Abstract
Background & aims
Although laparoscopic liver resection (LLR) has been widely accepted and considered a safe alternative to open liver resection in patients with hepatocellular carcinoma (HCC), it is still inevitable that some patients will encounter difficulties during LLR and need to be converted to open liver resection (OLR). It is currently uncertain whether unplanned intraoperative conversion to open liver resection (UCOLR) during LLR in HCC patients has a negative impact on patient prognosis, and there are still no comparative studies between HCC patients who underwent successful LLR and those who underwent UCOLR. Therefore, the aim of this study was to compare the short- and medium-term outcomes of LLR and UCOLR for HCC between two matched groups.
Methods
We retrospectively studied patients with HCC who underwent LLR or UCOLR between November 2016 and November 2022 at West China Hospital, Sichuan University. After 1:4 propensity score matching (PSM) was performed to reduce selection bias, the short-term and medium-term oncological outcomes of LLR and UCOLR were compared.
Results
Out of 846 patients included in this study (806 in the LLR group and 40 in the UCOLR group), 150 patients in the LLR group and 40 patients in the UCOLR group were selected for further comparison after 1:4 PSM. Compared to those who underwent successful LLR, patients who experienced UCOLR during LLR had significantly more intraoperative bleeding (500 ml vs. 200 ml, p < 0.001), required more blood transfusions (p < 0.001), had higher transfusion rates (47.5% vs. 6.0%, p < 0.001), and experienced longer operative times (244 min vs. 210 min, p = 0.042). Additionally, the overall complication rate was significantly greater in the UCOLR group than in the LLR group (45.0% vs. 20.7%, p = 0.002). Further analysis revealed that patients in the UCOLR group had a significantly greater risk of pulmonary infections (37.5% vs. 15.3%, p = 0.002), pleural effusion (27.5% vs. 7.3%, p < 0.001), anemia (22.5% vs. 4.7%, p < 0.001), and bile leakage (10.0% vs. 2.0%, p = 0.017). Moreover, those who experienced conversion to UCOLR reported significantly more postoperative pain (62.5% vs. 7.3%, p < 0.001) and longer hospital stays (6 days vs. 5 days, p = 0.005). In terms of quality of life (QOL) assessment, the LLR group showed a trend toward better general health at 1 and 3 months after surgery. However, no significant differences were detected between the LLR and UCOLR groups in terms of 3-year disease-free survival (76.4% for LLR vs. 63.5% for UCOLR, p = 0.075) or overall survival (82.2% for LLR vs. 71.7% for UCOLR, p = 0.124).
Conclusion
Compared to patients who underwent successful LLR, patients in the UCOLR group experienced worse short-term outcomes, although medium-term survival outcomes at 3 years were comparable. Additionally, segment 7 or 8 lesions with high AFP have a greater chance of conversion and an increased rate of recurrence after unplanned conversion. We should be cautious while selecting patient for laparoscopic liver resection.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12957-025-03984-y.
Keywords: Hepatectomy, Hepatocellular carcinoma, Laparoscopic, Conversion
Introduction
Since the first report of laparoscopic liver resection (LLR) in 1991 [1], LLR has become an acceptable standard procedure for treating hepatocellular carcinoma (HCC) [2–6]. This is because LLR has comparable long-term oncologic outcomes to open liver resection (OLR) [2, 7, 8] and better perioperative outcomes than OLR, including faster recovery [9], shorter hospital stays [10, 11], less blood loss [12], and fewer complications. However, for reasons such as tumor diameter, location, degree of cirrhosis, difficulty with intraoperative hemostasis, and extent of resection [13, 14], even experienced surgeons may still need to convert some patients to OLR. According to reports, an average of approximately 10% of patients who underwent LLR experienced conversion to OLR [15], and the conversion rate for laparoscopic major liver resection patients can reach 20% [16–18]. Nevertheless, as there is still no comparative study between HCC patients who underwent successful LLR and those who underwent unplanned intraoperative conversion to open liver resection (UCOLR), it is currently unknown whether UCOLR in HCC patients would affect the aforementioned advantages of LLR, and additionally, it is still uncertain whether UCOLR in HCC patients would have a negative impact on their prognosis.
Currently, many studies have explored the risk factors for UCOLR during LLR, such as older patients, patients with a high body mass index, patients with cirrhosis, patients with tumors located in the posterior superior segments of the liver, patients who underwent major resection, patients with greater intraoperative blood loss, and surgeons in the early stages of the learning curve [13–15, 19]; additionally, scoring systems have also been developed [20]. Moreover, some studies have reported increased morbidity and perioperative mortality in patients who were unexpectedly converted to OLR during LLR [21, 22], but few studies have focused on the impact of unplanned conversion on the long-term prognosis of HCC patients.
Furthermore, it is important to note that for unexpected surgical events, such as the UCOLR discussed in this article, it is difficult to perform prospective and randomized comparisons. Therefore, no prospective randomized comparative studies have been conducted to compare the short- and long-term outcomes of LLR and UCOLR thus far. In this study, we retrospectively compared the short- and medium-term outcomes of HCC patients who underwent LLR or UCOLR based on propensity score matching analysis.
