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Risk factors for organ-space surgical site infections after minimally invasive rectal cancer surgery: a retrospective cohort study

Abstract

Background

The study focused on identifying risk factors for organ-space surgical site infections (SSIs) in patients undergoing minimally invasive rectal cancer surgery and examining the impact of these infections on oncological outcomes.

Methods

This retrospective study included 1304 patients who underwent either robotic surgery or laparoscopic surgery for rectal cancer. Patients were divided into two groups: those with organ-space SSIs (9.7%, n = 126) and those without organ-space SSIs (n = 1178). Univariate and multivariable analyses were conducted to identify predictors or independent risk factors for organ-space SSI. The post-operative pathological data, short-term outcomes, and oncological prognosis were compared between patients with and without organ-space SSIs.

Results

The multivariable analysis revealed that males (OR 1.875; 95% CI 1.213–2.896, P = 0.005), conversion to laparotomy (OR 8.428; 95% CI 2.892–24.557, P < 0.001), diabetes (OR 2.013; 95% CI 1.210–3.348, P = 0.007), colonic J pouch (CJP) and transverse coloplasty (TCP) (OR 2.517; 95% CI 1.114–5.687, P = 0.026), and hand-sewn anastomosis (OR 5.194; 95% CI 2.115–12.753, P < 0.001) were identified as independent risk factors for organ-space SSIs. Patients with more risk factors had a higher risk of developing organ-space SSIs (P < 0.001). The risk of organ-space SSI increased with the number of risk factors present: 4.1% in patients without any risk factors, 10.0% in patients with 1 risk factor (RR = 2.571, 95% CI 1.495–4.423), 17.8% in patients with 2 risk factors (RR = 5.022, 95% CI 2.636–9.567), and 62.5% in patients with 3 or 4 risk factors (RR = 38.627, 95% CI 12.571-118.689). There were no significant differences in 3-year OS (94.4% vs. 94.3%, P = 0.712) and DFS (85.6% vs. 86.7%, P = 0.636) between the organ-space SSI and non organ-space SSI groups. However, the organ-space SSI group had a higher incidence of bone metastases compared to the non organ-space SSI group (2.4% vs. 0.4%, P = 0.036). Recurrence rates at other sites, including local recurrence, liver metastases, lung metastases, and peritoneal metastases, did not differ significantly between the two groups.

Conclusion

This study found that 5 risk factors (male gender, conversion to laparotomy, diabetes, CJP and TCP, and hand-sewn anastomosis) can be used to categorize the likelihood of postoperative organ-space SSI.

Peer Review reports

Introduction

Surgical site infection (SSI) is a prevalent nosocomial infection that significantly impacts surgical patients [1]. It is categorized into superficial/deep incisional, and organ-space SSI. Among various surgical procedures, colorectal surgery patients have a higher susceptibility to SSI [2], with reported rates ranging from 3–45% [3]. The presence of SSI is associated with unfavorable clinical outcomes, including prolonged hospital stays and increased healthcare costs [4]. While some studies have reported a negative impact of SSI on long-term survival [5], conflicting results have been observed following colorectal surgery [6]. For instance, a retrospective study found worse disease-free survival (DFS) in patients with SSI. However, SSI was not identified as an independent predictor of survival in multivariable analysis [7]. Another retrospective study demonstrated no significant differences in recurrence rate and overall survival (OS) between SSI and non-infected patients. However, when stratified analysis was performed, patients with organ-space SSI exhibited a higher recurrence rate and decreased 5-year overall and DFS [6].

Several risk factors for SSI following colorectal cancer surgery have been widely recognized, with most studies primarily focusing on overall SSI or incisional SSI. For instance, a recent meta-analysis identified obesity, male sex, diabetes mellitus, ASA score ≥ 3, stoma creation, intraoperative complications, perioperative blood transfusion, and operation time ≥ 180 min as risk factors for overall SSI [3]. In addition to obesity and stoma creation, preoperative steroids or radiation were also identified as factors associated with incisional SSI [8, 9]. However, it is important to note that the risk factors for incisional SSI and organ-space SSIs may differ. For example, drainage of the surgical area and stoma creation may increase the risk of incisional SSI, whereas these measures serve as preventive or therapeutic interventions for organ-space SSI. However, there remains a notable dearth of research dedicated to the identification of predictive factors for organ-space SSI.

