Analysis of Bacterial Culture of Fluid in the Surgical Area in Transanal Total Mesorectal Excision and Laparoscopic Total Mesorectal Excision

Abstract

Purpose:

To investigate the clinical value of the bacterial culture of fluid in the surgical area in laparoscopic transanal total mesorectal excision (Lap-taTME) and laparoscopic total mesorectal excision (Lap-TME).

Methods:

Clinical data of 106 patients with rectal cancer who had undergone surgery were retrospectively collected, including 56 patients in the Lap-taTME group and 50 patients in the Lap-TME group. In the Lap-taTME group, the initial pelvic fluid, the rectal cavity fluid after purse-string suture, and the pelvic cavity fluid after anastomosis were collected and recorded as culture No. 1, No. 2, and No. 3, respectively. In the Lap-TME group, culture No. 1 and No. 3 were collected as done in the Lap-taTME group. The culture results and postoperative complications were statistically analyzed.

Results:

The positive rate of culture No. 1 was zero in both groups, and there were 6 cases (10.7%) with positive culture No. 2 in the Lap-taTME group. However, the number of patients with positive culture No. 3 (7, 12.5%) and cumulative positive culture cases (11, 19.6%) in the Lap-taTME group were significantly higher than those in the Lap-TME group (0) (all P < .05). Pelvic infection occurred in 4 (7.1%) of the 11 cases (19.6%) with positive culture in the Lap-taTME group, accounting for 36.4% (4/11). There were no significant intergroup differences in anastomotic leakage and pelvic infection (all P > .05).

Conclusion:

Positive bacterial culture of fluid during Lap-taTME indicates an increased risk of pelvic infection after operation. Lap-taTME is more prone to intraoperative contamination than Lap-TME but does not significantly increase the risk of postoperative pelvic infection.

Introduction

Total mesorectal excision (TME)—proposed by Professor Heald in 1982—has greatly contributed to the reduction in the local recurrence rate of the pelvic cavity,¹ improvement of the R0 resection rate of the tumor, and increased safety of the circumferential resection margin (CRM) of the specimens. At present, laparoscopic total mesorectal excision (Lap-TME) is a preferred treatment method for rectal cancer in centers that adhere to the concept of minimally invasive surgery and have mature endoscopic techniques. In 2010, Professor Sylla reported transanal total mesorectal excision (taTME)²; laparoscopic transanal total mesorectal excision (Lap-taTME) has shown operational advantages in patients with prostatic hypertrophy, pelvic stenosis, and low rectal cancer.

However, compared with Lap-TME, Lap-taTME is still controversial in terms of no touch and aseptic principle. There are still few studies on whether postoperative pelvic infection after Lap-taTME is associated with a positive bacterial culture of the fluid in the surgical area. Therefore, we analyzed the results of fluid culture in patients with rectal cancer who underwent Lap-TME and Lap-taTME in our hospital to discover the relationship between positive culture and postoperative pelvic infection, as well as to provide a reference for surgical procedures and postoperative treatment.

Methods

Patients

Inclusion criteria were as follows: (1) rectal malignant tumor with the lower edge of the tumor being 2 to 10 cm from the anal edge; (2) preoperative clinical stages I–III or stage IV with liver metastasis that can be resected; (3) no serious underlying disease, and no serious heart, liver, lung, and kidney dysfunctions so that surgery can be tolerated. Exclusion criteria were as follows: (1) Miles surgery; (2) inability to radically remove metastasis; (3) obstruction or perforation caused by tumor and necessity to undergo emergency surgery; and (4) preoperative pulmonary infection and urinary tract infection. This retrospective study was approved by the Ethics Committee of the First Affiliated Hospital of Chongqing Medical University Hospital (No. 20193501) and individual informed consent for this retrospective analysis was waived. During the study, Declaration of Helsinki was adhered to.

