Techniques, perioperative outcomes, prognosis, and survival associated with laparoscopic surgery for T3-T4a colon cancer

Abstract

BACKGROUND

The efficacy of laparoscopic surgery for the treatment of T3-T4a colon cancer remains a subject of debate in the medical community.

AIM

To explore the surgical techniques, perioperative outcomes, follow-up results, patient prognosis, and survival status associated with laparoscopic surgery for T3-T4a colon cancer.

METHODS

A total of 202 patients with T3-T4a colon cancer treated at the Affiliated Hospital of Hebei University between January 2020 and December 2024 were selected for this study and divided into two groups based on the type of surgery: Open surgery group (101 cases) and laparoscopic surgery group (LAP group, 101 cases). Perioperative indicators (surgical time, postoperative drainage, first flatus, hospital stay, intraoperative blood loss, and number of lymph nodes removed), disease-free survival, and overall survival at 1-year and 3-year follow-ups, as well as the incidence of complications, were compared between the two groups.

RESULTS

The LAP group had longer surgical times and a greater number of lymph nodes removed compared to the open surgery group (P < 0.05). The LAP group also had less blood loss, shorter drainage time, faster time to flatus, and a lower incidence of complications compared to the open surgery group (P < 0.05). There was no significant difference in hospital stay, disease-free survival, or overall survival between the two groups during the follow-up period, and this remained true even after adjusting for subgroups based on left-sided colon, right-sided colon, and T4a stage (P > 0.05).

CONCLUSION

The long-term outcomes of laparoscopic radical surgery for T3-T4a colon cancer are comparable to those of open surgery and can accelerate patient recovery and reduce the risk of short-term complications, offering better immediate outcomes.

Key Words: Laparoscopic surgery; T3-T4a colon cancer; Clinical research; Prognosis; Survival

Core Tip: Owing to its minimally invasive nature, laparoscopic surgery has shown better postoperative recovery and cosmetic outcomes in colon cancer treatment. This study explored the clinical effectiveness of laparoscopic surgery for treating T3-T4a colon cancer, which is of great significance for further exploring treatment options for these patients. Our findings revealed that laparoscopic surgery has good immediate effects as well as a long-term survival rate comparable to open surgery, providing a valuable reference for clinical practice.

INTRODUCTION

Epidemiological surveys indicate that in China, the incidence of colon cancer accounts for 9.87% of all malignant tumors, while rectal cancer accounts for 8.01%. Among these, the incidence of colorectal cancer ranks fourth among men and third among women. Data also show that between 2000 and 2005, the incidence of colorectal cancer in China grew at an annual rate of 4.2%[1], while it slowed to an annual rate of 1.3% between 2006 and 2011. Surgical intervention remains one of the primary treatments for colorectal cancer, especially as the development of laparoscopic technology has gradually increased the precision and cure rate of surgeries[2]. However, the development of surgical treatments for colon and rectal cancers has been uneven.

Since the late twentieth century, the introduction of treatment concepts and techniques such as total mesorectal excision and 2-cm resection margins has rapidly advanced the therapeutic outcomes and recurrence inhibition effects of rectal cancer surgery. In contrast, the development of surgical concepts for colon cancer, which has a slightly higher incidence, has been slower. Laparoscopic surgery is a conventional procedure for colon cancer, and numerous reports have confirmed its efficacy, which is comparable to traditional open surgery, with significantly better safety. However, most reports do not involve patients with T3 and T4 stages, especially the effects of laparoscopic surgery for patients with T4 stage cancer are only seen in some retrospective studies[3].

T3 colon cancer is characterized by the invasion of the tumor cells into the serosal layer of the colon wall, while T4a colon cancer indicates that cancer cells have penetrated the visceral peritoneal surface[4]. Theoretically, a radical treatment can be achieved by surgically removing multiple organs as a single block. However, due to the complexity of the condition of the patient, intraoperative plans need to be frequently adjusted, and incomplete resection is a likely outcome, resulting in a higher rate of conversion to open surgery during laparoscopic treatment and a higher risk of postoperative recurrence. Therefore, the American Joint Committee on Cancer does not currently recommend this procedure for serosal invasion-type colon cancer (such as T3 and T4a stages). European guidelines go so far as to consider laparoscopic surgery to be absolutely contraindicated for T4 colon cancer[5].

