IN VIVO SENTINEL LYMPH NODE DETECTION WITH INDOCYANINE GREEN IN

COLORECTAL CANCER

Daniel Stăniloaie1,2 , Constantin Budin1,2, Alexandru Ilco2 , Dănuţ Vasile1,2, Amalia Loredana Călinoiu 3 ,
Adina Rusu 3 , George Iancu1,4, Tarek Ammar 2, Cristian Florin Georgescu2, Maria-Daniela Tănăsescu1,5,6,
Marcel Palamar7, Dorin Ionescu1,5,6, Alexandru Mincă1.
1
University of Medicine and Pharmacy “Carol Davila”, Bucharest, Romania
2
First General Surgery Department , Emergency University Hospital, Bucharest, Romania
3
Emergency Clinical Hospital “Prof. Dr. Agrippa Ionescu”, Bucharest, Romania
4
Clinical Hospital of Obstetrics and Gynecology “Filantropia”, Bucharest, Romania
5
Department of Semiology, Emergency University Hospital, Bucharest, Romania
6
Department of Nefrology, Emergency University Hospital, Bucharest, Romania
7 Department of Nefrology, Emergency Hospital, Deva, Romania
*Corresponding author: Maria-Daniela Tănăsescu, Nephrology Department, University Emergency
Hospital, Bucharest, Splaiul Independentei no. 169, Sector 6, Bucharest, Romania; Tel: 021.3180519;
e-mail: .

Abstract
Background: The indocyanine green fluorescence imaging system allows the identification of lymphatic
vessels, lymph nodes and blood flow during surgery. Colorectal cancer is the second commonest cancer
in women, the third in men, being the fourth commonest cause of cancer death. One of the most important
factor for staging and prognosis in colorectal cancer is the involvement of the regional lymph nodes. In
literature, there are several methods for identifying sentinel lymph nodes, like methylene blue, technetium
(99m Tc) and indocyanine green. The current article presents the use of indocyanate in the identification of
the sentinel node/nodes in malignant tumors of colon, by a technique performed in vivo, before the
primary ligation of the vascular pedicles.
Methods: The study was conducted prospectively on a group of 23 patients who had undergone standard
surgical resection in 1st General Surgery Department, Emergency University Hospital, Bucharest,
Romania, between January 2020- March 2022, 21 patients for a malignant tumor of colon and 2 patients
for malignant rectal tumor. During the surgery sentinel lymph node detection was performed using
indocyanine green and the Karl Storz® Vitom ICG probe. Sentinel lymph nodes were excised separately
and sent to the Department of Pathological Anatomy for analysis.
Results: Sentinel nodes were successfully identified in 13 patients, the overall identification rate was
56,52% ( 13/23 cases). In 7 cases, the number of invaded nodes was the same as the number of sentinel
nodes identified and invaded. Complete lymphadenectomy was performed in all cases regardless of the
staining status of the sentinel lymph nodes.
Conclusion: The use of fluorescence imaging with ICG in colorectal cancer remains controversial. Since
no specific receptor target is used, the fluorescent signal is not specific for lymph node metastases.The
learning curve is particularly important for increasing the accuracy of the technique and is responsible for
the negative results in some cases. Cases in which the lymph nodes have not been invaded, require further
evaluation such as immunohistochemistry and the chain polymerization reaction (RT-PCR).
Key words : indocyanine green, sentinel lymph node, colorectal cancer, oncology

1. Introduction

Colorectal cancer is on the first place among the incidence of neoplasms in Romania, the
data being quantified for 2020, for both sexes (1). Lately, the aplications of indocyanine green (ICG)
for fluorescent-guided surgery has been expanding. Here we assessed the use of fluorescence
imagining in gastrointestinal tract surgery (2). The principal advantages of using ICG are the presence
of the absorption maximum, the confinement to the vascular compartment through binding with plasma
proteins, the low toxicity and the rapid excretion, almost exclusively into the bile. ICG is stable at room
temperature. This is also the form of pharmaceutically available ICG. ICG is soluble in water (1 mg/mL)
but is not readily soluble in saline. ICG should first be dissolved in water and only after this diluted with
saline if an isotonic solution is needed (3). The concept of the sentinel node is not new, being used in
breast cancer and melanoma surgeries (4-7) since … .