Organ-space SSIs are severe complications that can occur following colorectal resection surgeries. Improving the understanding of factors that predict organ-space SSIs has the potential to aid in early detection and improve treatment outcomes. Additionally, identifying risk factors for organ-space SSIs can enable valid comparisons of organ-space SSI rates among surgeons or hospitals. Thus, our study aimed to identify risk factors or predictors for organ-space SSIs in patients undergoing minimally invasive rectal cancer surgery, performed by a cohort of highly skilled surgeons. Furthermore, we sought to investigate the impact of organ-space SSIs on oncological prognosis.

Methods

Patients

Between January 2017 and December 2021, a total of 1576 consecutive patients underwent either robotic or laparoscopic surgery for rectal cancer at the Department of Colorectal Surgery, Union Hospital, Fujian Medical University. Rectal cancer was defined as confirmed adenocarcinoma within 15 cm from the anal verge, as determined by pathology. The surgical procedures were performed by a team of highly skilled surgeons, each with an accumulated experience of over 350 cases of laparoscopic or robotic colorectal cancer surgery. Exclusion criteria included patients who underwent open surgery (n = 43), had stage IV disease (n = 112), underwent surgery for recurrent cancer (n = 22), had synchronous or metachronous colorectal cancer (n = 22), or had missing data on crucial baseline information such as pathological T or N stages or tumor distance to the anal verge (n = 58). Furthermore, patients with specific pathological types, such as rectal malignant melanoma (n = 2), rectal stromal tumor (n = 7), and rectal neuroendocrine tumor (n = 6), were also excluded from the analysis. Ethical approval for the present study was obtained from the Institutional Review Board of the Affiliated Union Hospital of Fujian Medical University.

Treatment and follow-up

Prior to surgery, all patients underwent preoperative staging evaluations, which included a digital rectal examination, colonoscopy, chest radiography, endorectal ultrasound examination (ERUS), abdominopelvic computed tomography (CT), and pelvic magnetic resonance imaging (MRI). Patients with clinical T3/4 and threatened mesorectal fascia (< 1 mm due to tumor or lymph nodes), regardless of N stage, received neoadjuvant chemoradiotherapy. Following preoperative radiotherapy, surgery was advised to be scheduled within 6–10 weeks.

A standardized protocol for preoperative bowel preparation was uniformly implemented in our department. This protocol encompassed the administration of oral laxatives for patients without endoscopic obstruction, as well as tap water rectal irrigation for those with such obstruction. The oral laxative regimen consisted of taking polyethylene glycol electrolyte powder orally until the water sample is excreted and the stool is clear. Additionally, patients were given oral antibiotics (metronidazole and gentamicin) starting one day before the operation. All patients received a single dose of second-generation cephalosporins intravenously 30 min before the incision, as well as during the first 3 h after the incision. Intravenous prophylactic antibiotics were then administered every 12 h after the operation and discontinued 48 h post-surgery.

All patients underwent the standard surgical resection procedure, which included total mesorectal excision (TME) for mid/low rectal cancers and partial mesorectal excision with a distal margin of at least 5 cm for high rectal cancers.

Reconstructive techniques and anastomosis: to carry out a transverse coloplasty (TCP), a 5 cm longitudinal incision was made 5 cm above the resection margin of the colon. Following this, a transverse suture was meticulously performed. In the case of a colonic J pouch (CJP), the proximal colon was folded and a linear stapler was employed to create a J-shaped pouch, with dimensions ranging from approximately 6 to 8 cm. Only after the creation of coloplasty and pouch, the anastomosis was then performed stapled or handsewn. Thus, the choice of stapled or handsewn anastomosis was independent of the creation of TCP and CJP. For instance, a double-stapled anastomosis was carried out. In cases where it was not possible to achieve an adequate distal margin using a linear stapler through an abdominal approach, a perineal dissection was performed, followed by a handsewn anastomosis. Prophylactic drainage near the anastomosis was uniformly implemented. According to the risk of leaks, surgeons may decide to place a transanal drainage tube, create a stoma, or do neither.