In the field of colon cancer treatment, laparoscopic surgery, as a minimally invasive surgical method, has attracted much attention in recent years. Especially for patients with T3-T4a colon cancer, the applicability and effectiveness of laparoscopic surgery have become a hot topic of academic discussion. On the one hand, supporters believe that laparoscopic surgery has the advantages of less trauma, quick recovery, and slight pain, which can reduce postoperative complications and improve the quality of life of patients. These views are usually based on some preliminary clinical studies and meta-analyses showing that laparoscopic surgery may bring better short-term outcomes in some cases[6]. On the other hand, some researchers have also expressed concerns about the long-term effect and oncological safety of laparoscopic surgery for the treatment of T3-T4a colon cancer. These concerns primarily stem from the consideration of the risk of tumor spread and the challenges of demanding surgical techniques and a steep learning curve[7]. Some studies indicate that laparoscopic surgery may increase the risk of tumor cell dissemination through the pneumoperitoneum route and may not achieve the same radical effect as traditional laparotomy when handling more complex locally advanced tumors. However, since colon cancer is more prevalent in the elderly, the decline in physical function and the prevalence of comorbidities make it difficult for many older patients to withstand open surgery. Currently, international scholars such as Bretagno and Leroy[6] believe that laparoscopic surgery is feasible for patients with advanced colon cancer and can improve safety. Based on these considerations, we aimed to addresses this controversial issue by retrospectively analyzing patients with T3-T4a colon cancer treated in our hospital to explore the effects of laparoscopic surgery.

MATERIALS AND METHODS

Basic patient characteristics

A total of 202 patients with T3-T4a colon cancer treated at the Affiliated Hospital of Hebei University, China between January 2020 and December 2024 were divided into two groups based on the surgical procedure adopted: Open surgery group and laparoscopic surgery group (LAP group), with 101 cases in each group. In the open surgery group, there were 53 men and 48 women; their ages ranged from 49 to 73 years (mean age 61.30 ± 5.72 years); histological typing revealed 91 cases of adenocarcinoma and 10 cases of adenosquamous carcinoma; tumor-node-metastasis staging detected 56 cases at the T3 and 45 cases at the T4a stage; the sites of lesion included 58 cases in the left and 43 cases in the right colon. In the LAP group, there were 59 men and 42 women; their ages ranged from 51 to 73 years (mean age 61.98 ± 5.11 years); histological typing revealed 93 cases of adenocarcinoma and 8 cases of adenosquamous carcinoma; tumor-node-metastasis staging detected 52 cases at the T3 and 49 cases at the T4a stage; the sites of lesion included 61 cases in the left and 40 cases in the right colon. There was no statistically significant difference in baseline data between the two patient groups (P > 0.05).

The inclusion criteria were as follows: (1) Both groups underwent pathological examination after surgical resection, which confirmed the T3-T4a status; (2) All patients were able to tolerate surgery and had not received other anti-tumor treatments such as radiotherapy, chemotherapy, or immunotherapy before surgery; (3) Patients with single-site colon cancer; (4) Patients without a history of abdominal surgery; (5) Patients with normal cognitive and language functions; and (6) Patients with complete clinical data. The exclusion criteria were as follows: (1) Secondary colon cancer; (2) Patients with severe organic diseases; (3) Patients with impaired function and integrity of vital organs; (4) Distant metastasis of the tumor; (5) Patients who underwent palliative surgery; (6) Patients with abnormal coagulation function; (7) Severe adhesion of the cancer lesion with surrounding tissues; (8) Patients with immunological diseases; and (9) Patients who died of non-tumor-related causes during the follow-up period.

