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Abstract

Background

Endoscopic tattooing of colorectal lesions has been performed employing several markers. The indocyanine green (ICG) that uses near infrared fluorescence technology, has been recently adopted in laparoscopic colorectal cancer surgery. This study aims to systematically review the international literature to validate the ICG in laparoscopic colorectal surgery, in order to include the ICG in the therapeutic protocol.

Methods

Following AMSTAR 2 criteria, we performed a systematic review to evaluate the use of green indocyanine as a marker for preoperative endoscopic tattooing and for lymph nodes mapping. The study selection was conducted using the PubMed database from January 1989 to July 2022.

Results

We identified 25 eligible studies. 13 based on fluorescent tumor localization in laparoscopic colorectal surgery using ICG while 12 of them reported the lymphatic road mapping and sentinel node identification by ICG using a near-infrared camera system. One study analyzed both topics.

Conclusions

In laparoscopic colorectal cancer surgery indocyanine green can be used to localize fluorescent tumors and mapping fluorescence lymph node. The use of ICG appears to be a valid and safe technique that helps the surgeon to achieve a better oncological radicality. However, the protocols need to be clarified by further studies.

Keywords

indocyanine endoscopic tattooing lymphatic mapping sentinel node fluorescent endoscopic clipping

Introduction

Endoscopic tattooing of colorectal lesions has been performed employing several markers so far. A new one, the indocyanine green (ICG) that uses near infrared fluorescence technology, has been recently adopted in laparoscopic colorectal cancer surgery. ICG has different applications such as fluorescent tumor localization, lymph node mapping and intraoperative angiography.^1,2 Few studies have shown that ICG is feasible and safe, easy to handle because readily available and supplied in sterile package. It does not cause complications unlike other tattooing agents such as India ink that has some collateral effects: focal peritonitis, inflammation, abscesses, adhesions and pseudo-tumor.^3-9 In laparoscopic surgery the preoperative colonoscopy tattooing with ICG allows to identify the site of the lesion carefully due to the fluorescence property of the marker and the development of the surgical NIR camera system. Accurate tumor localization will enable an adequate margin resection.^10,11 Unlike other endoscopic markers, the preoperative ICG tattooing allows to visualize lymphatic drainage by submucosal injection around the tumor under the near-infrared (NIR) imaging systems. An adequate fluorescence lymph node mapping (FLNM) supports the surgeon when visualizing the lymphatic pathway and while performing an accurate lymph node dissection to reach greater oncological radicality.² The usefulness of ICG in this clinical field needs to be clarified.

This study aims to review systematically the international literature to validate the use of ICG in laparoscopic colorectal surgery, in order to include the ICG technique in the therapeutic protocol of this disease.

Methods

Following current AMSTAR 2 criteria, we performed an extensive systematic review of the English literature to evaluate the use of green indocyanine as a marker for preoperative endoscopic tattooing and for lymph nodes mapping. The research and its study selection were conducted using the PubMed database and articles in English language were selected from January 1989 to July 2022. Further searches were conducted using Web of Science (WOS), SCOPUS, and Google Scholar. We made the research using the following terms: “green indocyanine colonoscopy”, “preoperative colonoscopy tattoo”, “green indocyanine tattoo”, “lymph node mapping“, “green indocyanine and colon cancer”. To avoid data duplication, we only considered the most recent papers in front of articles written by the same research group with overlapping study periods. Forty-three articles were selected, but 18 of them were excluded because they were representative of animal or cadaveric studies, case reports, reviews and editorials. We included 25 articles. The checklist of PRISMA-ScR (Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews) was performed.¹² For the purposes of our review, the inclusion criteria were as follows: green indocyanine as an endoscopic marker and its use in lesion localization and during lymph node mapping. The exclusion criteria were animal and cadaveric studies, case reports, reviews and editorials. Data were extracted by one author (M.V.), based on the model of the CHARMS Checklist (Critical Appraisal and Data Extraction for Systematic Reviews of Prediction Modelling Studies). The discordances were solved by discussion with all coauthors and consensus. The analysis of the collected data was carried out in a double-blind fashion by two authors (S.P. and A.L.).

Results

We identified 25 eligible studies published between January 1989 and July 2022, 13 based on fluorescent tumor localization in laparoscopic colorectal surgery using ICG while 12 of them reported the lymphatic road mapping and sentinel node identification by ICG using a near-infrared camera system. One study analyzed both topics.² These 25 studies were evaluated and analyzed. The selection process is shown in Figure 1.

