Does minimally invasive anatomical hepatectomy reduce surgical site infections?
Abstract
Aim: This study aims to clarify the effectiveness of laparoscopic anatomical liver resections (ALRs) in surgical site infections (SSIs).
Methods: We included 95 cases (44.0%) of laparoscopic ALRs (LALRs) and 121 (56.0%) of open ALRs (OALRs). Retrospective comparisons were performed between the two groups.
Results: In preoperative factors, tumor size was significantly smaller in LALRs than in OALRs (34.4 ± 23.0 mm vs. 45.9 ± 35.7 mm, P = 0.007). The operative duration was longer in LALRs than in OALRs (523.0 ± 186.5 min vs. 356.3 ± 100.5 min, P < 0.001). However, the blood loss and the blood transfusion were fewer in LALRs than in OALRs (592.1 ± 911.7 mL vs. 1,240.6 ± 1,131.8 mL, P < 0.001, 26.3% vs. 48.8%, P = 0.001, respectively). Postoperative complications above the Clavien-Dindo grade IIIb were one case (1.1%) in LALRs and two in OALRs
Conclusion: Although this is a limited study at a single institution, minimally invasive anatomical hepatectomy can reduce ISSIs.
Keywords
INTRODUCTION
In recent years, laparoscopic surgery has become widespread for lesions occurring in intraperitoneal organs. In the field of liver surgery, laparoscopic liver resections (LLRs) are performed mainly at high-volume centers, and their application is expanding to more difficult hepatectomies. Laparoscopic surgery, which allows for precise surgery with the effect of magnification, has been reported to be less invasive than open surgery and has been shown to reduce postoperative complications in various organs, such as the stomach[1] and colon[2]. However, although there have been some previous reports on the occurrence of postoperative infectious complications, including surgical site infections (SSIs), in liver surgeries, this is still open to debate. On the other hand, systematic anatomical liver resections (ALRs) are more complex and have a higher complication rate than non-systematic partial hepatectomy. Therefore, we compared the treatment outcomes of laparoscopic ALRs (LALRs) and open ALRs (OALRs) performed at our facility and described the effectiveness of minimally invasive surgeries in ALRs in reducing postoperative infectious complications, especially SSIs.
METHODS
Patients and methods
Of the 651 cases of all liver resections performed in our department between January 2006 and May 2022, 216 ALRs were studied [Figure 1], excluding biliary reconstruction, cases of combined resection of other organs, and emergency cases. Of these, 95 cases (44.0%) were LALRs, and 121 (56.0%) were OALRs. By performing a retrospective comparison between these two groups, we verified whether LALRs reduce SSIs. The study was conducted in line with the principles of the Declaration of Helsinki. It was reviewed and approved (No. M22194 21242) by the ethics committee of Toho University Omori Medical Center, Japan. The details about the study were disclosed on the web page of Toho University Omori Medical Center (https://www.lab.toho-u.ac.jp/med/omori/gastro_surgery/patient/crl21600000000ku-att/20230214_M22194_21242.pdf), and the potential participants were given the opportunity to opt-out.
Indications for systematic LLRs
When we first introduced LLRs, the tumor factor was tumors 5 cm or less located on the periphery or superficial surface of the lateral or infero-hepatic segments (S3, S4b, S5, S6). The surgical procedure factor was only partial hepatectomies or left lateral sectionectomy. In addition, the candidates were patients who could tolerate similar open liver resections (OLRs) as host factors, and cases with apparent bleeding tendency or ascites were excluded. By accumulating these cases, standardizing the procedure, and improving surgical outcomes, we gradually expanded the indications for hepatic systemic anatomical resection equivalent to OLRs. Anatomical hepatic resections were planned as segmentectomies, sectionectomies, or two or more section resections from the perspective of tumor size, tumor number, and achieving radical surgery[3-5].
Perioperative management of LLRs
In preoperative systemic evaluation, the American Society of Anesthesiologists physical status (ASA-PS) and the Charlson comorbidity index (CCI)[6] were used.
In intraoperative anesthetic management, maximum airway pressure (MAP) was maintained at 15 cmH2O or less. In addition to significant hepatectomy and tumor resection near the hepatic vein or inferior vena cava, a central venous catheter (CVC) was placed in cases where monitoring of circulatory and respiratory dynamics was deemed necessary, and central venous pressure (CVP) was managed with a target of
Standard surgical technique
Pneumoperitoneum pressure (PP) was 8-10 mmHg with CO2 insufflation to ensure visibility. For hepatectomy, preparation for hepatic portal blockade using the Pringle method was performed in all cases, and portal blockade was performed when necessary. The area of ischemic blood flow was confirmed by securing and ligating the dominant Glissonean sheath on the hepatic portal side, and the anatomical resection area was confirmed using the indocyanine green (ICG) fluorescence method. The vessels were exposed using a cavitron ultrasonic surgical aspirator (CUSA) or clump crushing, and the liver parenchyma was resected using an Ultrasonic Activated Device, Monopolar Device, or Bipolar Device. A stapling device was used to dissect a relatively large Glissonean pedicle and significant hepatic veins. The approach started as pure laparoscopy but was changed to hybrid or hand-assisted laparoscopic surgery (HALS) to ensure safety, such as improving the visual field and controlling bleeding. For LLRs, the specimen was placed in a plastic bag and removed from the body. If bile leakage was observed during surgery, a C-tube was placed through the cystic duct. A closed suction drain was placed in all cases. The wound was closed by irrigating with saline and then suturing the dermis with absorbable sutures.
