx or hypopharynx with a clinically negative neck: (Chemo)radiotherapy to the PRIMary tumor only. Protocol of the PRIMO study","volume":"44","author":"Takes","year":"2024","journal-title":"Clin. Transl. Radiat. Oncol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1007\/s00405-018-5050-0","article-title":"SPECT\/CT-guided lymph drainage mapping for the planning of unilateral elective nodal irradiation in head and neck squamous cell carcinoma","volume":"275","author":"Jonker","year":"2018","journal-title":"Eur. Arch. Otorhinolaryngol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"de Veij Mestdagh, P.D., Schreuder, W.H., Vogel, W.V., Donswijk, M.L., van Werkhoven, E., van der Wal, J.E., Dirven, R., Karakullukcu, B., Sonke, J.J., and Van Den Brekel, M.W. (2019). Mapping of sentinel lymph node drainage using SPECT\/CT to tailor elective nodal irradiation in head and neck cancer patients (SUSPECT-2): A single-center prospective trial. BMC Cancer, 19.","DOI":"10.1186\/s12885-019-6331-8"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.radonc.2020.03.012","article-title":"SPECT\/CT-guided elective nodal irradiation for head and neck cancer is oncologically safe and less toxic: A potentially practice-changing approach","volume":"147","author":"Walraven","year":"2020","journal-title":"Radiother. Oncol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2777","DOI":"10.1016\/j.ejca.2015.08.023","article-title":"Sentinel European Node Trial (SENT): 3-year results of sentinel node biopsy in oral cancer","volume":"51","author":"Schilling","year":"2015","journal-title":"Eur. J. Cancer"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.2967\/jnumed.120.246819","article-title":"Technologic (R)Evolution Leads to Detection of More Sentinel Nodes in Patients with Melanoma in the Head and Neck Region","volume":"62","author":"Berger","year":"2021","journal-title":"J. Nucl. Med."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/23\/7052\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:37:21Z","timestamp":1760114241000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/23\/7052"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,22]]},"references-count":40,"journal-issue":{"issue":"23","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["jcm13237052"],"URL":"https:\/\/doi.org\/10.3390\/jcm13237052","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,22]]}}}