Value of Indocyanine Green Tracing Combined with Ex-Vitro Anatomical Sorting of Lymph Nodes in Clinical Prognosis of Patients with Gastric Cancer

doi:10.21203/rs.3.rs-1420873/v1

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Research Article

Value of Indocyanine Green Tracing Combined with Ex-Vitro Anatomical Sorting of Lymph Nodes in Clinical Prognosis of Patients with Gastric Cancer

https://doi.org/10.21203/rs.3.rs-1420873/v1

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Objective: In order to increase the detection rate of lymph nodes (LNs) in radical gastrostomy, we applied indocyanine green (ICG) tracing and Ex vitro anatomical sorting to LNs dissection, and explored the guiding role of LNs number detected in the prognosis of patients with gastric cancer (GC).

Methods: The clinical data of 88 GC patients who underwent D2 radical gastrostomy were retrospectively analyzed, and they were divided into ICG group and non-ICG group according to ICG usage and LN sorting method. Total LN number, positive LN number, clinical treatment, tumor marker, and patients’ prognosis between two groups were compared. Furthermore, we discussed the correlation between total LN and positive LN, and evaluated the role of ICG tracing in their detection.

Results: Total LNs number, total positive LNs number, and LNs number in different LN sub stations detected in ICG group were higher. Furthermore, positive LNs number was positively correlated with total LNs number. In the evaluation of ICG tracing effect on LNs, it was found that fluorescent labeled LNs accounted for nearly 62% of total LNs and about 74% of positive LNs. In terms of clinical prognosis, the levels of CEA, CA199, CA242, and CA724 in ICG group were better controlled. Besides, GC patients’ in ICG group were not prone to relapse and metastasize, and their long-term survival rate were better.

Conclusion: ICG tracing combined with Ex vitro anatomical sorting can significantly improve the detection rate of total LNs and positive LNs, which has a positive impact on patients’ long-term prognosis.

Indocyanine green

Ex vitro anatomical sorting

Lymph nodes

Gastric cancer

Gastric cancer (GC) is common among malignant tumor of digestive system, and its incidence occupies the third place among all tumors in China [1]. In recent years, due to the change of eating habits and poor living habits, the incidence of GC has increased year by year, and has a younger trend. At present, the main treatment principles of GC are early diagnosis, early surgery, and postoperative adjuvant chemotherapy, so as to improve patients’ prognosis of patients. With the progress of medical technology, surgical methods of GC are also changing, gradually changing from large incision laparotomy to small incision and fast healing laparoscopic surgery, which is in line with the concept of rapid rehabilitation in clinical surgery [2]. However, laparoscopic minimally invasive surgery will affect operator's hand feeling, as a result, the exact location of tumors and LNs cannot be accurately located via visual observation and clinical experience, thus affecting the detection rate of LNs. The American Joint Commission on cancer suggests that in GC patients undergoing distal resection or total gastrostomy, at least 16 or 21 LNs need to be detected in order to accurately guide the clinical staging of patients [3]. According to statistics, every 10 additional LNs can improve the detection rate of positive LNs, so as to further optimize the postoperative treatment plan [4]. Therefore, in D2 radical gastrostomy, increasing the detected number of LNs is very important to improve patients’ prognosis.

Because regional LN metastasis is common in GC, in order to improve the detection of LNs, nanocarbon suspension is often used for LN labeling during surgery, and good localization effect has been achieved [5]. However, if serous membrane is broken due to improper operation in the positioning process, it will have an adverse impact on the operation field, which will affect the accurate positioning of tumor and LNs, thus further increasing the difficulty of operation [6]. Therefore, indocyanine green (ICG) tracing is more and more widely used in radical gastrostomy [7]. As a near-infrared fluorescent dye, ICG can achieve good fluorescence development effect in the near-infrared camera with only a small amount of injection, so as to effectively avoid the occurrence of excessive injection affecting the imaging [8, 9]. Otherwise, the fluorescence emitted by ICG has good penetrability [10], which can effectively display the drainage and positioning of LNs under fat layer, thus contributing to the transformation of LN dissection mode in GC from "empirical dissection" to "accurate dissection". Furthermore, the operator can observe the blood supply of the anastomosis through the fluorescence of ICG [11, 12], which is important to prevent the occurrence of postoperative anastomotic leakage. Therefore, ICG tracing can effectively assist the operator to complete D2 radical gastrostomy.