Based on the above criteria, the clinical data of 106 patients who had successfully undergone radical resection of rectal cancer from September 2017 to August 2019 were retrospectively collected. Divided by the surgical approach, there were 56 patients in the Lap-taTME group and 50 patients in the Lap-TME group. The two groups did not show significant differences in sex, height, body mass index, and preoperative carcinoembryonic antigen concentration (P > .05) (Table 1).

Table 1.

Comparison of Clinical Data Between Two Groups of Rectal Cancer Patients

Clinical data	Lap-taTME	Lap-TME	Statistics	P
Sex, n (%)		c² = 2.08	0.149
Male	42 (75)	31 (62)
Female	14 (25)	19 (38)
Height (cm)	164.09 ± 6.68	161.68 ± 6.40	t = 1.89	.061
BMI (kg/m²)	23.27 ± 2.61	22.66 ± 2.73	t = 1.18	.242
CEA (ng/mL)	6.08 ± 12.76	5.74 ± 6.29	t = 1.72	.863

BMI, body mass index; CEA, carcinoembryonic antigen; Lap-taTME, laparoscopic transanal total mesorectal excision; Lap-TME, laparoscopic total mesorectal excision.

The patients received mechanical bowel preparation including a liquid diet and oral polyethylene glycol electrolytes powder on the day before surgery and also received antibiotic bowel preparation including oral metronidazole tablets (400 mg tid) and streptomycin (1 g bid) on the day before surgery.

Sampling timing for bacterial culture

In the Lap-taTME group, the initial pelvic fluid before transabdominal operation was collected and recorded as culture No. 1. The rectal cavity fluid after disinfecting with 100 mL diluted iodophor and purse-string suture during transanal operation was also collected and recorded as culture No. 2. The pelvic cavity fluid after anastomosis and rinsing with 500 mL sterilized physiological saline was collected and recorded as culture No. 3. In the Lap-TME group, culture No. 1 and No. 3 were collected as in the Lap-taTME group.

Observation indicators

Postoperative pathology included positive rate of distal and proximal margins; positive rate of CRM (where CRM is evaluated according to the definition of Quirke and CRM <1 mm is defined as positive)³; the number of lymph nodes detected and the pathological TNM staging (according to the eighth edition TNM staging).⁴ Bacterial culture results of the fluid in the surgical area and postoperative complications, including anastomotic leakage, anastomotic bleeding, and pelvic infection, were recorded.

Statistical analysis

SPSS software was used for statistical data processing. The measurement data were expressed by $\bar{x}$ ± s, and the t-test was used for intergroup comparisons, whereas the count data were expressed by the percentage, and the c²-test or Fisher exact probability test was used for intergroup comparisons. A P value <.05 indicated that the difference was statistically significant.

Results

Postoperative pathology

The postoperative pathological results showed that the positive rates of distal margin, proximal margin, and CRM were zero in both groups, and there were no significant intergroup differences in the total number of lymph nodes detected and pathological TNM stage (all P > .05) (Table 2).

Table 2.

Comparison of Pathological Data Between the Two Groups

Pathological data	Lap-taTME	Lap-TME	Statistics	P
Distal margin, n (%)	0	0
Proximal margin, n (%)	0	0
CRM, n (%)	0	0
Lymph nodes	14.59 ± 7.91	14.42 ± 2.92	t = 0.15	.880
pTNM stage, n (%)			c² = 8.67	.070
Stage 0	2 (3.6)	0
Stage I	23 (41.0)	10 (20)
Stage II	14 (25)	20 (40)
Stage III	15 (26.8)	19 (38)
Stage IV	2 (3.6)	1 (2)

CRM, circumferential resection margin; Lap-taTME, laparoscopic transanal total mesorectal excision; Lap-TME, laparoscopic total mesorectal excision.