Methods
Patient selection
Patients with HCC who underwent either successful LLR or experienced UCOLR during LLR at West China Hospital between November 2016 and November 2022 were retrospectively analyzed using data from a prospectively established database, the West China Laparoscopic Hepatectomy Database. The follow-up cutoff was May 2024, and the median follow-up time was calculated using the reverse Kaplan-Meier method. The inclusion criteria were as follows: (1) patients who underwent laparoscopic hepatectomy or unplanned conversion during laparoscopic hepatectomy; (2) patients over 18 years of age; (3) patients with Child A/B liver function; and (4) patients whose postoperative pathology confirmed HCC. The exclusion criteria included (1) postoperative pathology indicating mixed hepatocellular carcinoma (hepatocellular carcinoma-cholangiocarcinoma) or metastatic hepatic carcinoma; (2) HCC with invasion into the first hepatic hilum, second hepatic hilum, or inferior vena cava; (3) inability to tolerate intraoperative pneumoperitoneum; and (4) tumors with diaphragmatic invasion leading to dense adhesions.
The patients were categorized into two groups based on the surgical approach: the LLR group and the UCOLR group. The choice of surgical procedure was made after discussions with the patients and their families, taking into account their preferences. The operating surgeons were skilled in both laparoscopic and open hepatectomy. This study was approved by the Ethics Committee of West China Hospital, Sichuan University (Ethics No: 2023 − 1928).
Preoperative evaluation
All patients underwent comprehensive preoperative laboratory evaluation, including full blood count, coagulation tests, liver function tests, hepatitis B serology, hepatitis C antibody, and serum alpha-fetoprotein (AFP) analysis. Medical imaging evaluations, including chest radiographs or chest computed tomography (CT) scans, abdominal ultrasonography, abdominal CT, and/or abdominal magnetic resonance imaging, were also performed to assess tumor resectability. Moreover, to assess liver functional reserve, all patients underwent an indocyanine green 15-minute retention test. After consensus was reached on the resectability of the tumor in a multidisciplinary meeting, the patient was scheduled for surgery.
Surgical procedures
For LLR, patients are generally placed in a supine position and, in some cases, may also be placed in a left decubitus position for right posterior sectionectomy. All LLRs were performed under general anesthesia. During LLR, surgeons usually create five incisions in the abdominal wall. A laparoscope was placed around the umbilicus using a 12-mm hole. Carbon dioxide was insufflated to establish pneumoperitoneum, and the intra-abdominal pressure was maintained at approximately 13 mmHg. Two more 12-mm incisions and two 5-mm incisions were made for the surgical operation. To confirm the location of the tumor and guide the resection, laparoscopic ultrasonography was routinely used. To control blood loss, the Pringle maneuver was performed while maintaining low central venous pressure (within 5 mmHg). Harmonic scalpels (Ethicon, EndoSurgery, USA) are commonly used for transecting superficial parenchyma, while laparoscopic cavitron ultrasonic surgical aspirators (CUSA, Valleylab, Inc., USA) or Ligasure (Valleylab, Inc., USA) are frequently used for deeper parenchyma transactions. Small branches (≤ 5 mm) of Glisson pedicles and hepatic veins were ligated using Hem-o-lock clips (Weck Surgical Instruments), and the main Glisson pedicle or hepatic vein was transected using a laparoscopic linear stapler (Endopath Endocutter; Ethicon Endo-surgery). The resected specimen was placed in a plastic bag and extracted through either a suprapubic or an upper abdominal midline incision. After hemostasis and irrigation of the resected liver surface, a drainage tube is routinely placed near the surgical site [23, 24].
During the UCOLR procedure, the patient is repositioned from the left lateral position to the supine position, and the surgery is then performed through a right subcostal incision. Intraoperative ultrasonography was routinely used, as was LLR. The Pringle maneuver was performed in response to massive bleeding. The liver parenchyma was also transected using an ultrasonic scalpel.
Postoperative management and follow-up
On the 1 st, 3rd, and 5th postoperative days, each patient routinely underwent complete blood count, liver and renal function, and coagulation function tests. After being discharged from the hospital, all patients received regular follow-up as described below: (1) Once a month for the first 6 months, we performed a complete blood count, liver function test, coagulation function test, serum AFP level test, and abdominal ultrasonography. (2) Six months after surgery, if the patient’s liver function had recovered well and there was no sign of tumor recurrence, we performed the above examinations every 3 months for regular follow-up until the patient’s death. (3) If there were signs of tumor recurrence, additional examinations, such as chest CT, abdominal contrast-enhanced CT, or abdominal contrast-enhanced MRI, were needed.
Outcomes
The primary outcomes measured in this study were intraoperative variables and short-term postoperative outcomes. The intraoperative variables assessed included operative time, blood loss, blood transfusion, and transfusion rate. The short-term postoperative outcomes included length of hospital stay, total hospitalization costs, postoperative pain scores, rates of various complications, and quality of life scores at 1 and 3 months after surgery. Additionally, the secondary outcomes were 3-year disease-free survival (DFS) and overall survival (OS) for the two matched groups.
QOL assessment
QOL generally refers to the assessment of a patient’s status across three main aspects: physical health, psychological well-being, and social functioning. QOL has increasingly become an important measure for evaluating surgical outcomes. Among the various tools available for assessing QOL, the Short Form-36 (SF-36) Health Survey is a widely recognized and validated questionnaire [25]. The SF-36 evaluates eight different domains of health quality: physical functioning (PF), role-physical (RP), bodily pain (BP), general health (GH), vitality (VT), social functioning (SF), role-emotional (RE), and mental health (MH). The questionnaire consists of 36 items, with each domain containing between 2 and 10 items, scored on a scale from 0 to 100, where 0 represents the worst health status and 100 the best [26]. In this study, the SF-36 questionnaire was used to assess patients’ quality of life at 1 and 3 months postsurgery. The surveys were conducted either during clinic visits, via telephone, or by e-mail, depending on the patient’s preference and availability. This approach allowed us to obtain a comprehensive view of the patients’ recovery and overall well-being following surgery.
