Navigating the Gastric Cancer Maze: Embracing Laparoscopic D2 Lymphadenectomy for Safer and Faster Treatment: A retrospective cohort study

doi:10.21203/rs.3.rs-3299751/v1

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Navigating the Gastric Cancer Maze: Embracing Laparoscopic D2 Lymphadenectomy for Safer and Faster Treatment: A retrospective cohort study

https://doi.org/10.21203/rs.3.rs-3299751/v1

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Objective: This retrospective comparative study aimed to evaluate the feasibility and outcomes of laparoscopic subtotal gastrectomy (LSG) with D2 lymphadenectomy compared to open subtotal gastrectomy (OSG) for distal gastric adenocarcinoma.

Methods:A total of 42 patients with biopsy-proven distal gastric adenocarcinoma underwent either LSG or OSG with D2 lymphadenectomy at AIIMS Bhubaneswar, India, from March 2019 to July 2022. Baseline characteristics, operative parameters, postoperative outcomes, and one-year follow-up data were reviewed. Statistical analysis was performed using IBM SPSS Statistics 25.0.

Results: LSG was performed in 26 patients, with 4 cases (15.38%) requiring conversion to OSG due to technical challenges or bleeding. Both LSG and OSG groups were comparable in age, sex, BMI, comorbidities, and clinical stage. Neoadjuvant chemotherapy was administered to 86.4% and 85.0% of patients in LSG and OSG groups, respectively. The mean number of harvested lymph nodes in the LSG group was 20.77, meeting the AJCC criteria for radical gastrectomy. The mean operative time and blood loss were similar between the groups. LSG patients had significantly lower pain scores at 3 and 12 hours post-operation, faster resolution of postoperative ileus, and earlier mobilization compared to OSG. The incidence of postoperative complications was comparable between the groups, with no significant difference in disease-free survival after one year.

Conclusion: LSG with D2 lymphadenectomy is a feasible and safe option for resectable distal gastric adenocarcinoma, offering comparable outcomes to OSG. While the mean number of harvested lymph nodes in LSG was slightly lower than OSG, it still met the AJCC criteria. Careful patient selection and surgeon expertise are essential due to the potential need for conversion to open surgery. The impact of neoadjuvant chemotherapy on lymph node harvest rates in LSG cases warrants further investigation. The choice between LSG and OSG should be individualized based on patient factors and tumor characteristics.

Laparoscopic subtotal gastrectomy

open subtotal gastrectomy

D2 lymphadenectomy

distal gastric adenocarcinoma

feasibility

outcomes

lymph node harvest

Carcinoma of the stomach is a significant contributor to cancer-related mortality, particularly in the eastern regions [1]. High-quality surgical resection, including lymphadenectomy, constitutes the standard of care in a multidisciplinary approach and represents the only potential cure. The Japanese Gastric Cancer Association (JGCA) has anatomically defined and numerically classified the lymph node stations around the stomach, recommending D1 or D1 + lymphadenectomy for early gastric cancer and D2 lymphadenectomy for advanced gastric cancer (T2-4a and/or N+) to achieve improved survival outcomes [2].

D2 lymphadenectomy poses technical challenges even in open surgery, and its compliance remains a subject of debate. In the Dutch Gastric cancer trial, noncompliance with D2 lymphadenectomy exceeded 80% [3]. Across most gastrointestinal malignancies, the standard of care has shifted from open surgery to laparoscopic surgery. While adopting a laparoscopic approach is hindered by technical difficulties, required expertise, and variations in reconstructive methods, Laparoscopic subtotal gastrectomy with D2 lymphadenectomy is now considered oncologically safe and technically viable for locally advanced distal gastric cancer[4]. However, due to the long learning curve and increased difficulty in laparoscopic dissection, compliance with D2 lymphadenectomy is still questionable, particularly in cases of locally advanced gastric cancer.

The primary objective of this study was to assess our experience with laparoscopic subtotal gastrectomy (LSG) and compare it with the open approach (OSG), while also evaluating the compliance with D2 lymphadenectomy.

This study constitutes a retrospective analysis of 42 patients who underwent laparoscopic subtotal gastrectomy (LSG) and open subtotal gastrectomy (OSG) with D2 lymphadenectomy for biopsy-proven distal adenocarcinoma of the stomach at AIIMS Bhubaneswar, Odisha, India, spanning the period from March 2019 to July 2022. The study aimed to evaluate the feasibility of D2 lymphadenectomy in the LSG group compared to the OSG group. Before commencement, the study received ethical approval from the Institutional Ethics Committee.

