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Minimally Invasive Therapy & Allied Technologies
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Lymph node mapping with ICG near-infrared fluorescence imaging: technique and results
Ludovica Baldari, Luigi Boni & Elisa Cassinotti
To cite this article: Ludovica Baldari, Luigi Boni & Elisa Cassinotti (2023) Lymph node mapping with ICG near-infrared fluorescence imaging: technique and results, Minimally Invasive Therapy & Allied Technologies, 32:5, 213-221, DOI: 10.1080/13645706.2023.2217916
To link to this article: https://doi.org/10.1080/13645706.2023.2217916
Published online: 01 Jun 2023.
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Lymph node mapping with ICG near-infrared fluorescence imaging: technique and results
Ludovica Baldari, Luigi Boni and Elisa Cassinotti Department of General and Minimally Invasive Surgery, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy
ABSTRACT
Purpose: Lymphadenectomy represents a fundamental step during gastrointestinal cancer resection, as the removal of an adequate number of lymph nodes is crucial to define the stage of the disease and prognosis. Lymphadenectomy during gastric and colorectal resection and adrenalectomy for cancer are technically demanding and can be associated with risk of bleed- ing. To date, lymphadenectomy is often performed without any visual aid. Indocyanine green fluorescence for lymph node mapping can provide better intraoperative visualization. The pur- pose of this review is to report the current evidence on this topic.
Materials and Methods: A systematic research of the electronic databases Medline, Embase and Google Scholar was conducted from the inception to December 2022.
Results: This review summarizes the current evidence of techniques and results of fluorescence guided lymphatic mapping during gastrointestinal and adrenal surgery.
Conclusion: According to this review, ICG guided lymphadenectomy for gastrointestinal tumours and adrenocortical carcinoma is feasible and safe. In gastrointestinal tumours it allows higher number of harvested lymph nodes.
ARTICLE HISTORY Received 16 January 2023 Accepted 18 May 2023
KEYWORDS
Indocyanine green; lymph node mapping; lymphadenectomy; ICG injection; inguinal lymph node injection
Introduction
Indocyanine Green (ICG) fluorescence imaging has been widely applied in abdominal surgery for intrao- perative cholangiography during laparoscopic chole- cystectomy and visceral perfusion assessment for upper and lower gastro-intestinal anastomosis. However, this technology is also applied in various fields of surgical oncology, and among its possible clinical applications, one of the most promising is nodal navigation and real-time lymphography in different types of cancers [1]. Following submucosal, subserosal or intradermal injection, ICG disperses in lymph, binds to lipopro- teins, and is drained via lymphatic pathways and nodes. ICG lymphography has already achieved satis- factory results in the localization of sentinel lymph nodes in patients with breast cancer, melanomas and endometrial and cervical cancer [2].
Several studies on ICG intraoperative lymphatic mapping in visceral surgery for gastrointestinal malig- nancies have shown wide variability and heterogeneity both in results and technical protocols, and its prog- nostic value has not been cleared yet [3,4]. This
technique has shown promising results for gastric cancer, showing high sensitivity in identifying a group of lymph nodes and lymphatic channels that repre- sents the first drainage stations from the tumor, which has been referred as the ‘lymphatic basin’ [2,4] as well as in identifying the lymph nodes draining the tumoral area: lymphatic mapping.
The same strategy has been applied for assessing lymphatic routes in colorectal tumors, investigating both the sentinel node basin and the mesocolic area draining the tumor site. Especially in the debated con- text of right colectomy complete mesocolic excision (CME), ICG lymphatic mapping could help surgeons identifying the mesentery as a continuous structure, comparable to an ‘organ’ with its own lymphatic drain- age and to remove all lymph nodes that have received ICG as possible sites of metastases or micrometastases from the tumor site [5]. ICG lymphatic mapping could also serve as intraoperative guidance for particularly challenging procedures such as extended lateral pelvic lymphadenectomy in locally advanced rectal cancers or cases of paraaortic or paracaval lymphadenectomy for adrenal tumors, where patterns of lymphatic spread are
unknown and a laparoscopic approach could be demanding. The aim of this paper is to summarize the current evidence in the fields of gastric cancer surgery, colorectal cancer surgery, and adrenal cancer surgery and to describe our technique to perform ICG admin- istration in these fields.