Definitions
Unplanned conversion was defined as open surgery for any reason other than extraction of the resected specimen during LLR. IWATE Criteria is a scoring system for the difficulty of laparoscopic hepatectomy that includes the following 6 dimensions: (1) tumor size (score, 0 or 1); (2) tumor location (score, 1–5); (3) proximity to major blood vessels (score, 0 or 1); (4) liver function (score, 0 or 1); (5) HALS/hybrid (score, 0 or −1); and (6) extent of hepatic resection (score, 0–4). Based on the total score, the following 4 levels of difficulty were categorized: low (0–3), intermediate (4–6), advanced (7–9), and expert difficulty (10–12) [27]. R0 resection indicates complete removal of the tumor with clean margins as determined by the naked eye during surgery and confirmed by pathological examination, with no residual cancer cells [28]. Liver failure is diagnosed when the serum bilirubin level exceeds 50 µmol/L on postoperative day 5 and the prothrombin time is less than 50% [29]. Bile leakage is defined as the concentration of bilirubin in the abdominal drain being three times greater than that in the serum on or after postoperative day 3 [30]. Postoperative anemia was defined as a postoperative hemoglobin level less than 90 g/L and within the normal range preoperatively. Hemorrhage is defined as a postoperative decrease in hemoglobin of more than 3 g/dL from the postoperative baseline and/or postoperative transfusion of red blood cells due to decreased hemoglobin [31]. Thirty-day or 90-day mortality was defined as death within 30 or 90 days after surgery. DFS was defined as the time interval from the date of surgery to the date of the first diagnosis of HCC recurrence or the date of the last follow-up. OS was calculated from the date of surgery to the date of death or the date of the last follow-up.
Statistical analysis
To reduce selection bias caused by different covariate distributions in the LLR and UCOLR groups, we conducted propensity score matching (PSM) at a 1:4 ratio, which maximizes the use of the available data and produces more reliable results. Multivariate logistic regression analysis was performed to calculate the PS of each subject, which included the following variables: age, sex, hepatitis status, history of previous upper abdominal surgery, Child‒Pugh class, laboratory indicators (hemoglobin, aminotransferases, albumin, total bilirubin, coagulation time, etc.), AFP level, maximal tumor diameter, number of tumors, and location of tumors. The matching caliper value was set to 0.02. The baseline characteristics of the patients were analyzed using appropriate statistical tests. Continuous variables are expressed as medians (ranges) or means ± standard deviations and were compared using the Mann‒Whitney U test or Wilcoxon rank test. Categorical variables are expressed as frequencies (percentages) and were analyzed using the Pearson chi-square test or Fisher’s exact test. Survival data were analyzed using Kaplan‒Meier analysis and compared using the log-rank test. A significance level of P < 0.05 was used. Statistical analysis and PSM were conducted using SPSS software version 22.0 (IBM SPSS Inc., Chicago, IL).
Results
A total of 846 patients with HCC, such as those with cholangiocellular carcinoma, HCC-cholangiocellular carcinoma, and metastatic carcinoma, and those who were lost to follow-up after hospital discharge, were ultimately enrolled in the study. Following a 1:4 PSM process, 190 patients were matched, with 150 in the LLR group and 40 in the UCOLR group.
Baseline patient characteristics
The baseline characteristics of the 846 HCC patients with HCC before and after PSM are presented in Tables 1 and 2, respectively. Significant differences in the following characteristics were detected between the LLR and UCOLR groups before matching: alanine transaminase (ALT) level (p = 0.066), aspartate transaminase (AST) level (p = 0.034), history of upper abdominal surgery (p = 0.043), and maximal tumor diameter (p < 0.001). However, after PSM, the baseline characteristics of the two groups were well balanced, indicating that the matching process successfully minimized the differences in these key parameters.
Table 1.