Figure 1.

Prisma flow chart of literature search.

Indocyanine Tattooing

In Table 1

Table 1.

ICG as fluorescent marker for tumor localization.

Reference	Author	Year	Nation	Study	n. pts	Green injection	Green dilution	Median interval between ICG marking operation days (range)2	Adverse effects	Colonic wall reactions	Intraop visibility green (pts)	Tattooing site number	Tumor site	Submucosal/Subserosal
8	Ahn et al	2021	Korea	Prospective not controlled	192	0,5-1 mL	25mg/10.0mL	12-18 h	N/A	N/A	N/A	2-3.	all	submucosal
16	Lee et al	2021	Korea	Prospective single center not randomized not controlled	27	CLIPS	N/A	2 days	no	no	22/27	3 distals	all
28	Namikawa et al	2020	Japan	Retrospective not controlled	8	CLIPS	N/A	2 days	no	no	6/8.	2 cm away from the oral margin	gastric-rectum
27	Satoyoshi et al	2020	Japan	Prospective case series	165	0.5 mL	25mg/5ml	6 days	no	no	147/165	2	all	submucosal
26	Goo et al	2019	Korea	Retrospective controlled	1079 (200/879)	N/A	8mg/2mL	within 7 (most 1)	N/A	N/A	N/A	3	all	submucosal
25	Lee et al	2018	Korea	Retrospective not controlled	174	1.0-1.5 mL	N/A	1 day	no	no	172/174	2-3.	all	submucosal
24	Park et al	2018	Korea	Retrospective controlled	342 (114/228)	0.5-1mL	25mg/2 mL	1 day	1 abdominal leakage of ICG	1 mucosal edema	N/A	4	all	submucosal
23	Watanabe et al	2017	Japan	Prospective not controlled	80	0,5 mL	25mg/10.0mL	3 days	no	no	N/A	1 distal	all	submucosal
22	Ozawa et al	2016	Japan	3 cases report	3	0.5 mL	25mg/10.0mL	1-2 days	no	no	3/3.	N/A	all	submucosal
17	Nagata et al	2016	Japan	Prospective not controlled	24	0,5 mL	25mg/10.0mL	1.3 day	no	no	24/24	1	all	submucosal
21	Handgraaf et al	2015	Netherlands	Technical report	5	1 mL	5mg/10.0ml	3/5 days	no	no	4/5.	4	rectum	submucosal
20	Watanabe et al	2009	Japan	Prospective not randomized not controlled	10	0,5 mL	25mg/10.0mL	3 days	no	no	10/10.	4	all	submucosal
10	Miyoshi et al	2009	Japan	Prospective not randomized not controlled	39	1 mL	25mg/2ml	4 days (1-73)	no	no	31 strong/5 weak/3 no	duble opposite site	all	submucosal

we have included the articles regarding fluorescent tumor localization. ICG has been used in all studies and in most cases its concentration varies between .5 and 1.0 mL with a dilution of 25 mg/10.0 mL of sterilized water.^2,11,13-15 In all the articles the injection of the ICG follows the submucosal route and takes place around the tumor. The number of injections varies between 2 and 4, only in two cases one injection was performed.^11,13 The endoscopic tattoo was performed from 1 to 3 days before the surgery while the study of Satayoshi et al³ did the tattoo 6 days earlier; in many cases ICG fluorescence marking was visualized when the tattoo was performed 1 or 2 days before surgery.^{10,11,14,16,17} No complications related to endoscopy or tattooing were reported in 10 articles,^{3,4,10,11,13-18} only in one case abdominal leakage of ICG was observed but without inflammation or adhesions.¹⁹ The data related to two reports were not available.^2,20 Two recent papers^10,16 used indocyanine green-coated endoscopic clips to determine the site of the lesion by placing 2 or 3 clips through the preoperative colonoscopy two days before surgery and in many patients the clips were correctly displayed. We analyzed the site of the lesion and we found that in eleven articles the whole intestinal tract was considered,^{2-4,10,11,13-15,17,19,20} in one case the rectum¹⁸ and finally in one paper the stomach and the rectum.¹⁶ Nagata et al¹¹ enrolled 24 patients who underwent both indocyanine green and india ink tattoos. India ink was injected near the lesion while ICG on the other side of the lesion. ICG fluorescence tumor localization was visualized in all 24 patients while India ink staining was negative in 10 patients. There were no complications related to ICG while in six cases the India ink spilled into the peritoneal cavity.

