Robot-assisted fluorescent sentinel lymph node identification in early-stage colon cancer

Abstract

Background: Patients with cT1-2 colon cancer (CC) have a 10-20% risk of lymph node metastases. Sentinel lymph node identification (SLNi) could improve staging and reduce morbidity in future organ-preserving CC surgery. This pilot study aimed to assess safety and feasibility of robot-assisted fluorescence-guided SLNi using submucosally injected indocyanine green (ICG) in patients with cT1-2N0M0 CC.

Methods: Ten consecutive patients with cT1-2N0M0 CC were included in this prospective feasibility study. Intraoperative submucosal, peritumoral injection of ICG was performed during a colonoscopy. Subsequently, the near-infrared fluorescence 'Firefly' mode of the da Vinci Xi robotic surgical system was used for SLNi. SLNs were marked with a suture, after which a segmental colectomy was performed. The SLN was postoperatively ultrastaged using serial slicing and immunohistochemistry, in addition to the standard pathological examination of the specimen. Colonoscopy time, detection time (time from ICG injection to first SLNi), and total SLNi time were measured (time from the start of colonoscopy to start of segmental resection). Intraoperative, postoperative, and pathological outcomes were registered.

Results: In all patients, at least one SLN was identified (mean 2.3 SLNs, SLN diameter range 1-13 mm). No tracer-related adverse events were noted. Median colonoscopy time was 12 min, detection time was 6 min, and total SLNi time was 30.5 min. Two patients had lymph node metastases present in the SLN, and there were no patients with false negative SLNs. No patient was upstaged due to ultrastaging of the SLN after an initial negative standard pathological examination. Half of the patients unexpectedly had pT3 tumours.

Conclusions: Robot-assisted fluorescence-guided SLNi using submucosally injected ICG in ten patients with cT1-2N0M0 CC was safe and feasible. SLNi was performed in an acceptable timespan and SLNs down to 1 mm were detected. All lymph node metastases would have been detected if SLN biopsy had been performed.

Keywords: Colon cancer; Image-guided surgery; Indocyanine green (ICG); Near-infrared fluorescence (NIRF); Robotic surgical procedures; Sentinel lymph node (SLN).

Fig. 1

a The near-infrared fluorescence (NIRF) view of the mesocolon, b annotated picture, and c and the white-light picture of the same view as a reference. a Two sentinel lymph nodes (SLNs) and the corresponding lymphatic vessels were visible using NIRF. b The first and second visible SLN are highlighted with a white and red circle, respectively; both SLNs were to become brighter after waiting some time. The lymph vessels are highlighted in green. Bringing the camera closer to the tissue would also improve visibility of the SLNs (Color figure online)

Fig. 2

Massive lymph node metastases in a SLN. a Ex vivo macroscopic view with the Firefly after the SLN (9 mm in diameter) was isolated from the specimen. NIRF in the SLN was unevenly distributed. b, d Two intervals of the same SLN on microscope slides with hematoxylin and eosin (H&E) staining with a black bar demonstrating 1 mm. c, e The NIRF view of the same slides with the LI-COR Odyssey CLx flatbed imager (LI-COR Biosciences Inc., NE, USA); bright yellow represents a high fluorescence signal, while dark purple represents a low signal. b Lymph node metastases, displayed in the green circle, surrounded by normal lymph node tissue. Sidenote: ink from the endoscopic tattoo was visible in the SLN; an example is magnified. c The flatbed scanner showed reduced NIRF in and near the lymph node metastases. d Metastases almost entirely occupied this SLN interval with only a small area of residual normal lymph node tissue displayed in the blue circle. e The NIRF signal is low to absent in the microscope slide compared to panel (c) (Color figure online)