Patients with clinical stage II/III tumors who had neoadjuvant chemoradiation prior to surgery were advised to undergo adjuvant chemotherapy based on 5-fluorouracil. Postoperative surveillance included imaging studies, chest radiography, abdominopelvic MRI/CT, and annual colonoscopy. Initially, visits were scheduled every three months during the first two years, after which they transitioned to annual assessments.

Definition

An organ-space SSI is defined as intra-abdominal/pelvic abscess (an intraabdominal or pelvic collection of pus diagnosed by ultrasonography, computed tomography, or laparotomy) or anastomotic leakage. Anastomotic leakage was defined in accordance with the proposed definition by the International Study Group of Rectal Cancer (ISREC) as a defect in the intestinal wall at the anastomotic site—including suture and staple lines of neorectal reservoirs—that results in communication between the intra- and extraluminal compartments [10]. This abscess may or may not be accompanied by clinical evidence of anastomotic leakage. Complications were classified using the modified Clavien system [11]. For the diagnosis of diabetes, the criteria include the presence of classic symptoms such as polydipsia, polyuria, polyphagia, and weight loss, along with a random blood glucose level of ≥ 11.1 mmol/L (200 mg/dL), a fasting plasma glucose (FPG) level of ≥ 7.0 mmol/L (126 mg/dL), or a 2-hour plasma glucose (2-h PG) level of ≥ 11.1 mmol/L (200 mg/dL) after a glucose load. It is important to note that individuals without diabetes symptoms should be re-tested on a separate day to confirm the diagnosis [12]. A positive pathological circumferential resection margin (CRM) is determined when there is a cancer-free margin of 1 mm or less. Conversion to open laparotomy involves using a laparotomy wound at any point during the mesorectal dissection. DFS is the period of time from surgery until the first occurrence of recurrence, metastasis, or death from any cause. OS is the duration from surgery until death or the last confirmed date of being alive. Local recurrence is characterized by tumor growth within the pelvic cavity, regardless of its direction or relationship with the anastomosis. Distant recurrences are defined as tumor recurrence outside of the pelvic cavity, including metastases to the liver, lung, bone, or peritoneum.

Statistical analysis

Graphpad Prism 7 and STATA 15.0 were utilized for all statistical analyses. The patients were categorized into two groups: organ-space SSI and non organ-space SSI group. For univariate analysis, discrete variables between the groups were compared using Fisher’s exact test and chi-square test, while continuous outcomes were compared using parametric tests (Student’s t-test) and nonparametric tests (Mann-Whitney U test, Kruskal-Wallis test), as appropriate. The Kaplan-Meier method was employed to summarize DFS and OS, and a log-rank test was conducted to compare them. When determining the p-value threshold to include variables in a multivariable model, a higher threshold of 0.25 is frequently adopted in exploratory analyses to consider a wider range of variables, whereas a lower threshold of 0.1 is typically chosen for confirmatory studies or when a stricter control of Type I errors is desired. Furthermore, in large-sample studies, a more stringent p-value of 0.1 may be preferred to prevent the overestimation of minor effects, whereas small-sample studies might necessitate a more lenient p-value, such as 0.25, to avoid the erroneous exclusion of potentially significant variables due to sample size limitations [13, 14]. In the current study, which included a large sample of 1,304 patients and was designed with a confirmatory approach, variables with a p-value less than 0.1 in univariate analysis were selected for inclusion in a logistic regression model to identify independent risk factors for organ-space SSI. A significance level of P < 0.05 was considered statistically significant.

Results

Patient characteristics

During the study period, a group of 1304 patients received treatment for rectal cancer, with 295 undergoing robotic surgery and 1009 undergoing laparoscopic surgery. The median age of the patients was 60.0 years, and 61.7% of them were men. The median distance of the tumor from the anal verge was 7.0 cm. The majority of patients (1237 out of 1304, 94.9%) underwent sphincter preservation surgery, with 1134 patients having anterior resection and 103 patients having intersphincteric resection. The remaining 67 patients underwent abdominoperineal resection. Only 1.2% of patients (16 out of 1304) required conversion to laparotomy. Of the 57 patients who underwent CJP and TCP procedures, 25 (43.8%) had hand-sewn anastomosis following the creation of coloplasty and pouch, and the remaining 32 (56.1%) had double-stapled anastomosis following the same procedures.

