In recent years, changes in dietary patterns and lifestyle habits have led to colorectal cancer becoming a common malignancy within the gastrointestinal tract, with its incidence rate gradually increasing. Annually, approximately 1.2 million new cases and 600,000 deaths are attributed to this disease [50, 51, 52]. Moreover, the age of onset has been trending younger [53]. Colorectal cancer ranks fourth in incidence and second in mortality among all types of cancer worldwide, posing a serious threat to patient's health and safety [54, 55, 56]. Currently, the preferred treatment for colorectal cancer patients is radical surgery to remove the lesion [57, 58, 59]. Laparoscopic surgery, which allows for the visualization of surrounding tissues, nerves, blood vessels, and ureters, helps minimize damage to surrounding tissues and has shown significant clinical outcomes [60]. However, patients with colorectal cancer are susceptible to the adverse effects of their condition, leading to poor physical health and reducing their capacity to undergo surgery [5, 38, 61]. The high bacterial content and complex microbiota within the human colorectal cavity also increase the risk of postoperative incision infection [62, 63]. During surgery, the spillage of intestinal contents can lead to the displacement and colonization of intestinal pathogens, resulting in a high rate of postoperative incision infections. Incision infections are common complications in clinical surgery and, in severe cases, can lead to systemic infections and sepsis, severely impacting postoperative recovery [64, 65, 66]. Literature reports the rate of incision infections following colorectal surgery ranging from 2.7–26.0% [67, 68, 69]. Colorectal cancer, being a debilitating disease, leads to a decline in patients' immune function, making them more prone to postoperative incision infections [70].
This study, through a systematic literature review and meta-analysis, delved into several potential risk factors for postoperative incision infection in colorectal cancer, including a BMI of ≥ 24kg/m2, diabetes, preoperative low albumin levels, the method of laparoscopic surgery, preoperative malnutrition, and surgical duration exceeding 3 hours. It identified that a BMI of ≥ 24kg/m2, preoperative low albumin levels, preoperative malnutrition, and extended surgical duration are significant risk factors for postoperative incision infection, with diabetes also being a crucial risk factor. In contrast, laparoscopic surgery methods appear to be associated with a lower risk of infection (Fig. 5). Our findings reveal a significant correlation between these factors and the risk of postoperative incision infection in colorectal cancer, offering essential insights for clinicians in preoperative assessment and postoperative management.
Patients with colorectal cancer having a BMI > 24 kg/m2 indicate obesity, which is problematic due to the substantial subcutaneous fat affecting surgical field exposure and complicated surgical procedures. This condition can increase the difficulty of surgery, extend the operation time, and raise the risk of postoperative incision infection. Obese patients have high-fat content that can inhibit the proliferation of immune cells, thereby increasing the risk of incision infection. Postoperative patients with higher body weight are more prone to abdominal fat liquefaction, with significant body weight being related to enlarged fat tissue and inadequate blood supply. Moreover, such patients often have chronic diseases like hypertension and diabetes, reducing their immune function and thus increasing the likelihood of postoperative incision infection. The incision length is also closely associated with the occurrence of postoperative infection. Additionally, overweight individuals have a higher chance of developing diabetes, altering their immune cell function and inflammatory responses, making overweight and diabetic patients more susceptible to surgical incision infections. Therefore, perioperative anti-infection measures should be taken for patients with high BMI, and appropriate plans should be formulated before surgery to prevent postoperative infections. Previous studies have indicated that a higher BMI in colorectal cancer patients increases the risk of surgical site infections [71, 72, 73]. Hirao et al. found a significant increase in the incidence of incision infections at a BMI ≥ 25 kg/m2 (OR = 2.28, 95% CI: 1.05 ~ 7.52), consistent with our study findings. Research by Chen Yan et al. showed that obesity affects surgical field exposure and maneuverability due to subcutaneous fat [74, 75, 76]. The surgical incision may be extended to achieve better visibility during surgery, increasing the exposure area and airways. Postoperatively, the incision is prone to liquefaction and necrosis, slowing healing and increasing surgical incision infection incidence.