Standard perioperative antimicrobial management
Prophylactic antibiotics were cefmetazole (CMZ) or cefotiam (CTM). In patients with normal renal function, antibiotics were administered every 3 h during surgery from before the start of surgery. Postoperative antibiotics were administered continuously for up to 48 h. In cases where a peritoneal drain was inserted, it was generally removed on the third postoperative day after confirming neither bleeding nor bile leakage.
Definition of postoperative complications
SSIs were classified into incisional SSIs (ISSIs) and organ/space SSIs (OSSIs) according to the Centers for Disease Control and Prevention (CDC) guidelines[7]. ISSIs were defined as cases in which wounds were opened due to signs of wound infection within 30 days after surgery, and drainage cultures were positive. OSSIs were defined as positive when purulent drainage was observed from peritoneal drains within 30 days after surgery or when pathogens were isolated from aseptically collected specimens. Bile leakage was defined as positive according to the International Study Group of Liver Surgery (ISGLS) criteria[8] when bile leakage continued for three days or more after surgery, containing three times or more the T-Bil value than the blood test in biliary drainage juice, or when surgical or radiological treatment was required for drainage due to bile leakage. According to TG18[9], cholangitis was considered positive if, in addition to fever or worsening inflammatory symptoms, serum total bilirubin levels were 2 mg/dL or higher, hepatobiliary test results were 1.5 times higher than the reference values or bile duct dilation was observed on abdominal ultrasound (US) or computed tomography (CT) scans. Furthermore, cases of Clavian-Dindo[10] (CD) grade 3a or higher that required interventional radiology (IVR) or endoscopic treatment were considered positive. Intestinal obstruction was considered positive if symptoms of gastrointestinal obstruction such as nausea and vomiting were present, stomach or small intestine dilation was observed on plain abdominal X-rays or abdominal CT scans, and fasting treatment was required as CD grade 3a or higher. Deep vein thrombus (DVT) was considered positive if, in addition to clinical symptoms such as edema and pain, the coagulation and fibrinolysis levels were elevated, whole-leg venous ultrasound (whole-leg US) was performed on all patients, and the diagnosis was positive if intravenous thrombus was demonstrated. Portal vein thrombosis (PVT) was also considered positive if demonstrated on percutaneous US or contrast CT scans. According to the ISGLS criteria[11], liver failure was determined to be positive if the prothrombin time was prolonged or the serum total bilirubin level was elevated on the fifth postoperative day or later, and if the patient had ISGLS Grade B or higher, requiring treatment such as blood transfusion. All the above complications were graded according to the CD; cases with CD grade 3a or higher were considered positive.
Statistical analysis
Statistical analysis was performed using EZR on R commander, version 1.55, and the Mann-Whitney U test or chi-square test was used to compare the two groups. Univariate and multivariate analyses were performed using a logistic regression model to determine independent risk factors of ISSIs. Each group used receiver operating characteristic curve analysis to calculate cut-off values for logistic regression analysis.
RESULTS
Table 1 shows a comparison of preoperative factors. Age was 64.0 ± 13.0 years in the LALRs compared with 67.6 ± 10.0 years in the OALRs, with the LALRs being statistically significantly younger (P = 0.022). There were 66 male cases (69.5%) compared with 85 male cases (70.2%) in the OALRs, and body mass index (BMI) was 23.2 ± 3.6 kg/m2 in the LALRs compared with 22.8 ± 3.5 kg/m2 in the OALRs, with no statistically significant difference between the two groups (P = 1.000 and P = 0.460, respectively). Alcohol consumption was 35 (36.8%) in LALRs and 34 (28.1%) in OALRs. Smoking history was 63 (66.3%) in LALRs and 84 (69.4%) in OALRs, with no statistically significant differences between the two groups (P = 0.188, P = 0.661, respectively). Regarding comorbidities, insulin use was 34 (35.8%) in LALRs and 33 (27.3%) in OALRs. Chronic kidney disease was 26 (27.4%) in LALRs and 34 (28.1%) in OALRs. Steroid use before surgeries was 2 (2.1%) in LALRs and 2 (1.7%) in OALRs, with no statistically significant differences between the two groups (P = 0.186, P = 1.000, P = 1.000, respectively). In evaluating the physical condition, the ASA classification showed no statistically significant difference between the two groups. On the other hand, the number of cases with a low CCI was 19 (20.0%) in LALRs and 13 (10.7%) in OALRs, showing a tendency for the LALRs to have a higher CCI score (P = 0.081). In terms of preoperative hepatic functional reserve, the number of cases with cirrhosis was 11 (11.6%) in LALRs and 10 (8.4%) in OALRs, showing no statistically significant difference between the two groups (P = 0.492). The preoperative ICG R15 values were 9.2% ± 6.4% in LALRs and 9.8% ± 6.3% in OLRs, and there was one case (1.1%) of Child-Pugh Grade B in LALRs and two cases (1.7%) in OALRs, with no statistically significant difference between the two groups (P = 0.462 and P = 1.000, respectively). Regarding tumor factors, the proportion of malignant disease was 79 cases (83.2%) in LALRs and 108 cases (89.3%) in OALRs, with a tendency for malignant disease to be more prevalent in OALRs (P = 0.229). Hepatocellular carcinoma (HCC) was in 55 cases (57.9%) in LALRs and 56 cases (46.3%) in OALRs, with no statistically significant difference between the two groups (P = 0.101). Metastatic carcinoma (Mets) was 22 cases (23.2%) and 36 cases (29.8%) in OALRs, with no statistically significant difference between the two groups (P = 0.354). The tumor diameter was 34.4 ± 23.0 mm in LALRs and 45.9 ± 35.7 mm in OALRs, significantly smaller in LALRs (P = 0.007). Preoperative chemotherapy was administered in 16 cases (16.8%) compared to 35 cases (28.9%) in OALRs, with a tendency for preoperative chemotherapy to be more frequent in OALRs (P = 0.052).
