The association between the increased performance of laparoscopic colon surgery and a reduced risk of surgical site infection

Our analysis of patients in the Kansai area of Japan who were enrolled in the NNIS system revealed three findings: (1) Both the occurrence of SSI and the risk factors for SSI changed significantly from year to year. (2) As laparoscopic surgery became increasingly common, the incidence of SSI decreased. (3) In the late study period (2012–2015), laparoscopic surgery was significantly associated with a lower incidence of organ/space SSI, indicating a decreased rate of anastomotic leakage.

Various risk factors for SSI have been reported previously, including sex [14], body mass index [8, 15, 16], ASA score [9, 14], wound classification [9, 14, 16], operating time [8, 14, 15, 17], prophylactic antibiotic use [8], creation or closure of an ostomy [9, 15, 16], use of preoperative nonabsorbable oral antibiotics [17], smoking [8], type of suture material used for fascial closure [18], type of skin closure [18], postoperative hyperglycemia [19], and total parenteral nutrition [20]. The common risk factors in our surveillance data were the ASA score, wound classification, operating time, and presence of a stoma. However, these risk factors changed to non-risk factors and back from year to year. This suggests that the true risk factors for SSI may adjust in accordance with the changing conditions surrounding surgery. The widespread use of laparoscopic surgery is one condition that changed markedly during the study period. Laparoscopic surgery is minimally invasive and usually performed with less blood loss than open surgery. However, the operating time is longer, and the cost of surgery is higher. The advantageous features of laparoscopic surgery may contribute to a decreased risk of SSI, as suggested in a previous study [5]. Furthermore, a study that used data from a large national database yielded results similar to ours, with laparoscopic colon surgery found to be associated with a significantly lower incidence of SSI than was open colon surgery [21]. When we investigated other surgeries covered by the surveillance data, such as gastric and appendiceal surgery, the results were also similar to those of our study. Laparoscopic surgery was significantly associated with a decreased risk of SSI in any year for gastric surgery, but the rate of laparoscopic gastric surgery did not reach 50% during our study period. A decreased incidence of SSI was significantly associated with the laparoscopic approach in appendiceal surgery after the rate of laparoscopic surgery had increased to > 50% (Supplementary Figs. 1, 2). Therefore, we believe that an important reason for the reduction in the rate of SSI over the study period was the increasingly routine use of laparoscopy to perform colon surgery.

To our knowledge, this is the first study to investigate the relationship between the rate at which laparoscopic surgery is performed and the risk of SSI in colon surgery. We found that a laparoscopic surgery rate of > 50% was associated with a significant decrease in the incidence of SSI in colon surgery. The major differences between laparoscopic and open procedures are the method of access, method of exposure, and extent of operative trauma. The contributing factors to the lower SSI rates associated with laparoscopic surgery are believed to be a smaller surgical incision, decreased tissue trauma, and elimination of mechanical retraction of the abdominal wall [16]. These findings suggest that laparoscopic surgery should decrease the risk of SSI at the incision site but will not affect organ/space SSI rates because organ/space SSI is mainly caused by anastomotic leakage [22].

Some laparoscopic instruments appear to prevent anastomotic leakage; however, these instruments are also used for open surgery. We therefore expected that a comparison of open and laparoscopic surgery within the same time period would reveal a similar rate of organ/space SSI as has been reported in most previously published studies on this topic [23, 24]. Instead, the incidence of organ/space SSI was significantly different between the two methods. Some previously published findings support our results: a large multicenter sample analysis of patients undergoing colon surgery revealed that laparoscopy is associated with a lower incidence of leakage than is open surgery (1.8% vs. 2.7%, respectively) [6]. Furthermore, Murray et al. [24] showed that laparoscopic surgery is a reduced-risk factor for anastomotic leakage after adjusting for the patient’s background (odds ratio 0.69; 95% CI 0.58–0.82). The authors suggested that the laparoscopic approach may improve access for difficult mobilizations, allowing for greater bowel length and reduced tension on the anastomosis. Laparoscopic surgery may also afford better anatomical visualization in complex cases; however, why anastomotic leakage is reduced with laparoscopic surgery remains largely unclear. The laparoscopic approach lends itself to minimally invasive tissue trauma and has been shown to reduce the systemic inflammatory response compared with conventional open surgery [25]. Rettig et al. [26] stated that perioperative inflammatory conditions affect postoperative complications, including anastomotic leakage. Laparoscopic surgery performed by well-trained surgeons can reduce the postoperative C-reactive protein concentration by decreasing surgical stress; it may also decrease organ/space SSI by reducing systemic cytokine concentrations. Further investigations are necessary to determine the mechanisms by which laparoscopic surgery leads to reduced rates of organ/space SSI. Nevertheless, based on the available evidence, we highly recommend that extensive training in laparoscopic surgery be implemented to reduce SSI rates, especially in patients at increased risk of SSI, such as those of advanced age.