The overall incidence of organ-space SSI was 9.7% (126 out of 1304), while the rate of anastomotic leakage was 6.8% (84 out of 1237). In the analysis of anastomotic leakage rates, we excluded 67 individuals who had undergone abdominoperineal resection from our calculations. Among the patients with organ-space SSIs, 42 individuals, representing 33% of this cohort, experienced postoperative localized peritonitis. This condition was further complicated by intra-abdominal abscesses in 31 patients (25% of the organ-space SSIs cohort) and pelvic abscesses in 11 patients (9% of the organ-space SSIs cohort). Microbiological examination of the drainage fluid from these patients identified pathogenic bacteria, thereby confirming the diagnosis of intra-abdominal and pelvic SSIs. Importantly, none of these cases exhibited clinical evidence of anastomotic leakage or suture leakage. It is hypothesized that these complications may be linked to fecal bacterial contamination that occurred intraoperatively.

Of the 84 patients experiencing anastomotic leakage, 63 (75.0%) required only antibiotic therapy and total or partial parenteral nutrition, along with delayed removal of intraoperatively placed pelvic drains (Clavien-Dindo grade II). Three (3.6%) patients necessitated additional percutaneous drainage under ultrasound or CT guidance (Clavien-Dindo grade IIIa). Eleven (13.1%) patients underwent reoperation involving the creation of a defunctioning stoma under general anesthesia (Clavien-Dindo grade IIIb), while seven (8.3%) patients required intensive care unit (ICU) management (Clavien-Dindo grade IVa). There were no perioperative mortality cases.

Among the 42 patients experiencing intra-abdominal and pelvic SSIs without clinical evidence of anastomotic leakage, 34 (81.0%) were treated with only antibiotic therapy and total or partial parenteral nutrition, along with delayed removal of intraoperatively placed pelvic drains (Clavien-Dindo grade II). Three (7.1%) patients necessitated additional percutaneous drainage under ultrasound or CT guidance (Clavien-Dindo grade IIIa). One (2.4%) patient required reoperation due to a concomitant acute gastric mucosal lesion that led to gastric bleeding (Clavien-Dindo grade IIIb), while four (9.5%) patients required ICU management (Clavien-Dindo grade IVa). There were no perioperative mortality cases.

Risk stratification for organ-space SSI

The clinical characteristics of patients with and without organ-space SSIs were subjected to univariate analysis (Table 1). It was found that males had a higher rate of organ-space SSI compared to females (11.4% vs. 6.8%, P = 0.007). Patients with diabetes also had a higher rate of organ-space SSI compared to patients without diabetes (15.2% vs. 8.9%, P = 0.020). There was a trend towards longer operative times in the organ-space SSIs group compared to the non organ-space SSIs group, however, this difference was not statistically significant (220 min vs. 191 min, P = 0.378). Robotic surgery showed a non-significant increase in the rate of organ-space SSI compared to laparoscopic surgery (12.5% vs. 8.8%, P = 0.072). Notably, Robotic surgery had significantly longer operative times than laparoscopic surgery [210.00 (185.50, 240.00) minutes vs. 190.00 (160.00, 226.50) minutes, P = 0.032]. Among the different surgical procedures, intersphincteric resection had the highest rate of organ-space SSI (23.3%), followed by anterior resection (8.6%) and abdominoperineal resection (7.5%, P < 0.001). However, operative times did not align with the risk of organ-space SSI. Abdominoperineal resection exhibited the most extended operative times, with intersphincteric resection coming in second, and anterior resection being the shortest among them [280 (235, 325) minutes vs. 245 (214, 267) minutes vs. 190 (160, 220) minutes, P < 0.001]. Conversion to laparotomy was associated with a higher risk of organ-space SSI (37.5% vs. 9.3%, P < 0.001). In terms of reconstructive and anastomosis techniques, CJP and TCP had a higher risk of organ-space SSI compared to straight colorectal anastomosis (SCA, 31.6% vs. 8.7%, P < 0.001), while hand-sewn anastomosis had a higher rate of organ-space SSI compared to stapled anastomosis (43.2% vs. 8.8%, P < 0.001). Notably, CJP and TCP had significantly longer operative times than straight colorectal anastomosis [240 (220, 260) minutes vs. 190 (160, 220) minutes, P < 0.001], and hand-sewn anastomosis also took longer than stapled anastomosis [252 (241, 263) minutes vs. 190 (160, 220) minutes, P = 0.003]. After adjusting for the time of the procedure, CJP and TCP continued to demonstrate an increased risk for organ-space SSIs compared to SCA (P = 0.017), and hand-sewn anastomosis maintained a higher risk for organ-space SSIs compared to stapled anastomosis (P = 0.021).