Comparison of preoperative factors between OALRs and LALRs
Variables | OALRs (n = 121) | LALRs (n = 95) | P-value | |
Age, years | 67.6 ± 10.0 | 64.0 ± 13.0 | 0.022 | |
Gender | Female, % | 36 (29.8) | 29 (30.5) | 1.000 |
Male, % | 85 (70.2) | 66 (69.5) | ||
Body mass index, kg/m2 | 22.8 ± 3.5 | 23.2 ± 3.6 | 0.460 | |
Comorbidity | Alcohol, % | 34 (28.1) | 35 (36.8) | 0.188 |
Smoking, % | 84 (69.4) | 63 (66.3) | 0.661 | |
Diabetes mellitus, % | 33 (27.3) | 34 (35.8) | 0.186 | |
Chronic renal disease, % | 34 (28.1) | 26 (27.4) | 1.000 | |
Steroid use, % | 2 (1.7) | 2 (2.1) | 1.000 | |
ASA score | I, % | 6 (5.0) | 7 (7.4) | 0.568 |
II, % | 100 (82.6) | 81 (85.3) | 0.711 | |
III, % | 15 (12.4) | 7 (7.4) | 0.263 | |
IV, % | 0 (0.0) | 0 (0.0) | NA | |
V, % | 0 (0.0) | 0 (0.0) | NA | |
CCI | Low (0), % | 13 (10.7) | 19 (20.0) | 0.081 |
Medium (1-2), % | 46 (38.0) | 33 (34.7) | 0.670 | |
High (3-4), % | 21 (17.4) | 17 (17.9) | 1.000 | |
Very high (≥ 5), % | 41 (33.9) | 26 (27.4) | 0.374 | |
Liver function | Cirrhosis, % | 10 (8.4) | 11 (11.6) | 0.492 |
ICG R15, % | 9.8 ± 6.3 | 9.2 ± 6.4 | 0.462 | |
Child Pugh grade A, % | 119 (98.3) | 94 (98.9) | 1.000 | |
B, % | 2 (1.7) | 1 (1.1) | 1.000 | |
C, % | 0 (0.0) | 0 (0.0) | NA | |
Tumor factor | Malignant disease, % | 108 (89.3) | 79 (83.2) | 0.229 |
Hepatocellular carcinoma, % | 56 (46.3) | 55 (57.9) | 0.101 | |
Metastatic caricinoma, % | 36 (29.8) | 22 (23.2) | 0.354 | |
Intrahepatic cholangiocarcinoma, % | 10 (8.3) | 2 (2.1) | ||
Gallbladder carcinoma, % | 4 (3.3) | 0 (0.0) | ||
Neuroendocrine carcinoma, % | 1 (0.8) | 0 (0.0) | ||
Benigin disease, % | 13 (10.7) | 16 (16.8) | ||
Tumor size, mm | 45.9 ± 35.7 | 34.4 ± 23.0 | 0.007 | |
Preoperative chemotherapy, % | 35 (28.9) | 16 (16.8) | 0.052 |
A comparison of intraoperative factors is shown in Table 2. The initial hepatectomy was performed in 91 cases (95.8%) in LALRs and 105 cases (86.8%) in OALRs, with a statistically significant difference between the two groups (P = 0.032). The approach in LLRs was pure in 67 cases (70.5%), hybrid in 17 cases (18.5%), HALS in 7 cases (7.6%), and conversion to conventional open procedure in 4 cases (4.2%). The surgical procedures performed were hemi-hepatectomies in 30 cases (31.6%) in LALRs and 47 cases (38.8%) in OALRs, sectionectomies in 27 cases (28.4%) in LALRs and 30 cases (24.8%) in OALRs, and segmentectomies in 38 cases (40.0%) in LALRs and 48 cases (39.7%) in OALRs, with no difference between the two groups (P = 0.317, P = 0.641, and P = 1.000, respectively). In the LALRs, the operative duration was 523.0 ± 186.5 min, the blood loss was 592.1 ± 911.7 mL, and 25 cases (26.3%) required intraoperative blood transfusion. In contrast, in the OALRs, the operative duration was 356.3 ± 100.5 min, the blood loss was 1,240.6 ± 1,131.8 mL, and 59 cases (48.8%) required intraoperative blood transfusion, resulting in a statistically significantly longer operative time, lower blood loss, and fewer cases of blood transfusion in the LALRs (P < 0.001, P < 0.001, P = 0.001, respectively).