Surgical step of the multimodal oncological treatment must be as precise as possible in order to
and to achieve perform a complete excision of both tumor and precise lymphadenectomy, without
remaining invaded lymph nodes. that can be invaded by the tumor. The sentinel node identification and
biopsy technique is a valuable oncological method, which aims to evaluate the regional lymphatic
drainage, with the advantage of a correct staging of the disease, the prognosis of patients, and also the
indication of neodjuvant therapy in cancer treatment. This technique is currently used for malignant
melanoma and breast cancer. The sentinel node is the first lymph node that drains the lymph from the
tumor, as such it and has have a high risk to be invaded by malignant cells with metastases (8).

Usually, the cColorectal cancer is a lymphophilic cancer and the absence or presence of lymph
node metastases is the main prognostic factor. High mortality from colorectal cancers is caused by
locoregional recurrences and metastases. These are due to unidentified micrometastases by classical
histological examination of the lymph nodes. Indocyanine green is an anionic, water-soluble substance
with multiple applications currently in medicine (9). Photodynamic therapy involves the administration of
photosensitizing drugs and then the exposure of tissue or cells to light (10). This treatment has been
applied to malignant tumors but also to other non-malignant diseases. Indocyanine green is able to
penetrate cells without producing degenerative changes (11), and has been approved for use in human
medicine since 1959, for tests of cardiac and hepatic function (12).

Discovering an adequate number of lymph nodes on the surgical piece depends not only on the
practice of a large extension/dimension of the colorectal resection, which should always respects the
oncological principles, but also on the anatomopathological analysis of way the resected specimen.of
anatomopathological examination of the piece of colic excision.

The fluorescence imaging system is one of the most popular imaging techniques in the
biomedical field for visualizing tissues and cells both in vivo and ex vivo. ItsThe benefits of this
technique include a high contrast, high sensitivity and, low concentrations being able tocan highlight the
loco-regional lymphatic system efficiently (13). We aimed to evaluate the accuracy of indocyanate use in
the identification of the sentinel node/nodes in malignant tumors of colon, by a technique performed in
vivo, before the primary ligation of the vascular pedicles.

2. Material and Methods

We performed a cross‐sectional observational study, enrolling the patients admitted in our

surgical department between …2021 and …2022.
The data are presentedwas colected from the patients’ observation sheet and from the
histopathological exam report based onof the postoperative excision piece. The patients offered his
written consent to take these for using the data only for scientific and statistical purposes with respect for
patients' rights, ethics, law and medical ethics. Thies study was conducted in accordance with the General
Data Protection Regulation of the European Union and approved by the Ethics committee of Bucharest
Emergency University Hospital (has the approval no. 55321/15.10.2019) of the local Ethics Commission.
…
The flow diagram of the study is presented in Figure ?.

2.1. Participants
To perform the technique, it is necessary to meet a number of criterias.After signing the informed
consent, all the patients with a histopathological diagnosis of colorectal cancer were considered
potentially eligible for enrollment in the study.The inclusion criterion was the presence of a tumor with a
histopathological diagnosis of malignancy. The exclusion criteria were: (ai) age under 18 years, (b)
another synchronous malignancy, (cii) the presence of liver, lung, brain, peritoneal or other localization
metastases, and (diii) pregnant or breastfeeding.
2.2. Operatory protocol
Injected indocyanine green The technique was used to identify the sentinel node is in-vivo. The
techniqueis wasis performed intraoperatively immediately after laparotomy in all the patients who meet
the criteria for enrollment in the study. and checking of exclusion conditions. After the primary tumor
wasis identified, the indocyanate solution wasis prepared using as shown below.We used a a 25 mg vial
containing indocyanine green in powder form, which wase diluted with 10 mL of sterile water. The
solution thus obtained wasis extracted in a 10mL syringe to which a 26 Gauge needle wasis mounted
(14). 2.5mL of indocyanate solution were injected pPeritumorally injected at the 4 cardinal points. 2.5mL
of indocyanate solution and wait about After10-15 minutes the Vitom Karl Stortz probe for open surgery
was used (Figure 1). iIn order to visualize the sentinel nodes, we used. (Figure 1).
At the end of the intervention, the abdominal cavity was checked with the VITOM probe to
check for any remaining ganglion stations. For tumor staging and case clasification, we used the TNM
system of the American Joint Committee on Cancer (AJCC) (15).
Patients presenting with malignancies usually have a high risk of developing acute kidney injury
secondary to receiving chemotherapy, exposure to contrast agents used in medical imaging, radiation
therapy, tumor lysis syndrome, hypotension or caused as a by the direct effects of the malignancy. Since
tThis technique does not involve the intravenous administration of indocyanine green and no reactions
such asthere is not risk acute kidney injury can developdevelopment.