Surgical procedures

Patients in the open surgery group underwent traditional open surgery, while those in the LAP group underwent laparoscopic surgery. Due to the unique anatomical location of the colon, with its physiological structure and properties differing between the left and right sides of the colon, the specific surgical techniques employed are described separately based on the location of the colon in this study. Tumors located between the splenic flexure and the sigmoid colon were treated by left hemicolectomy; tumors located between the distal transverse colon and the appendix were treated by right hemicolectomy. Regarding preoperative preparations, all patients were switched to a liquid diet 1 day before surgery and could be given oral laxatives for bowel cleansing. If necessary, enemas could be used for bowel cleansing. If patients had preoperative comorbidities such as hypertension or anemia, these were managed with appropriate treatments. Patients were routinely asked to fast for 8 hours and prohibited from drinking for 6 hours before surgery. Antibiotics could be administered to patients 0.5 hours before surgery to prevent infection. All patients received general anesthesia followed by endotracheal intubation.

Laparoscopic radical surgery

All patients received routine analgesia and anti-infection medication as well as long-term follow-up.

Right hemicolectomy: After assisting the patient to lie in a supine lithotomy position or standard lithotomy position, and following satisfactory anesthesia, an indwelling urinary catheter was placed, and routine disinfection and draping were performed. A 10-mm incision was made below the umbilicus of the patient, and a Veress needle was used to create a 15 mmHg pneumoperitoneum. A 10-mm Trocar was inserted at the same site to introduce the laparoscope, which served as the observation port. Initially, the abdominal and pelvic cavities, as well as the basic condition of the tumor (location, size, number) and adhesion situation, were inspected through the observation port. A 5-mm incision was made at the McBurney’s point on the left side of the abdomen as the secondary operating port, and a 10-12-mm incision was made approximately 4 cm below the left midclavicular line along the costal margin as the main operating port. Surgical instruments were inserted into the abdominal cavity along the operating ports. The small intestine and omentum were pushed to one side, the colon was gently lifted to obtain a view of the mesentery, and the ileocolic vessels were mobilized. At the root of the vessels, 5-mm double clamps were placed, and the vessels were ligated and cut using a locking method. After mobilizing the colon, the right colic vessels were visualized and ligated, thus obtaining a view of the middle colic vessels. After clearing the lymph nodes at the root of the middle colic artery, the gastrocolic ligament was incised, and the transverse colon was separated from its corresponding omentum. After the entire removal of the affected colon and the adjacent transverse colon, the intestinal tract was reconstructed. The opening was closed with inverted barbed sutures, the seromuscular layer was buried, and the mesenteric defects were closed. The pneumoperitoneum was released, the specimen was removed, and the abdominal cavity was irrigated. The patient was monitored for active bleeding; if none was present, a routine abdominal drain was placed to prevent fluid accumulation. After the procedure, the abdomen was closed routinely, and the incisions were sutured, concluding the surgery.

Left hemicolectomy: The patient was placed in a supine lithotomy position, and disinfection and draping were carried out. A 10-mm incision was made above the umbilicus of the patient, and the pneumoperitoneum was created using the same method as for the right side, with the laparoscope inserted to create the observation port. The abdominal cavity was inspected through the observation port (the inspection method and content were the same as those employed for the right colon). The main and secondary operating ports were created in the same manner as that employed for right colon surgery, except that the right McBurney’s point and the right midclavicular line along the costal margin were used, with all other operations being consistent. After the procedure, the position of the patient was adjusted to a head-low, feet-high right lateral position, and the sigmoid colon was gently lifted. An ultrasonic scalpel was used to incise along the right side of the root of the mesentery at the sacral promontory. The resection range extended from the root of the inferior mesenteric artery upwards, where the vessels were ligated and the lymphatic and fatty tissues were cleared, down to the rectovesical excavation. The sigmoid mesentery was separated laterally to obtain a view of the ureter and reproductive vessels. The peritoneum on the left posterior side of the sigmoid mesentery and the peritoneum of the left paracolic gutter were incised and joined with the separation plane on the right side. The descending colon and transverse colon mesentery were deeply separated, and the transverse colon, descending colon, and sigmoid colon were mobilized. After the entire block of the intestinal tube containing the cancer focus was removed, routine anastomosis was performed. The pneumoperitoneum was closed, and subsequent operations were the same as described above, concluding the surgery.

Observation indicators

Perioperative indicators: A comparison was made of the intraoperative indicators (surgical time, intraoperative blood loss, and number of lymph nodes removed) and postoperative indicators (drainage time, time to first flatus, and hospital stay) between the two patient groups.