As societal lifestyles change and populations age, the incidence of diabetes is on the rise, leading to an increase in colorectal cancer patients with diabetes. These patients are more susceptible to postoperative incision infections due to immune system dysregulation and suppressed immune functions [40, 77, 78]. Studies have shown that diabetes disrupts glucose metabolism, reduces glycolytic capacity, and weakens neutrophil migration, phagocytosis, and bactericidal functions [79]. Protein synthesis decreases while degradation accelerates, reducing immunoglobulins' production, complements, and chemotactic factors, thereby diminishing immune function [80, 81, 82]. The immune response in diabetic patients is relatively lower, and surgical trauma exacerbates glucose metabolism disorder. In a hyperglycemic environment, inflammation cell migration to the surgical site is hindered, further lowering the body's immunity and increasing infection risks, consistent with findings by Wukich et al. [83]. The rate of incision infection in diabetic patients is significantly higher than in non-diabetic patients. The abnormal glucose metabolism in patients with diabetes impairs the normal function of inflammatory factors, facilitating pathogen colonization and growth in a high-glucose microenvironment, thus diminishing the patient's infection resistance.
Diabetic patients have microcirculation disorders, leading to a higher risk of anastomotic leakage post-surgery and potential abdominal infections. Diabetes-induced vascular plaque formation causes the narrowing of blood vessels, reducing tissue oxygenation, which can lead to tissue hypoxia, affecting oxidative-mediated microbial killing mechanisms and tissue oxygenation, and delaying tissue healing. Postoperative malnutrition is more likely in diabetic patients, adversely affecting recovery. Furthermore, wound healing in diabetic patients is slower. In healthy individuals, the metabolic level of glucose in diabetic patients is lower than usual, resulting in lower protein synthesis capacity and poorer cellular tissue repair abilities. Severe patients have impaired inflammatory cell function, affecting leukocyte phagocytosis. Immune function is below average, with fewer fibroblasts, hindering granulation tissue formation at the wound site, delaying wound healing, and even causing local edema. Surgical trauma can lead to postoperative stress-induced hyperglycemia, conducive to bacterial growth; a high glucose environment in the blood promotes bacterial colonization. Numerous studies have confirmed the impact of diabetes and perioperative hyperglycemia on surgical site infection. Hyperglycemia provides conditions for bacterial growth, and exudate in a high-glucose environment facilitates bacterial growth, reducing the body's immunity and leading to postoperative incision infections. Immune response functions are relatively lower in colorectal cancer patients with a history of diabetes. Post-laparoscopic surgery, surgical trauma further disrupts glucose metabolism, promoting inflammatory cell migration to the incision site, weakening immunity, and increasing the risk of postoperative incision infections. Persistent hyperglycemia in diabetic patients fosters bacterial growth, thereby increasing the rate of surgical site infections. Glucose metabolism disorder leads to a decreased pathogen clearance capacity, impaired immune function, and reduced infection resistance. Therefore, for colorectal cancer patients with diabetes, perioperative blood glucose management should be strengthened, aiming to keep blood glucose levels between 5.6-11.2mmol/L, minimizing glucose fluctuations and thereby reducing the incidence of postoperative abdominal infections following colorectal cancer resection surgery.
Albumin levels directly reflect the nutritional status of the body [84, 85, 86]. Low albumin levels indicate a higher risk of malnutrition, compromising immune function and increasing incision infection risk [87, 88, 89]. Albumin, a significant component of human plasma proteins, is crucial in maintaining internal homeostasis [90]. Low albumin levels reduce a patient's immunity, leading to drug absorption and metabolic disorders and complicating wound healing [91, 92]. Therefore, clinical nutritional support should be intensified for such patients to boost their resistance, emphasizing the importance of preoperative nutritional interventions to enhance patient resilience [93, 94].
Surgical methods include traditional open surgery and laparoscopic surgery [95]. Studies have shown that traditional open surgery, with its extensive trauma and significant blood loss, complicates postoperative recovery [96, 97, 98]. Laparoscopic surgery, a significant advancement in modern science, has emerged as a new option for curative resection of colorectal cancer [67, 99, 100]. It allows for precise observation of the surrounding tissue of the lesion, thus minimizing damage [101].