In addition to the application of developer to improve the detection of LNs, Ex vitro LN sorting after operation is a supplement to LN dissection in D2 radical operation, which is conducive to further increase the detection of LNs, especially micro LNs. Relevant studies show that about 40% of the positive LNs are less than 5 mm in diameter [13]. Because micro LNs are hidden in the adipose layer, they are difficult to distinguish from adipose tissue and are easy to be missed. Therefore, optimizing the sorting technology of Ex vitro LNs is very important to improve the accurate staging of GC patients. By establishing a professional LN sorting team and training team members in professional theory and practical operation, the detection amount of micro LNs can be effectively improved, which is of great significance for predicting patient’s condition and accurate clinical staging [14, 15]. Therefore, we applied ICG tracing combined with Ex vitro anatomical sorting in D2 radical gastrostomy, and discussed their impact on the detection rate of LNs and patients’ prognosis.

2.1 The choice of research object

The clinical date of GC patients treated in our hospital from January 2018 to January 2020 was analyzed retrospectively. Inclusion criteria: 1. GC was diagnosed according to the criteria in Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up [16]; 2. Age range: 18–60 years old; 3. D2 radical gastrostomy was performed;4.Preoperative CT and ultrasonic gastroscopy showed no distal metastasis; 5. Complete clinical data. Exclusion criteria: 1. Preoperative radiotherapy or immunotherapy༛2. Patients with recurrent GC༛3. Previous history of abdominal operation; 3. Combined with other types of malignant tumors༛4. Allergic to the drugs used in this experiment༛5. Combined with severe cardiovascular and cerebrovascular diseases. A total of 88 GC patients were chosen and divided into ICG group and non-ICG group. In ICG group, ICG was used to label the location of cancer focus and LN during operation, and Ex vitro anatomical LN sorting was combined, while conventional LN collection method was used in non-ICG group. The general data of the two groups were shown in Table 1.

Table 1

General information table
	Factor	ICG group (n = 49)	non-ICG group (n = 39)	F	P
Gender	Male	28 (57.14)	26 (66.67)	0.831	0.362
Gender	Female	21 (42.86)	13 (33.33)	0.831	0.362
Age		56.78 ± 12.65	54.63 ± 11.79	0.816	0.417
BMI (kg/m2)		25.63 ± 2.65	24.77 ± 2.56	1.535	0.128
Tumor diameter (cm)		6.63 ± 2.78	5.97 ± 2.38	1.178	0.242
Tumor location	Upper 1/3 stomach	8 (16.33)	9 (23.08)	0.642	0.726
	Middle 1/3 stomach	16 (32.65)	12 (30.77)
	Lower 1/3 stomach	25 (51.02)	18 (46.15)
Radical gastrostomy	Proximal gastrostomy	4 (8.16)	6 (15.38)	1.425	0.490
	Distal gastrostomy	15 (30.61)	13 (33.33)
	Total gastrostomy	30 (61.23)	20 (51.28)
Lauren typing	Intestinal type	15 (30.61)	11 (28.21)	0.197	0.906
	Diffuse type	21 (42.86)	16 (41.03)
	Mixed type	13 (26.53)	12 (30.77)
TNM stage	I	16 (32.65)	13 (33.33)	-0.022	0.982
	II	21 (42.86)	16 (41.03)
	III	12 (24.49)	10 (25.64)

2.2 Application of ICG tracing in surgical LN dissection

ICG (3599-32-4, Beijing Kezhan Biotechnology Co., Ltd) is configured as a diluted solution with a concentration of 1.25 mg/L, and was injected around cancer focus under the guidance of endoscope one day before operation. Before injection, 0.5-mL normal saline was injected under the mucosa to lift the tumor, and then 0.5-mL ICG diluent was injected, at last, 0.5-mL normal saline was used to block it. The same injection method was used to inject ICG diluent at the oral side, anal side, and left and right sides of the cancer focus, so as to locate tumor and LNs. During operation, the chief surgeon observed the fluorescence of tumor and LNs through near-infrared laparoscopy (OTV-S300, Olympus), gastrostomy was performed by locating tumor boundary through fluorescence. Then, resected specimen were sent to rapid pathological examination to judge whether the far and near cutting edges were negative. After digestive tract reconstruction, 2-mL ICG solution with a concentration of 2.5 mg/L was injected intravenously into the blood vessels, and the fluorescence intensity of the anastomosis was observed through the laparoscopic system to evaluate the blood perfusion of the anastomosis. In addition, D2 LN dissection was performed by switching the modes of green fluorescence, gradient fluorescence, and natural light of the laparoscopic system.