Indocyanine Mapping

In Table 2 we have included the articles regarding lymph node mapping and sentinel node identification. The submucosal injection technique was used in five studies,^2,21-24 subserosal injection in other five^25-29 papers, while both techniques were used in two report.^30,31 For the detection of lymph flow five studies reported an injection from 1 to 2.5 mg/mL,^{2,22,26,27,31} in two cases 5 mg/mL,^24,25 in one report from 2,5 to 10 mg/mL²², in two articles from 5 to 20 mg/mL,^23,28 in one study was injected an amount of 20 mg/mL³¹ and finally the data related to one paper were not available.²⁹ The number of injections varied between 1 and 4, in one study only one injection was performed,² in three cases 2 injections,^21,25,26 in one case the number varied between 1 and 4,³¹ in one article two or three injections were performed,³¹ in four articles 4 injections were performed^22,24,27,29 and finally data were not available in two reports.^23,28

Table 2.

ICG Lymph Node Mapping and Sentinel Node Identification.

Reference	Author	Year	Study	n. pts	Location of tumor	ICG dosage (mg)	Tattooing site number	Complications	Waiting time	Submucosal/Subserosal	Lymph node (mean)	SLN (mean)	SLN assessment
39	Ho et al	2022	Prospective study	21	All	2.5	2-3	Yes (spillage)	10 min	Submucosal/subserosal	N/A	N/A	In vivo
8	Ahn et al	2021	Retrospective	192	All	1	1	No	12-18 h	Submucosal	33.3	N/A	In vivo
29	Park et al	2020	Retrospective	25	Right colon	2.5-10	2	No	3-24 h	Submucosal	41.0	N/A	In vivo
38	Ankersmit et al	2019	Prospective single center	30	Cecum to sigmoid	20	1-4.	N/A	3-10 min	Submucosal/subserosal	13.0	3.5	In vivo
30	Currie et al	2017	Prospective pilot study	30	All	2.5	4	No	7 min	Submucosal	34.0	3.0	In vivo
33	Andersen et al	2017	Retrospective	29	Cecum to sigmoid	5	2	Yes (spillage)	20 min	Subserosal	24.0	0/1	Ex vivo/in vivo
34	Watanabe et al	2016	Retrospective	20	Hepatic and splenic flexure	2.5	2	No	30 min	Subserosal	17.5	10.4	In vivo
35	Liberale et al	2016	Prospective study	20	Cecum to sigmoid	2	4	N/A	152 min	Subserosal	22.4	1.5	Ex vivo
36	Hirche et al	2012	Prospective study	26	All	5-20.	N/A	No	3-10 min	Subserosal	32.9	1.7	In vivo
31	Cahill et al	2012	Retrospective	18	All	5-7.5	N/A	No	N/A	Submucosal	N/A	3.6	In vivo
32	Noura et al	2010	Retrospective	25	Rectum	5	4	No	30 min	Submucosal	N/A	2.1	In vivo
37	Kusano et al	2008	Retrospective	26	All	N/A	4	No	N/A	Subserosal	13.5	2.4	In vivo

N/A, not available.

Moreover we analyzed the site of the lesion and we found that in six papers the whole intestinal tract was considered,^{2,22,23,28,29,31} three cases reported the tract from the cecum to sigmoid,^25,27,30 in one paper the rectum,²⁴ in one article the right colon²¹ and finally the hepatic and splenic flexure in a further study.²⁶ No complications related to ICG were reported except the study of Andersen et al and Ho et al^26,32 in which 7 out of 29 patients experienced spillage. In two papers data were not available.^27,30