The research involved a meticulous review of existing medical records, capturing various parameters, including age, sex, body mass index (BMI), comorbidities, ASA grade, clinical stage (cStage), type of gastrectomy (LSG or OSG), operative parameters, number of harvested lymph nodes, resection margin status, postoperative pathological staging, postoperative ambulation, postoperative oral feeding, postoperative hospital stay, postoperative complications, and one-year follow-up data.

Inclusion criteria encompassed patients who underwent LSG or OSG with D2 lymphadenectomy for resectable gastric cancer with a curative intent. Resectable gastric cancer comprised both early gastric cancer (EGC) and resectable locally advanced gastric cancer (LAGC) from clinical stages I, IIA, IIB, and III. All patients underwent clinical staging, involving UGI Endoscopy, CECT abdomen, and staging laparoscopy. The study excluded patients with proximal growth necessitating total gastrectomy, those who underwent palliative or emergency surgery, as well as those with unresectable gastric cancer. Cases where the laparoscopic approach was converted to open gastrectomy were analyzed as part of the OSG group.

The primary outcome under scrutiny was the number of lymph nodes harvested in each group, whereas secondary outcomes included operative time, intraoperative blood loss, postoperative ambulation, postoperative oral feeding, postoperative hospital stay, postoperative complications, and one-year follow-up outcomes between the OSG and LSG groups.

Data collection and subsequent statistical analysis were carried out using IBM SPSS Statistics 25.0 for Windows. Continuous variables were presented as means and standard deviations (SD), while categorical variables were expressed as frequencies and percentages. To compare continuous variables, the Shapiro-Wilk Student's t-test was employed, while the Chi-square test or Fisher's exact test was used for categorical variables. A significance level of p < 0.05 was adopted to determine statistical significance.

Operative Technique:

All surgeries were conducted following the standardized operative steps of laparoscopic distal gastrectomy with Roux-en-Y gastrojejunostomy, utilizing a total of five abdominal ports. Staging laparoscopy was carried out for all cases. The dissection of the left side of the gastrocolic ligament was performed adjacent to the transverse colon, extending toward the lower splenic pole until the lower edge of the tail of the pancreas was exposed. The origin of the left gastroepiploic vessels was ligated, concomitant with the dissection of station 4sb and 4d lymph nodes.

The hepatic flexure of the colon was meticulously separated from the duodenal bulb and the surface of the pancreatic head. The right gastroepiploic vessels were transected concurrently with the dissection of station 6 lymph node. The gastroduodenal artery was meticulously exposed, followed by the transection of the right gastric artery at its root, in conjunction with the dissection of station 12a and 5 lymph nodes.

The three branches of the celiac trunk were carefully denuded, subsequently leading to the transection of the left gastric artery at its root, along with the dissection of station 7, 8a, 9, and 11p lymph nodes (refer to Fig. 1). The hepatogastric ligament and the anterior lobe of the hepatoduodenal ligament were then transected, allowing for the full separation of the lesser curvature and the dissection of station 1 and 3 lymph nodes.

The procedure continued with the intracorporeal execution of distal gastrectomy and Roux-en-Y reconstruction.

Over the course of three years, from 2019 to 2022, a total of 42 cases of gastric carcinoma underwent curative intent surgery. Among them, 26 patients were treated with a laparoscopic subtotal gastrectomy (LSG) approach, out of which 4 patients (15.38%) required a conversion to open surgery. The primary reasons for conversion were suspected infiltration hindering tumor dissection (50%), technical challenges (25%), and uncontrollable bleeding (25%). On the other hand, 20 patients underwent an open subtotal gastrectomy (OSG). The decision to use either the laparoscopic or open approach was based on surgeon preference, patient fitness for a laparoscopic procedure, and the patient's individual preferences.

The LSG and OSG groups were similar in terms of age, sex distribution, comorbidities, and other baseline variables (see Table 1). Although not statistically significant, body mass index (BMI) was lower in the patients who had undergone a LSG. Neoadjuvant chemotherapy was administered to 19 patients (86.4%) in the LSG group and 17 patients (85.0%) in the OSG group. The two groups also exhibited comparable TNM staging (see Table 2).