Material and methods
A systematic research of the electronic databases Medline, Embase and Google Scholar was conducted in the field of gastric, colorectal and adrenal indocya- nine green fluorescence-guided surgery, from its inception to December 2022.
Techniques
Lymph node mapping with ICG near-infrared fluor- escence imaging for gastric cancer
Two methods have been described for fluorescence- guided lymph node mapping in gastric cancer: endo- scopic submucosal injection and intraoperative subserosal injection. Currently, there is no consensus on the best ICG lymphography technique. ICG concentration and amount of dilution injected vary among authors.
In our experience a 25 mg ICG vial is diluted with 20 ml of 20% albumin or saline solution. Endoscopic submucosal injection is performed to the four quad- rants of the neoplastic lesion 24h before surgery. In order to avoid full thickness injection and that ICG reaches or goes beyond the serosa in depth, before carrying out each marking, 1 ml of saline solution is injected to create a wheal in the submucosa where 0.5 ml of the ICG dilution is put immediately after- wards (Figures 1 and 2).
-
Lymph node mapping with ICG near-infrared fluor- escence imaging for colorectal cancer
As regards colorectal resections, ICG intraoperative lym- phography is performed both for right colectomies (cae- cum, ascending colon and hepatic flexure cancers) and transverse colon/splenic flexure segmental resections, as well as for locally advanced rectal cancers with suspect lateral pelvic lymph node metastases at preoperative imaging staging. Endoscopic submucosal preoperative and intraoperative subserosal ICG injection have been reported for lymphatic mapping in colorectal cancer.
In our experience, a 25 mg ICG vial is diluted with 20 ml of 20% albumin or saline solution. To avoid a full colonoscopy to the patient we perform intraoper- ative subserosal injection of ICG dye at the beginning of surgery, although it takes 15-20 min for the tracer to reach lymphatic channels and nodes and there is also the possibility to spill the tracer on the operating field, staining surrounding tissues and surgical instru- ments. For rectal cancer only, we maintain the sub- mucosal injection technique by performing a rectoscopy in the immediate preoperative time, using the same dilution and technique as for gastric lesions mentioned above (Figures 3 and 4). The indication
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and the surgical technique are not modified by the lymphographic findings, with the exception of supple- mentary fluorescent lymph nodes sampling in case of locally advanced disease.
Lymph node mapping with ICG near-infrared fluor- escence imaging for adrenal cancer
A 25 mg ICG vial is diluted with 20 ml of 20% albu- min or saline solution. Just before starting surgery, after general anesthesia, 10 ml of ICG are injected under ultrasound guidance in the layer between the cortex and the medulla of an inguinal lymph node, ipsilateral with respect to the adrenal tumor. About 15 min after the injection, the homolateral paraortic, paracaval and inter-aortocaval lymph nodes become fluorescent allowing visual aid during the procedure (Figures 5 and 6).
Results
Lymph node mapping with ICG near-infrared fluorescence imaging for gastric cancer
ICG fluorescence lymphatic mapping is intended as a guide to verify the completeness of lymphatic removal,
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to ensure the integrity of anatomical plans during dis- section and, in some cases, for sampling of additional lymphatic tissue. Some retrospective studies, prospect- ive studies and one randomized clinical trial compared the results of standard lymphadenectomy with near infrared fluorescence-guided lymphadenectomy. Some authors reported a major number of harvested lymph nodes through fluorescence-guided lymphadenectomy, while others report some limitations when compared to the standard procedure [6,7].
Through a propensity score matching analysis, Cianchi et al. compared two groups of 37 patients each who underwent robotic gastrectomy with D2 lymph node dissection, with and without ICG fluores- cent lymphography. The mean total number of har- vested lymph nodes was significantly higher in the ICG group than in the non-ICG group (50.8% vs 40.1%, p-value = 0.03) [8].