2.3 Ex vitro anatomical LNs sorting

In order to focus on the collection of LNs in postoperative isolated specimens, a LN sorting team was established in ICG group, which was composed of 5 Department postgraduates and guided by the Department Director. Reserve of theoretical knowledge: team members should be familiar with perigastric anatomy and the location of regional LNs, so as to facilitate the sorting of LNs. Specimen location identification: by observing operation process, team members can further understand and master the morphological characteristics of LNs in vivo, and correspond them with the morphology of LNs in isolated specimens, so as to improve LNs sorting ability of team members. Key points of sorting: Because LNs are distributed along blood vessels, relevant arteries in isolated specimens should be firstly identified before sorting LNs, and then LNs were collected along the arteries, which can effectively improve the detection rate of LNs; LNs hidden in the fat layer need to be distinguished layer by layer to avoid the omission of relevant LNs, especially micro LNs; Compared with fat particles, LNs are more resilience, not easy to crush, and relatively white. Experience summary and technical improvement: Finally, team members should summarize and exchange the experience of LN sorting every week, so as to explore the existing shortcomings and improve them in the subsequent sorting process. The collected specimens will be placed in the order of LNs at each station, and then be classified for pathological examination (Fig. 1). Traditional methods were used to sort LNs in non-ICG group. After routine HE staining, the LN metastasis of the two groups was judged and recorded.

2.4 Observation indicators and Assessment Methods

2.4.1 Number of LNs sorted

The number of LNs obtained is an important index to evaluate the standardization of D2 radical gastrostomy and clinical stage. The number of total LNs, positive LNs, and micro LNs detected in both groups were recorded. At the same time, LN number sorted in different sub stations were also compared to further evaluate the effect of ICG tracing and Ex vitro anatomical sorting in LN localization

2.4.2 Correlation between total LNs number and positive LNs number

In order to explore the correlation between total LNs number and positive LNs number, total LNs number of patients with different TNM stages was analyzed, and positive LNs number at different TNM stages was evaluated according to the results of HE staining. Otherwise, Pearson correlation analysis was used to evaluate the correlation between total LN number and positive LN number.

2.4.3 ICG Fluorescence staining in obtained LNs

In order to evaluate the effect of ICG tracing in LN sorting, fluorescence staining in total LNs and micro LNs were analyzed and recorded. At the same time, for evaluating the tracing effect of ICG in LN metastasis of GC, we analyzed proportion of positive LNs in fluorescent and non-fluorescent LNs.

2.4.4 Clinical treatment

We evaluated the clinical treatment of both groups in terms of operation time, intraoperative bleeding, postoperative exhaust time, postoperative feeding time, hospital stay, and postoperative complications. Otherwise, specimen and boundary conditions were compared in terms of gastric greater curvature length, gastric lesser curvature length, proximal tangent distance, and distal margin distance. In terms of postoperative complications, the occurrence of gastroparesis, chylous fistula, duodenal stump fistula, adhesive ileus, anastomotic fistula, and Petersen hernia were compared.

2.5 Prognosis evaluation of GC patients in both groups

Changes of tumor marker level can effectively reflect clinical treatment and patients’ prognosis. CEA, CA199, CA242, and CA724 were selected as malignant biological indicators of GC. Before and 1 month after operation, 5-mL venous blood samples were taken and anticoagulated with EDTA. After centrifugation at 1000 rpm, the supernatant was taken and stored in − 80°C medical refrigerator for standby. The levels of CEA, CA199, CA242, and CA724 were detected by Human CEA ELISA Kit (ab99992, Abcam, USA), human CA199 ELISA Kit (ab108642, Abcam), human CA242 ELISA Kit (CSB-E04774h, Shanghai Feixuan Biotechnology Co., Ltd), and human CA724 ELISA Kit (ml057569, Shanghai enzyme linked Biotechnology Co., Ltd). In order to further explore the impact of LN sorting on the prognosis of GC patients, we recorded the postoperative survival rate and recurrence rate of patients in different groups. The primary end point was disease progression events, such as recurrence and metastasis, and the secondary end point was all-cause death. The follow-up period ended in January 2022.

3.1 More LNs and positive LNs were detected in ICG group

The number of total LNs detected is an important index to judge the standardization of radical gastrostomy, and the number of positive LNs is beneficial to accurate TNM staging. The number of total LNs, positive LNs, and micro LNs in ICG group increased significantly (Fig. 2A). In the comparison of LN number detected in different sub stations, more LNs and positive LNs were also found in ICG group (Fig. 2B–D). The above results suggest that ICG tracing and Ex vitro LN sorting are helpful to find more LNs and positive LNs, so as to make more accurate clinical staging for GC patients.