Comparison of intraoperative factors between OALRs and LALRs
Variables | OALRs (n = 121) | LALRs (n = 95) | P-value | |
Initial resection, % | 105 (86.8) | 91 (95.8) | 0.032 | |
Approach | open | 121 (100.0) | ||
pure | 67 (70.5) | |||
hybrid | 17 (18.5) | |||
HALS | 7 (7.6) | |||
conversion | 4 (4.2) | |||
Procedure | Hemihepatectomy, % | 47 (38.8) | 30 (31.6) | 0.317 |
left hepatectomy, % | 21 (17.4) | 15 (15.8) | 0.855 | |
Right hepatectomy, % | 26 (21.5) | 15 (15.8) | 0.301 | |
Sectionectomy, % | 30 (24.8) | 27 (28.4) | 0.641 | |
Anterior sectionectomy, % | 10 (8.3) | 1 (1.1) | 0.025 | |
Medial sectionectomy, % | 6 (5.0) | 2 (2.1) | 0.471 | |
Posterior sectionectomy, % | 8 (6.6) | 6 (6.3) | 1.000 | |
Left lateral sectionectomy, % | 7 (5.8) | 18 (18.9) | 0.005 | |
Segmentectomy, % | 48 (39.7) | 38 (40.0) | 1.000 | |
Operative duration, min | 356.3 ± 100.5 | 523.0 ± 186.5 | < 0.001 | |
Blood loss, mL | 1,240.6 ± 1,131.8 | 592.1 ± 911.7 | < 0.001 | |
Intraoperative transfusion, % | 59 (48.8) | 25 (26.3) | 0.001 |
In terms of postoperative complications, there was one 30-day postoperative death in the OALRs (0.8%) and one 90-day postoperative death in the OALRs (0.8%) compared with none in the LALRs (P = 1.000 and P = 1.000, respectively) [Table 3]. Regarding infectious complications, ISSIs were observed in 1 case (1.1%) in LALRs and 9 cases (7.4%) in OALRs, which was statistically significantly less in LALRs (P = 0.045). OSSIs were observed in 5 cases (5.3%) in LALRs and 7 cases (5.8%) in OALRs (P = 1.000). There were no significant differences between the two groups. Details of cases with OSSIs are shown in Table 4. In the OSSI cases, bile leakage was observed in 4 cases (57.1%) in OALRs and 4 cases (80.0%) in LALRs. In Table 3, bile leakage was observed in 6 cases (6.3%) in LALRs and 10 cases (8.3%) in OALRs, with no difference between the two groups (P = 0.794). On the other hand, it showed a strong correlation between bile leak and OSSIs in Table 5 (P < 0.001). No cases of cholangitis were observed in either group. Catheter-related bloodstream and urinary tract infections were observed in 1 case (0.8%), respectively, in OALRs, but none in LALRs (all P = 1.000). No cases of pneumonia and enteritis were observed in either group. Sepsis was observed in 1 case (0.8%) in OALRs, but none in LALRs (P = 1.000). Antimicrobial resistance bacteria were detected postoperatively in 2 patients (1.7%) in OALRs and two patients (2.1%) in LALRs (P = 1.000). MRSA was detected in all four cases and found in the bile juice and wound in LALRs [Table 6]. There were no cases of steroid use, liver cirrhosis, or preceding chemotherapy in these four cases. In Table 3, no cases of gastrointestinal bleeding were observed in either group. Intraperitoneal bleeding occurred in 1 patient (0.8%) in OALRs, not LALRs (P = 1.000). No cases of ileus, DVT, and PVT were observed in either group. Liver failure was detected in 2 patients (1.7%) in OALRs; one patient expired due to liver failure, but none in LALRs (P = 0.505). In the CD, 3b or higher cases were observed, with one case (1.1%) performed reoperation for biliary peritonitis due to accidental removal of a biliary drainage tube in LALRs and 2 cases (1.6%) in OALRs. The postoperative hospital stay was 14.8 ± 16.5 days in LALRs and 20.7 ± 18.9 days in OALRs, with significantly shorter hospitalization in LALRs (P = 0.017). Univariate and multivariate analyses were used to reveal those factors predicting ISSIs. In Table 7, univariate analysis of LALRs on the incidence of ISSIs showed that two factors were extracted and identified as being useful for discriminating between those who would develop ISSIs: BMI ≥ 29.2 kg/m2 (P = 0.042), Operative duration ≥ 871 min (P = 0.032). Multivariate logistic regression analysis revealed no predictive factor for developing ISSIs. On the other hand, in univariate analysis of OALRs, four factors were extracted and identified as being useful for discriminating between those who would develop ISSIs: Operative duration ≥ 388 min (P = 0.001), Blood loss ≥ 1,786 mL (P < 0.001), Transfusion yes (P = 0.015), and OSSIs yes (P < 0.001) [Table 8]. Multivariate logistic regression analysis of OALRs revealed that OSSIs (Odds ratio 31.200, 95%CI: 2.380-409.000, P = 0.009) were the significant predictive factors for developing ISSIs.