We analyzed the mean number of sentinel lymph nodes (SLNs) that were identified by fluorescence, the mean number of resected lymph nodes (LNs) and the median time to detect the lymph nodes. In the prospective study of Liberale et al²⁷ 20 patients were enrolled comparing indocyanine green fluorescence imaging (ICG-FI) with blue dye. The mean number of SLNs identified with ICG was 1.5 after 152 min, while the mean number of recovered LNs was 22.4. Ankersmith et al³⁰ in a prospective single center study identified on 30 patients a mean of 3.5 SLNs, 3-10 min after dye injection, and recovered approximately 13 LNs. Currie et al²² performed a pilot study on 30 patients with ICG for intraoperative sentinel lymph node mapping in early colon cancer by identifying a mean of 3 mesocolic SLNs with a mean detection time of 7 minutes and a resection of 34 LNs. Andersen et al²⁵ compared, through a retrospective study on 29 patients, the use of ICG in vivo and methylene blue ex vivo to identify sentinel lymph nodes. The median number of analyzed lymph nodes was 24. The median number of SLNs identified by in vivo mapping was 1 and 0 in ex vivo mapping, the mean time to visualize the SLNs was 20 min. In the retrospective study by Watanabe et al²⁶ 20 patients were analyzed and the tumor was located in the splenic or hepatic flexure, the mean number of resected lymph nodes was 17.5 with a mean SLNs of 10.4 while lymphatic flow was observed 30 min after injection. In the retrospective study of Kusano et al²⁹ 22 patients with colorectal cancer were enrolled, the number of dissected lymph nodes was 13.5 while the number of SLNs was 2.4. In the retrospective study by Ahn et al² 192 patients were analyzed and ICG injection was performed 12-18 h before surgery. The mean number of lymph nodes collected was 33.3. Park et al²¹ enrolled 20 patients with advanced right colon cancer and examined the clinical value of an ICG D3 dissection compared to conventional laparoscopic surgery in a retrospective study. The median number of N3 lymph nodes collected by ICG was 41, greater than in the conventional group. The time interval between ICG injection and the operation was from 3 to 24 h. The retrospective study by Noura et al²⁴ analyzed on 25 patients the feasibility of sentinel lymph node biopsy of the lateral region in lower rectal cancer guided by ICG: the number of lateral SNs per patients was 2.1 and the mean time to visualize the SLNs was 30 min. The prospective study by Hirche et al²⁸ conducted on 26 patients revealed a mean number of 32.9 excised lymph nodes and showed a mean number of 1.7 SLNs. Cahill et al²³ conducted a retrospective study on 18 patients with early stage colorectal cancer identifying a mean number of 3.6 SNLs. Ho et al³¹ compared, in a prospective study of 21 patients, the injection of ICG before or during surgery by either intraluminal submucosal or laparoscopic peritumoral injection. The timing to demonstrate lymphatic drainage was 10 min.

Discussion

Indocyanine Tattooing

Endoscopic marking of colonic lesions was firstly described in 1975 by Ponsky and King using India ink.³² For many years India ink has been the standard colonic marking agent.³³ Different markers have been used over the years to locate the site of lesions including India ink, indigo carmine, metal clips, methylene blue and indocyanine green. The use of the ICG as a tattooing agent was initially described in few reports based on animal models by Hammond, Price and Lee^34-36 as an alternative to India ink. In 1993 Hammond et al³⁷ conducted a study on 12 patients by using ICG as an endoscopic marker in order to allow an accurate localization of small or non-palpable lesions of the colon. Over the years several articles compared India ink and ICG as endoscopic markers. In 2009 a study by Miyoshi et al⁴ evaluated the usefulness of indocyanine green as an alternative to India ink by examining the visibility, duration and adverse effects of ICG. India ink has higher visibility and longer duration compared to ICG whose visibility depends on: the intervals between endoscopic marking and surgery, omentum, pericolonic fat, mesentery and the posterior abdominal wall which can block the surgeon's view. Regarding the adverse effects, ICG is considered an excellent colonic marking because it does not present adverse reactions such as fever, abdominal pain or allergy symptoms differently from India ink where many articles^3-9 report complications such as focal peritonitis, abscess, intestinal perforation, inflammatory pseudotumors, adhesions. This review of the literature has shown that an injection of indocyanine green for the tattoo of the tumor must be performed at an adequate dosage varying from .5 mg to 12.5 mg in 1 or more peritumor lesion sites to avoid incorrect identification of the tumor. The interval between the injection of ICG and surgery is on average 2.3 days and it is important to perform it within 7 days since Miyoshi et al⁴ have shown that from the seventh day the detection with indocyanine green is reduced to 80%. An important difference between indocyanine green and India ink is the cost. In laparoscopic surgery, the preoperative tattoo using ICG identifies the site of the lesion thanks to the fluorescence properties of the marker and through the use of surgical NIR camera systems. Due to high costs these technologies are not currently widely available.¹¹ Recent studies have introduced a new innovative technique to localize the site of the lesions in laparoscopic surgery, especially in the early stages of cancer, through the use of ICG-coated endoscopic clips.^10,16 This method is safe, easy, accurate, without complications but in few cases the clips are not visible due to fat tissue or mesorectum so it is necessary to perform an intraoperative colonoscopy.¹⁰ Unlike endoscopic ICG tattooing, the use of clips does not allow the visualization of the lymphatic drainage during laparoscopic surgery. ICG-coated clipping is a promising technique but since it involves the use of surgical NIR camera systems has not been widely used so far.