3.2 Obvious correlation exists between total LN number and positive LN number

By analyzing the number of total LNs and positive LNs detected in GC patients with different clinical stages, it was found that with the increase of stage, the number of total LNs and positive LNs increased, especially in ICG group (Fig. 3A–B). Otherwise, we found that there was a significant positive correlation between total LN number and positive LN number (Fig. 3C–D), suggesting that increasing the sorting number of LNs is helpful to the detection of positive LNs, thus better guiding patients’ postoperative chemotherapy.

3.3 ICG tracing improved the detection rate of total LNs and positive LNs

In order to further evaluate the importance of ICG tracing in improving the detection rate of total and positive LNs, we analyzed the fluorescence staining of the obtained LN specimens. It was found that ICG stained LNs accounted for about 62% of total LNs, and about 52% of micro LNs (Fig. 4A). These results suggest that ICG tracing is beneficial to improve the detection of LN samples. In addition, approximately 31% of the fluorescent stained LNs were positive LNs, accounting for 74% of total positive LNs (Fig. 4B), suggesting that ICG tracing is conducive to the discovery of positive LNs.

3.4 Similar clinical treatment was found in both groups

We evaluated patients’ clinical treatment in terms of operation time, intraoperative blood loss, postoperative exhaust time, postoperative feeding time, length of stay, and secondary operation rate, and the above indexes decreased in different degrees in ICG group, but no significant difference was found between two groups (Table 2). Otherwise, obvious difference was also not found in the length and cutting edge of specimens (Fig. 5A). Moreover, Similar results were found in the incidence of postoperative complications (Fig. 5B). The above results show that ICG tracing can assist doctors in surgical operation and reduce the incidence of complications to a certain extent, but the effect is not obvious.

Table 2

Clinical treatment and recovery
Group	Cases	Operation time (min)	Intraoperative bleeding (mL)	Postoperative exhaust time (d)	Postoperative feeding time (d)	Length of stay (d)	Secondary operation
ICG group	49	218.63 ± 28.65	34.27 ± 12.56	1.63 ± 0.65	4.83 ± 1.17	7.75 ± 1.78	2/49
non-ICG group	39	221.54 ± 30.13	42.54 ± 13.38	1.79 ± 0.76	5.23 ± 1.31	8.32 ± 1.87	1/39
t/χ2		-0.463	-1.539	-1.064	-1.511	-1.459	0.152
P		0.645	0.127	0.290	0.135	0.148	0.697

3.5 The clinical prognosis of GC patients in ICG group was better

The level of tumor markers can reflect the malignant degree of tumor and patients’ recovery to a certain extent. After treatment, the levels of CEA, CA199, CA242, and CA724 decreased more significantly in ICG group (Fig. 6A–D). In addition, recurrence and metastasis of GC were less prone to occur in ICG group, and the 2-year survival rate was higher (Fig. 6E–F). The above results suggest that the increase in total LNs number is helpful to find positive LNs, so as to better evaluate patients’ condition and carry out subsequent individualized treatment, thus reducing the risk of recurrence and death.

Due to the abundant LN drainage in the perigastric area, LN metastasis is prone to occur in GC patients, which will have an adverse impact on the treatment and patients’ prognosis [17]. In order to improve the accuracy of clinical staging long-term prognosis of GC patients, increasing the detection of positive LNs is an important part of the treatment process and the key point of formulating follow-up treatment plan. Wang et al. [18] found that the increase in total number of LNs was more conducive to the discovery of positive LNs, especially micro LNs. Otherwise, with the increase of the number of detected LNs, the 5-year survival rate of GC patients also increased [19]. Therefore, the acquisition of total LNs can be used as an independent risk factor for the prognosis of GC patients. However, the acquisition of LNs in GC patients is easily affected by many factors. For example, in patients with BMI more than 27, LNs are easy to hide in adipose layer and are not easy to separate from adipose tissue, which increases the difficulty of LN acquisition [20]. In addition, the way of radical gastrostomy and the depth of tumor invasion will also affect the number of total LNs detected [21]. Therefore, improving regional LN tracing method during operation and optimizing LN sorting scheme of isolated specimens are the key points to improve the total detection rate of LNs, especially micro LNs.

In this study, we used ICG as a fluorescent dye to label LNs. Due to the strong tissue penetration, a very small amount of ICG can show eye-catching fluorescence under near-infrared irradiation, which has great advantages for the labeling of LNs around GC, thus effectively displaying the drainage range of LNs [22]. Therefore, ICG fluorescence labeling can effectively guide the surgeon to clean LNs, which is of great significance to improve the detection rate of total LNs. Moreover, in order to avoid the omission of LNs during operation, we established a professional LN sorting team. Through continuous theoretical study and practical operation, team members can effectively summarize and accumulate LN sorting experience and apply it to the continuous optimization of LN sorting methods, thus further improving the number of LNs detected [23]. Therefore, the acquisition of total LNs, positive LNs, and micro LNs were significantly increased in ICG group, and the same results were also found in LN statistics of each substation. Otherwise, by analyzing the acquisition of total LNs and positive LNs in GC patients at different stages, we found that there was a significant positive correlation between them, indicating that increasing the sampling amount of LNs can better improve the detection rate of positive LNs, so as to carry out more accurate clinical staging for GC patients.