Complications: We monitored and recorded the incidence of complications within 1 year of follow-up for both patient groups, primarily documenting the rates of incisional infection, intra-abdominal infection, intestinal obstruction, and anastomotic leak.

Follow-up and prognostic survival: A comparison was made of the disease-free survival (DFS) and overall survival (OS) between the two patient groups, the DFS and OS durations for the left and right hemicolectomy subgroups within each group, and the DFS and OS periods of the T4a stage subgroup within each group.

Statistical analysis

Data were analyzed using SPSS 20.0 statistical software; if quantitative data followed a normal distribution, t-tests were used, with results expressed as the mean ± SD. Qualitative data were analyzed using the χ²-test, with results expressed as percentages (%). The level of significance was set at α = 0.05. In addition, we performed deletions for missing data.

RESULTS

Perioperative indicators

For intraoperative indicators, operation time and lymph node clearance in the LAP group were higher than those in the open surgery group, and blood loss was lower than that of the open surgery group (P < 0.05). For postoperative indicators, drainage time and time to first flatus in the LAP group were lower than those of the open surgery group (P < 0.05), while the hospitalization time was not different between these two groups (P > 0.05, Table 1).

Table 1 Comparison of perioperative indicators in the two groups, n = 101, mean ± SD.

Group	Operation time, minutes	Intraoperative blood loss, mL	Number of lymph nodes cleared, count	Drainage time, days	Time to first flatus, days	Hospital stay, days
Open	201.02 ± 9.24	310.10 ± 10.57	14.11 ± 1.16	9.70 ± 2.33	4.81 ± 1.07	11.44 ± 2.67
Laparoscopic	208.21 ± 10.43	299.22 ± 8.48	16.23 ± 2.27	8.02 ± 1.79	3.98 ± 0.93	11.31 ± 2.43
t	5.186	8.069	8.358	5.746	5.884	0.362
P value	< 0.001	< 0.001	< 0.001	< 0.001	< 0.001	0.718

Complications

The overall rate of complications in the LAP group was lower than that of the open surgery group (31.68% vs 45.54%, respectively, P > 0.05, Table 2).

Table 2 Comparison of complication rates in the two patient groups, n = 101, n (%).

Group	Wound infection	Pelvic infection	Iliac passion	Anastomotic fistula	Total incidence
Open	16 (34.78)	19 (41.30)	9 (8.91)	2 (1.98)	46 (45.54)
Laparoscopic	12 (26.09)	13 (12.87)	6 (5.94)	1 (0.99)	32 (31.68)
χ2					4.093
P value					0.043

Follow-up, prognosis and survival status

DFS and OS durations were higher at the 1-year and 3-year follow-ups in the LAP group, but the results were not statistically different (P > 0.05, Table 3). The 1-year and 3-year DFS and OS did not differ significantly between the two groups even after adjusting for subgroups based on left-sided colon (P > 0.05, Table 4), right-sided colon (P > 0.05, Table 5), and T4a stage (P > 0.05, Table 6).

Table 3 Comparison of prognosis and survival during the follow-up period in the two groups, n = 101, n (%).

Group	1-year DFS	3-year DFS	1-year OS	3-year OS
Open	90 (89.19)	66 (65.35)	92 (91.09)	79 (78.22)
Laparoscopic	93 (92.08)	71 (70.30)	96 (95.05)	83 (82.18)
χ2	0.522	0.567	1.227	0.499
P value	0.470	0.451	0.268	0.480

DFS: Disease-free survival; OS: Overall survival.

Table 4 Comparison of survival outcomes in the follow-up period of the left-sided colon subgroup of patients, n (%).

Group	1-year DFS	3-year DFS	1-year OS	3-year OS
Laparotomy (n = 58)	53 (91.37)	40 (68.97)	54 (93.10)	49 (84.48)
Laparoscopic (n = 61)	57 (93.44)	43 (70.49)	58 (95.08)	51 (83.61)
χ2	0.181	0.032	0.210	0.017
P value	0.670	0.856	0.647	0.896

DFS: Disease-free survival; OS: Overall survival.

Table 5 Comparison of survival in the follow-up period of the right-sided colon subgroup of patients, n (%).

