Exploratory analysis of lateral pelvic sentinel lymph node status for optimal management of laparoscopic lateral lymph node dissection in advanced lower rectal cancer without suspected lateral lymph node metastasis

Yasui et al. BMC Cancer (2021) 21:911 https://doi.org/10.1186/s12885-021-08480-6 RESEARCH ARTICLE Open Access Exploratory analysis of lateral pelvic sentinel lymph node status for optimal management of laparoscopic lateral lymph node dissection in advanced lower rectal cancer without suspected lateral lymph node metastasis Masayoshi Yasui1*, Masayuki Ohue1, Shingo Noura2, Norikatsu Miyoshi3, Yusuke Takahashi4, Chu Matsuda1, Junichi Nishimura1, Naotsugu Haraguchi1, Hajime Ushigome1, Nozomu Nakai1, Shiki Fujino3, Keijiro Sugimura1, Hiroshi Wada1, Hidenori Takahashi1, Takeshi Omori1 and Hiroshi Miyata1 Abstract Background: Total mesorectal excision (TME) and lateral lymph node dissection (LLND) without radiotherapy (RT) are standard treatment for lower cT3/4 rectal cancers in Eastern countries. In comparative studies, both TME + LLND and RT + TME yield good local control. Although Japanese guidelines recommend LLND for locally advanced rectal cancers below the peritoneal reflection, LLND dissection of clinically negative lateral pelvic lymph nodes (LPLN) is controversial, and laparoscopic TME + LLND is technically challenging and time-consuming. New optical instruments for laparoscopy allow easy perioperative sentinel lymph node (SLN) identification using ICG. The SLN concept may facilitate accurate diagnosis of LPLN involvement, and thus reduce LLND in laparoscopic rectal cancer surgery. Here we investigated lateral pelvic SLN navigation surgery for SLN detection during laparoscopic rectal cancer surgery. Methods: This study included 21 patients with clinical StageII/III lower rectal cancer without LPLN enlargement, who underwent curative laparoscopic surgery. All patients underwent TME, followed by lateral SLN identification and biopsy using ICG, and then laparoscopic LLND. ICG fluorescence imaging was conducted using the laparoscopic near-infrared camera system. Results: Lateral SLNs were successfully identified in 16 (76.2%) of the 21 patients. Among the 15 patients without SLN tumor metastasis, the dissected lateral non-SLNs were all negative. * Correspondence: 1 Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Yasui et al. BMC Cancer (2021) 21:911 Page 2 of 8 Conclusions: A lack of metastasis in the lateral pelvic SLN seems to reflect a lack of metastases to all lateral LNs. Our present results suggest that this laparoscopic ICG-guided SLN strategy may be a low-risk and time-saving method to prevent laparoscopic LLND in cases with negative lateral pelvic lymph nodes. Keywords: Rectal cancer, Sentinel lymph node, Lateral lymph node dissection, Laparoscopic surgery Background Total mesorectal excision (TME) is the international standard surgical procedure for lower rectal cancer. Anatomical studies have revealed that advanced tumors below the peritoneal reflection have a greater risk of spreading to lateral nodes [1–4]. Treatment of lymph node metastasis in the lateral pelvis has developed differently in Eastern versus Western countries. In the West, TME is commonly combined with neoadjuvant radiotherapy (RT) or chemoradiotherapy (CRT) treatment. On the other hand, in the East (principally in Japan), the standard treatment for lower cT3/4 rectal cancers is a surgical approach that combines TME with lateral lymph node dissection (LLND) without RT or CRT. Eastern surgeons prefer LLND for sterilization of the lateral compartment, based on fears of CRT-associated late complications, such as radiation proctitis, pelvic fracture, and second carcinogenesis. The Japanese JCOG0212 trial [5] included patients with clinical stage II/III lower rectal cancer, and reported a local recurrence incidence of only 7% among patients who underwent TME with LLND, which is comparable to incidence rates reported in several Western studies. Moreover, the results of a comparative study between Japan and the Netherlands demonstrate that both TME + LLND and RT + TME resulted in good local control [6]. There are several drawbacks to LLND, including potentially increased incidences of sexual and urinary dysfunction after rectal cancer surgery. Additionally, the reported 7% incidence of pathological LN metastasis after LLND without CRT, among patients with clinical stage II/III cancer who were clinically negative for lateral pelvic LN metastasis, indicates that lateral lymphadenectomy is performed in over 90% of patients without histologically positive lateral pelvic lymph nodes (LPLN). All locally advanced rectal cancers below the peritoneal reflection are considered an indication for LLND according to the Japanese guidelines for lower rectal cancer treatment [7]. However, based on the low incidence of lymph node metastasis and the possibility of dysfunction due to autonomic nerve impairment, LPLN dissection is controversial, especially in patients with clinically negative lateral pelvic LNs. It would be ideal to perform LLND only when LPLN metastasis is highly suspected, to avoid overtreatment and morbidity. However, preoperative radiological examination remains insufficient for the detection of LPLN metastasis [8, 9]. A recently introduced concept is focused on the sentinel lymph node (SLN), i.e., the first lymph node to receive lymphatic flow from the tumor. SLN navigation surgery may lead to reasonable LN retrieval, and is clinically performed in breast cancer [10] and malignant melanoma [11]. More recently, the SLN concept has also been accepted for gastrointestinal cancer [12, 13]. We previously reported application of the SLN concept for detection of the lateral pelvic SLN (LPSN), and as an indication of LPLN dissection using a dye method with indocyanine green and a near-infrared camera system in open rectal surgery [14, 15]. Laparoscopic surgery for rectal cancer (...truncated)