Surgical site infections (SSIs) increase the risk of long-term morbidity among postoperative patients, with a higher rate of rehospitalization and postdischarge outpatient expenses [1]. In fact, SSIs are the most common cause of unplanned postoperative readmission [2]. Colorectal surgical procedures, which account for a relatively high volume of gastrointestinal operations, pose a high risk for SSIs [3]. Several factors, such as age, the American Society of Anesthesiologists (ASA) physical status classification, diabetes mellitus, body mass index (BMI), smoking, and tumor location, are known to be independent risk factors of SSIs [3]. Other operative characteristics, including blood transfusion [4], emergency cases, and longer operative time [5], have also been associated with an increased risk for SSIs. A clearly modifiable factor is the type of surgical wound closure used, which is also known to be associated with the risk for SSIs [6].

Skin stapling provides surgeons with a convenient and quick technique for surgical wound closure. However, skin staples can increase postoperative pain and carry a risk for scarring. Surgical skin adhesives have been developed to overcome these shortcomings of skin stapling. Surgical skin adhesives create a strong polymeric bond across the edges of the wound, promoting natural healing, with the synthetic flexible microbial barrier providing in-vitro protection against penetration of organisms [7]. A prospective randomized study further reported a trend to better cosmetic outcomes with the use of skin adhesives compared to staples for the closure of surgical wounds in open elective colectomies for benign or malignant indications [8]. However, there has been less comparative study evaluating the effect of surgical skin adhesives compared to that of skin stapling on the risk of SSIs after elective colorectal cancer surgery. In fact, although the effects of skin stapling on the risk of SSIs have been evaluated in clean surgeries, such as spinal surgery [9], the risk for SSIs with the use of skin stapling in clean-contaminated surgery, such as colorectal surgery, has not been evaluated. Considering the decreasing rate of SSIs with the increasing use of minimally invasive surgical (MIS) techniques for colorectal surgery, there is a need to evaluate the effect of different surgical wound closures on the risk of SSIs for colorectal MIS. The objective of this study was, therefore, to comparatively evaluate the role of surgical skin adhesives with that of skin stapling in reducing the rate of SSIs following MIS for colorectal cancer surgery.

The characteristics for the 284 patients in group I (surgical skin adhesive bond) and the 208 in group II (skin stapler) are shown in Table 1. There were no differences in patients' characteristics between the 2 groups, including patient-related factors (age, BMI, ASA physical status, and underlying disease), systemic inflammation factors (neutrophil-lymphocyte ratio, C-reactive protein level), and nutritional status (albumin). The mean ages of patients in group I and group II were 63.6 ± 12.7 years and 64.4 ± 12.8 years, respectively (P = 0.505). The mean BMI in group I and group II was 23.4 ± 3.9 kg/m² and 23.8 ± 3.0 kg/m², respectively (P = 0.791). The distribution of location of the cancer was also not different between the groups. Similarly, the prevalence of diabetes mellitus (50 cases vs. 40 cases, P = 0.723) and smoking history (67 cases vs. 60 cases, P = 0.247) was not different between the groups. The robotic approach was more in group I (55 cases vs. 5 cases, P < 0.001).

With regard to perioperative outcomes (Table 2), the estimated intraoperative blood loss and rate of intraoperative transfusion were not different between the groups. However, the operative time was significantly longer in group I (222.5 ± 72.2 minutes) than in group II (145.4 ± 63.8 minutes) (P < 0.01). Superficial SSIs were observed more frequently in group II (5/208 cases) than in group I (0/284 cases) (P = 0.024). The rate of deep and organ/space SSIs was not significantly different between the groups (deep SSIs: 1/284 vs. 1/208, P > 0.990; and organ: 3/284 vs. 7/208, P = 0.703). The mean visual analogue pain score was also not different between group I and group II on postoperative day (POD) 1 (4.1 ± 1.8 vs. 4.0 ± 2.0, P = 0.429) and POD 3 (3.7 ± 1.6 vs. 3.77 ± 1.8, P = 0.732). Postoperative hospital stay was not significantly different between group I (5.8 ± 4.6 days) and group II (6.1 ± 5.6 days) (P = 0.504). The average total cost for wound care was significantly lower in group I (48.0 ± 5.3 vs. 68.7 ± 14.3 USD, P < 0.001).