Group	1-year DFS	3-year DFS	1-year OS	3-year OS
Open (n = 43)	37 (86.05)	26 (60.47)	38 (88.37)	30 (69.77)
Laparoscopic (n = 40)	36 (90.00)	28 (70.00)	38 (95.00)	32 (80.00)
χ2	0.306	0.829	1.179	1.148
P value	0.580	0.363	0.278	0.284

DFS: Disease-free survival; OS: Overall survival.

Table 6 Comparison of survival between the two groups of T4a patients during the follow-up period, n (%).

Group	1-year DFS	3-year DFS	1-year OS	3-year OS
Open (n = 45)	39 (86.67)	28 (62.22)	41 (91.11)	31 (68.89)
Laparoscopic (n = 49)	44 (89.80)	33 (67.35)	46 (93.88)	36 (73.47)
χ2	0.222	0.270	0.016	0.240
P value	0.637	0.603	0.900	0.624

DFS: Disease-free survival; OS: Overall survival.

DISCUSSION

The treatment landscape for patients with colon cancer has undergone significant changes with the continuous iteration of chemotherapeutic agents and the advent of targeted therapies. However, surgery remains an essential treatment modality for patients with both early and advanced-stage colon cancer. In the context of malignant tumors, achieving satisfactory therapeutic outcomes while also considering long-term prognosis and safety is a common pursuit among surgeons[8,9]. Given the lack of consensus on surgical approaches for T3-T4a colon cancers that have penetrated the serosal layer, it is necessary to further explore the clinical efficacy differences between laparoscopic and open surgeries. Our present findings revealed that the LAP group had longer surgical times, but lower intraoperative blood loss, drainage time, and time to first flatus (P < 0.05). The complexity of the techniques involved in laparoscopic surgery accounts for the extended duration of surgery, which is consistent with the findings of Ding et al[8]. Laparoscopy allows for magnified visualization, aiding surgeons in obtaining a clearer field of view, which facilitates precise resection and hemostasis, thereby reducing blood loss. Additionally, controlling blood loss can minimize the impact of blood on the surgical field, creating a synergistic effect. The smaller incisions associated with laparoscopic surgery result in less disruption to the abdominal wall and intestinal circulation, reducing intra-abdominal bleeding[10]. By controlling intra-abdominal hemorrhage and minimizing damage to healthy tissues, postoperative drainage of blood and secretions is reduced, shortening the duration of drainage. The reduced impact of laparoscopy on organs and circulation helps to decrease postoperative pain and stress responses, which in turn accelerates patient mobilization. Early patient mobilization promotes gastrointestinal motility, thereby shortening the time to anal flatus. Additionally, some scholars have pointed out[9] that the peritoneum secretes special fluids that can prevent intestinal adhesions, and laparoscopic surgery reduces direct contact between the hands of the surgeon and the intestines of the patient, minimizing the loss of peritoneal secretions, which also helps to speed up the recovery of gastrointestinal function. The recovery of gastrointestinal function allows patients to resume diet earlier, promoting the restoration of nutritional levels and aiding rapid recovery. However, this study did not find a significantly shorter hospital stay for patients in the LAP group compared to the open surgery group, which may be related to the multitude of factors affecting the recovery of patients with malignant tumors[11].

Our present results revealed that the number of lymph nodes removed in the LAP group was greater than that of the open surgery group (P < 0.05). Infiltration and distant metastasis are the main pathological characteristics of malignant tumors, and the primary mode of metastasis for colon cancer is through lymph node transfer. Therefore, whether lymph nodes have been involved is considered one of the main factors affecting colon cancer prognosis. Hence, maximizing the clearance of lymph nodes is of significant importance for controlling postoperative recurrence and metastasis of the cancer focus. Laparoscopy can magnify local images, allowing surgeons to more clearly and intuitively observe the lymph nodes in the abdominal cavity, which helps to increase the number of lymph nodes cleared. In contrast, open surgery involves greater blood loss, and the surgical field can become blurred, which can also reduce the effectiveness of lymph node clearance[12].

