This series of postoperative SSIs in colorectal surgery, to date, is the largest multi-center prospective study in China. Overall, we identified SSIs in 134(3.66%) cases among 3663 patients with colorectal surgery. Historically, the prevalence of SSI in CRS has showed a wide range in prevalence mostly due to differences in the definition and the follow-up period[13, 15–17]. Recent reports[6, 18–20], however, continued to range widely in prevalence (2.4%-21.6%) despite the fact that the current definition of SSI issued by American CDC was globally accepted. Our SSI rate in colorectal surgery ranges in the lower field compared to other studies. Several factors may explain the discrepancy in SSI rates between our work and other surveys. First, the SSI rate of CRS varied across different hospitals; small hospital size (༜250 beds) and community hospitals have been reported higher rates, while all member hospitals in our study are university-affiliated or tertiary-care hospitals which are generally thought to have more experience and high skills in colorectal operations. Also, the results from single-center and multicenter settings, benign and malignant neoplasms, and colon and rectal diseases may lead to the differences in CRS SSIs rates. Finally, our survey combines data from complex (deep incisional or organ-space) and superficial SSIs while some reports[19, 20] only reported complex SSI rates in CRS which, to some extent, explained the disparities.
The analysis revealed a statistically significant but modest decrease in the prevalence rate of CRS SSI over the 4-year study period. We hypothesized our surveillance program and improved SSI control practices were 2 of several factors that contributed to the decreased prevalence of SSI in CRS. It has been reported that SSI surveillance could help to reduce SSI[10, 13, 21]. Our surveillance program calculated the SSI rates according to stratification of NNIS index, determined procedure-specific risk factors, and periodical feedback of actual SSI rates to hospitals, which partly explained the reduction in SSI rates of CRS[13, 22]. Moreover, ‘Guidelines for prevention and control of surgical site infection (Trial)’ was issued by National Health Commission of the People’s Republic of China (NHCPC; formerly the Chinese Ministry of Health) in 2010[23], and thoroughly described the pre-, intra- and post-operative preventive measures, such as surgical hand preparation, implement perioperative glycemic control, maintain perioperative normothermia, administration antibiotic prophylaxis within 120 minutes and no hair removal or clipping if needed, most of them were still recommended with high- or moderate-quality evidence by the latest guidelines released by American CDC in 2017[24] and WHO in 2016[25]. These measures had positive effect on reducing SSI which had be described through some previous studies[26, 27], however, the impact that these infection control measures had upon SSI rates in CRS could not be quantified in our study because we were not accessible to the hospitals involved.
Many factors, including patient- and procedure-related variables, influence surgical wound healing and affect a patient’s risk of developing an SSI. NNIS risk index has been proved to be an useful tool to assess the risk of developing SSI and widely used to adjust the risk of SSI for the comparison among different institutions or surgeons[28–30]. In our survey, the risk of SSI after colorectal operations was found to increase as the NNIS risk index score increased like other studies[6, 19], and SSI rates stratified by NNIS index were similar to the corresponding U.S. NNIS rates[31]. Patient-dependent variables had little effect on the prevalence of SSI in our study. Age was reported to be a significant risk factor in few of the other operative procedures[32], but not in CRS[15, 16, 19, 33–35]. Interestingly, our present data indicated that patients older than 60 years showed a decreased risk tendency for SSI, even though the difference was not statistic significant. This result was mainly consistent with the data from NHSN in which age was not a risk factor in rectal surgery but showed an inverted relationship with risk of SSI in colon surgery[32]. We presumed that this inverse association could be in part explained by surgeons’ additional consideration about older patients. They might be selected on the basis of indications for operation, and surgeons might also tend to avoid invasive techniques in treating older individuals. ASA score has been confirmed as an independent risk factor of SSI in a few studies[6, 16, 35], but this association could not be detected in some other surveys[5, 18, 19, 36]. The present data indicated the ASA score more than 2 was a predictive factor in SSI in CRS by the univariate analysis, whereas, not confirmed in the multivariate analysis. The controversy was also found for BMI index and sex. Higher BMI index and male sex were expected to be associated with the increasing risk of SSI higher BMI index [15, 18, 37], whereas, did not be confirmed in this study as well as some other surveys[5, 34, 35]. More researches are needed to clarify the effect of patient-dependent factors on the risk of SSI after CRS.