Kwon et al. published a prospective study including 40 patients (IGC group) who underwent robotic radical gastrectomy with fluorescence-guided lymphadenec- tomy. The results of the ICG group were compared with 40 historical control patients without ICG-guided lymphadenectomy. A mean of 23.9 fluorescent lymph nodes were harvested among a mean of 48.9 overall lymph nodes retrieved in the ICG group. The mean number of overall lymph nodes harvested was signifi- cantly higher in the ICG group than in the control group (48.9 vs 35, p<0.001). All metastatic lymph nodes of the ICG group were fluorescent [6].
Chen et al. reported a randomized clinical trial including 258 patients who underwent laparoscopic D2 gastrectomy with or without ICG mapping. The number of perigastric and extraperigastric lymph nodes retrieved was significantly higher in the ICG group than in the non-ICG group (50.5% vs 42.0% lymph nodes, respectively, p <0.001). Significantly more perigastric and extraperigastric lymph nodes were harvested in the ICG group than in the non-
ICG group. Moreover, the lymph node noncompli- ance rate was lower in the ICG group than in the non-ICG group (31.8% vs 57.4% respectively, p < 0.001). There was no difference in post-operative complications [7].
A recent cohort study, including individual data of two randomized clinical trials on this topic [7,9], including 385 and 129 patients in the ICG and non- ICG groups, respectively, evaluated the clinical impli- cation of fluorescence guided lymphadenectomy. A significantly higher number of lymph nodes were retrieved in the ICG group compared with the non- ICG group (49.9 vs 42, p<0.001). Defining as ‘noncompliance’ the absence of lymph nodes from the dissected station, the lymph nodes noncompliance rate of the ICG group was significantly lower than in the non-ICG group (31.9% vs. 57.4%, p < 0.001). Moreover, the sensitivity of ICG for detecting all metastatic lymph nodes was 86.8%, with a negative predictive value of 92.2% for non-fluorescent stations [10]. It is interesting that all data included in this study were from patients who did not undergo neoad- juvant treatment that would affect nodal drainage pattern.
The effectiveness and feasibility of ICG-guided D2 lymphadenectomy for advanced gastric cancer after neoadjuvant treatment was evaluated by a propensity matching analysis including 94 patients for each group (ICG vs non-ICG). ICG was associated with a significantly higher number of lymph nodes harvested (40.8±13.7 vs 31.8±13.5, p<0.001) and the lower lymph nodes noncompliance rate (35.1% vs 51.15, p= 0.027). These advantages were confirmed even in case of stable disease after neoadjuvant treatment by subgroup analysis [11].
Lymph node mapping with ICG near-infrared fluorescence imaging for colorectal cancer
Extension of lymphadenectomy during colorectal resection is defined by embryological anatomical planes associated with central vascular ligation. Indeed, e.g., total mesorectal excision for rectal cancer and complete mesocolic excision for right colon can- cer allows removal of draining lymph node basins [12]. However, it is possible to find lymph node metastases beyond the tumor related mesentery exci- sion: defined as aberrant metastases. This is more fre- quent in cases of right colon or splenic flexure cancer. Moreover, rectal cancer can metastasize to lateral pel- vic lymph nodes. Thus, near-infrared (NIR)
fluorescent lymphatic mapping helps in identification of draining lymphatic structures.
In a case series of ten colon resections, Chand et al. found that fluorescent lymphatic mapping was possible in all patients ten minutes after intraoperative subserosal ICG injection. Additional lymph nodes located outside the proposed resection margins were reported in two cases. In both cases the resection was extended to include them, and lymph nodes were positive for metastases [13].
In a prospective study of 21 colorectal resections, Nishigori et al. found that ICG fluorescence lymph node mapping let to modification in the extent of mesenteric resection in 23.5% cases. The metastatic rate of ICG positive nodes was 10%, while the meta- static rate of ICG negative nodes was 5.3%. Moreover, there were no metastatic ICG negative nodes more than 5 cm away from the tumor [14]. Petz et al. reported a series of 50 patients who underwent CME for right colon cancer after submucosal injection of ICG the day before surgery. Visualization of lymph- atic structures into the D3 area was possible in all cases and in 34% (17/50) of cases fluorescent lymph- atic structures outside the standard lymphadenectomy extension were identified. In 14 cases fluorescent lymph nodes were located along the left branch of the middle colic artery, while three were located along gastroepiploic vessels [15].