Open surgery requires an extended incision to ensure an excellent surgical field of view [102, 103]. The larger incision, exposed to air for an extended period during surgery, significantly increases the risk of infection and may impact wound healing [104]. Laparoscopic surgery facilitates precise observation of the lesion's surrounding tissues, nerves, blood vessels, and ureters, minimizing damage [105]. With the advancement of laparoscopic techniques, pain post-colorectal cancer surgery has significantly reduced, and the recovery time has considerably shortened [106, 107, 108]. The incision length in laparoscopic surgery is notably shorter than in open surgery, reducing skin integrity damage, bacterial displacement within the skin, and challenges in incision healing [109, 110, 111, 112]. Additionally, laparoscopic surgery, with its minimal tissue damage and smaller incisions, facilitates postoperative recovery, encouraging early patient mobilization to support wound healing and lower postoperative incision infection rates [110, 111, 112]. Some studies have found that laparoscopic surgery minimally impacts human immune function and injury, making postoperative incision infections less likely [113, 114]. Therefore, the choice of surgical method is particularly crucial, with a preference for laparoscopic surgery when possible [115, 116]. Research indicates that in a single-center randomized controlled trial, the postoperative incision infection rate for patients undergoing laparoscopic surgery for colorectal cancer was 4.9% (47/961), significantly lower than the open surgery group (9.6%, 95/986) [117, 118, 119, 120]. This difference may be due to laparoscopic surgery reducing the direct contact between organs and environmental pathogens. Additionally, laparoscopic surgery avoids factors like peritonitis, increased intestinal permeability, and intestinal edema that are prone to surgical site infections, thereby lowering the rate of postoperative incision infections [121, 122, 123].
Nutritional status is a primary concern in the perioperative management of colorectal cancer patients [124, 125]. Malnutrition lowers cellular and humoral immune responses, and correcting malnutrition can reduce the incidence of perioperative complications by up to 10% [126, 127, 128]. The occurrence rate of perioperative complications is as high as 10% [129, 130, 131]. Although no universal definition for diagnosing malnutrition, it typically encompasses conditions related to inadequate food intake, weight loss, and a low BMI [132, 133, 134]. The European Society for Clinical Nutrition and Metabolism (ESPEN) defines malnutrition to include at least one of the following criteria: a weight loss of more than 10% of the original weight within six months, a BMI lower than 18.5 kg/m2, serum albumin less than 35 g/L, in the absence of liver or kidney dysfunction [135, 136, 137, 138, 139, 140]. Fujimichi et al. reported that malnutrition is an independent risk factor for postoperative incision infection in colorectal cancer patients (OR = 2.52, 95%, p = 0.01) [42, 141, 142]. Furthermore, a registry study at the Hokeland University Hospital in Norway showed that among 1194 patients undergoing surgical treatment, those at nutritional risk were more likely to develop incision infections, with a positive correlation between the incidence of incision infections and nutritional risk (OR = 1.81, p = 0.047) [143, 144, 145, 146]. ESPEN recommends that severely malnourished patients scheduled for major gastrointestinal surgery should receive preoperative nutritional support for 10–14 days. Enteral nutrition should be the first choice if there are no contraindications [147, 148, 149, 150]. Enhancing perioperative nutrition and supportive care is crucial for malnourished patients, ensuring sufficient energy and nutrient intake to prevent perioperative incision infections. Malnourished colorectal cancer patients often have electrolyte imbalances, anemia, and lower immunity, increasing the risk of postoperative incision infections. Patients should receive enteral nutrition as soon as gastrointestinal recovery permits, maintaining the intestinal barrier and immune barrier, reducing endotoxin absorption and intestinal flora displacement, thereby providing a conducive internal environment for wound healing [49, 151, 152, 153, 154, 155].