Comparison of postoperative factors between OALRs and LALRs
Variables | OALRs (n = 121) | LALRs (n = 95) | P-value | |
30-day mortality, days | 1 (0.8) | 0 (0.0) | 1.000 | |
90-day mortality, days | 1 (0.8) | 0 (0.0) | 1.000 | |
Incisional SSIs, % | 9 (7.4) | 1 (1.1) | 0.045 | |
Organ/space SSIs, % | 7 (5.8) | 5 (5.3) | 1.000 | |
Bile leakage, % | 10 (8.3) | 6 (6.3) | 0.794 | |
Cholangitis, % | 0 (0.0) | 0 (0.0) | NA | |
Gastro-intestinal bleeding, % | 0 (0.0) | 0 (0.0) | NA | |
Intraabdominal bleeding, % | 1 (0.8) | 0 (0.0) | 1.000 | |
Ascites, % | 2 (1.7) | 0 (0.0) | 0.505 | |
Pleural effusion, % | 2 (1.7) | 1 (1.1) | 1.000 | |
Heart failure, % | 0 (0.0) | 0 (0.0) | NA | |
Renal dysfunction, % | 2 (1.7) | 0 (0.0) | 0.505 | |
Ileus, % | 0 (0.0) | 0 (0.0) | NA | |
Deep vein thrombosis, % | 0 (0.0) | 0 (0.0) | NA | |
Portal vein thrombosis, % | 0 (0.0) | 0 (0.0) | NA | |
Liver failure, % | 2 (1.7) | 0 (0.0) | 0.505 | |
Pneumonia, % | 0 (0.0) | 0 (0.0) | NA | |
CRBSI, % | 1 (0.8) | 0 (0.0) | 1.000 | |
Enteritis, % | 0 (0.0) | 0 (0.0) | NA | |
UTI, % | 0 (0.0) | 0 (0.0) | NA | |
AMR bacteria, % | 2 (1.7) | 2 (2.1) | 1.000 | |
Clavian-Dindo | < IIIa, % | 119 (98.3) | 94 (98.9) | 1.000 |
clasification | IIIb, % | 0 (0.0) | 1 (1.1) | 0.440 |
IVa, % | 1 (0.8) | 0 (0.0) | 1.000 | |
IVb, % | 0 (0.0) | 0 (0.0) | NA | |
V, % | 1 (0.8) | 0 (0.0) | 1.000 | |
Hospital stay, days | 20.7 ± 18.9 | 14.8 ± 16.5 | 0.017 |
Details of cases with OSSIs
Case | Diagnosis | Inslin use | CRD | Steroid use | LC | Preceding chemotherapy | Approach | Procedure | ISSIs | Bile leakage |
1 | Mets | Negative | Positive | Negative | Negative | Positive | OALRs | Sectionectomy (Post) | Positive | Positive |
2 | ICC | Negative | Negative | Negative | Negative | Negative | OALRs | Sectionectomy (Ante) | Positive | Positive |
3 | ICC | Negative | Positive | Negative | Negative | Negative | OALRs | Segmentectomy (S6) | Positive | Negative |
4 | HCC | Negative | Negative | Negative | Negative | Negative | OALRs | Hemihepatectomy (Lt) | Negative | Negative |
5 | HCC | Negative | Positive | Negative | Positive | Positive | OALRs | Hemihepatectomy (Rt) | Positive | Negative |
6 | HCC | Negative | Negative | Negative | Negative | Negative | OALRs | Segmentectomy (S7) | Negative | Positive |
7 | HCC | Negative | Negative | Negative | Negative | Negative | OALRs | Sectionectomy (Ante) | Negative | Positive |
8 | HCC | Positive | Positive | Negative | Negative | Negative | LALRs | Segmentectomy (S4a + S5) | Negative | Positive |
9 | HCC | Negative | Negative | Negative | Negative | Negative | LALRs | Segmentectomy (S5) | Negative | Positive |
10 | HCC | Positive | Negative | Negative | Negative | Negative | LALRs | Sectionectomy (Ante) | Negative | Negative |
11 | HCC | Negative | Negative | Negative | Negative | Negative | LALRs | Hemihepatectomy (Rt) | Negative | Positive |
12 | HCC | Positive | Positive | Negative | Negative | Negative | LALRs | Hemihepatectomy (Rt) | Negative | Positive |
Relationship between bile leakage and OSSIs
Bile leakage | P-value | |||
negative | positive | |||
OSSIs | negative | 196 | 8 | < 0.001 |
positive | 4 | 8 |
Details of cases with antimicrobial resistance bacteria
Case | 1 | 2 | 3 | 4 |
Diagnosis | HCC | ICC | HCC | Intrahepatic calculosis |
Inslin use | Negative | Negative | Positive | Negative |
CRD | Negative | Negative | Positive | Negative |
Steroid use | Negative | Negative | Negative | Negative |
LC | Negative | Negative | Negative | Negative |
Preceding chemotherapy | Negative | Negative | Negative | Negative |
Approach | OALRs | OALRs | LALRs | LALRs |
Procedure | Rt. hepatectomy | Sectionectomy (Ante) | Segmentectomy (S4a + 5dor) | Lt. hepatectomy |
ISSIs | Positive | Positive | Negative | Positive |
OSSIs | Negative | Positive | Positive | Negative |
Bile leakage | Negative | Positive | Positive | Negative |
Detected bacteria | MRSA | MRSA | MRSA | MRSA |
Detected site | Wound | Drain | Bile | Wound |
Univariate and multivariate analyses of the predictive factors for incisional surgical site infection in laparoscopic anatomical liver resections
Variables | No. patients (n = 95) | Univariate analysis | Multivariate analysis | ||
Odds ratio (95%CI) | P-value | Odds ratio (95%CI) | P-value | ||