On univariate analyses, age > 75 years, tumor location, stoma formation, and method of surgical wound closure were associated with SSIs. On multivariate analysis, age > 75 years, stoma formation, and the method of surgical wound closure was retained as an independent risk factor of SSIs (Table 3).

According to our findings, surgical skin adhesive bond significantly lowered the incidence of superficial SSIs compared to skin stapling. Moreover, despite the longer operative time in the surgical skin adhesive bond group, due to more robot-assisted MIS, which is usually considered as one of the risk factors of SSIs [16], the rate of SSIs was significantly low compared to that in the skin stapler group.

Generally, the use of surgical skin adhesive bond for wound closure reduces postoperative pain compared to conventional staples. However, in this study, there was not significantly different between the 2 groups. Since 2017, our institute applied ERAS protocol including postoperative pain management and reported less postoperative pain in ERAS group [12]. Due to the effective postoperative pain management program, we could not find significant difference in postoperative pain between the groups.

In this study, we find that the benefit of surgical skin adhesive bond, over skin staples, for reducing superficial SSI is clinically valuable. The benefits of tissue surgical skin adhesive bond for skin closure have previously been reported. For cesarean delivery, the use of n-butyl-2-cyanoacrylate skin closure provides more favorable cosmetic results than skin sutures, with no increase in the rate of wound complication [17]. Another recent study reported that cyanoacrylate glue serves better cosmetic results and patient satisfaction than skin suture for wound closure after brain surgery [18]. One randomized controlled trial reported that n-butyl-2-cyanoacrylate yielded better results than nylon sutures in terms of wound infection and dehiscence and necrosis of tissue edges, for extra oral maxillofacial wound closure [19].

To date, surgical skin adhesives have not been commonly used in practice and the clinical role of adhesives, including in lowering the risk of SSIs, in colorectal cancer surgery has not been previously evaluated. To our knowledge, our study is the first to describe the clinical impact of adhesives in patients who have undergone MIS for colorectal cancer.

Operation time is now considered as one of the risk factors of SSI, and operative time was significantly longer for the surgical skin adhesive bond group than for the skin stapler group because of more robotic surgeries were in skin adhesive bond group (group I, 55 [19.4 %] vs. group II, 5 (2.4 %); P < 0.001). Previous studies have identified increased operative time as a specific disadvantage of robot-assisted colorectal surgery [2021]. But it was so interesting that the benefit of skin adhesives bond over skin staples in terms of reducing SSI was maintained even for longer operative times.

Surgical skin adhesive bond closure methods have already been proven to provide a number of advantages that include fast and painless application, reduction in total wound closure time, antibacterial and waterproof properties that allow patients to take a shower, and unnecessary application of stitches or clip removal [22]. However, the cost of surgical skin adhesive bond is still expensive compared to that of traditional suture or skin stapling techniques. However, the higher cost of adhesives can be balanced with fewer dressings and fewer visits on an outpatient basis. When we calculated the average of total cost for wound care which included surgical adhesive, skin stapler, dressing material, and dressing charge, the total cost for wound care in surgical adhesive bond group was significantly lower than skin stapler group, because routine surgical wound dressing was not necessary after applying surgical adhesive bond. Moreover, considering the time and costs needed to manage SSIs, adhesive might be more economical overall.

The limitations of our study included the following. First, because of the retrospective design of the study, an effect of selection bias cannot be denied. Second, the study sample was not large, and the rate of SSIs was quite low, which makes it difficult to clearly differentiate the risk factors for SSIs. A large-scale multi-institutional prospective validation study is necessary to confirm our findings. Third, bacterial cultures were not used; therefore, the mechanism of SSIs could not be confirmed. Finally, other risk factors of postoperative pain, such as surgical incision length, could not be measured exactly. Despite these limitations, all procedures were performed by experienced colorectal surgeons and perioperative care and intraoperative treatment including fascia and subcutaneous layers closure technique were same.

In conclusion, our study indicated that surgical skin adhesive bond is a safe and feasible technique for wound closure in reducing superficial SSI following MIS for colorectal surgery.