Modified Laparoscopic Anatomic Hepatectomy: Two-Surgeon Technique Combined with the Simple Extracorporeal Pringle Maneuver

Summary

Here, we present a protocol to perform a modified laparoscopic anatomic hepatectomy using improved techniques and instruments.

Abstract

Laparoscopic anatomic hepatectomy (LAH) has become increasingly prevalent worldwide in recent years. However, LAH remains a challenging procedure due to the anatomical characteristics of the liver, with intraoperative hemorrhage being a primary concern. Intraoperative blood loss is the leading cause of conversion to open surgery; therefore, effective management of bleeding and hemostasis is crucial for a successful LAH.

The two-surgeon technique is proposed as an alternative to the traditional single-surgeon approach, with potential benefits in reducing intraoperative bleeding during laparoscopic hepatectomy. However, there remains a lack of evidence to determine which mode of the two-surgeon technique yields superior patient outcomes. Besides, to our knowledge, the LAH technique, which involves the use of a cavitron ultrasonic surgical aspirator (CUSA) by the primary surgeon while an ultrasonic dissector by the second surgeon, has been rarely reported before.

Herein, we present a modified, two-surgeon LAH technique, wherein one surgeon employs a CUSA while the other uses an ultrasonic dissector. This technique is combined with a simple extracorporeal Pringle maneuver and low central venous pressure (CVP) approach. In this modified technique, the primary and secondary surgeons utilize a laparoscopic CUSA and an ultrasonic dissectorconcurrently to achieve precise and expeditious hepatectomy. A simple extracorporeal Pringle maneuver, combined with the maintenance of low CVP, is employed to regulate the hepatic inflow and outflow in order to minimize intraoperative bleeding. This approach facilitates the attainment of a dry and clean operative field, which allows for the precise ligation and dissection of blood vessels and bile ducts. The modified LAH procedure is simpler and safer due to its effective control over bleeding as well as the seamless transition between the roles of primary and secondary surgeons. It holds great promise for future clinical applications.

Introduction

The safety of hepatectomy has significantly improved in recent decades¹, and with the rapid advancements in diagnostic imaging, energy devices, and surgical techniques, laparoscopic hepatectomy has become a widely performed procedure that yields favorable clinical outcomes^2,3. Studies have demonstrated that anatomical hepatectomy yields superior outcomes compared to nonanatomic resection in patients with hepatocellular carcinoma^4,5. Consequently, laparoscopic anatomic hepatectomy (LAH) has gained popularity worldwide⁶. However, intraoperative hemorrhage remains the primary concern during liver resection procedures-in laparoscopic and open surgeries involving both anatomic and nonanatomic resection⁷. Besides, intraoperative hemorrhage is the primary cause for conversion from laparoscopic surgery to open surgery during parenchymal transection^8,9. To effectively control and minimize intraoperative bleeding, it is widely recommended to maintain the central venous pressure (CVP) below 5 cmH₂O in patients undergoing hepatectomy^10,11. Additionally, various instruments, such as a cavitron ultrasonic surgical aspirator (CUSA) and an ultrasonic dissector have been utilized^12,13, and numerous liver resection techniques, including the liver hanging maneuver¹⁴, Pringle maneuver^15,16, and the "two-surgeon technique"^17,18, have also been documented.

The Pringle maneuver, first reported in 1908¹⁹, represents the most straightforward technique for hepatic inflow occlusion and is currently readily achievable during laparoscopic hepatectomy with high efficacy^20,21.

The two-surgeon technique, proposed as an alternative to the traditional single-surgeon approach, was initially employed in open liver resections¹⁷. This method blurs the division of labor between primary and secondary surgeons, with both participating concurrently during parenchymal transection, as well as hemostasis using different energy instruments. Studies have shown that this technique can reduce operation time and intraoperative complications^18,22. Takahisa et al. provided us with some recommendations for performing the two-surgeon laparoscopic technique²³, but different centers may select different devices to transect the liver parenchymal tissue, and there remains a lack of evidence to demonstrate which mode of the two-surgeon technique yields superior patient outcomes.

The CUSA, a commonly used device in liver resection, employs ultrasonic energy to fragment and aspirate parenchymal tissue, thereby allowing for precision transection with minimal damage to blood vessels and bile ducts¹³. Another frequently used tool is the ultrasonic dissector, which utilizes the vibrations of two blades to disrupt hydrogen bonds and effectively cut liver parenchyma while coagulating small vessels ≤3 mm in diameter¹³.