Most of the operation-related variables were detected to be associated with higher risk of developing SSI after CRS in the univariate analysis in this study, and 2 variables were finally confirmed in the multivariate analysis. Our results indicated that contaminated or dirty wound class significantly increased the risk of developing SSI after CRS, with 3.38 times higher risk compared to clean or clean-contaminated wound class. The National Research Council (1964) laid the foundation for a system of surgical wound classification[38] and higher bacterial contamination load was recognized as a greater risk for developing SSI that has been confirmed by numerous reports[9, 16, 18]. Preoperative hospital stay more than 48 h was also an independent risk factor in this survey, in keeping with the results of previous studies[34, 39–41]. It is difficult to explain why longer preoperative hospital stay increased risk of CRS SSI. One possible explanation derived from the finding that sicker or more elderly patients who need more diagnostic tests before surgery, as reflected in the American Society of Anesthesiologists classification. Besides, longer preoperative hospital stay may also increase patients’ risks in developing SSIs by contacting with medical environment or personnel and colonization by microorganisms[34]. Some studies reported that emergent operation was associated with higher rate of SSI after CRS[6, 36], and longer surgery duration was an independent risk factor for development of SSI in CRS[16, 19, 36]. Nevertheless, neither of these factors were confirmed in our data, despite that increasing susceptibility of SSI was detected, whereas, not statistically significant. The impact of these 2 variables on developing SSI was remained questionable, because negative results were also found in some other reports[5, 34]. The association between SSI and the individual surgeon has been reported by some previous studies[10, 16, 42]. Our analysis showed surgeon with less experience in operation was a significant predictor in the univariate modeling analysis, although it did not remain so in the multiple regression model. Senior surgeons were generally thought to have more experience and high surgical technique in operation. A moderate quality of evidence showed that surgical procedures performed by high- or medium-volume surgeons had lower SSI rates compared to low volume ones in an unpublished systematic review conducted by WHO[43], however, there was controversial evidence when high- and medium-volume hospitals were compared, thus it remained unclear whether there was a linear relationship between procedure/surgeon volume and the SSI rate. Above all, more well-designed epidemiology study, including case-control study, cohort study and meta-analysis, or biological mechanism studies are needed to clarify the association of host- and surgery-dependent variables with SSI after CRS in the future.
Besides the host and operation factors, microorganism was also important in development of SSI. Physicians should be, particularly, cautious about the increases in high-virulence microorganisms, such as Staphylococcus aureus and Streptococcus pyogenes, and multidrug-resistant pathogens[44]. In our population, gram-negative microorganisms constituted more than 80% of the isolated strains, and Escherichia coli and Klebsiella pneumonia were the two most frequently isolated pathogens. Noticeably, high rates of multidrug-resistant were observed in Escherichia coli and Klebsiella pneumonia when compared with other series[36]. This discrepancy could be explained by the higher antibiotic pressure, use of broad-spectrum antibiotics, illness severity and prolonged treatment periods. Nevertheless, the results should be treated cautiously because of the relatively small number of isolated microorganism strains.
There were several limitations that should be acknowledged. First, we did not gather data from smaller hospitals in this study which may result in selection bias. However, the cases we studied were from 19 hospitals that were distributed nationwide. Besides, considerable patients in China preferred to perform colorectal surgeries in large healthcare settings such as university-affiliated or tertiary-care hospitals because of their better medical circumstances, more advanced armamentariums and higher qualified staffs. Thus, we believed that the results of this study in part reflected the situation in hospitals in China nationwide. Second, the retrospective analysis of prospectively collected data might lead to bias and the statistical correlations between the risk factors and SSI did not determine any “cause-and-effect” relationship between them. Third, certain risk factors that have been reported associated with SSI such as perioperative hypothermia, hyperglycaemia and blood transfusion were not collected. Last, nearly 37% of the patients who developed an SSI did not available for information of causative pathogens; besides, no anaerobic culture was done and lack of antibiotic policy may also have affected the SSI rate.
Despite of that, this study is to date the first time describing a prospective nationwide survey with a large number of patients undergoing colorectal surgery in China. Our survey provides an insight into the burden and microbiology of SSI after CRS in China. Moreover, physicians and administrators in medical institutions should be aware of the relative high antibiotic resistance in pathogens causing SSI. We also identifies that preoperative hospital stay ≥ 48 h and contaminated or dirty wound are both significantly associated with the increasing risk of SSI after CRS. However, more well-designed cohort with large population or meta-analysis and biological researches are needed to further clarify the relationship between risk factors with development of SSI after CRS, concerning that controversies are commonly observed among current surveys.