Combined ultrasonic aspiration and saline-linked radiofrequency precoagulation: a step toward bloodless liver resection without the need of liver inflow occlusion: analysis of 313 consecutive patients

Hepatic resection is widely accepted as the only potential curative treatment for patients with a wide variety of liver conditions[1‐5]. Hemorrhage is one of the main factors contributing to morbidity and mortality in major liver resections[6‐11]. However, bleeding and subsequent blood transfusion may increase the recurrence rate and reduce the survival rate for malignant diseases[7, 12‐14].

The concept of introducing bloodless techniques to facilitate surgical resection of liver tumors has stimulated hepatobiliary surgeons to experiment with new procedures. Initial techniques involved clamping of outflow (total vascular exclusion), and inflow vessels (Pringle maneuver), aiming to reduce bleeding during parenchymal transaction[15‐17]. The Pringle maneuver, which involves the control of the hepatic vascular inflow by clamping the hepatoduodenal ligament, represents the most simple of these methods of vascular control[18]. This maneuver represents a valuable tool for managing intraoperative bleeding, but at the same time places the patient at a high risk of liver damage due to ischemic reperfusion syndrome and many other complications[18‐24]. Consequently, the use of liver occlusion has reduced among liver surgeons but is still used in a few centers. One European survey revealed that 19% of surgeons apply the Pringle maneuver routinely[25].

The need to avoid the complications related to major vascular occlusions has resulted in the use of liver parenchymal transection without clamping techniques. Parenchymal transection tools such as the Cavitron ultrasonic surgical aspirator (CUSA®), saline-linked radiofrequency precoagulation, harmonic scalpel, bipolar scissors, Ligasure device, hydrodissectors, or monopolar floating ball, single or in combinations, are commonly used by experienced surgical teams and the published results are encouraging. The combination of new transection tools, concomitant anesthetic and critical care improvements have dramatically reduced morbidity and mortality rates.

We report the efficacy and complications of a combined technique for liver resection without liver inflow occlusion in 313 consecutive patients with primary or metastatic liver malignancies. This technique uses combinational Cavitron ultrasonic surgical aspirator (CUSA; ValleyLab, Boulder, CO, USA) and a saline-linked radiofrequency dissecting sealer (Aquamantys®).

From September 2007, to March 2013, all patients who underwent liver resection for liver malignancies, with combined technique using CUSA® and Aquamantys® at the following 4 hepato-pancreato-biliary (HPB) units: 1) Department of Academic Surgery, Royal Marsden Hospital, London, UK, 2) The London Clinic Hospital, London, UK, 3) Nicosia Department of Surgery, Division of HPB Surgery, Nicosia General Hospital, Nicosia, Cyprus, 4) First Department of Surgery, University of Athens Medical School, Laikon Teaching Hospital, Athens, Greece have been included. During this period, this combined technique was used by three HPB surgeons (FE, PA, MS).

In accordance with international guidelines, all the patients underwent the necessary preoperative assessment of their disease, including spiral computed tomography, magnetic resonance imaging, and/or positron emission tomography.

Patient data was collected retrospectively and included demographic details, histological type and number of tumors, surgical procedure, overall operating time, parenchymal transection time, overall amount of intraoperative blood loss (IBL) and blood loss during parenchymal transaction (PTBL). Major and critical abnormalities of preoperative and postoperative liver function tests, intraoperative and postoperative complications, mortality rate, the length of hospital stay, and outcome were also recorded. Post hepatectomy liver failure was defined as the presence of serum bilirubin >50 μmol/l and prothrombin index <50% in the fifth postoperative day according to the ‘50-50 criteria’[26].

The resection time was defined as the time from the start of CUSA® to the completion of parenchymal transection. The overall blood loss was estimated by weight of the surgical swabs, the amount of blood in the suction system and the CUSA® suction container following the entire hepatectomy. Blood loss during liver parenchyma transection was recorded in a similar way. Blood was transfused accordingly to maintain the hematocrit above 28 to 30% perioperatively or if the patient developed hemodynamic instability as a result of blood loss.

This retrospective analysis of liver resection using a combination of CUSA® and Aquamantys® devices without the need for the Pringle maneuver focuses on the following outcomes; intraoperative blood loss , parenchymal transection blood loss, need for packed red blood cell (PRBC) transfusion, length of liver resection time and postoperative morbidity and 30-day mortality.

For each participating institution, the study was approved by the local ethics committee and Institutional Review Board.

Three hundred and thirteen patients were included in the series (137 female and 176 males). The median age was 62 years (range 31 to 85 years). The median age among patients who underwent major liver resections (a resection of 3 segments or more) was 61 years and among patients undergoing minor liver resections (a resection of 2 or fewer segments) was 63 years (P-value 0.29). The majority of the patients (247 patients; 78.9%) had colorectal liver metastases (CRLM) and the rest had non-colorectal liver metastases (12 patients; 3.8%), hepatocellular carcinoma (24 patients; 7.7%), cholangiocarcinoma (25 patients; 8%), and gallbladder carcinoma (5 patients; 1.6%). The patient and tumor characteristics are given in Table 1.