In July 2020, our center implemented the two-surgeon technique for the first time. One surgeon used a CUSA while the other used an ultrasonic dissector. This was combined with a simple extracorporeal Pringle maneuver and low CVP technique to treat a 54-year-old female patient who had been experiencing liver mass and an increased serum alpha-fetoprotein (AFP) level of 104 ng/mL for 1 week. Magnetic resonance imaging (MRI) (Figure 1A,B) indicated a tumor measuring about 2 cm in size located in the S5 and S8 segments, which was considered the primary hepatocellular carcinoma. This article presents the protocol of our center's experience with the CUSA-ultrasonic dissector-extracorporeal Pringle maneuver technique.

Protocol

This protocol and surgery video demonstration obtained the patient's informed consent before surgery, and also obtained approval from The Fifth Affiliated Hospital of Sun Yat-sen University.

1. Preoperative preparation

1. Perform laboratory tests, including blood routine examination, liver and renal function tests, tumor markers of the digestive system (alpha-fetoprotein, AFP; carcinoembryonic antigen, CEA), prothrombin time, international normalized ratio (INR), and indocyanine green retention rate at 15 min (ICG-R15), to evaluate the general condition of the patients.
2. Perform imaging examinations, including a plain thoracic computed tomography (CT) scan, plain and contrast-enhanced upper abdominal CT scan, and liver magnetic resonance imaging (MRI), to evaluate the tumor location, size, and presence of distant metastasis.
3. Calculate the hepatic volume by CT volumetry calculation. If patients are considered for performing major hepatic resections (more than two hepatic segments), ensure that the future liver remnant (FLR)/total liver volume (TLV) ratio is ≥40%.
4. Perform ancillary tests, including electrocardiography (ECG), cardiac ultrasound, and pulmonary function tests, to evaluate the patient's heart and lung condition.
5. Ensure that the patients fully understand their medical condition and are calm enough to achieve good physical and mental preparation for the operation.

2. Patient inclusion and exclusion criteria

1. Inclusion criteria
   1. Include patients having both primary and secondary liver malignancies, as well as benign liver disease, and require segmentectomy.
   2. Perform surgery on both males and females between 15-85 years of age.
   3. Ensure that the patient is in good general condition and can tolerate both anesthesia and laparoscopic hepatectomy.
   4. Ensure that the preoperative liver function classification according to Child-Pugh is either A or B, the ICG-R15 is <10%, and the FLR/TLV ratio is ≥40%.
2. Exclusion criteria
   1. Do not include patients with hepatocellular carcinoma with portal and hepatic vein invasion.
   2. Do not perform surgery on patients with uncontrolled systemic infection.
   3. Do not perform this surgery if severe portal hypertension has been diagnosed by preoperative CT or endoscopy.
   4. Ensure that there has been no recent history of gastric or esophageal variceal bleeding, or refractory ascites.
   5. Ensure there is no diffuse intrahepatic metastasis or distant metastasis.
   6. Do not perform this surgery in cases where laparoscopic surgery is not feasible due to a history of severe abdominal adhesions resulting from multiple prior abdominal operations.

3. Surgery

NOTE: As the preoperative MRI revealed that most of the tumor was located in the S5, with a small portion located in the ventral segment of S8 and without any adjacent large blood vessels or bile ducts, S5 and partial S8 removal was planned to ensure a wide resection margin for complete tumor removal. Therefore, ligation of both S5 pedicles and the ventral branches of the S8 pedicles, as well as their branch veins draining into the middle hepatic vein, was planned. The resection was then performed by dissecting the ventral branch of the S8 segment and following along the hepatic pedicle of the S5.