Baseline characteristics of patients with hepatocellular carcinoma (Before PSM)
| UCOLR(n = 40) | LLR(n = 806) | P Value | SMD | |
|---|---|---|---|---|
| Age(y) | 53(26–77) | 56(21–87) | 0.198 | 0.225 |
| Sex | 0.802 | 0.049 | ||
| Male | 31(77.5%) | 638(79.2%) | ||
| Female | 9(22.5%) | 168(20.8%) | ||
| Basic liver disease | 0.591 | 0.078 | ||
| Yes | 34(85.0%) | 658(81.6%) | ||
| No | 6(15.0%) | 148(18.4%) | ||
| HBV | 34(85.0%) | 644(79.9%) | 0.430 | 0.125 |
| HCV | 2(5.0%) | 36(4.5%) | 0.874 | 0.048 |
| Child–Pugh class | 0.988 | < 0.001 | ||
| A | 36(90.0%) | 726(90.1%) | ||
| B | 4(10.0%) | 80(9.9%) | ||
| HB(g/L) | 140.1 ± 15.8 | 137.4 ± 17.9 | 0.339 | 0.151 |
| RBC(10^12/L) | 4.6 ± 0.6 | 4.5 ± 0.6 | 0.228 | 0.208 |
| PLT (10^9/L) | 144(62–246) | 140(28–536) | 0.434 | 0.075 |
| ALT (IU/L) | 25(8–51) | 27(8-885) | 0.066 | 0.334 |
| AST (IU/L) | 24(12–43) | 25(2-835) | 0.034 | 0.320 |
| Albumin (g/L) | 42.0 ± 4.9 | 41.7 ± 5.4 | 0.874 | 0.046 |
| Total bilirubin (umoI/L) | 13.3(6.8–25.7) | 13.5(2.4–98.2) | 0.470 | 0.145 |
| Prothrombin time (s) | 11.6 ± 1.2 | 11.7 ± 1.3 | 0.839 | 0.016 |
| AFP (ng/mL) | 0.772 | 0.054 | ||
| < 400 | 34(85.0%) | 671(83.3%) | ||
| ≥ 400 | 6(15.0%) | 135(16.7%) | ||
| Epigastrium surgery history | 4(10.0%) | 192(23.8%) | 0.043 | 0.348 |
| Tumor diameter (cm) | 6.3(1.6–10.0) | 4.0(0.8–13.0) | < 0.001 | 0.560 |
| Tumor diameter | < 0.001 | 0.648 | ||
| ≥ 3 cm | 30(75.0%) | 348(43.2%) | ||
| < 3 cm | 10(25.0%) | 458(56.8%) | ||
| Proximity to major vessel | 0.623 | 0.068 | ||
| No | 32(80.0%) | 718(89.1%) | ||
| Yes | 8(20.0%) | 88(10.9%) | ||
| Tumor location (Couinaud segment) | 0.247 | 0.193 | ||
| S1 | 2(5.0%) | 17(2.1%) | ||
| S2 | 1(2.5%) | 123(15.3%) | ||
| S3 | 2(5.0%) | 99(12.3%) | ||
| S4a | 1(2.5%) | 87(10.8%) | ||
| S4b | 6(15.0%) | 32(4.0%) | ||
| S5 | 6(15.0%) | 143(17.7%) | ||
| S6 | 4(10.0%) | 125(15.5%) | ||
| S7 | 8(20.0%) | 96(11.9%) | ||
| S8 | 10(25.0%) | 84(10.4%) | ||
| Extent of liver resection | 0.127 | 0.258 | ||
| Partial resection | 5(12.5%) | 278(34.5%) | ||
| Left lateral sectionectomy | 3(7.5%) | 86(10.7%) | ||
| Segmentectomy | 10(25.0%) | 124(15.4%) | ||
| Segmentectomy and more | 22(55.0%) | 318(39.4%) | ||
| Difficulty level (IWATE Criteria) | 0.036 | 0.478 | ||
| Low (0–3) | 4(10.0%) | 207(25.7%) | ||
| Intermediate (4–6) | 7(17.5%) | 268(33.3%) | ||
| Advanced (7–9) | 20(50.0%) | 202(25.0%) | ||
| Expert (10–12) | 9(22.5%) | 129(16.0%) |
AFP Indicates alpha-fetoprotein, HB Hemoglobin, RBC Erythrocyte, ALT Alanine aminotransferase, AST Aspartate aminotransferase, HBV Hepatitis B virus, HCV Hepatitis C virus, LLR Laparoscopic liver resection, UCOLR Unplanned conversion to open liver resection, PLT Platelet, PSM Propensity score matching
Table 2.
Baseline characteristics of patients with hepatocellular carcinoma (After PSM)
| UCOLR(n = 40) | LLR(n = 150) | P Value | SMD | |
|---|---|---|---|---|
| Age(y) | 53(26–77) | 54(26–80) | 0.429 | 0.162 |
| Sex | 0.454 | 0.154 | ||
| Male | 31(77.5%) | 124(82.7%) | ||
| Female | 9(22.5%) | 26(17.3%) | ||
| Basic liver disease | 0.872 | 0.028 | ||
| Yes | 34(85.0%) | 129(86.0%) | ||
| No | 6(15.0%) | 21(14.0%) | ||
| HBV | 34(85.0%) | 128(85.3%) | 0.958 | < 0.001 |
| HCV | 2(5.0%) | 9(6.0%) | 0.810 | 0.043 |
| Child–Pugh class | 0.646 | 0.091 | ||
| A | 36(90.0%) | 131(87.3%) | ||
| B | 4(10.0%) | 19(12.7%) | ||
| HB(g/L) | 140.1 ± 15.8 | 139.0 ± 18.7 | 0.788 | 0.062 |
| RBC(10^12/L) | 4.6 ± 0.6 | 4.5 ± 0.7 | 0.510 | 0.134 |
| PLT (10^9/L) | 144(62–246) | 142(38–276) | 0.997 | 0.015 |
| ALT (IU/L) | 25(8–51) | 24(8–95) | 0.930 | 0.005 |
| AST (IU/L) | 24(12–43) | 22(12–75) | 0.301 | 0.087 |
| Albumin (g/L) | 42.0 ± 4.9 | 41.3 ± 6.0 | 0.869 | 0.122 |
| Total bilirubin (umoI/L) | 13.3(6.8–25.7) | 13.5(5.9–35.3) | 0.693 | 0.079 |
| Prothrombin time (s) | 11.6 ± 1.2 | 11.7 ± 1.4 | 0.806 | 0.021 |
| AFP (ng/mL) | 0.656 | 0.078 | ||
| < 400 | 34(85.0%) | 123(82.0%) | ||
| ≥ 400 | 6(15.0%) | 27(18.0%) | ||
| Epigastrium surgery history | 4(10.0%) | 18(12.0%) | 0.725 | 0.062 |
| Tumor diameter (cm) | 6.3(1.6–10.0) | 4.0(0.8–13.0) | 0.455 | 0.087 |
