Laparoscopic Surgery is Associated with Increased Risk of Postoperative Peritoneal Metastases in T4 Colon Cancer: A Propensity Score Analysis

doi:10.21203/rs.3.rs-5098253/v1

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Laparoscopic Surgery is Associated with Increased Risk of Postoperative Peritoneal Metastases in T4 Colon Cancer: A Propensity Score Analysis

https://doi.org/10.21203/rs.3.rs-5098253/v1

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Background

This study aims to evaluate the postoperative safety, long-term survival, and postoperative peritoneal metastases (PPM) rate associated with laparoscopic surgery (LS) for T4 colon cancer.

Materials and methods

After propensity score matching, there were 85 patients in each of the LS and Open surgery groups. The primary outcomes were the 2-year OS, DFS, and PPM rates.

Results

After matching, 85 patients in each of the groups. The LS group had a higher cumulative 2-year peritoneal metastasis rate (13.9% vs. 3.9%, P = .029), while the 2-year OS (83.0% vs. 84.2%, P = .860) and 2-year DFS (70.9% vs. 74.4%, P = .540) showed no significant difference, compared to the open surgery group. The time to resume diet and the postoperative hospitalization in the LS group were shorter. There were no significant difference harvested lymph nodes, time to remove the drainage and gastric tube, and postoperative complications. The multivariate analysis revealed that LS (HR = 10.783, P = .002), postoperative complications (HR = 17.181, P < .001), and pN stage (N1: HR = 5.786, P = .045; N2: HR = 8.579, P = .027, respectively) were all independent risk factors for PPM.

Conclusion

For non-metastatic T4 colon cancer, the LS does not affect postoperative safety and long-term survival. Therefore, it should not be considered an contraindication for locally advanced T4 colon cancer. However, it is crucial to fully recognize the potential risk of increased PPM associated with LS.

laparoscopic surgery

propensity score matching

non-metastatic pT4 colon cancer

Colorectal cancer is among the most common cancers globally[1], with about 10–15% of patients diagnosed at stage T4[2, 3]. Currently, radical surgery plus postoperative adjuvant chemotherapy is the standard treatment for T4 colon cancer without metastases. In some cases, more extensive multivisceral surgery may be required[4]. Laparoscopic surgery (LS) offers several advantages, including reduced surgical trauma, improved postoperative recovery, and comparable survival compared to the open surgery[5, 6]. Therefore, an increasing number of surgeons tend to choose LS when dealing with T4 colon cancer[7].

T4 stage colon cancer has completely invaded the bowel wall, even after radical surgery, approximately 20–40% of patients experience metastasis or recurrence[8–10]. Meta-analyses have shown a positive association between T4 and metachronous peritoneal metastases[11]. Once peritoneal metastases occur postoperatively, symptoms such as bowel obstruction and ascites often develop, rapidly leading to death[12–15]. Some clinical studies suggest that LS for stage T4 colon cancer may increase the risk of postoperative peritoneal metastases (PPM)[16, 17]. Especially at the port site[18, 19]. However, this potential risk has not been thoroughly evaluated and remains controversial[20].

This study aims to evaluate the postoperative safety, long-term survival, and postoperative peritoneal metastases (PPM) rate associated with LS for non-metastatic T4 colon cancer.

Patient selection

Between January 2015 and December 2021, we collected clinical and pathological data from patients with non-metastatic pT4 stage colon cancer who underwent surgery at the Department of Anorectal Surgery, First Affiliated Hospital of the Naval Military Medical University. The data were collected from electronic medical records.

Inclusion criteria were as follows: (1) age ≥ 18 years; (2) postoperative pathological examination indicating T4 stage colon adenocarcinoma (including cecum and rectosigmoid junction); (3) preoperative examination revealed no metastasis to distant organs; (4) surgical approach was either laparoscopic or open; (5) complete data were available.

Exclusion criteria were as follows: (1) patients with other malignant tumors; (2) distant organ metastases discovered during surgery; (3) hereditary cancer (e.g. familial adenomatous polyposis); (4) combination of other serious diseases requiring palliative treatment; (5) emergency surgery (e.g. acute obstruction, perforation); and (6) recurrent or multiple primary colon cancers.