Our study has several limitations. This was a multicenter retrospective observational study using our surveillance data. The surgeons involved in our surveillance basically selected a surgical approach according to the current guideline at that time. Our surveillance did not include several variables that might be associated with SSI development, such as the site of resection (right, transverse, left colon), type of anastomosis (manual, mechanic), and rate of conversion to open surgery. According to a previous analysis using the 2005–2008 American College of Surgeons National Surgical Quality Improvement Program database, superficial SSI was more likely to occur in patients who underwent left-sided colectomy than in those who underwent right-sided colectomy [27]. Information on the site of resection is important because it is correlated with the incidence of infection. Unfortunately, we did not collect this information; however, we do not believe that there was a significant change in the rates of right- and left-sided colectomy from 2002 to 2015. Therefore, we do not believe that the site of resection substantially affected the incidence of superficial SSI in this study. Mechanical anastomosis was performed in most cases in our hospitals; functional end-to-end anastomosis or the double stapling technique was performed as necessary. A few cases involving manual anastomosis were included in this study because the anastomosis type is dependent on the surgeon; however, numerous randomized controlled trials and three meta-analyses have demonstrated no significant difference in organ SSI between hand-sewn and stapled anastomosis [28‐30]. We therefore regarded the contamination of anastomosis types to be in an acceptable error range. Although we lack data on the exact number of conversions that occurred each year, the rate of conversion to open surgery is now less than 1% in our hospitals. Conversion cases were enrolled into the laparoscopic group in this study, but we do not believe that this substantially affected the conclusion. Further information must be collected to better evaluate the impact of laparoscopic surgery on SSI development.

The incidence rate of SSI from 2003 to 2015 was not decreased in patients who underwent laparoscopic surgery, possibly because the indications for laparoscopic colon resection have expanded to include advanced colon cancer and emergency operations. Advanced colon cancer requires radical lymph node resection and sometimes combined resection, and these procedures may be risk factors for SSI. Therefore, we considered that the expanded indications for laparoscopic surgery did not decrease the actual SSI incidence rate. We reanalyzed the odds ratio for the incidence of SSI using data that excluded combined resection and emergency operations. The resulting odds ratio was almost the same as that for the total data (Supplementary Table 3). In the latter period of the study, the indications for laparoscopic colon resection were being expanded; accordingly, open surgery was performed in more complicated cases, such as those requiring combined resection of more than two organs, organ reconstruction, or resection for local recurrence. Furthermore, the odds ratio of SSI was decreased even after the indications were expanded. Our society began to perform laparoscopic surgery for advanced colon cancer, combined resection, and emergency operations around 2010. The decrease in the odds ratio after 2011 indicates that familiarization with laparoscopic surgery reduced the risk of SSI, regardless of the indication for laparoscopic surgery.

In conclusion, we found that the widespread use of laparoscopic surgery to treat colon disease may confer protection against SSI. The results of this study should encourage surgeons to view laparoscopic surgery as an evidence-based approach to reducing the risk of SSI. Further advances in and familiarity with laparoscopic techniques will help improve patients’ clinical courses while reducing the risk of SSI. However, our study has some limitations, as the data were based on our SSI surveillance conducted according to the established guidelines at that time. Further investigations are necessary to determine the mechanisms by which laparoscopic surgery leads to reduced rates of organ/space SSI. We are now prospectively collecting SSI-related data, including the type of surgery.