Patients in the LAP group had a lower incidence of complications (P < 0.05). The smaller incisions associated with laparoscopic surgery can significantly reduce the exposure time of the intestines to the air, helping to reduce contamination and the rate of infection. Intestinal obstruction is a more common and severe complication in laparoscopic colorectal surgery and is directly related to intra-abdominal adhesions. As mentioned above, laparoscopic surgery may reduce intra-abdominal adhesions by minimizing the loss of peritoneal secretions. On the other hand, laparoscopic surgery causes less damage to the intestines, and the postoperative recovery of intestinal motility occurs more quickly, which can accelerate the reconstruction of blood circulation, reduce blood exudation, and lower the incidence of intra-abdominal adhesions. Moreover, laparoscopy can provide a clearer surgical field, which helps to improve the effectiveness of abdominal irrigation, thus better clearing inflammatory and purulent effusions in the abdominal cavity and also reducing the risk of intra-abdominal adhesions[12-14]. Anastomotic leak is widely considered one of the most serious complications in radical surgery for colorectal cancer, with insufficient blood circulation and infection at the anastomosis being the main inducing factors. These considerations suggest that the reshaping of blood circulation occurs more effectively after laparoscopic surgery and the incidence of abdominal infection remains low[15].

In the comparison of follow-up and survival at 1 and 3 years, there was no statistical difference in DFS or OS durations between the two patient groups (P > 0.05). Even after adjusting for subgroups based on the side of the lesion and cancer stage, the results remained non-significant (P > 0.05). This indicates that, based solely on the results of this study, the long-term efficacy of laparoscopic surgery for patients with T3-T4a cancer is comparable to that of open surgery, which is consistent with the study by Kang et al[11]. A meta-analysis of laparoscopic colectomy for T4 colon cancer suggests that laparoscopic surgery may reduce patient survival rates by increasing the rate of postoperative peritoneal metastasis. This may be explained by the occurrence of “dead angles” in the surgical field during laparoscopic surgery, caused by factors such as pneumoperitoneum and deep anatomical locations, which may lead to peritoneal nodules remaining undetected by the surgeon. However, other studies have indicated that laparoscopic surgery does not increase the risk of postoperative recurrence and distant metastasis in patients with colon cancer. Therefore, we speculate that there may be some independent risk factors in laparoscopic surgery for colon cancer that can interfere with long-term survival rates; however, overall, the difference in long-term survival between laparoscopic and open surgery is minimal. Owing to the small sample size, this study did not include cases of laparoscopic conversion to open surgery. Previous studies by Jayne et al[14] have found that the incidence of complications in patients undergoing conversion to open surgery for T4 colon cancer was significantly higher than that of patients undergoing laparoscopic surgery. However, Liu et al[15] found no difference in DFS or OS values when the 5-year survival rates of patients who underwent conversion to open surgery were compared with those who had laparoscopic surgery for colon cancer. This suggests that while conversion to open surgery during laparoscopic surgery may increase the risk of short-term complications, there is no consensus on whether it reduces long-term efficacy.

This study acknowledges certain limitations that may affect the generalizability of its findings. First, as a single-center study, our results may be influenced by specific practices and patient demographics unique to our institution, potentially limiting their applicability to other settings. Second, the relatively small sample size could reduce the statistical power of our analysis and increase the risk of type II errors, which may affect the robustness of our conclusions. These limitations should be considered when interpreting the present results, and future studies with larger, multicenter cohorts are needed to validate our findings and enhance the external validity of our conclusions.

CONCLUSION

In summary, for patients with T3-T4a colon cancer, the choice of surgical procedure is complex when considering laparoscopic surgery, especially for right hemicolectomy, which has a higher operational difficulty, leading to longer surgery times and a steeper learning curve for surgeons. However, compared to open surgery, laparoscopic surgery can shorten patient recovery time, improve the lymph node clearance rate, and reduce the incidence of complications within 6 months, showing better short-term outcomes. The long-term follow-up DFS and OS values for both surgical methods show no difference, indicating similar long-term efficacy. However, this study is a single-center retrospective study with a small number of cases and a relatively short follow-up period, which may introduce bias into the results. Future studies with larger multicenter cohorts and longer follow-up periods are needed to further assess the effectiveness of laparoscopic radical surgery.