We performed 199 (63.58%) major hepatectomies and 114 (36.42%) minor hepatectomies (Table 2). One hundred and five (33.5%) hepatectomies were performed at the Royal Marsden Hospital, 80 (25.6%) at the The London Clinic Hospital, 48 (15.3%) at the Nicosia General Hospital and 80 (25.6%) in Laikon Teaching Hospital. The proportion of different tumor types (P <0.001) varied in each of the 4 HPB units; however the type of operation (major versus minor liver resection) regarding each tumor type was the same (P >0.05). Forty-two re-do hepatectomies were successfully performed (41 of recurrent CRLM and 1 of non-colorectal liver metastases). In addition, 41 of the patients suffering from CRLM underwent a synchronous liver resection in combination with colon resection. The liver lesions per patient rate, was statistically significant for the patients who underwent major liver resections compared to the patients who underwent minor liver resections (P-value 0.016) (Table 1).

In Tables 1 and2, it is clearly demonstrated that for patients suffering from hepatocellular carcinoma, hilar/intrahepatic cholangiocarcinoma, and gallbladder carcinoma that major hepatectomy as a treatment decision was more frequent compared to patients suffering from liver metastasis (96.29 versus 56.75%, P-value <0.001). When comparing the type and the extent of liver resection among patients with CRLM with those with non-colorectal liver metastases it is observed that major hepatectomies were more frequently performed in the first group of patients (42.1 versus 25%, P = 0.023).

The mean overall intraoperative blood loss was 377 ml (SD 335 ml, range 50 to 2,400 ml), and the mean blood loss during parenchymal transection was 223 ml (SD 224 ml, range 40 to 2,100 ml) (Table 3). Amongst the checked factors that potentially affect blood loss during parenchymal transection (gender, age, simultaneous procedures, extent of resection (major versus minor liver resection), re-do (second or third) hepatectomy, type of minor liver resection (anatomic versus non-anatomic liver resection)), the only factor that actually affected blood loss during parenchymal transection was the extent of liver resection (Table 4). In patients undergoing major hepatectomies, the mean blood loss during parenchyma transection was 274 ml (SD 264 ml), while in patients undergoing minor hepatectomies it was 131 ml (SD 55.06 ml) (274 ml versus 131 ml P <0.001). Although the PTBL was greater in non-anatomical liver resection than in anatomical minor liver resections (124 ml versus 145 ml), this difference was not statistically significant (P = 0.088). Contrary to the PTBL, the IBL was affected by more factors (Table 4). So, in patients undergoing major hepatectomies, the IBL was 436 ml, while in patients undergoing minor hepatectomies it was 273 ml (P <0.001). Moreover, in patients who underwent re-do liver resections and in patients who underwent combined colon and hepatic resection the IBL was higher (539 ml versus 352 ml, P <0.001 and 501 ml versus 358 ml, P = 0.001 respectively).

Interestingly, while the IBL in major hepatectomies was higher than in minor hepatectomies (436 ml versus 273 ml) the blood transfusion rate was higher in minor liver resections although this difference was not statistically significant (8.5% versus 14%, P = 0.128). As is demonstrated in Table 1, within the group of patients with minor liver resection, the percentage of patients with CRLM was higher than the corresponding one within the group of patients with major liver resection (103 patients with CRLM/114 minor liver resections versus 144 patients with CRLM/199 major liver resections P <0.001). This corresponds to the fact that the highest percentage of patients within the minor liver resection group had received neoadjuvant chemotherapy when compared to the major liver resection group (92/114 versus 124/199, 80.7% versus 62.3%, P <0.001). This feature raises the possibility that the cause for higher transfusion rates in the minor liver resection group, despite the fact of a lower intraoperative blood loss, was the lower preoperative hematocrit as a result of neoadjuvant chemotherapy.

The length of hospital stay ranged from 3 to 42 days with a mean value of 6 days.

A total of 119 complications occurred in 84 patients (26.8%). Complications and their management are summarized in Table 5. Analysis of complications between major and minor liver resections revealed no statistical differences between outcomes (Table 5). According to the Clavien Classification of Surgical Complications, only 21 patients (6.7%) developed major complications (grade III and IV). Regarding the 16 patients (5.11%) who developed a bile leak, 7 of them had a biliary anastomosis in addition to a liver resection.

Thirty-day mortality was 0.63% (2 deaths during the postoperative period). One patient died of pulmonary embolism (PE) caused by deep vein thrombosis (DVT) on postoperative day two and the other died of liver failure on postoperative day eight. The first patient, a 78-year-old obese female, developed DVT and received low molecular weight heparin subcutaneously. The second patient underwent extended right hepatectomy for a Klatskin tumor and developed liver failure immediately postoperatively.

Hemorrhage is one of the main factors contributing to morbidity and mortality in major liver resections. It is well known that, in cases of malignant tumors, perioperative administration of blood affects not only the disease-free survival period of the hepatectomized patient, through modulation of the immune response, but also the overall survival. An additional source of concern is the increased risk of infectious disease transmission through blood transfusion[6‐11].

Conversely, the Pringle maneuver represents a valuable tool for managing intraoperative bleeding but places the patient at a high risk of liver damage due to ischemic reperfusion syndrome and other complications, such as splanchnic congestion and hemodynamic alterations due to vascular occlusion[18‐24]. Intermittent occlusion, hemihepatic vascular occlusion[27], and ischemic preconditioning of the liver[28] have been used to minimize liver damage while simultaneously reducing intraoperative bleeding.

In conclusion, the limitations associated with a retrospective, single-institution study are acknowledged. However, the fairly large number of this series allows us to conclude that combined technique of saline-linked radiofrequency ablation and ultrasonic aspiration for liver resection is a safe method for both major and minor liver resections. The method is associated with decreased blood loss, reduced postoperative morbidity, and minimal mortality rates. We believe that this combined technique is comparable to other techniques and should be considered as an alternative.

Written informed consent was obtained from the patient for the publication of this report and any accompanying images.