…..

Results
In this prospective study only 23 patients were enrolled and met the inclusion criteria. The novel
COVID-19 pandemic has generated substantial disruptions worldwide and impaired the ability of the
hospitals to diagnose and treat cancer patients (16). Patients had limited access to medical services and
arrived at the hospital in more advanced stages. Sentinel nodes were successfully identified in 13
patients, the overall identification rate was 56,52% ( 13/23 cases). The characteristics of study group are
shown in Table 1.
In 7 cases, the number of invaded nodes was the same as the number of sentinel nodes identified
and invaded. We notice that once the tumor is more advanced, the number of invaded nodes is higher and
the number of sentinel nodes detected is increased. Also, 9 of the 23 cases did not have any lymph nodes
invaded. In none of the 9 cases indocyanine green was captured in the lymph nodes. Case no. 6, showed 6
lymph nodes with metastases. Only 3 caught ICG and 2 were tumor invaded, 1 was false-positive. This
situation has also been encountered in the case no. 9 and 22. In each case, a false-positive sentinel node
was found.

Discussion

Indocyanine green is a widely available dye of clinical importance that has been used for more
than 50 years (17). When injected intravenously, indocyanine (800 nm fluorophore) binds to plasma
proteins, thus being limited to the intravascular compartment with minimal clearance to the interstitium.
Subserous or sub-mucosal injection of indocyanate leads to absorption by lymphatic vessels, binding
again to plasma proteins, transporting the indocyanate to the Chyli sac where it enters the circulation. ICG
is exclusively excreted by the liver through bile without being metabolised (18).
It seems that cardiovascular disease, diabetes, diabetic arteriopathy and the degree of calcification
of the arteries influence would be important both in the blood perfusion of the colon and as a consequence
they might modify in the dispersion of indocyanate through the lymphatic vessels and lymph nodes .
(19,20).
A literature review of the literature published in 2011 including 17 specialized studies in breast
cancer, gastric cancer, colorectal cancer, skin cancer and lung cancer searched in the PubMed/ and
Medline databases showeds that indocyanine is was still in its early stages and must be performed further
studies to assess its potential and limitations were required (21).

A comparison study performed on a group of 132 patients with endometrial cancer showed that
when injecting between the use of methylene blue andvs. indocyanine green on the sides of the same
patients uterus, indocyanine increased sentinel lymph node detection by 26.5%.
included a group of 132 patients with endometrial cancer; 46 underwent robotic surgery and 86
underwent laparoscopic surgery. The injection of methylene blue was done on one side of the uterus and
indocyanine on the contralateral side. The use of indocyanine instead of methylene blue resulted in a
26.5% increase in sentinel lymph node detection rates in women with endometrial cancer (22).
PANA AICI AM REUSIT SA CITESC

The Chongqing China Department of Breast Surgery included 471 breast cancer patients in its
study, which were divided into two groups. The first group was given methylene blue + radioisotope (271
patients) 4-12 hours before surgery and the second group was given methylene blue + indocyanate (200
patients) 10 minutes before surgery. The result of the study did not identify significant differences
between the two groups which shows that the use of indocyanine in combination with methylene blue
may be a very good alternative in sentinel node identification as both substances are non-radioactive (23).
Another study performed on 227 patients with uterine neoplasm who were divided into two groups - the
first 179 patients used only indocyanate and had a success rate of 79%; in the second group of 30 patients
indocyanine was used in combination with methylene blue had a success rate of 77% (24).
After finishing of the procedure, in the case presented, the site of tumor excision and the
emergence of vascular pedicles were checked to ensure that there were no remaining areas stained with
indocyanine. The fluorescence imaging system is one of the most popular imaging techniques in the
biomedical field for visualizing tissues and cells both in vivo and ex vivo. The benefits of this technique
include high contrast, high sensitivity, low concentrations can highlight the loco-regional lymphatic
system (25). Despite the major progress of chemotherapy, surgery remain the treatment of choice, and it
implies the complete resection of the tumor (26). Early diagnosis of colon neoplasms should be made
through screening programs. Most people diagnosed with a malignant tumor form, subsequently have an
untreated anxiety-depressive syndrome, can lead to suicide according to a retrospective and observational
study, based on records of 210 patients of Titan "Dr. Constantin Gorgos ” Psychiatric Hospital,
Bucharest, between January 1st 2010 and December 31st 2014 (27).