Table 1 Comparison of clinical characteristics between patients with and without organ-space SSI

In order to determine the predictors or independent risk factors for organ-space SSI, a multivariable analysis was conducted using variables that had a P-value of less than 0.1 in the univariate analysis (Table 2). Among these factors, it was found that males (odds ratio [OR] 1.875; 95% confidence interval [CI] 1.213–2.896, P = 0.005), conversion to laparotomy (OR 8.428; 95% CI 2.892–24.557, P < 0.001), diabetes (OR 2.013; 95% CI 1.210–3.348, P = 0.007), CJP and TCP (OR 2.517; 95% CI 1.114–5.687, P = 0.026), and hand-sewn anastomosis (OR 5.194; 95% CI 2.115–12.753, P < 0.001) were identified as independent risk factors for the development of organ-space SSIs.

Table 2 The multivariable analysis of risk factors for organ-space SSI

Based on the multivariable analysis, 5 risk factors (male gender, conversion to laparotomy, diabetes, CJP and TCP, and hand-sewn anastomosis) can be used to categorize the likelihood of postoperative organ-space SSI. The presence of more risk factors was linked to a higher risk of organ-space SSI (P < 0.001). The risk of organ-space SSI was 4.1% in patients without any risk factors, 10.0% in patients with 1 risk factor (RR = 2.571, compared to patients without risk factors, 95% CI 1.495–4.423), 17.8% in patients with 2 risk factors (RR = 5.022, 95% CI 2.636–9.567), and 62.5% in patients with 3 or 4 risk factors (RR = 38.627, 95% CI 12.571-118.689). The relationship between the number of risk factors and the risk of organ-space SSI is detailed in Table 3.

Table 3 Association of the number of risk factors with the risk of organ-space SSI

Impact of organ-space SSIs on short-term outcomes

The post-operative pathological data of patients with and without organ-space SSIs were analyzed, revealing no significant differences in various factors such as (y)pT stage, (y)pN stage, histopathology, differentiation, distal margin involvement, pathologic circumferential margin involvement, neural invasion, lymphovascular invasion, and number of lymph nodes retrieved between the two groups (all p > 0.05, Table S1). Furthermore, the short-term outcomes of patients with and without organ-space SSIs were compared. Patients with organ-space SSIs exhibited a higher incidence of anastomotic bleeding, postoperative pneumonia, and early postoperative small bowel obstruction compared to those without organ-space SSIs (all p < 0.05). Additionally, the duration of hospitalization was significantly longer by 13 days in patients with organ-space SSIs compared to those without (P < 0.001, Table 4).

Table 4 Comparison of short-term outcomes in patients with and without organ-space SSI

Impact of organ-space SSIs on oncological prognosis

The analysis included 1265 patients for whom oncologic outcomes and recurrence data were available. The median follow-up period was 31 months, with a range of 16 to 45 months. The 3-year DFS rate was 85.6% in the organ-space SSI group and 86.7% in the non organ-space SSI group, with no significant difference observed (P = 0.636) (Fig. 1A). When stratified by TNM stage, the 3-year DFS rates remained comparable between the organ-space SSI group and the non organ-space SSI group, with no significant differences noted for stages 0-I, II, and III, respectively (Fig. 1C, E, G). Similarly, in the organ-space SSI group, the 3-year OS rate was 94.4%, while in the non organ-space SSI group it was 94.3%, again showing no significant difference (P = 0.712) (Fig. 1B). When stratified by TNM stage, the 3-year OS rates were comparable between the organ-space SSI group and the non organ-space SSI group, with no significant differences for stages 0-I, II, and III, respectively (Fig. 1D, F, H).