| Tumor diameter | 0.756 | 0.047 | ||
| ≥ 3 cm | 30(75.0%) | 116(77.3%) | ||
| < 3 cm | 10(25.0%) | 34(22.7%) | ||
| proximity to major vessel | 0.778 | 0.043 | ||
| No | 32(80.0%) | 124(82.7%) | ||
| Yes | 8(20.0%) | 26(17.3%) | ||
| Tumor location (Couinaud segment) | 0.767 | 0.045 | ||
| S1 | 2(5.0%) | 4(2.7%) | ||
| S2 | 1(2.5%) | 1(0.7%) | ||
| S3 | 2(5.0%) | 6(4.0%) | ||
| S4a | 1(2.5%) | 3(2.0%) | ||
| S4b | 6(15.0%) | 24(16.0%) | ||
| S5 | 6(15.0%) | 22(14.7%) | ||
| S6 | 4(10.0%) | 14(9.3%) | ||
| S7 | 8(20.0%) | 33(22.0%) | ||
| S8 | 10(25.0%) | 43(28.7%) | ||
| Extent of liver resection | 0.545 | 0.067 | ||
| Partial resection | 5(12.5%) | 23(15.3%) | ||
| Left lateral sectionectomy | 3(7.5%) | 9(6.0%) | ||
| Segmentectomy | 10(25.0%) | 28(18.7%) | ||
| Segmentectomy and more | 22(55.0%) | 90(60.0%) | ||
| Difficulty level (IWATE Criteria) | 0.696 | 0.059 | ||
| Low (0–3) | 4(10.0%) | 13(8.7%) | ||
| Intermediate (4–6) | 7(17.5%) | 23(15.3%) | ||
| Advanced (7–9) | 20(50.0%) | 81(54.0%) | ||
| Expert (10–12) | 9(22.5%) | 33(22.0%) |
AFP Indicates alpha-fetoprotein, HB Hemoglobin, RBC Erythrocyte, ALT Alanine aminotransferase, AST Aspartate aminotransferase, HBV Hepatitis B virus, HCV Hepatitis C virus, LLR laparoscopic liver resection, UCOLR Unplanned conversion to open liver resection, PLT Platelet, PSM Propensity score matching
Intraoperative outcomes
Among the 40 patients in the UCOLR group, 17 patients were converted to open surgery due to uncontrollable intraoperative bleeding of approximately 800 ml or more, 13 conversions were necessitated by the proximity of the tumor to large blood vessels or the fragile structure of the tumor leading to rupture, and the remaining 10 conversions occurred due to either prolonged periods without progression or difficulties in surgical exposure.
Compared to the successful LLR group, the UCOLR group had a significantly longer operative time (244 min vs. 210 min, p = 0.042), significantly more blood loss (500 ml vs. 200 ml, p < 0.001), and significantly greater transfusion rate (47.5% vs. 6.0%, p < 0.001). However, there was no significant difference in the R0 resection rate between the two groups. These findings are summarized in Table 3.
Table 3.
Intraoperative data of patients with hepatocellular carcinoma (After PSM)
| UCOLR(n = 40) | LLR(n = 150) | P Value | |
|---|---|---|---|
| Resection margin | 0.599 | ||
| R0 | 39(97.5%) | 148(98.7%) | |
| R1 | 1(2.5%) | 2(1.3%) | |
| Operative time (min) | 244(155–345) | 210(60–535) | 0.042 |
| Blood loss (mL) | 500(60-2500) | 200(5-1000) | < 0.001 |
| IVC clamping Duration (min) | 50(10–158) | 45(0-176) | 0.324 |
| RBCs transfusion | 19(47.5%) | 9(6.0%) | < 0.001 |
| RBCs (mL) | 0(0-2500) | 0(0-800) | < 0.001 |
| Conversion | |||
| Uncontrolled bleeding | 17(42.5%) | ||
| Oncologic reason | 13(32.5%) | ||
| Technical reason | 10(25.0%) |
IVC Indicates inferior vena cava, LLR Laparoscopic liver resection, UCOLR Unplanned conversion to open liver resection, PSM Propensity score matching
Postoperative outcomes
Patients in the UCOLR group had a longer mean postoperative hospital stay than did those in the LLR group (6 days vs. 5 days, p = 0.005). Additionally, the percentage of patients with pain scores greater than 3 was significantly greater in the UCOLR group than in the LLR group (62.5% vs. 7.3%, p < 0.001). No significant differences were observed between the two groups with regard to peritoneal invasion, microvascular invasion, satellite foci, or pathologic grading. However, the overall complication rate was significantly greater in the UCOLR group than in the LLR group (45.0% vs. 20.7%, p = 0.002). There were also significant differences in the incidence of postoperative pulmonary infections (37.5% vs. 15.3%, p = 0.002), pleural effusion (27.5% vs. 7.3%, p < 0.001), anemia (22.5% vs. 4.7%, p < 0.001), and bile leakage (10.0% vs. 2.0%, p = 0.017), with the UCOLR group showing higher rates of each of these complications. In terms of total hospitalization costs, there was no significant difference between the two groups. A detailed analysis of these outcomes is provided in Table 4.