In the interim analysis of their prospective observa- tional study, Ribero et al. reported the results of D3 ICG guided lymphadenectomy in colorectal surgery including 70 patients. The main aim of the study was defining the number of patients in whom ICG changed the extent of the lymphadenectomy, resulting in 35 (50%) patients, mostly due to fluorescent lymph nodes outside the standard draining basin [16]. Similarly, Ho et al. reported a change in the lympha- denectomy extent in 19% of patients in a smaller study including 21 colorectal resections after both submucosal or subserosal injection of ICG [17].
A retrospective study including 1079 patients who underwent colorectal resection for cancer with and without ICG peritumoral injection, by Goo et al. compared the number and adequacy of lymph nodes harvested according to tumor location and stage. There was no significant difference in the number of retrieved lymph nodes between the ICG and non-ICG groups. However, T1 colorectal cancer in the ICG group had significantly more adequate lymph node harvested (91.6% vs 82.1%, OR 2.370, p=0.048) [18].
There are few papers that report the use of indoc- yanine green fluorescence to guide lateral pelvic
lymph node dissection, which is performed in case of rectal cancer associated with metastases in the internal iliac or obturatory lymph nodes, in Western coun- tries. The technique was initially described to investi- gate the feasibility to identify the sentinel lymph nodes in the later space in rectal cancer [19-21]. In two different studies, Zhou et al. and Boni et al. reported the feasibility of lateral pelvic fluorescence- guided lymphatic mapping. Authors concluded that the technique allows easier identification of lymph nodes, especially in obese patients with significantly higher numbers of harvested lymph nodes (11.5±5.9 vs. 7.1±4.8, p=0.017), with lower blood loss (55.8±37.5ml vs. 108.0±52.7ml, p=0.003) [22-24].
Lymph node mapping with ICG near-infrared fluorescence imaging for adrenal cancer
To date, to the best of our knowledge, no previous reports have been published on the use of ICG fluores- cence to guide inter-aortocaval lymphadenectomy for adrenal tumors. In our institute ICG intraoperative lymphography is performed in patients affected by adrenal cancer or with suspected locoregional recur- rence after adrenalectomy for carcinomas. In all cases paraortic/paracaval/inter-aortocaval lymphadenectomy is preoperatively planned based on PET-CT scan or MRI staging and after multidisciplinary discussion.
Discussion
Lymph node mapping with ICG near-infrared fluorescence imaging for gastric cancer
Lymphadenectomy is a crucial step during gastro- intestinal resection for cancer since the removal of an adequate number of lymph nodes improves accuracy of staging, regional disease control and patient sur- vival [25,26]. To date, lymphadenectomy is often per- formed without any visual aid, representing a challenge for the surgeon. As a consequence, it seems plausible that ICG fluorescent lymphatic can increase the number of harvested lymph nodes due to better intraoperative visualization. It has been demonstrated that ICG provides better lymph node visualization than other dye visible by the naked eye under visible light [6,8]). This review summarizes the current evi- dence of technique and results of fluorescence-guided lymphatic mapping during gastrointestinal and adrenal surgery.
According to the 8th edition of the UICC/AJCC TNM staging system for gastric cancer, at least 16 lymph nodes are required to perform a correct
staging but the desirable amount is 30 or more. To date, according to ESMO and Japanese gastric cancer treatment guidelines, it remains to be shown if lap- aroscopic surgery can achieve the same results as open surgery requiring D2 lymphadenectomy [27,28]. Indeed, minimally invasive lymphadenectomy along greater vessels is technically demanding. Near-infrared fluorescence-guided lymphadenectomy has emerged as an effective technique to identify lymph nodes intraoperatively and to remove more metastatic lymph nodes within the extent of the planned lymphadenectomy.