Fig. 1
figure 1

Comparative analysis of Disease-Free Survival (DFS) and Overall Survival (OS) in patients with and without organ-space surgical site infections. A: DFS in the overall cohort. B: OS in the overall cohort. C: DFS for patients at stage 0-I. D: OS for patients at stage 0-I. E: DFS for patients at stage II. F: OS for patients at stage II. G: DFS for patients at stage III. H: OS for patients at stage III

The overall rates of distant metastases were similar between the organ-space SSI and non organ-space SSI groups (6.4% vs. 6.8%, P = 0.88). Upon stratification by pTNM stage, the overall rates of distant metastases remained comparable between the organ-space SSI group and the non organ-space SSI group, with no significant differences observed across stages 0-I, II, and III. Regarding specific metastatic sites, the organ-space SSI group showed a higher incidence of bone metastases compared to the non organ-space SSI group (2.4% vs. 0.4%, P = 0.036). There were no statistically signific ant differences in recurrence rates at other sites, including local recurrence, liver metastases, lung metastases, and peritoneal metastases, between the two groups as shown in Table 5.

Table 5 Comparison of recurrence data in patients with and without organ-space SSI

Discussion

In this study, the overall incidence of organ-space SSI was found to be 9.7%, falling within the reported range of 1.7–22.3% for patients undergoing colorectal cancer surgery [5, 15, 16, 17, 18]. Several inherent factors in this study, including the anatomical location of the cancer, preoperative bowel preparation, and surgical approach, may impact the occurrence of organ-space SSI. Rectal resections for cancer were shown to be independently associated with a higher likelihood of organ-space SSI compared to surgery for cancer in other anatomical locations of the colon [19]. In terms of preoperative bowel preparation, both mechanical and chemical bowel preparations were utilized in the present study. Although the effectiveness of these preparations in minimally invasive surgery is still debated [20], a Bayesian network meta-analysis involving 46 studies and 12,690 patients found that oral antibiotics in combination with mechanical bowel preparation can reduce the risk of SSI following elective colorectal surgery. A prospective study involving 1011 patients who underwent elective colorectal resection at a university teaching hospital examined the impact of surgical approach on SSI. The study found that laparoscopic surgery was associated with a more than 50% reduction in the rate of SSI compared to open surgery, highlighting its potential to significantly lower the risk of SSI [18]. Furthermore, research utilizing the American College of Surgeons-National Surgical Quality Improvement Program database (ACS-NSQIP) demonstrated that a minimally invasive approach significantly decreased the risk of SSI in obese patients undergoing proctectomy, with rates dropping from 22.3 to 13.3% [21]. Therefore, our focus was specifically on patients undergoing minimally invasive rectal cancer surgery. This choice was also influenced by the widespread adoption of minimally invasive techniques at our center. Over the study period from January 2017 to December 2021, only a minority of rectal cancer surgeries, specifically 54 cases (less than 5%), were conducted using traditional open surgical techniques (data not shown).

Identifying risk factors for organ-space SSIs is essential for accurately comparing SSI rates among surgeons or hospitals. Additionally, understanding predictors for organ-space SSIs can facilitate early detection and enhance treatment outcomes. It is important to note that the risk factors for incisional SSIs and organ-space SSIs may differ. While numerous studies have focused on identifying risk factors for overall SSIs or incisional SSIs, there is limited research on rectal cancer surgery specifically examining risk factors for organ-space SSIs. Through the multivariable logistic regression model, we discovered that five high-risk factors (male gender, conversion to laparotomy, diabetes, CJP and TCP, and hand-sewn anastomosis) were significantly linked to a higher risk of organ-space SSI. It is commonly believed that longer operating times may contribute to a higher risk of organ-space SSIs, as a Multicenter surveillance study has identified operating time as an independent risk factor for SSIs following radical resection of colon or rectal carcinoma [22]. It is noteworthy that our analysis revealed only a non-significant trend towards longer operative times in the organ-space SSIs group compared to the non organ-space SSIs group (220 min vs. 191 min, P = 0.378). In addition, Robotic surgery had a non-significantly higher organ-space SSI rate (12.5% vs. 8.8%, P = 0.072) and significantly longer operative times compared to laparoscopic surgery [210 (185.5, 240) minutes vs. 190 (160, 226.5) minutes, P = 0.032]. In an early single-center prospective study conducted by Tang et al. [1], diabetes and blood transfusion were identified as risk factors for organ-space SSI following elective resection of the colon and rectum. Our analysis similarly found diabetes to be an independent risk factor for organ-space SSI. Interestingly, the use of prophylactic drainage, which was common in our study, was associated with an increased risk of leakage in Tang et al.‘s study, possibly due to the foreign body effect of the drain [1]. A multicenter observational study revealed that organ-space SSI was linked to low anterior resection and Hartmann’s procedure [23]. In our study, intersphincteric resection had the highest rate of organ-space SSI at 23.3%, followed by anterior resection at 8.6% and abdominoperineal resection at 7.5% (P < 0.001). This may have been attributed to more difficult and prolonged dissection associated with these surgeries. Intersphincteric resection is known for its technical demands, particularly in the confined operating space and the need to preserve the anal sphincter for very low tumors that may involve the anal canal mucosa and/or internal sphincter. Interestingly, abdominoperineal resection, rather than intersphincteric resection, had the longest operative times, which did not align exactly with the organ-space SSI risk in our study. In addition, our current study identified male gender as an independent risk factor for organ-space SSI, consistent with previous research [24].