1. Preparation phase
   1. Under general anesthesia, place the patient in a supine position, with the legs apart, head elevated, and feet lowered, forming a body angle of 30°.
   2. Reduce the liquid infusion to 1 mL/kg/h (by the anesthetist) to keep the CVP below 5 cmH₂O during the operation.
   3. Disinfect the abdominal skin with iodine and drape the patient to prepare a sterile field.
   4. Ensure that the primary surgeon stands on the right, the secondary surgeon stands on the left, and the assistant stands between the patient's legs.
2. Trocar placement
   1. Establish a carbon dioxide pneumoperitoneum of 12-14 mmHg. Insert the trocars according to the location of the tumor.
   2. For this 54-year-old female patient, establish an observation port by inserting a 10 mm trocar 1 cm below the umbilicus.
   3. Position two 12 mm trocars bilaterally at the lateral border of the rectus abdominis muscle, 2 cm superior to the umbilicus.
   4. Position two 5 mm trocars bilaterally below the subcostal margin along the midclavicular line. The trocar layout is shown in Figure 2.
3. Exploration phase
   1. Explore the abdominal cavity and omentum to determine whether there are ascites, cirrhosis, intra-abdominal adhesions, or metastases.
   2. Use laparoscopic ultrasound to evaluate the tumor location, size, and its relationship with adjacent blood vessels or biliary structures, and confirm the preoperative MRI findings regarding the tumor.
4. Locating the tumor
   1. Locate the tumor using laparoscopic ultrasound.
   2. Use an electric coagulation hook to demarcate the area of liver tissue that needs to be excised.
5. Establishing the extracorporeal Pringle maneuver
   1. Locate the first porta hepatis and open the omental bursa using a cordless ultrasonic dissector.
   2. Place another 5 mm trocar (Pringle trocar) in the left hypochondrium along the axillary line. Put the cotton rope into the abdominal cavity through this port.
   3. Use laparoscopic forceps with an elongated head to horizontally pass the cotton rope through Winslow's foramen and encircle the hepatoduodenal ligament. Ensure that there are no adhesions behind the hepatoduodenal ligament, so that the forceps and cotton rope can pass horizontally without resistance, avoiding injury to the inferior vena cava and first porta hepatis.
   4. Pull both ends of the cotton rope through the Pringle trocar using laparoscopic forceps after encircling the hepatoduodenal ligament, and then remove the Pringle trocar.
   5. Pass the end of the cotton rope through a plastic tube, known as a Lumir device, and insert it up to the level of the hepatic pedicle through the opening where the Pringle trocar was removed. The extracorporeal Pringle maneuver is now ready for application.
   6. Insert the Lumir device into the cavity to tighten the cotton rope and occlude hepatic inflow, then secure it with a vascular clamp (Figure 2).
6. Liver parenchyma dissection phase
   1. Limit the clamping time to 15 min, followed by a 5 min declamping period during the operation.
   2. Ensure that the secondary surgeon opens the liver capsule along the marked border using an ultrasonic dissector, while the primary surgeon smashes the hepatic parenchyma using a laparoscopic CUSA in an archeological way. Directly cauterize each of the encountered small blood vessels and bile ducts with an ultrasonic dissector, while dividing the large ones after being clamped by Hem-o-lok.
   3. Dissect the dorsal and ventral branches of the S8 segment within the middle hepatic vein. Clamp and ligate the ventral branch using an Endo-GIA stapler, while preserving the dorsal branch and dorsal segment of the S8.
   4. Dissect the hepatic vein of the S5 segment and divide it after being clamped by Hem-o-lok.
   5. Dissect the hepatic pedicle of the S5 segment and cut it with the Endo-GIA stapler. At this point, the planned resection of the liver segments has been successfully completed.
7. Surgical end stage
   1. Loosen the cotton rope, cauterize the surgical wound to stop bleeding. Rinse the operation area, drain thoroughly, and cut the cotton rope to remove the Lumir device.
   2. Cover the operation area with a layer of absorbable hemostat.
   3. Insert a closed-suction drain.
   4. Close the abdomen layer by layer.

4. Postoperative follow-up

1. Adopt the following management to the patients after returning to the general ward: monitoring of vital signs, intravenous nutrition, rapid recovery of internal organ functions, and prevention of infection and deep venous thrombosis.
2. Provide a full-fluid diet and gradually transition to a regular diet over the next few days if the patients have no significant discomfort. Keep the rest of the treatments unchanged for the first 3 days.
3. Perform lab examination of the whole blood cells, liver and kidney function, electrolyte levels, and blood coagulation function. Additionally, perform early thoracic and abdominal ultrasounds to check for hydrothorax and ascites.
4. Perform a plain upper abdominal CT scan to confirm the absence of residual tumor, bleeding, and bile leakage. Then, remove the drain once the drainage fluid is minimal and clear, which is typically 5-6 days post-operation.
5. Patients are typically discharged from the hospital 1 week after surgery and return to the outpatient clinic 1 month later. If necessary, surgeons may take appropriate measures and extend the course of treatment according to the patient's condition.