Bacterial culture results

The positive rates of all bacterial cultures in the Lap-TME group and culture No. 1 in the Lap-taTME group were zero. There were 6 cases (10.7%) with positive culture No. 2 and 7 cases (12.5%) with positive culture No. 3 in the Lap-taTME group. Postoperative pelvic infection occurred in 4 (7.1% of all cases) of the 11 cumulative positive cases (19.6% of all cases) with positive culture in the Lap-taTME group, accounting for 36.4% of the cases with positive culture (4/11). The number of patients with positive culture No. 3 in the Lap-taTME group (7, 12.5%) was significantly higher than that in the Lap-TME group (0) (P < .05), and the number of cumulative positive culture cases in the Lap-taTME group (11, 19.6%) was significantly higher than that in the Lap-TME group (0) (P < .05) (Table 3).

Table 3.

Comparison of Culture Results Between the Two Groups

Bacterial culture, n (%)	Lap-taTME	Lap-TME	Statistics	P
Culture No. 1	0	0
Culture No. 2	6 (10.7)	NA
Culture No. 3	7 (12.5)	0	c² = 4.82	.028
Cumulative positive cases	11 (19.6)	0	c² = 10.96	.001

Lap-taTME, laparoscopic transanal total mesorectal excision; Lap-TME, laparoscopic total mesorectal excision.

Postoperative complications

No anastomotic bleeding occurred in any of the groups, and there were no significant intergroup differences in anastomotic leakage and pelvic infection (all P > .05) (Table 4).

Table 4.

Comparison of Postoperative Complications Between the Two Groups

Postoperative complications, n (%)	Lap-taTME	Lap-TME	Statistics	P
Anastomotic bleeding	0	0
Pelvic infection	4 (7.1)	0	c² = 2.01	.157
Anastomotic leakage	7 (12.5)	4 (8)	c² = 0.58	.448

Lap-taTME, laparoscopic transanal total mesorectal excision; Lap-TME, laparoscopic total mesorectal excision.

Discussion

Compared with traditional Lap-TME, taTME operation has advantages in male patients with obesity, large tumors, and low rectal cancer. Specifically, taTME reduces the damage to the prostate and pelvic nerves, decreases the CRM positive rate, and can achieve a better distal margin, thereby improving quality of life and prognosis.^5–9 An international multicenter randomized controlled trial, COLOR III,¹⁰ on laparoscopic TME and taTME procedures is ongoing, and it aims to provide evidence for clinical practice. The postoperative pathological reports showed that the positive rates of distal margin, proximal margin, and CRM were zero in both groups, and there were no significant intergroup differences in the total number of lymph nodes detected and pathological TNM stage. These findings suggest that Lap-taTME has been equivalent to Lap-TME in radical resection of the tumor, but the long-term prognosis needs to be confirmed by further studies.

Furthermore, taTME also faces postoperative anastomotic-related complications, such as leakage and bleeding, as well as infectious complications brought by breaking the principle of sterility, such as pelvic infection and abscess. Furthermore, whether the reverse operation will result in more intraoperative complications must also be considered. A retrospective study from 66 centers in 23 countries around the world showed that among 720 taTME cases, the incidence of anastomotic leakage was 6.7% and that of abdominal or pelvic abscess was 2.4%.¹¹ Subsequently, Penna et al.¹² continued to report the results of an international taTME study with a larger sample size and found the overall anastomotic failure rate of 15.7%, including the anastomotic leakage rate of 9.8% and the pelvic abscess rate of 4.7%.

In this study, there were 7 cases (12.5%) of anastomotic leakage in the Lap-taTME group, and 4 cases (7.1%) of pelvic infection or localized abscess, which was slightly higher than what was reported in Penna et al.'s study. These differences could be caused by the following reasons: first, the patients who had undergone taTME surgery combined with preoperative pulmonary infection and urinary tract infection were excluded; second, patients with class A anastomotic leakage that was difficult to locate were included; third, the results of bacterial cultures were the primary focus, and pelvic infection was defined as a positive bacterial culture of postoperative pelvic drainage fluid, including some infected cases without clinical symptoms and cases in which bacterial colonization of the drainage tube was considered. Finally, this was a single-center study with a small number of cases. Thus, it is necessary to reduce the incidence of anastomotic leakage after Lap-taTME surgery through various methods such as preventive stoma, ensuring good blood supply and tension-free anastomosis.