Table 4.
Postoperative data of patients with hepatocellular carcinoma (After PSM)
| UCOLR(n = 40) | LLR(n = 150) | P Value | |
|---|---|---|---|
| Capsular invasion | 12(30.0%) | 48(32.0%) | 0.809 |
| Microvascular invasion | 14(35.0%) | 45(30.0%) | 0.544 |
| Satellites | 4(10.0%) | 7(4.7%) | 0.199 |
| Postoperative stay (d) | 6(4–16) | 5(2–21) | 0.005 |
| Edmonson Steiner grade | 0.204 | ||
| I | 0(0) | 4(2.7%) | |
| II | 33(82.5%) | 104(69.3%) | |
| III | 7(17.5%) | 42(28.0) | |
| IV | 0(0) | 0(0) | |
| Pain score | < 0.001 | ||
| ≤ 3 | 15(37.5%) | 139(92.7%) | |
| > 3 | 25(62.5%) | 11(7.3%) | |
| Overall complications | 18(45.0%) | 31(20.7%) | 0.002 |
| Type of complication | |||
| Pulmonary infection | 15(37.5%) | 23(15.3%) | 0.002 |
| Pleural effusion | 11(27.5%) | 11(7.3%) | < 0.001 |
| Abdominal fluid | 3(7.5%) | 8(5.3%) | 0.602 |
| Pericardial effusion | 5(12.5%) | 17(11.3%) | 0.838 |
| Anemic | 9(22.5%) | 7(4.7%) | < 0.001 |
| Hemorrhage | 5(12.5%) | 7(4.7%) | 0.070 |
| Incision infection | 2(5.0%) | 3(2.0%) | 0.292 |
| Biliary leakage | 4(10.0%) | 3(2.0%) | 0.017 |
| Liver failure | 1(2.5%) | 5(3.3%) | 0.789 |
| Portal vein thrombosis | 1(2.5%) | 3(2.0%) | 0.845 |
| Deep venous thrombosis | 2(5.0%) | 6(4.0%) | 0.780 |
| Pulmonary embolism | 0(0) | 1(0.7%) | 0.605 |
| Clavien-Dindo grade | 0.020 | ||
| I | 8(20.0%) | 12(8.0%) | |
| II | 5(12.5%) | 9(6.0%) | |
| III | 4(10.0%) | 5(3.3%) | |
| IV | 1(2.5%) | 5(3.3%) | |
| V | 0(0) | 0(0) | |
| Total cost |
47,998 (27810–104856) |
46,735 (21052–56955) |
0.289 |
LLR Laparoscopic liver resection, UCOLR Unplanned conversion to open liver resection, PSM Propensity score matching
The descriptive statistics for the SF-36 scores at 1 and 3 months postsurgery in the LLR and UCOLR groups are presented in Tables 5 and 6, respectively. At 1 month postoperatively, there were no significant differences between the two groups for PF, RP, VI, SF, RE, or MH. However, the LLR group had significantly greater BP and GH scores than did the UCOLR group (P < 0.001 and P = 0.004, respectively) at 1 month. By 3 months postoperatively, only GH remained significantly greater in the LLR group than in the UCOLR group (P = 0.045).
Table 5.
Comparison of SF-36 scores between LLR group and UCOLR group (After PSM) 1 month postoperatively
| SF-36 items | UCOLR | LLR | P Value |
|---|---|---|---|
| Physical functioning | 65.4(11.8) | 65.3(11.3) | 0.432 |
| Role-physical | 65.6(17.6) | 70.5(21.7) | 0.179 |
| Bodily pain | 52.4(15.4) | 69.0(17.5) | < 0.001 |
| General health | 58.4(16.0) | 61.0(16.1) | 0.004 |
| Vitality | 63.9(12.6) | 61.6(14.1) | 0.699 |
| Social functioning | 64.4(13.4) | 67.4(19.6) | 0.303 |
| Role-emotional | 65.0(23.8) | 64.0(22.0) | 0.716 |
| Mental health | 69.3(15.0) | 72.7(12.0) | 0.287 |
LLR Laparoscopic liver resection, UCOLR Unplanned conversion to open liver resection, PSM Propensity score matching, SF-36 Short form-36 healthy survey
Table 6.