As reported by this review, several studies, includ- ing a randomized clinical trial, show that the tech- nique is feasible and safe and is associated with an increased number of harvested lymph nodes, and lower noncompliance lymph node rate, without an increase in intraoperative and postoperative complica- tions. Recently, Pant et al. published a systematic review and meta-analysis of 13 studies, with one RCT, three prospective cohort studies and nine retro- spective cohort studies, including 1882 patients, show- ing that ICG lymphadenectomy is associated with a significantly higher number of harvested lymph nodes in minimally invasive gastrectomy (40.33 vs 33.40; MD 6.93; CI 95%, p<0.0001). However, there was high heterogeneity (I 2 86%; p < 0.0001) due to differ- ent study designs, sample size, surgical approach, ICG injection. No significant difference was found between the ICG and the control groups regarding metastatic lymph nodes; indeed ICG has no specificity for cancer tissue. These results were confirmed in all subgroup analyses, except for the non-preoperative ICG injec- tion group. Probably this is due to the insufficient spread time of ICG when injected with this technique. Thus, the authors recommend pre-operative injec- tion [29].
As described above, pre-operative submucosal ICG injection is the technique used in our institute for NIR fluorescent lymphatic matting. Chen et al. pub- lished a randomized clinical trial, including 266 patients, comparing subserosal and submucosal approaches. The submucosal injection was performed the day before surgery, while the subserosal injection was performed 20 min before starting lymphadenec- tomy. The authors did not find any significant differ- ences regarding the number of retrieved lymph nodes, the number of collected lymph nodes station by sta- tion and the noncompliance lymph node rate. In regards to subserosal injection, authors recommend Huang’s hexa-point manoeuvre, with ICG administra- tion in six points of the stomach curvatures. Even if
there are no significant differences, authors conclude that subserosal injection is cheaper, but data from patients after neoadjuvant therapy should be ana- lyzed [7].
Lymph node mapping with ICG near-infrared fluorescence imaging for colorectal cancer
It is established that an adequate lymphadenectomy in colorectal oncologic surgery is fundamental both for the therapeutic aim and for accurate disease stag- ing, defining the need for adjuvant therapy. The European Society of Medical Oncology (ESMO) and the National Comprehensive Cancer Network (NCCN) guidelines still recommend the removal of a minimum number of 12 regional lymph nodes around the arterial arcades for adequate pathological staging [30,31]. In contrast with European and American guidelines, the Japanese Society for Cancer of the Colon and Rectum (JSCCR) introduced the nomen- clature ‘D’, differentiating the extension of lymphade- nectomy according to tumor wall invasion and evidence of suspect lymph node metastases on pre- operative staging. In relation to TNM staging, these guidelines suggest the following lymphadenectomy:
· DO and D1: cTis
· D2: cT1, cT2
· D3: cT2, cT3, cT4 and/or cN+ [32].
It has been demonstrated that in 19% of patients the lymph node metastases do not always follow a lin- ear pattern but a ‘jump’ one. Thus, it is possible to find metastatic lymph nodes far from the tumor (e.g., station 3) but not next to it (e.g., station 1 and/or 2). These metastases are defined as skip metastases [33,34]. In addition, as already reported, it is possible to find lymph node metastases beyond the tumor- related mesocolic excision: these are defined as aber- rant metastases. Lately, in view of this contrasting overview of the literature, the differences in clinical practice between Western and Eastern countries and the absence of clear data have led to an open discus- sion about the technique and the extension of lym- phadenectomy in colorectal resection, especially in the case of right colectomy or splenic flexure resection. Indeed, the risks are, on the one hand, performing an unnecessary wide lymphadenectomy for small tumors without lymph node metastasis and, on the other hand, leaving in place metastatic lymph nodes for advanced tumors, if the technique is not defined.