Considering that taTME surgery violates the principle of sterility and that there have been few research reports on the bacterial culture of fluid in the surgical area, this study focused on the bacterial culture results and postoperative pelvic infection. The results showed that the initial pelvic fluid culture (culture No. 1) and the pelvic cavity fluid culture (culture No. 3) after anastomosis were negative in all of the patients in the Lap-TME group. The positive rate of the rectal cavity fluid culture (culture No. 2) after purse-string suture in the Lap-taTME group was 10.7%, indicating that over 1–10th of taTME surgeries were performed in a sterile environment from the transanal part to confluence with the abdominal part.

The main reasons for this result could be the following: some patients had inadequate bowel preparation before surgery, and some watery stool remained in the intestinal cavity; bacteria propagated through normal intestinal secretions during the interval between the completion of bowel preparation and the surgery; there was still a possibility of an outflow of upper intestinal fluid during the operation after the purse-suturing blocked the intestinal cavity; and the rectal cavity could not be sterilized completely during the operation.

The positive rate of the pelvic cavity fluid culture (culture No. 3) after anastomosis in the Lap-taTME group was 12.5%, which was significantly higher than that in the Lap-TME group, and similar was found for the number of cumulative positive cases. This suggests that Lap-taTME was more likely to cause intraoperative contamination; however, the number of postoperative pelvic infections was not significantly different between the two groups, indicating that Lap-taTME did not significantly increase the risk of postoperative pelvic infection. The reasons may be as follows: the cases with only a positive rate of culture No. 2 in the Lap-taTME group had a lower possibility to develop postoperative pelvic infection; positive culture only indicates the presence of bacteria, and antibiotics and drainage can prevent the development of a pelvic infection.

Professor Velthuis found that among the three bacterial cultures taken at standardized locations from the pelvic area after the completion of the taTME procedure, gastrointestinal flora was found in 9 cases (39%),¹³ and 4 of these patients (44%) developed presacral abscesses. In this study, the total number of cases with positive culture was 11 in the Lap-taTME group, and 4 cases (36.4%) developed postoperative pelvic infection. Therefore, the aseptic principle of taTME procedure needs to be further improved keeping in mind the following suggestions based on clinical operation and treatment experience.

First, for patients scheduled to undergo taTME surgery, bowel preparation should be strictly performed before operation to minimize the residual intestinal feces; second, the surgical procedures should be strictly aseptic, especially the transanal part, which should be sterilized with diluted iodophor for many times, and sufficient amount of sterilized physiological saline should be used to rinse the pelvic cavity after anastomosis; third, a threaded siphon negative-pressure drainage tube should be placed in the pelvic cavity after the operation and a semirecumbent position is required after the patient awakens, ensuring that the residual pelvic fluid is drained as early as possible, and postoperative support treatment should be strengthened to close the pelvic adhesions; lastly, patients undergoing taTME surgery should routinely receive antibiotics until the third day after surgery according to the infection index, and the result of postoperative pelvic fluid culture should be used to decide whether to continue the use of antibiotics or not on the fourth day.

Conclusions

In summary, this study suggests that Lap-taTME is more prone to intraoperative contamination than Lap-TME, but does not significantly increase the risk of postoperative pelvic infection. Positive fluid bacterial culture during Lap-taTME indicates an increased risk of pelvic infection after operation, so perioperative management should be strengthened. However, this was a single-center retrospective study with a small sample, so further rigorously designed and multicenter randomized controlled trials are needed to provide higher-level evidence.

Footnotes

Authors' Contributions

L.D.: review and editing (equal). Y.X.: Conceptualization (lead); writing—original draft (lead); formal analysis (lead); writing—review and editing (equal). J.L.: Software (lead); writing—review and editing (equal). H.Z.: Conceptualization (supporting); Writing—original draft (supporting); Writing—review and editing (equal).

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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