This work has been reported according to the STROCSS criteria[21].

Assessment parameters

Demographic variables including age, gender, American Society of Anesthesiologists (ASA) grade, BMI, preoperative CEA and CA199 levels, tumor location, preoperative neoadjuvant chemotherapy, and adjuvant postoperative chemotherapy were collected. Additionally, we assessed intraoperative and postoperative data, including operative time, complications (using the Clavien–Dindo classification), surgical approach, estimated blood loss, removal of the drainage tube, time to resume diet, removal of the gastric tube, and length of postoperative hospital stay. Histopathological data were also extracted, including tumor maximum diameter, pT stage, pN stage, harvested lymph nodes, surgical surgery margin, tumor differentiation, lymphovascular invasion, nerve invasion, and KRAS/NRAS/BRAF status.

Outcome measurement and follow-up

The main outcomes of the study were the 2-year OS rate, DFS rate, and incidence of PPM. PPM were defined as the presence of any tumor lesion at the peritoneal level after surgery, whether radiologically suspected or pathologically confirmed[22].

The follow-up protocol included clinical examinations, tumor marker evaluations, colonoscopy, CT of the chest and abdomen. Survival data were collected through chart reviews and telephone follow-ups. The last date of follow-up was December 31, 2023.

Statistical analysis

For continuous variables, the Mann-Whitney U test or Student's t-test was used. Categorical variables were compared using Fisher’s exact test. Due to the imbalance of patient characteristics between the two groups, propensity score matching (PSM) was performed. The surgical approach was set as the dependent variable. Patients were then matched with the nearest neighbor method. Covariates included age, gender, ASA grade, BMI, preoperative CEA, preoperative CA199, pT stage, pN stage, tumor maximum diameter, and surgical surgery margin[23]. Survival analyses were conducted with Kaplan–Meier analysis. Significant variables in the univariate analysis were further evaluated using multivariate Cox regression analysis. A P-value of less than 0.05 was considered significant. All of the statistical analyses were performed using R (version 4.3.2).

Baseline characteristics

A total of 292 patients were enrolled, including 97 patients in the LS group and 195 patients in the open group (Fig. 1). Before matching, the LS group had a higher proportion of obesity and overweight patients (P = .033) and a smaller tumor maximum diameter compared to the open group (P = .024).

After matching, each group consisted of 85 patients. No significant differences were found in the baseline characteristics or histopathological outcomes between the two groups. (Tables 1 and 2).

Intraoperative and postoperative outcomes

The LS group had a significantly longer operation time (198 ± 80.7 min vs. 165 ± 61.9 min, P = .004) but less estimated blood loss (P = .008). Additionally, patients in the LS group resumed their diet more quickly (3.54 ± 1.21 days vs. 4.18 ± 1.90 days, P = .012) and had shorter postoperative hospital stays (7.31 ± 3.50 days vs. 8.01 ± 3.75 days, P = .012). In contrast, there was no significant difference in number of harvested lymph nodes, time to remove the drainage and gastric tube, and postoperative complications between the two groups (Table 3).

Long-term outcomes

The 2-year cumulative peritoneal metastasis rate in the LS group was 13.9%, which was significantly higher (P = .029). However, no statistically significant difference was observed in the 2-year OS rate (83.0% vs. 84.2%, P = .860) or DFS rate (70.9% vs. 74.4%, P = .540) between the two groups (Fig. 2).

The results of the multivariate Cox analysis revealed that LS (HR = 10.783, 95% CI = 2.326–49.978, P = .002), pN stage (N1: HR = 5.786, 95% CI = 1.037–32.283, P = .045; N2: HR = 8.579, 95% CI = 1.277–57.625, P = .027, respectively), and postoperative complications (HR = 17.181, 95% CI = 3.973–74.297, P < .001) were all independent risk factors for PPM. Furthermore, although it did not reach statistical significance in the multivariate analysis, lymphovascular invasion was identified as a potential risk factor for PPM in the univariate analysis (Table 4).