Indocyanine Mapping

Over the years the use of indocyanine green has been found to have different functions in laparoscopic colorectal cancer surgery based on different administration ways. When intravenously administered, it allows to perform an angiography of the colonic stumps to assess their adequate vascular perfusion. When injected into the subserosal or submucosal layer near the lesion it allows to visualize the lymphatic flow and lymph nodes by using the NIR light system.^2,38 Indocyanine green was initially used in breast cancers and melanomas as a tool to identify sentinel lymph nodes, minimizing surgical procedures and complications.³⁹ In 2008 Kusano et al²⁹ conducted the first study to determine the feasibility of sentinel node mapping guided by ICG fluorescence imaging in gastrointestinal cancer. Since the injection of ICG can be performed closer to the lesion, in literature several studies have shown that the identification of the sentinel lymph node in colorectal cancer is becoming important in selected patients with early colorectal cancer but its efficacy in improving outcome is still questionable.^2,22,23 In colorectal cancer an adequate fluorescence lymph node mapping supports the surgeon in visualizing the lymphatic pathway and in performing an accurate lymph node dissection thus reaching greater oncological radicality.⁴⁰ If the surgeon identifies a fluorescent lymph node outside the conventional dissection plane, he can extend the dissection for complete lymph node removal.² This review of the literature has shown that lymph node mapping should be performed at an optimal ICG dosage ranging from 1 to 20 mg. If the dosage is too high, there is a risk of activating accessory lymphatic pathways, not allowing the correct lymphatic drainage of the tumor to be visualized. The injection can be performed from 1 to 4 peritumor lesion sites in the submucosal or subserosal layer with an average waiting time of three hours. Patients with a high body mass index (BMI) can affect the visualization of the lymph node mapping due to the presence of a fatty mesocolon.² In a recent article dated 2020, Park et al²¹ highlighted the efficacy and safety of the use of ICG for FLNM in right colon advanced cancers considered that in their study-group patients a higher number of lymph nodes were removed compared to the control-group ones, and in one third of cases the extent of the lymphadenectomy was modified to achieve a radical D3 dissection. In colon cancer, lymphadenectomy is not influenced by the positive or negative status of the sentinel lymph node. ICG in the intraoperative detection of lymph nodes during laparoscopic colon cancer surgery can be used during lymphadenectomy: this aspect could be important only if these nodes are not present in the usual dissection area because this information would change the surgical strategy. Conversely in laparoscopic rectal surgery, it could be of added value in assessing the need to remove the lateral lymph node chains: moreover, the preoperative identification by ICG of lymph nodes with possible invasion could be compared with TC findings after neoadjuvant chemotherapy, improving preoperative staging and subsequently guiding laparoscopic surgical management.

Conclusions

In laparoscopic colorectal cancer surgery indocyanine green can be used for various functions including the localization of fluorescent tumors and fluorescence lymph node mapping using the surgical NIR camera system. To date, the use of ICG appears to be a valid and safe technique that helps the surgeon to achieve a better oncological radicality but, however, the protocols regarding the adequate dosage and the time interval between tattooing and surgery need to be clarified by further studies.

Footnotes

Author Contributions

Conceptualization, S.P. and A.L.; formal analysis, M.V.; data curation, C.P, C.H. and R.P.; writing—original draft preparation, M.V.; writing—review and editing, D.M. and S.A.; supervision, A.L. and S.P. All authors have read and agreed to the published version of the manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Chiara Eberspacher

Stefano Pontone

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Indocyanine Green Tattooing During Colonoscopy as a Guide to Laparoscopic Colorectal Cancer Surgery: A Literature Review

Abstract

Background

Methods

Results

Conclusions

Keywords

Introduction

Methods

Results

Indocyanine Tattooing

Indocyanine Mapping

Discussion

Indocyanine Tattooing

Indocyanine Mapping

Conclusions

Footnotes

Author Contributions

Declaration of Conflicting Interests

Funding

ORCID iDs

References