Age (years) | |||||
≥ 76/< 76 | 15/80 | infimum (0.137-infimum) | 0.158 | ||
Gender | |||||
male/female | 66/29 | infimum (0.011-infimum) | 1.000 | ||
Body mass index | |||||
≥ 29.2 kg/m2/< 29.2 kg/m2 | 4/91 | infimum (0.583-infimum) | 0.04 | infimum (0.295-infimum) | 0.999 |
Malignant disease | |||||
yes/no | 79/16 | 0.000 (0.000-7.899) | 0.168 | ||
Smoke | |||||
yes/no | 63/32 | 0.000 (0.000-19.810) | 0.337 | ||
Diabetes mellitus | |||||
yes/no | 23/72 | 0.000 (0.000-121.856) | 1.000 | ||
Chronic renal disease | |||||
yes/no | 26/69 | 0.000 (0.000-103.335) | 1.000 | ||
Steroid use | |||||
yes/no | 2/93 | 0.000 (0.000-1763.556) | 1.000 | ||
Cirrhosis | |||||
yes/no | 11/84 | 0.000 (0.000-296.443) | 1.000 | ||
Tumor size (mm) | |||||
≥ 15/< 15 | 79/16 | 0.000 (0.000-7.899) | 0.168 | ||
Preoperative chemotherapy | |||||
yes/ no | 16/79 | 0.000 (0.000-191.988) | 1.000 | ||
Initial resection | |||||
yes/no | 91/4 | infimum (0.001-infimum) | 1.000 | ||
Operative duration (min) | |||||
≥ 871/< 871 | 3/92 | infimum (0.786-infimum) | 0.032 | infimum (0.295-infimum) | 0.999 |
Blood loss (mL) | |||||
≥ 1,100/< 1,100 | 15/80 | infimum (0.137-infimum) | 0.158 | ||
Transfusion | |||||
yes/no | 25/70 | 0.000 (0.000-109.016) | 1.000 | ||
Organ/ space surgical site infection | |||||
yes/no | 5/90 | 0.000 (0.000-694.394) | 1.000 | ||
Bile leakage | |||||
yes/no | 6/89 | 0.000 (0.000-573.327) | 1.000 |
Univariate and multivariate analyses of the predictive factors for incisional surgical site infection in open anatomical liver resections
Variables | No. patients (n = 121) | Univariate analysis | Multivariate analysis | ||
Odds ratio (95%CI) | P-value | Odds ratio (95%CI) | P-value | ||
Age (years) | |||||
≥ 75/< 75 | 27/94 | 3.060 (0.561-15.511) | 0.111 | ||
Gender | |||||
male/female | 85/36 | 3.607 (0.454-165.775) | 0.277 | ||
Body mass index | |||||
≥ 20.1 kg/m2/< 20.1 kg/m2 | 99/22 | infimum (0.442-infimum) | 0.362 | ||
Malignant disease | |||||
yes/no | 108/13 | 0.960 (0.111-46.103) | 1.000 | ||
Smoke | |||||
yes/no | 84/37 | 0.873 (0.174-5.707) | 1.000 | ||
Diabetes mellitus | |||||
yes/no | 32/89 | 0.329 (0.007-2.628) | 0.442 | ||
Chronic renal disease | |||||
yes/no | 34/87 | 2.171 (0.403-10.845) | 0.267 | ||
Steroid use | |||||
yes/no | 2/119 | 0.000 (0.000-69.190) | 1.000 | ||
Cirrhosis | |||||
yes/no | 10/109 | 1.398 (0.028-12.713) | 0.559 | ||
Tumor size (mm) | |||||
≥ 15/< 15 | 105/16 | infimum (0.295-infimum) | 0.605 | ||
Preoperative chemotherapy | |||||
yes/no | 35/86 | 1.248 (0.190-6.276) | 0.717 | ||
Initial resection | |||||
yes/no | 105/16 | infimum (0.295-infimum) | 0.605 | ||
Operative duration (min) | |||||
≥ 388/< 388 | 44/77 | 16.520 (2.085-755.923) | 0.001 | 8.250 (0.647-105.000) | 0.104 |
Blood loss (mL) | |||||
≥ 1,786/< 1,786 | 28/93 | 14.701 (2.561-154.736) | < 0.001 | 3.670 (0.400-33.600) | 0.250 |
Transfusion | |||||
yes/no | 59/62 | 9.425 (1.197-430.474) | 0.015 | 6.710 (0.217-208.000) | 0.277 |
Organ/ space surgical site infection | |||||
yes/no | 7/114 | 26.792 (3.557-238.232) | < 0.001 | 31.200 (2.380-409.000) | 0.009 |
Bile leakage | |||||
yes/no | 10/111 | 3.652 (0.320-24.225) | 0.162 |
DISCUSSION
For malignant liver tumors, there are a wide variety of treatments, including local ablation therapy, systemic chemotherapy, and trans-arterial chemo-embolization therapy, in addition to hepatectomy. Individuals have tailor-made these treatment strategies in recent years[12]. Therefore, there have been more opportunities to experience cases of liver resection after local therapy or chemotherapy in clinical practice. In addition, the number of elderly patients with coexisting major organ diseases is increasing due to the aging society, and the environment surrounding liver surgery is rapidly diversifying. On the other hand, gastrointestinal surgery has a higher incidence of postoperative infectious complications than surgery in other fields, and there are particularly many cases of SSIs in the hepato-biliary-pancreatic field[13]. Therefore, hepato-biliary-pancreatic surgeons must respond to various cases, including judging surgical suitability, dealing with major coexisting organ diseases, and taking perioperative infection control measures more than ever before.