Table 1

Baseline characteristics of the study population
Parameter	Laparoscopic Gastrectomy (n = 22)	Open Gastrectomy (n = 20)	P value
Age (years) (Mean (SD)	57.41, 8.06	55.88, 8.17	0.28*
Sex: n,(%) Male Female	18 (81.8%) 4 (18.2%)	15 (75%) 5 (25%)	0.59^$
BMI (kg/m²) (Mean (SD)	20.93, 0.87	21.14, 0.61	0.36*
DM: n,(%)	4 (18.2%)	4 (20%)	0.88^$
HTN: n,(%)	4 (18.2%)	1 (5%)	0.19^$
COPD: n,(%)	8 (36.4%)	7 (35%)	0.93^$
ASA: n,(%) II III	10 (45.5%) 12 (54.5%)	13 (65%) 7 (35%)	0.29^$
Hb (g/dL) (Mean (SD)	11.59, 1.58	10.89, 1.53	0.15*
Alb (g/dL) (Mean (SD)	3.75, 0.46	3.91, 0.52	0.31*
Neoadjuvant therapy: n,(%)	13 (59.1%)	9 (45.0%)	0.36^$

^$: Chi-square test used for comparison, *: student’s t-test used for comparison, ^#: Mann-Whitney U test used.

Table 2

Staging and operative characteristics of the study population
Parameter	Lap gastrectomy	Open gastrectomy	p-value
T staging: n,(%) T1 T2 T3 T4	3 (13.6%) 10 (45.4%) 7 (31.8%) 2 (9.1%)	2 (10.0%) 8 (40.0%) 6 (30.0%) 4 (20.0%)	0.92^$ 0.69^$ 0.57^$ 0.74^$
N staging: n,(%) N0 N1 N2 N3	1 (4.5%) 9 (40.9%) 9 (40.9%) 3 (13.6%)	4 (20.0%) 2 (10.0%) 9 (45.0%) 5 (25.0%)	0.47^$ 0.15^$ 0.89^$ 0.57^$
TNM staging: n,(%) IIA IIB III	8 (36.4%) 8 (36.4%) 6 (27.3%)	3 (15.0%) 9 (45.0%) 8 (40.0%)	0.37^$ 0.31^$ 0.92^$
Operative time in mins (Median, IQR)	295.5, 93.25	272.5, 127.5	0.70^#
Blood loss in ml (Median, IQR)	207.5, 120	202.5, 120	0.26^#

^$: Chi-square test used for comparison, *: student’s t-test used for comparison, ^#: Mann-Whitney U test used.

Operative time was slightly longer in the LSG group (295.5 ± 93.25 mins) compared to the OSG group (272.5 ± 127.5 mins), but this difference was not statistically significant (p-value = 0.70). Similarly, there was no significant difference in the amount of blood loss between the two groups (207.5 ± 120ml in LSG vs 202.5 ± 120ml in OSG, p-value = 0.26) (see Table 2).

In terms of post-operative outcomes, the LSG group had significantly lower pain scores at 3 hours (3.68 ± 1.52 vs 4.6 ± 1.14 in OSG, p-value = 0.03) and 12 hours (2.72 ± 1.80 vs 4.75 ± 2.27 in OSG, p-value = 0.00) after the procedure (see Table 3). Additionally, the LSG group demonstrated faster resolution of postoperative ileus (2 ± 1 day vs 4 ± 0.75 in OSG, p-value = 0.00) and achieved earlier mobilization out of bed (2 ± 1 day vs 3 ± 1 in OSG, p-value = 0.00).

Table 3

Post-operative parameters of the study population
Parameter	Lap Gastrectomy	Open Gastrectomy	p-value
Pain score (0-10mm) (Mean, SD) 3 hrs 6 hrs 12 hrs 24 hrs 30 hrs	3.68, 1.52 5.09, 1.79 2.72, 1.80 3.95, 1.93 2.90, 1.57	4.6, 1.14 4.6, 1.42 4.75, 2.27 4.75, 1.80 3.75, 2.28	0.03* 0.34* 0.00* 0.17* 0.16*
First oral liquid in days (Median, IQR)	2,1	4,0.75	0.00^#
First out of bed ambulation in days (Median, IQR)	2,1	3,1	0.00^#
Clavien-Dindo grade: n,(%) III or higher	4 (18.2%)	8 (40%)	0.11^$
Anastomotic leak: n,(%)	3 (13.6%)	2 (10.0%)	0.72^$
Postoperative intraabdominal bleeding: n,(%)	0 (0%)	2 (10.0%)	0.21^$
Duodenal stump leak: n,(%)	1 (4.5%)	2 (10.0%)	0.49^$
Reexploration: n,(%)	1 (4.5%)	2 (10.0%)	0.38^$
Mortality within 30 days: n,(%)	0 (0.0%)	1 (5.0%) [Cause: refractory sepsis]	0.24^$
Length of stay in days (Median, IQR)	8, 2.25	11.5, 4.75	0.00^#
6 months DFS: n,(%)	22 (100.0%)	19 (95.0%)	0.29^$
12 months DFS: n,(%)	22 (100.0%)	18 (90.0%)	0.17^$
^$: Chi-square test used for comparison, *: student’s t-test used for comparison, ^#: Mann-Whitney U test used. DFS = Disease free survival