Thus, in order to clarify this issue, several studies examined the role of ICG fluorescence imaging in guiding lymphadenectomy in colorectal cancer. On this topic, a systematic review and meta-analysis of Emile et al. selected 12 prospective case series, com- prising 248 patients, evaluating the capability of ICG fluorescence lymphography to detect metastatic lymph nodes in colorectal cancer. After injection (submuco- sal or subserosal or both) of ICG fluorescent lymph nodes were detected after 5-30 min. Nine authors reported the total number of harvested lymph nodes to be 3351, 1175 (35.1%) of which were metastatic. Of the 1175 lymph node metastases, 859 (73%) were fluorescent-positive and 316 (27%) fluorescent-nega- tive. A total of 1759 lymph nodes were fluorescent, 859 (74%) of which were malignant, whereas 300 (26%) were negative. The pooled sensitivity of ICG in detecting malignant lymph nodes was 71% and the pooled specificity was 84.6%. In this review, it was notable that the best results were achieved when ICG was administered in a concentration depending on body weight. Furthermore, combined submucosal and subserosal injections achieved the highest sensitivity, specificity and accuracy [35].
Another systematic review published by Liberale et al. reports a specificity of 65-100% and an extremely variable sensitivity between 0-100% for colon cancer among the included studies. One of the main limits is the variability of early vs advanced stages of the disease in some studies. Indeed, as reported by other authors [18], the technique is more suitable for early cancer stages [36]. Metastatic lymph nodes, more frequent in advanced stages of the dis- ease, can present obstruction of lymphatic ducts and replacement of normal lymph node tissue by cancer cells, so ICG cannot bind to macrophages and meta- static lymph nodes would drain ICG less easily. This limitation of ICG fluorescence explains why many studies report an increase of the total number of lymph nodes but not of the metastatic ones, resulting in low specificity. Indeed, one of the main limitations of the fluorophore is that it is not cancer-specific.
Regarding the technique, as described for gastric cancer, both preoperative endoscopic submucosal and intraoperative subserosal injection have been described for colon cancer, while for rectal cancer intraoperative endoscopic subserosal injection should be performed. The main limit of the submucosal tech- nique for colon cancer is the need for a preoperative colonoscopy the day before surgery which may be refused by the patient. On the other hand, intraopera- tive subserosal injection, especially in the case of
minimally invasive surgery, has an increased risk of accidental intraoperative spillage with fluorescent con- tamination of the field and consequently decreased sensitivity of the procedure that can be, in this case, futile and time-consuming [35,36].
Lymph node mapping with ICG near-infrared fluorescence imaging for adrenal cancer
The prognostic and therapeutic significance of lym- phadenectomy for adrenocortical carcinoma remains to be established, as published literature data report contrasting results. Recent systematic literature and meta-analysis of 11 retrospective studies investigated the impact of lymphadenectomy on overall survival. The authors concluded that lymphadenectomy seems to have a benefit in disease-specific survival and in overall survival in case of localized disease (stage I- III), without increasing post-operative morbidity. However, this benefit in survival was not confirmed after including all disease stages (stage I-IV) in the meta-analysis [37]. Inter-aortocaval lymphadenectomy is a technically demanding procedure, as it can be associated with a high risk of bleeding. Identification of lymph nodes in this area through ICG fluorescence has already been described for other procedures after peritumoral injection [38]. However, to our know- ledge, the technique of lymph nodes identification after homolateral inguinal node ICG injection has never been described before for adrenocortical carcin- oma, but according to our experience, it is feasible and safe and can act as a guide during dissection in a challenging anatomic area. The technique of inguinal node ICG injection was obtained from the previous reported experiences of esophagogastric surgeons in order to delineate the thoracic duct during esophagec- tomy [39,40]. Further studies are needed to standard- ize the technique and define advantages when compared with standard lymphadenectomy.
In conclusion, according to this review, ICG- guided lymphadenectomy for gastrointestinal tumors is feasible and safe, yielding a higher number of har- vested lymph nodes. It seems to be better to apply the technology to early-stage tumors, as advanced stages can block the lymph channels and nodes. Further investigation is needed for indocyanine green fluores- cence-guided lymphadenectomy for adrenocortical carcinoma, even if the technique reported seems to be feasible and safe.
The main limitations are the fluorophore itself, which is currently non-specific to cancerous tissue, and the limited depth of penetration of the imaging
system. As a consequence, a higher body mass index can affect the success rate of fluorescence identifica- tion due to the presence of more visceral fat and decreased signal. Further studies are necessary to opti- mize and standardize the technique and the appropri- ate indications.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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