Seventeen previous studies comparing LLRs and OLRs for SSIs, including our study, were found and presented in Table 9[14-29]. LLRs reduced ISSIs in six studies[15,19,20,28,29]. Five of these studies did not find that LLRs reduced OSSIs[15,19,20,29]. Two reports could suggest that LLRs can reduce the incidence of OSSIs[16,28]. Only one study showed that LLRs reduce both ISSIs and OSSIs[28]. These differences might be due to factors such as anatomical or non-anatomical procedures, HCC or other diseases, primary or recurrence, the number of patients, and selection bias between LLRs and OLRs. Data from this study showed that LALRs reduce ISSIs, which is the same as suggested in the report targeting ALRs by Takahara et al.[20].
Comparison the incidence of SSIs between OLRs and LLRs on the previous reports
Author | Year | Disease | Procedure | Patient number | ISSIs (%) | OSSIs (%) | |||||||||||||
Propensity score analysis | Propensity score analysis | Propensity score analysis | |||||||||||||||||
LLRs | OLRs | LLRs | OLRs | LLRs | OLRs | P-value | LLRs | OLRs | P-value | LLRs | OLRs | P-value | LLRs | OLRs | P-value | ||||
Kanazawa et al.[14] | 2013 | rHCC | nAR | 20 | 20 | 0.0 | 15.0 | 0.231 | 0.0 | 15.0 | 0.231 | ||||||||
Kanazawa et al.[15] | 2013 | HCC | nAR | 28 | 28 | 0.0 | 17.9 | 0.019 | 0.0 | 3.6 | 0.313 | ||||||||
López-Ben et al.[16] | 2014 | All | AR + nAR | 50 | 100 | 0.0 | 7.0 | 0.054 | 2.0 | 12.0 | 0.033 | ||||||||
Takahara et al.[17] | 2015 | HCC | AR + nAR | 436 | 2,969 | 387 | 387 | 0.3 | 1.0 | NA | 1.0 | 1.0 | NA | ||||||
Tanaka et al.[18] | 2015 | HCC | nAR | 28 | 57 | 20 | 20 | 0.0 | 4.0 | 1.000 | 0.0 | 5.0 | 1.000 | 0.0 | 5.0 | 0.550 | 0.0 | 5.0 | 1.000 |
Han et al.[19] | 2015 | HCC | NA | 88 | 88 | 1.1 | 5.7 | < 0.050 | 0.0 | 4.5 | NA | ||||||||
Takahara et al.[20] | 2016 | All | AR | 929 | 1,4262 | 929 | 929 | 1.6 | 3.4 | 0.004 | 1.6 | 3.9 | 0.004 | 2.9 | 4.6 | 0.021 | 2.9 | 4.3 | 0.135 |
Cheung et al.[21] | 2016 | HCC | NA | 110 | 330 | 3.6 | 2.1 | NA | NA | NA | NA | ||||||||
Noda et al.[22] | 2018 | rHCC | AR + nAR | 20 | 48 | 0.0 | 4.2 | NA | 0.0 | 4.2 | NA | ||||||||
Tanaka et al.[23] | 2019 | HCC | AR + nAR | 117 | 117 | 193 | 314 | 0.5 | 3.5 | 0.031 | 0.9 | 3.4 | 0.370 | 1.6 | 5.1 | 0.042 | 1.7 | 1.7 | 1.000 |
Onoe et al.[24] | 2020 | rHCC | AR + nAR | 30 | 42 | 0.0 | 2.4 | NA | 6.7 | 2.4 | NA | ||||||||
Shirai et al.[25] | 2022 | HCC | AR + nAR | 252 | 194 | 100 | 100 | NA | NA | NA | 1.0 | 2.0 | 0.568 | NA | NA | NA | 1.0 | 6.0 | 0.091 |
Bao et al.[26] | 2022 | rHCC | AR + nAR | 30 | 22 | 19 | 19 | 3.3 | 0.0 | 0.577 | 5.3 | 0.0 | 0.311 | NA | NA | NA | NA | NA | NA |
Monden et al.[27] | 2022 | HCC | AR + nAR | 133 | 145 | 75 | 75 | NA | NA | NA | NA | NA | NA | NA | NA | NA | 1.3 | 0.0 | NA |
Pu et al.[28] | 2023 | HCC | AR + nAR | 845 | 3031 | 845 | 845 | 1.8 | 6.3 | <0.001 | 1.8 | 8.4 | <0.001 | 1.8 | 4.6 | <0.001 | 1.8 | 5.2 | <0.001 |
Shinkawa et al.[29] | 2024 | HCC | nAR | 193 | 123 | 304 | 304 | NA | NA | NA | 1.8 | 7.6 | 0.025 | NA | NA | NA | 6.4 | 9.7 | 0.380 |
Maeda | 2024 | All | AR | 95 | 121 | 1.1 | 7.4 | 0.045 | 5.3 | 5.8 | 1.000 |
OSSIs are considered to be related to ISSIs[30]. However, LALRs have smaller wounds and can also achieve sufficient drainage of the surgical site by drains in our LALRs. In univariate analysis of LALRs, the ISSIs showed statistically significant differences in BMI and operative duration as predictive factors for ISSIs. However, no significant predictive factors were found in multivariate analysis. Therefore, no association was found between ISSIs and OSSIs in LALRs; that is a rationale for LALRs to reduce the ISSIs in our study.