The incidence of post-operative complications was comparable between the two groups (see Table 3). Anastomotic leak occurred in 3 patients (13.6%) in the LSG group, compared to 2 patients (10%) in the OSG group. A duodenal stump leak was observed in 1 patient (4.5%) in the LSG group and 2 patients (10%) in the OSG group (p-value = 0.49). Among the OSG group, 2 patients required re-exploration due to duodenal stump failure, and one of them succumbed to refractory sepsis on postoperative day 21. Risk analysis revealed that Odds ratio for Clavein Dindo grade 3 or above for N3 stage, Age > 60y, Blood loss > 500ml, Diabetes mellitus, BMI were 6.43, 2.85, 2.73, 2.58, 2.4 respectively (see Fig. 2). The overall hospital stay was shorter for patients in the LSG group (4 ± 1.25 days vs 6 ± 1 day in the OSG group). After one year, no significant difference was observed in the disease-free survival rate between the two groups.

Regarding the radicality of dissection, there were no discernible differences in the rates of R0, R1, and R2 dissections between the LSG and OSG groups (see Table 4). Although the mean number of harvested lymph nodes was higher in the OSG group (30.25 ± 4.53 vs 20.77 ± 5.63 in the LSG group), there were no disparities in the margin status of the post-operative resection specimens. In the patients who had undergone an LSG with D2 lymphadenectomy, a higher BMI correlated with a lesser lymph node harvest (see Fig. 3).

Table 4

Pathological characteristics of the study population
Parameter	Lap Gastrectomy	Open Gastrectomy	p-value
Nodes harvested (Mean, SD) 1. After NACT 2. Without NACT	20.77, 5.63 18.69, 4.23 25.22, 4.29	30.25, 5.43 30.11, 3.62 30.36, 6.74	0.00* 0.00* 0.06*
Radicality of resection: n,(%) R0 R1 R2	18 (81.8%) 4 (18.2%) 0 (0.0%)	15 (75.0%) 4 (20.0%) 1 (5.0%)	0.64^$ 0.93^$ 0.89^$
Proximal margin positive: n,(%)	2 (9.1%)	1 (5%)	0.53^$
Distal margin positive: n,(%)	1 (4.5%)	0 (0%)	0.18^$

^$: Chi-square test used for comparison, *: student’s t-test used for comparison, ^#: Mann-Whitney U test used.

Gastric cancer remains a prevalent malignancy worldwide, and surgical resection stands as the primary potentially curative treatment. The extent of lymphadenectomy has been a subject of controversy. Songun et al.'s 15-year follow-up analysis of the DUTCH trial demonstrated a clear survival advantage of D2 lymph node dissection over D1 lymphadenectomy [5]. Other studies and meta-analyses have also shown substantial survival benefits from D2 dissection for locally advanced gastric cancer (stage T3 and T4) [6], [7]. However, the minimally invasive approach to oncological resection remains a topic of debate, with concerns about achieving adequate lymph node clearance and technical difficulties in tumor resection being key factors hindering its acceptance [8]. The KLASS-02 study estimated a mean learning curve of 42 cases for laparoscopic gastrectomy [9]. Several authors have compared laparoscopic subtotal gastrectomy (LSG) and open subtotal gastrectomy (OSG), favoring LSG due to its minimally invasive nature, faster post-operative recovery, and comparable long-term outcomes to OSG [10], [11].

Our study aimed to assess the feasibility of D2 lymphadenectomy by comparing the number of lymph nodes harvested in LSG and OSG. As per the 8th edition of the AJCC staging manual, a minimum of 16 lymph nodes should be retrieved for radical gastrectomy [12]. Our results indicated that the mean number of lymph nodes harvested in the OSG group was 30.25, while in the LSG group, it was 20.77. In the LSG group, the number of lymph nodes retrieved met the AJCC criteria, which requires at least 16 nodes. The average number of harvested lymph nodes varies among medical literature [13]. Some studies report a harvest of 18 nodes, while most Asian studies recommend a clearance rate of over 30 nodes [13]–[17]. These differences could be attributed to strict quality control measures and higher case volume in Asian studies. Additionally, most Asian studies exclude cases that received neoadjuvant chemotherapy (NACT), which has been shown to decrease the number of nodes harvested [18]. Indeed, in our study, patients who did not receive NACT had a mean of at least 25 nodes harvested in LSG, compared to 18.69 in those who received NACT. Given the current recommendation of a course of neoadjuvant therapy in cases of resectable gastric cancer by the MAGIC and FLOT4 trials, the findings in our study are justifiable[19], [20]. The optimal lymph node harvest after NACT remains less defined, warranting future studies to compare the effects of various NACT regimens on lymph node harvest rates.