This study's findings indicate that a surgical duration exceeding three hours is a risk factor for surgical site infections in patients with colorectal cancer, aligning with Katsuno's research. It has been shown that the risk of postoperative incision infection in colorectal cancer increases with the length of the surgery [156, 157, 158, 159]. Extended surgical times are often associated with increased blood loss, potentially leading to tissue hypoxia [160, 161, 162]. Longer surgeries inevitably carry a higher risk of bleeding and increased blood loss, reducing the body's resistance and inducing infection [163]. The longer the surgery, the more energy the patient expends, raising the risk of exogenous infection and, thereby, the risk of postoperative incision infection [164, 165, 166]. Prolonged surgical duration also means the sterile environment within the abdomen is exposed to air for a longer time [167, 168, 169]. Even in an operation meeting standard requirements, air cleanliness decreases with extended surgical times, increasing the probability of local bacterial contamination [170, 171, 172]. The wound's exposure to air also increases, leading to a higher bacterial count at the incision site and increasing the possibility of tissue cell destruction. Longer surgeries, extended exposure to tissue traction, and prolonged use of surgical energy devices can damage tissues. Moreover, extended anesthesia can adversely affect the patient's immune function. The body's immunity diminishes as anesthesia duration and intraoperative blood loss increase. The length of the surgery is not only related to the patient's physical condition but also largely depends on the surgeon's skill and proficiency in the operation. Thus, an increased rate of postoperative incision infection indicates that more complex, challenging, and traumatic surgeries with longer durations lead to higher infection rates [173, 174]. Therefore, enhancing the surgical skills and intraoperative proficiency of surgeons, reducing surgical trauma, shortening surgical duration, and lowering the incidence of incision infections is paramount. Zheng Hui's multivariate analysis of 2308 patients showed that surgical duration (OR = 1.007, 95% CI: 1.002 ~ 1.012) is an independent risk factor for incision infection [175]. Thus, effectively controlling surgical duration can significantly reduce the incidence of incision infections [176, 177, 178].
Based on the analysis of various risk factors, future clinical practices can implement the following strategies to prevent postoperative incision infections in patients with colorectal cancer:
(1) Preoperative: Implement infection prevention measures and avoid scheduling surgeries during summer. For diabetic patients, intensify monitoring and control of blood glucose levels and use insulin judiciously. Surgery should proceed only when blood glucose levels are within normal ranges. For elderly patients, complications should be vigilantly monitored and actively managed preoperatively. Additionally, patients' nutritional status should be assessed, and timely nutritional support should be provided to those with low serum albumin to ensure balanced daily nutrient intake and optimal preoperative nutrition.
(2) Intraoperative: Adhere to standard sterile procedures, minimize electrosurgical use in patients with thick adipose layers, and adjust the electrosurgical power as necessary. Inactive fatty tissue should be rinsed with saline during incision closure. Moreover, surgical preparations should be meticulously planned, requiring close cooperation among medical staff to enhance procedural proficiency and actively manage surgical duration. When appropriate, consider laparoscopic surgery for its reduced patient trauma and lower postoperative incision infection rates, taking into account the patient's specific health status and condition.
(3) Postoperative: Monitor changes in patient vitals, replenish energy promptly as needed, and encourage high-fiber and protein-rich foods to boost nutrition and maintain electrolyte balance. Pay attention to changes in the nature, volume, and color of drainage fluid, replace drainage bags timely to prevent incision-related infections, and regularly change wound dressings to prevent bacterial growth and infection.
Despite our study's rigorous design and execution, it has limitations. First, the significant heterogeneity among studies may affect the robustness of our conclusions, although sensitivity analysis and publication bias assessment have been conducted to ensure the reliability of the results. Second, the quality of included studies varies, and despite rigorous evaluation using the Cochrane risk of bias tool and NOS scoring system, the impact of low-quality studies must be partially ruled out. Additionally, language and database search limitations might have led to selection bias due to potentially relevant studies needing to be included.
Future research should further explore the causal relationships between these risk factors and postoperative incision infections in colorectal cancer and how they interact with other potential risk factors. Moreover, as medical technology advances, new surgical techniques and postoperative management strategies may influence the risk of postoperative incision infections in colorectal cancer. Therefore, ongoing research and updated meta-analyses must ensure our conclusions reflect the latest scientific evidence.
In summary, this study provides critical insights into the risk factors for postoperative incision infection in colorectal cancer, emphasizing the importance of comprehensive assessment and management of these risk factors in clinical practice. By early identification and intervention of these risk factors, the incidence of postoperative incision infections in colorectal cancer patients can potentially be reduced, thereby improving patient prognosis and quality of life. Future research should aim to explore additional potential risk factors and evaluate the effectiveness of various prevention and management strategies to optimize postoperative care for colorectal cancer patients further.