Comparison of SF-36 scores between LLR group and UCOLR group (After PSM) 3 months postoperatively
| SF-36 items | UCOLR | LLR | P Value |
|---|---|---|---|
| Physical functioning | 88.6(7.9) | 90.3(8.7) | 0.845 |
| Role-physical | 83.8(13.3) | 82.5(15.3) | 0.745 |
| Bodily pain | 88.7(11.9) | 90.7(12.5) | 0.160 |
| General health | 82.6(12.1) | 87.1(7.6) | 0.045 |
| Vitality | 83.6(10.3) | 84.2(13.6) | 0.392 |
| Social functioning | 81.3(11.0) | 81.4(17.4) | 0.506 |
| Role-emotional | 90.0(18.8) | 88.0(16.1) | 0.247 |
| Mental health | 83.3(11.9) | 86.0(11.2) | 0.126 |
LLR Laparoscopic liver resection, UCOLR Unplanned conversion to open liver resection, PSM Propensity score matching, SF-36 Short form-36 healthy survey
Medium-term oncological outcomes
Median follow-up was 39 months (range: 3–95 months). The overall survival rates at 1, 3, and 5 years postsurgery in the LLR group were 96.7%, 82.2%, and 72.7%, respectively, compared to 95.0%, 71.7%, and 61.7%, respectively, in the UCOLR group (Fig. 1). The differences in 3-year OS between the two groups were not statistically significant (p = 0.124). Regarding DFS, the rates at 1, 3, and 5 years postsurgery were 89.4%, 76.4%, and 72.8%, respectively, in the LLR group and 87.5%, 63.5%, and 63.5%, respectively, in the UCOLR group (Fig. 2). Although there was also no significant difference in 3-year DFS between the two groups (p = 0.075), the UCOLR group showed a notable downward trend in 5-year disease-free survival compared to the LLR group.
Fig. 1.
LLR, laparoscopic liver resection; UCOLR, unplanned conversion to open liver resection; PSM, propensity score matching; OS, overall survival 3-year Overall survival between the two groups after PSM (p = 0.124)
Fig. 2.
LLR, laparoscopic liver resection; UCOLR, unplanned conversion to open liver resection; PSM, propensity score matching; DFS, disease-free survival 3-year Disease-free survival between the two groups after PSM (p = 0.075)
Risk factor analysis
According to the univariate analysis, four factors were identified as having a negative impact on the 3-year OS rate: AFP level (≥ 400 ng/mL), Edmondson-Steiner grade (III + IV), Tumor size (≥ 3 cm) and Tumor location (S7 + S8). Multivariate Cox regression analysis confirmed these findings, showing that the AFP level (≥ 400 ng/mL), Edmondson-Steiner grade (III + IV) and Tumor location (S7 + S8) were independent risk factors for reduced long-term survival (Supplemental Table 1). For 3-year DFS, both univariate and multivariate Cox analyses indicated that AFP levels (≥ 400 ng/mL) and Edmondson-Steiner grade (III + IV) were risk factors associated with poorer outcomes (Supplemental Table 2).
Discussion
HCC is a common malignancy that ranked fourth in terms of morbidity and second in terms of mortality among all cancers in China in 2020 [32]. The use of laparoscopic hepatectomy has dramatically increased, and laparoscopic hepatectomy is considered a promising option for treating HCC. Despite this increase in adoption, the limitations of laparoscopic techniques and equipment have prevented laparoscopic hepatectomy from replacing open hepatectomy as the gold standard for hepatic resection [2]4– [8, 11, 12, 33]. A key concern is unplanned conversion during laparoscopic procedures and whether this affects patient prognosis. Current evidence on this topic is limited due to the lack of randomized controlled trials, with many existing studies having a broad patient inclusion scope or substantial baseline differences between successful LLR and UCOLR [34, 35]. This study aimed to address these issues by focusing specifically on HCC patients and utilizing 1:4 propensity score matching to balance the baseline characteristics.
The comparison of short-term outcomes in this study revealed that patients in the UCOLR group experienced greater intraoperative bleeding, a greater overall rate of postoperative complications, and a longer postoperative hospital stay. The leading cause of unplanned conversion was uncontrollable bleeding (greater than 800 ml), which accounted for 42.5% of cases [21, 22, 36]. Additionally, in the LLR group, techniques such as maintaining pneumoperitoneum throughout the procedure, intermittent Pringle maneuvers, and controlling central venous pressure lower than 5 mmHg during liver parenchyma resection contributed to reduced bleeding [37]. If the cause of conversion was mostly intraoperative bleeding, blood transfusion requirement would be more! Therefore, during the surgical process, surgical operation norms should be strictly followed to ensure the safety and effectiveness of the surgery. Countermeasures should be formulated in advance for possible complications, such as intraoperative bleeding and tumor rupture. In addition, minimally invasive surgical instruments should be used reasonably to reduce surgical trauma and shorten the operation time.
However, the potential adverse effects of unplanned conversion require further study. In this study, we found that the UCOLR group experienced significantly greater rates of postoperative lung infections and pleural effusions, with rates more than double those in the successful LLR group. Additionally, the risks of postoperative anemia and bile leakage were nearly five times greater in the UCOLR group, likely due to the larger abdominal incision, extended resection area, increased postoperative pain, and slower recovery, which impacts the patient’s ability to engage in breathing exercises and early mobilization [38]. This underscores the importance of preoperative chest CT evaluation, the use of perioperative antibiotics, and postoperative abdominal CT to reduce the risk of these complications. Enhanced postoperative pain management is also needed for patients who undergo unplanned conversion. In addition, special attention should be paid to the occurrence of postoperative complications, such as infection and bleeding, etc., and timely management should be carried out. At the same time, nutritional support and rehabilitation guidance for patients should be strengthened to promote rapid recovery.
The quality of life evaluations indicated that at one month postoperatively, the LLR group had higher scores in the bodily pain (BP) domain than did the UCOLR group. Nevertheless, this difference was not significant at three months. This finding aligns with the observation that a greater proportion of patients in the UCOLR group reported pain scores greater than 3. This may be related to the more intense and longer duration of pain experienced by these patients following open hepatectomy [39, 40]. Furthermore, the general health (GH) domain scores were greater in the LLR group at one and three months postoperatively, suggesting that unplanned conversion has a negative impact on the general health of patients in the short term after surgery. These outcomes may be influenced by various factors, and further studies are needed to evaluate the long-term QOL effects.