In order to further explore the effect of ICG on the detection rate of LNs in GC patients, we statistically analyzed the fluorescence staining of total LNs, micro LNs, and positive LNs. The results showed that fluorescent stained LNs account for 62% of total LNs and 52% of micro LNs, moreover, 74% of fluorescent stained LNs are positive LNs, suggesting that ICG tracing can better assist surgeon in collecting LNs and effectively improve the collection amount of positive LNs, so as to better stage patients. Otherwise, in terms of clinical treatment, the operation time, hospital stay, postoperative exhaust time, and postoperative feeding time of patients in ICG group were shortened to varying degrees, and the incidence of complications such as anastomotic fistula decreased to a certain extent, but no significant difference were found between two groups. The above results suggested that ICG tracing can assist the operator to complete LN dissection and show the blood supply of the anastomosis, which is conductive to improve patients’ clinical treatment reduce the occurrence of complications.

Accurate TNM staging is conducive to the formulation of postoperative chemotherapy and predict patients’ prognosis. Deng et al. analyzed the clinic pathological data of 2455 GC patients, and found that with the increase of LN number, patients’ TNM staging was more accurate, and their prognosis was better. We also found that after treatment, the levels of tumor markers in ICG group were better controlled, patients’ conditions were less prone to recur and metastasize, and their long-term survival rate was higher. Therefore, GC patients can better benefit from the increase in the number of harvested LNs, which can improve their prognosis.

ICG tracing combined with Ex vitro LN sorting is helpful to improve the detection number of total LNs and micro LNs in GC patients, as well as the number of positive LNs detected, which is of great significance to improve the accuracy of GC staging. Otherwise, about 62% of total LNs and 52% of micro LNs were found by ICG tracing, and the positive LNs stained by ICG account for 74% of total positive LNs. Therefore, ICG tracing plays an indispensable role in the sorting of GC LNs. In terms of prognosis, the levels of tumor markers in ICG group were better controlled, tumor recurrence and metastasis were less prone to occur, and patients’ mortality was significantly reduced. However, there are some deficiencies in this study. For example, whether ICG tracing combined with Ex vitro LN sorting is better than simple Ex vitro LN sorting has not been studied, and the study on relevant risk factors affecting LN detection is also not performed, which need to be improved in the follow-up study.

Author Contributions: JL, DL and QJ conceived and designed the study. QJ performed the data analysis. JL and DL interpreted the data, drafted the paper. All authors read and approved the final manuscript.

Funding: This work was not supported by any funding.

Data availability: The data used to support the findings of this study are available from the corresponding author upon request.

Ethics approval and consent to participate: The experimental protocols were approved by the Ethics Committee of the First Affiliated Hospital of Nanchang University (Reference cdyfy2022k). This paper has not been published elsewhere in whole or in part. All authors have read and approved the content, and agree to submit it for consideration for publication in your journal. Informed consent was obtained from all individual participants included in the study

Competing interests: The authors have declared no conflicts of interest in this work

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No competing interests reported.

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Value of Indocyanine Green Tracing Combined with Ex-Vitro Anatomical Sorting of Lymph Nodes in Clinical Prognosis of Patients with Gastric Cancer

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Version 1

Abstract

Figures

1 Introduction

2 Methods And Methods

2.1 The choice of research object

2.2 Application of ICG tracing in surgical LN dissection

2.3 Ex vitro anatomical LNs sorting

2.4 Observation indicators and Assessment Methods

2.4.1 Number of LNs sorted

2.4.2 Correlation between total LNs number and positive LNs number

2.4.3 ICG Fluorescence staining in obtained LNs

2.4.4 Clinical treatment

2.5 Prognosis evaluation of GC patients in both groups

3 Results

3.1 More LNs and positive LNs were detected in ICG group

3.2 Obvious correlation exists between total LN number and positive LN number

3.3 ICG tracing improved the detection rate of total LNs and positive LNs

3.4 Similar clinical treatment was found in both groups

3.5 The clinical prognosis of GC patients in ICG group was better

4 Discussion

Declarations

References

Additional Declarations

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