LS has been favored by a growing number of surgeons due to its faster recovery, shorter hospital stays, and long-term outcomes comparable to those of open surgery[20, 24, 25]. However, studies have suggested that LS may be associated with the increased risk of peritoneal metastasis[17, 26]. These studies were all retrospective and exhibited an imbalance in baseline characteristics. Currently, there are no randomized controlled trials addressing this issue[15]. Moreover, clinical trials for metastatic colon cancer have systematically excluded patients with peritoneal metastases, potentially due to challenges in imaging and assessment[27, 28].

Since larger tumors and local tissue invasion can significantly increase surgical difficulty, the decision between open or LS is made by the surgeon based on the individual characteristics of each patient. Consequently, in our study, the tumor diameter was smaller and the proportion of overweight and obese patients was higher in the LS group. In contrast to some previous studies addressing this issue [17, 26, 29], we used PSM to balance baseline characteristics and minimize bias.

Through multivariate analysis, we found that the LS was a risk factor for PPM. The use of cold, dry carbon dioxide for pneumoperitoneum during LS may damage peritoneal mesothelial cells[30–32], leading to the release of proinflammatory and proangiogenic mediators, including COX-2 and VEGF-A. This process could build a microenvironment conducive to tumor cell proliferation, enhance the adhesion of disseminated cells, and ultimately increase the risk of metastasis[33, 34]. Although laparoscopy offers a magnified view, it may result in the omission of small peritoneal metastases hidden behind organs or situated in blind spots of the camera's field of vision[35]. In contrast, during open surgery, the surgeon can palpate and explore areas beyond visual reach, potentially detecting peritoneal metastases that might otherwise go unnoticed[36]. Additionally, since the intraoperative lavage area is more restricted in LS, there may be a higher chance of residual free cancer cells remaining in the abdominal cavity postoperatively, which also increases the risk of PPM[37, 38].

Notably, we found pN stage and postoperative complications to be independent risk factors for PPM, which is consistent with previous studies[39, 40]. Since postoperative complications may trigger an inflammatory response[41, 42], the inflammation may promote tumor metastasis and recurrence through mechanisms such as damage to the intestinal vascular barrier[43].

When locally advanced tumors require multivisceral surgery, LS presents a significantly greater challenge[44, 45]. In this study, 5 patients were converted to open surgery. The reasons were as follows: in 2 cases, tumor invasion into adjacent organs made LS difficult; in 2 cases, severe intra-abdominal adhesions obstructed the view; and in 1 case, the tumor was too large to be safely resected. Conversion of laparoscopic colon cancer surgery introduces additional trauma and increased costs, and it may also elevate the risk of long-term recurrence and metastasis[46]. Before selecting LS for T4 colon cancer surgery, surgeons must thoroughly assess the surgical difficulty using imaging and colonoscopy findings to minimize the risk of conversion.

Our study has some limitations. Despite performing PSM to balance baseline characteristics, the retrospective, single-center design limits the generalizability of the results. A larger cohort could enhance the statistical power of our findings.

Compared to open surgery, LS offers faster postoperative recovery and comparable long-term survival outcomes. Therefore, it should not be considered an contraindication for T4 colon cancer. However, it is crucial to fully recognize the potential risk of increased PPM associated with LS and to prioritize early detection of peritoneal metastasis to facilitate further treatment. Multi-center prospective studies are necessary to provide insights into treatment effects across different patient populations, aiding in the determination of which subgroups might benefit from this.

Ethical approval

The study was approved by the Ethics Committee of the First Affiliated Hospital of the Naval Military Medical University (Ethics Approval No. CHEC2023-067).

Source of funding

This work was supported by Science and Technology Innovation Plan Of Shanghai Science and Technology Commission (No.23DZ2202000)

Conflicts of interest disclosure

The authors have no competing interests for this manuscript.

Acknowledgements

None.

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Laparoscopic Surgery is Associated with Increased Risk of Postoperative Peritoneal Metastases in T4 Colon Cancer: A Propensity Score Analysis

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Introduction

Materials and methods

Patient selection

Assessment parameters

Outcome measurement and follow-up

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Result

Baseline characteristics

Intraoperative and postoperative outcomes

Long-term outcomes

Discussion

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