To date, few studies have investigated the impact of unplanned conversion to open surgery on the medium- and long-term survival of patients with HCC. Our study revealed that unplanned conversion did not lead to worse 3-year overall survival or disease-free survival, which contrasts with the findings of Zachary E. Stiles, Do et al., who reported that unplanned conversion was associated with poorer overall survival in a retrospective analysis of 1,270 laparoscopic hepatectomies [4]. The difference in outcomes may be attributed to the relatively small sample size in our study. However, by using propensity score matching, we were able to minimize selection bias, lending greater confidence to our results. The comparable mid-term oncologic outcomes between the UCOLR group and the successful LLR group further suggest that unplanned conversion is not indicative of surgical failure but is often necessitated by patient safety concerns. While 3-year survival rates did not differ significantly in this cohort with limited follow-up, the potential impact of unplanned conversion on late recurrence > 5years warrants further investigation.
This study found that AFP ≥ 400 ng/mL and tumor located in segment 7 or segment 8 were independent risk factors affecting the postoperative survival of patients with hepatocellular carcinoma by univariate and multivariate Cox regression analyses. As a specific marker for hepatocellular carcinoma, elevated levels of AFP usually reflect the degree of active proliferation of tumor cells. High levels of AFP may imply that the tumor is more invasive and proliferative, leading to poor patient prognosis. Whereas Segment 7 and Segment 8 are specific anatomical regions of the liver, tumor location in these regions may affect liver blood flow and function, as well as potentially increase the difficulty and risk of surgical resection. In addition, tumor location may also be related to the growth pattern and invasive pathway of the tumor, thus affecting the patient’s prognosis. Therefore, in clinical practice, for tumors located in the segment 7 or segment 8, individualized treatment plans should be developed taking into account factors such as tumor size, grading, and AFP level to improve the long-term survival of patients.
However, this study has several limitations. First, it was a retrospective, nonrandomized study. Second, the sample size of the UCOLR group was small, resulting in an insufficient total sample size even after matching. Additionally, the data were derived from a single institution, limiting generalizability. Third, the intrinsic variability among variables could result in selection bias, even after propensity score matching. Fourth, potential confounding factors such as the surgeon’s level of experience, the hospital’s level of medical resources and facilities, the ability of the multidisciplinary team to collaborate, and individual patient differences may also have a significant impact on the decision and outcome of conversion to laparotomy. Given these limitations, further large-sample, multicenter, prospective observational studies are warranted.
In conclusion, unplanned conversion during laparoscopic liver surgery has a negative impact on short-term outcomes, leading to greater intraoperative bleeding and transfusion rates, longer operative times, a greater incidence of various complications, and increased postoperative hospital stays. Despite these short-term effects, the medium-term prognoses, including 3-year survival rates, remained comparable between the UCOLR and LLR groups. Additionally, segment 7 or 8 lesions with high AFP have a greater chance of conversion and an increased rate of recurrence after unplanned conversion. We should be cautious while selecting patient for laparoscopic liver resection.
Supplementary Information
Acknowledgements
The authors thank the Department of Liver Surgery, West China Hospital, Sichuan University, for their generous support.
Abbreviations
- AFP
Serum alpha-fetoprotein
- ALT
Alanine transaminase
- AST
Aspartate transaminase
- BP
Bodily pain
- CT
Computed tomography
- DFS
Disease-free survival
- GH
General health
- HCC
Hepatocellular carcinoma
- LLR
Laparoscopic liver resection
- MH
Mental health
- OLR
Open liver resection
- OS
Overall survival
- PF
Physical functioning
- PSM
Propensity score matching
- QOL
Quality of life
- RE
Role-emotional
- RP
Role-physical
- SF
Social functioning
- SF-36
The Short Form-36
- UCOLR
Unplanned intraoperative conversion to open liver resection
- VT
Vitality
Authors’ contributions
Conception and design of the study: Liang Wang and Yufu Peng; Collection and assembly of the data: Liang Wang, Yufu Peng; Data analysis and interpretation: Liang Wang, Lian Li, Liangliang Xu, Ming Zhang; Drafting the manuscript: Liang Wang; Writing – review & editing: Liang Wang, Yufu Peng, Ming Zhang, Yonggang Wei, Mingqing Xu and Bo Li; Contributed to the operations: Ming Zhang, Yonggang Wei, Mingqing Xu and Bo Li.
Funding
This work was supported by the National Natural Science Foundation of China (No. 82203785, No. 82270648, No. 82473470), Key research and development project of science and technology department of Sichuan Province (2024YFFK0310, 2024YFFK0309), the China Postdoctoral Science Foundation (No. GZB20240486), the Sichuan Science and Technology Program (No. 2024NSFSC1899) and the Postdoctoral Research Fund, West China Hospital, Sichuan University (2024HXBH073).
Data availability
No datasets were generated or analysed during the current study.
Declarations
Ethics approval and consent to participate
All included patients gave oral and written informed consent. This study was approved by the Ethics Committee of West China Hospital, Sichuan University (Ethics No: 2023 − 1928).
Consent for publication
Not applicable, as none of the material presented in this study compromises anonymity.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Data Availability Statement
No datasets were generated or analysed during the current study.