Although our study showed no significant difference in the reduction of OSSIs due to minimally invasive anatomical hepatectomy, eight reports of non-anatomical hepatectomy showed a tendency to reduce OSSIs[14-16,18,22,25,28,29]. In general, risk factors for OSSIs include obesity[31], smoking[32], and cirrhosis[33,34]. In addition, diseases and surgical procedures include intrahepatic stones, repeat hepatectomy, long-duration surgery[13], bi-lobal resections, and excessive bleeding[33]. In addition, postoperative factors, including long-term placement of abdominal drains[35], liver failure[36], and bile leakage[35,36], are suggested to be the risk factors for OSSIs. While cases are becoming more diverse, bile leakage is still considered to be the most essential factor associated with OSSIs in clinical practice. Although the risk factors for bile leakage are similar to those for OSSIs, difficult anatomical hepatectomies such as central bi-sectionectomy, anterior sectionectomy, medial segmentectomy, and caudate lobectomy are also considerable for high-risk procedures for bile leakage. Therefore, we considered that OSSIs were not improved by LALRs due to bile leakage.
In recent years, in the field of hepatectomies, as well as advances in various surgical techniques and perioperative management, improvements in equipment have been made in liver surgery. As a result, postoperative complications and surgical outcomes have been improving. The superiority of laparoscopic surgery, including its minimal invasiveness, has already been reported compared to laparotomy, and the magnified vision effect allows for precise surgery. However, bile leakage still occurs at a specific frequency in liver surgery. Further expansion of the indications for minimally invasive hepatectomies is expected for the highly complex procedure in the future; efforts to reduce the incidence of bile leakage are encouraged to take advantage of minimally invasive surgery. Standardizing the surgical procedure for the surgical team, confirming and sharing the detailed anatomy with imaging before surgery within the surgical team, identifying the actual anatomy with a good field of view during surgery, and reducing the surgery duration and blood loss are the bandle to do for the reduction of bile leakage.
Although this study is limited by its single center, we conclude that minimally invasive anatomical hepatectomy can reduce ISSIs. Further investigation with multicenter studies should be needed in the future.
DECLARATIONS
Authors’ contributions
Made substantial contributions to conception and design of the study and performed data acquisition, analysis and interpretation: Maeda T, Otsuka Y
Performed data acquisition and provided administrative, technical, and material support: Ito Y, Hosaka H, Yamazaki S, Kajiwara Y, Onishi K, Okada R, Matsumoto Y, Kimura K, Ishii J, Tsuchiya M
Availability of data and materials
The raw data supporting the conclusions of this article will be made available by the authors.
Financial support and sponsorship
None.
Conflicts of interest
All authors declared that there are no conflicts of interest.
Ethical approval and consent to participate
This study was reviewed and approved (No. M22194 21242) by the ethics committee of Toho University Omori Medical Center, Japan. The details about the study were disclosed on the web page of Toho University Omori Medical Center (https://www.lab.toho-u.ac.jp/med/omori/gastro_surgery/patient/crl21600000000ku-att/20230214_M22194_21242.pdf), and the potential participants were given the opportunity to opt-out. Informed consent from participants in the study has been waived by the ethics committee of Toho University Omori Medical Center due to the retrospective study.
Consent for publication
Not applicable.
Copyright
© The Author(s) 2025.
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Maeda, T.; Ito, Y.; Hosaka, H.; Yamazaki, S.; Kajiwara, Y.; Onishi, K.; Okada, R.; Matsumoto, Y.; Kimura, K.; Ishii, J.; Tsuchiya, M.; Otsuka, Y. Does minimally invasive anatomical hepatectomy reduce surgical site infections?. Mini-invasive. Surg. 2025, 9, 2. http://dx.doi.org/10.20517/2574-1225.2024.79
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