Previous research on reconstructive techniques predominantly concentrated on functional results [25]. In terms of surgical outcomes, prior research primarily examined rates of leakage, with organ-space SSIs receiving less emphasis [26]. The traditional belief was that CJP and TCP resulted in better bowel function outcomes compared to SCA, and there was no clear difference in terms of leak rates [26]. In our institution, male patients with a narrow pelvis and fatty mesentery might have undergone TCP or SCA instead of CJP if technical challenges arose. This may intruduce potential confounding in selection bias. Consequently, this bias may impact the risk assessment of organ-space SSI. A retrospective analysis found that CJP patients with handsewn anastomosis had a high leak rate of 44% [27]. However, a recent meta-analysis showed that TCP was associated with higher rates of leaks and strictures [28]. In terms of anastomosis techniques, studies showed that the rate of anastomotic leakage and stricture formation was significantly lower with stapled coloanal anastomosis during laparoscopic intersphincteric resection compared to hand-sewn coloanal anastomosis [29]. A small prospective study found similar rates of anastomotic leakage, post-operative ileus, and wound infection between the stapled and sutured groups [30]. However, neither study evaluated the incidence of organ-space SSIs. In our study, we found that comparing CJP and TCP to SCA, as well as hand-sewn anastomosis to stapled anastomosis, was linked to a greater likelihood of organ-space SSIs. Further analysis revealed that CJP and TCP had median operative times that were significantly 50 min longer than those for straight colorectal anastomosis, and hand-sewn anastomosis also took significantly longer than stapled anastomosis. This may partly explain the higher risk associated with these procedures. Additionally, the increased risk could be attributed to heightened exposure to intestinal bacteria and the more complex and difficult nature of the procedures.

According to risk stratification, patients with one risk factor were over 2.5 times more likely to develop organ-space SSI compared to those without any risk factors. Patients with two risk factors had over 4 times the likelihood, while those with three to four risk factors had a staggering 15 times higher risk of developing organ-space SSI. This stratification offers a straightforward way to pinpoint high-risk patients for postoperative organ-space SSI. By utilizing this approach, patients at significantly higher risk can receive more frequent monitoring and prompt intervention, including the use of ertapenem for perioperative prophylaxis [31].