Conclusion

The sentinel node identification technique using indocyanine green is a feasible method to use in
colorectal cancer. The learning curve is particularly important for increasing the accuracy of the technique
and is responsible for the negative results in some cases. To increase the sentinel lymph node
determination rate using indocyanine, a longer learning curve is needed. Early diagnosis is difficult to be
settled, but it is mandatory to be done due to the fact that any delay of the proper treatment could increase
mortality (28). Cases in which the lymph nodes have not been invaded, require further evaluation to rule
out the possibility of micrometastases; skip metastases using immunohistochemistry and chain
polymerization reaction (RT-PCR) techniques. With further validation, this technique could become a
valuable tool to guide personalized oncological colorectal resections (29). Unfortunately, colorectal
cancer has an increasing incidence among the young population, and adopting a healthy diet correlated
with regular medical analysis may decrease the incidence of this malignancy (30).

Authors’ Contribution
DS, CB, DEG, ALC, AR, GI, TA, CFG, MDT designed the study, wrote the manuscript and performed
the literature research. DV and AI evaluated and critically revised the manuscript and analyzed the results
for accuracy. All authors read and approved the final manuscript.
Availability of Data and Materials
All data generated to analyzed during this study are available from the author on reasonable request.
Conflicts of Interest
The authors have no related conflicts of interest to declare
Ethics Approval
This article conforms to the ethical norms and standards in the Declaration of Helsinki. The present study
was approved by the Ethical Committee of Emergency University Hospital, Bucharest, Romania,
approval statement number 55321/15.10.2019. The patients freely-given written informed consent before
the surgical intervention.

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Table 1. Characteristics of study group

Case Location pT pN G Stage No. of No. of invaded Sentinel Invaded
no. examined lymph nodes sentinel
lymph nodes

1 Ascending pT2 pN0 G2 I 8 0 0 0

2 Descending pT3 pN0 G1 IIA 18 0 0 0

3 Descending pT3 pN0 G2 IIA 21 0 0 0

4 Left splenic pT3 pN2a G2 IIIB 12 4 2 2

flexure
5 Left splenic pT4a pN1a G2 IIIB 13 1 0 0
flexure
6 Inferior rectum pT3 pN2a G3 IIIB 8 6 3 2
7 Descending pT3 pN1a G2 IIIB 23 1 1 1

8 Right hepatic pT3 pN0 G2 IIA 19 0 0 0

flexure
9 Sigmoid pT4a pN1b G2 IIIB 24 2 2 1
10 Ascending pT3 pN1b G1 IIIB 36 2 2 2
11 Cecum pT4b pN2b G2 IVC 23 8 3 3
12 Left splenic pT3 pN2a G2 IIIB 28 3 3 3
flexure
13 Inferior rectum pT2 pN0 G2 IIB 9 0 0 0
14 Recto-sigmoid pT4a pN0 G2 IIB 7 0 0 0

15 Cecum pT3 pN1 G2 IIIB 34 0 0 0

16 Sigmoid pT3 pN1a G2 IIIB 11 1 1 1

17 Transverse colon pT3 pN0 G2 IIA 11 0 0 0

18 Cecum pT3 pN1a G2 IIIB 22 1 1 1
19 Sigmoid pT3 pN0 G2 IIA 18 0 0 0
20 Cecum pT2 pN1c G3 IIIA 21 1 1 1
21 Cecum pT4b pN1b G3 IIIC 29 2 2 2

22 Left splenic pT4a pN2b G3 IIIC 24 21 3 2

flexure
23 Cecum pT4b pN2b G2 IIIC 40 25 4 4

Fig 1. Injecting indocyanine green in 4 cardinal points

Fig 2. Sentinel lymph node

Fig 3. Separate marked sentinel nodes on the piece of colic resection