In this study, the mean operating time was 295.5 minutes in the LSG arm and 272.5 minutes in the OSG group. These findings are consistent with other studies, which have reported durations ranging from 196 to 370 minutes for LSG and 168 to 296 minutes for OSG [13], [21], [22]. Despite this difference, it is crucial to consider the non-significance of the operative time disparity and weigh it against the numerous benefits offered by minimally invasive surgery. The mean blood loss of 207.5 ml in the LSG group was comparable to 202.5 ml in the OSG group and aligns with existing literature [13], [15], [17].

In our study, we successfully demonstrated that laparoscopic gastrectomy with D2 lymphadenectomy was feasible and yielded comparable results to open gastrectomy in terms of the number of harvested lymph nodes, postoperative ambulation, oral feeding, and hospital stay. These findings are consistent with previous studies that have reported similar outcomes between laparoscopic and open gastrectomy with D2 lymphadenectomy [12], [13], [15].

Another noteworthy observation from our study was that laparoscopic gastrectomy patients had a lower BMI compared to those undergoing open gastrectomy, although the result was statistically insignificant. This finding is consistent with previous research, which has reported a higher proportion of patients with lower BMI being selected for laparoscopic gastrectomy [9], [12]. In patients undergoing laparoscopic gastrectomy, a higher BMI correlated with a lower lymph node yield (R² = 0.29)The restricted operational space caused by excess adipose tissue can limit the surgeon's range of motion and hinder the ability to perform complex surgical tasks, such as lymphadenectomy and anastomosis, with optimal precision. However, a recent metanalysis by Li Sun et al. have demonstrated that LSG with D2 lymphadenectomy is safe and feasible in patients with increased BMI [23].

It is essential to acknowledge the limitations of our study, such as the small sample size, which may restrict the generalizability of our findings. Additionally, our study did not assess long-term oncologic outcomes, such as recurrence and survival, which should be evaluated in future studies to gain a more comprehensive understanding of the implications of laparoscopic gastrectomy with D2 lymphadenectomy. Also, the retrospective nature of the study limits its potential.

Further well designed prospective studies are needed to assess the feasibility of laparoscopic approach with adequate lymphadenectomy following various neoadjuvant chemotherapy regimes. They should aim to validate and expand upon our findings to establish more comprehensive evidence regarding the benefits, learning curve, cost effectiveness and potential challenges of laparoscopic gastrectomy with D2 lymphadenectomy in the management of gastric carcinoma. Continued advancements in surgical techniques and technology may also further enhance the feasibility and outcomes of this minimally invasive approach for the benefit of patients.

Laparoscopic subtotal gastrectomy (LSG) with D2 lymphadenectomy is a feasible and safe approach for distal gastric adenocarcinoma. It offers comparable outcomes to open surgery (OSG) with faster post-operative recovery. However, careful patient selection and surgeon expertise are essential due to potential conversion to open surgery and slightly lower lymph node harvest in LSG. Further studies are needed to assess the impact of neoadjuvant chemotherapy on lymph node harvest rates in LSG cases.

CONFLICTS OF INTEREST:

Dr Vikeerna Bharati, Dr. Kallol Kumar Das Poddar, Dr Manas Ranjan Sahoo, Dr Shriganesh Shastri state that they have no financial ties or conflicts of interest to disclose.

AUTHOR CONTRIBUTIONS:

The study was conceptualized by Dr. Vikeerna. Dr. Vikeerna did the data curation with Dr. Shriganesh. Dr. Vikeerna, Dr. Kallol and Dr. Manas designed the methodology. Dr. Kallol did data analysis and illustrations. Dr. Vikeerna and Dr Kallol prepared the initial draft. All the authors went through the draft and provided their inputs to finalize it before submission.

FUNDING:

No funding received

DATA AVAILABILITY STATEMENT:

The datasheet related to this study will be available from the corresponding author upon reasonable request.

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No competing interests reported.

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Navigating the Gastric Cancer Maze: Embracing Laparoscopic D2 Lymphadenectomy for Safer and Faster Treatment: A retrospective cohort study

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