The impact of organ-space SSI on the oncological prognosis of rectal cancer remains a topic of debate. A retrospective analysis of 326 colorectal cancer resections revealed that both incisional and organ-space SSIs were independent predictors of poor 3-year DFS and OS [5]. However, a study with a larger sample size (n = 3675) found that overall SSI was not a significant predictor of survival in multivariable analysis [7]. Another study by Lorente-Herce et al. [6], which examined 138 colorectal cancer patients, reported no significant differences in recurrence rate and OS between patients with SSIs and those without. However, a stratified analysis showed that patients with intra-abdominal abscesses or organ-space infections had a higher recurrence rate and decreased 5-year DFS and OS. One possible explanation for the poorer prognosis in patients with organ-space SSIs is that organ-space SSI may delay the initiation of adjuvant chemotherapy [32]. However, another study focusing on stage I colorectal cancer, where adjuvant chemotherapy was not administered, found that organ-space SSIs significantly increased postoperative recurrence rates [17]. This suggests that the presence of focal and systemic inflammation caused by organ-space SSIs may contribute to recurrence. Interestingly, in our study, rectal cancer patients with and without organ-space SSIs had similar 3-year OS and DFS rates, but the organ-space SSI group had a higher incidence of bone metastases compared to the non-organ-space SSI group (2.4% vs. 0.4%, P = 0.036). It is noteworthy that the observed association between bone metastases and organ-space SSIs may be a spurious correlation. This limitation arose from the fact that our analysis was not adjusted for the various metastatic sites, a challenge inherent in this study due to the limited number of patients with metastases in each specific site (with all cases numbering fewer than 10) within the organ-space SSI cohort. Bones are infrequently implicated as metastatic sites in CRC patients. Key risk factors for bone metastases include rectal origin of the primary tumor, lymph node invasion at the time of surgery, and the presence of lung metastases. The role of RAS mutation status as a risk factor remains uncertain [33]. It is hypothesized that organ-space SSIs might induce the release of inflammatory mediators, which could alter the bone microenvironment and augment the propensity for tumor colonization of the bone. Further research is needed to confirm the association between bone metastases and organ-space SSIs, as well as to elucidate the mechanisms underlying this potential association.

This study has limitations that should be acknowledged. Firstly, it is a retrospective analysis conducted at a single center, which may introduce patient selection bias. Furthermore, despite adherence to a standardized protocol for preoperative bowel preparation and the uniform implementation of prophylactic drainage near the anastomosis in our department during the study period, the selection between stapled and hand-sewn anastomosis could not completely eliminate selection bias. This is because surgeon experience might have varied in assessing whether an adequate distal margin could not be achieved with a stapled anastomosis, which could lead to a decision to switch to perineal dissection with a hand-sewn anastomosis. Furthermore, the timing of prophylactic drainage removal may influence the risk of organ-space SSIs. Therefore, further validation in a prospective, multicenter study with a larger sample size and standardized protocol is necessary. Secondly, we acknowledge that the retrospective design of our study limited the availability of data on other potential risk factors for organ-space SSIs, such as patients’ smoking histories [34]. We are committed to incorporating these variables in future prospective studies to enhance the comprehensiveness of our analysis. Thirdly, while patients with organ-space SSIs showed a higher occurrence of anastomotic bleeding, postoperative pneumonia, and early postoperative small bowel obstruction compared to those without organ-space SSIs, establishing a causal relationship between organ-space SSIs and other complications is challenging due to the retrospective nature of the study.

To summarize, this study demonstrated that male gender, conversion to laparotomy, diabetes, CJP and TCP, and hand-sewn anastomosis were identified as independent risk factors for organ-space SSI following minimally invasive rectal cancer surgery. This risk assessment tool offers a straightforward way to pinpoint the likelihood of postoperative organ-space SSI.

Data availability

The data used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

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Acknowledgements

None.

Funding

This study was financially supported by Joint Funds for the innovation of Science and Technology, Fujian province (2024Y9261) and Natural Science Foundation of Fujian Province (2023J01099, 2023J05144).

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Authors and Affiliations

Authors

Contributions

Xiaojie Wang contributed to the study design and implementation, analyzed the data and wrote the manuscript. Xiaojie Wang, and Yanwu Sun contributed to the data collection. Zhifang Zheng, Yongqin Tang, Shenghui Huang, Zhifen Chen, Heyuan Zhu, Jingyu Zou, Ying Huang, and Pan Chi revised the manuscript. All authors contributed to the critical interpretation of the results, reviewed the manuscript and approved the final version for publishing.

Corresponding authors

Correspondence to Ying Huang or Pan Chi.

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Declaration of Human Ethics and Consent to Participate. The present research, conducted in compliance with the Declaration of Helsinki, has been duly approved by the Institutional Review Board (IRB) of Union Hospital, Fujian Medical University. All data were collected and analyzed in an anonymous manner to ensure confidentiality. Given the retrospective nature of this study, the IRB has granted a waiver of informed consent, thereby eliminating the need for participants’ consent to participate in the research.

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Wang, X., Sun, Y., Zheng, Z. et al. Risk factors for organ-space surgical site infections after minimally invasive rectal cancer surgery: a retrospective cohort study. BMC Gastroenterol 25, 210 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12876-025-03617-4

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