Representative Results

This 54-year-old female patient underwent a successful total laparoscopic anatomic hepatectomy (S5 + S8v) using the CUSA-ultrasonic dissector-extracorporeal Pringle maneuver technique, resulting in favorable perioperative outcomes. During the operation, a total of four extracorporeal Pringle maneuvers were performed to control and minimize intraoperative bleeding. The operation lasted approximately 145 min, with an estimated blood loss of 150 mL. The patient made a rapid recovery, being discharged without complications on the 6th postoperative day. Post-surgical CT imaging showed no residual liver tumor, and the pathological result indicated primary hepatocellular carcinoma with a negative resection margin (Figure 1C,D).

Since 2020, the CUSA-ultrasonic dissector-extracorporeal Pringle maneuver technique has been routinely carried out in our center, and a total of 108 patients have been treated by this means. Here, we retrospectively analyzed 10 patients who received this procedure between July and August in 2021. The median age of these patients was 53.8 years (standard deviation [SD]: 7.73 years; range: 44 to 67 years). They underwent either segmentectomy or subsegmentectomy and received an average of 3.5 extracorporeal Pringle maneuvers during the operation. The operation time and estimated blood loss were fairly good, no patient suffered major intraoperative or postoperative complications, and there were no perioperative deaths. The final histopathological results of all patients were hepatocellular carcinoma (Table 1).

Figure 1: Preoperative and postoperative imaging data of the patient. (A) Preoperative diagnostic image of enhanced MRI; the red arrow denotes the tumor. (B)Preoperative diagnostic image of Gd-EOB-DTPA MRI; the red arrow denotes the tumor. (C) Postoperative examination image of enhanced CT. (D) Postoperative pathological image. Please click here to view a larger version of this figure.

Figure 2: Trocar and the Lumir device layout. Please click here to view a larger version of this figure.

Table 1: Characteristics of the 10 patients who underwent the CUSA-ultrasonic dissector-extracorporeal Pringle maneuver technique. Please click here to download this Table.

Discussion

The protocol details a modified LAH performed in our center using the CUSA-ultrasonic dissector-extracorporeal Pringle maneuver technique. In this modified combination technique, we used both the simple extracorporeal Pringle maneuver and a low CVP technique to control and minimize intraoperative bleeding. The primary and secondary surgeons concurrently used a laparoscopic CUSA and ultrasonic dissector, respectively, during parenchymal transection and hemostasis to acquire precise and expeditious hepatectomy.

The perioperative outcomes of the 54-year-old female patient, who was the first to undergo our new combination technique, showed promising results. The operative time was about 145 min, and the intraoperative blood loss was only 150 mL, both better than previously reported results²⁴. In addition, this patient had no major postoperative complications and was discharged within a few days after surgery. Collectively, these data indicate that the new combination technique can offer perioperative advantages, including reduced blood loss, fewer complications, shorter hospital stays, and no increase in mortality for patients who receive LAH.

The traditional single-surgeon technique has limitations in handling intraoperative emergencies, such as unexpected intraoperative bleeding²⁵. However, with the two-surgeon technique, both surgeons can work together to rapidly clear the surgical field and expose and control the bleeding point, so that the emergency treatment can be performed in a shorter time. Studies have shown that the two-surgeon technique is significantly better in terms of shortening operation time and reducing intraoperative blood loss in open and laparoscopic hepatectomy^18,22,23. Similar results were also obtained through this technique in our center. In contrast to the traditional single-surgeon technique, the two-surgeon technique places more emphasis on cooperation between the two senior surgeons and their experience. The division of labor between them becomes blurred, and they can swap roles as needed at any time. Therefore, the two-surgeon technique can greatly improve the management of unexpected emergencies during laparoscopic hepatectomy. Moreover, in our center, the CUSA is selected as the primary surgeon's operative instrument, while the ultrasonic dissector serves as the secondary surgeon's, which is rarely reported in LAH. Unlike other laparoscopic energy instruments, the CUSA can not only selectively fragment parenchymal tissue while avoiding damaging the blood vessels and bile ducts when properly used, but it can also sever as an aspirator to clean and dry the surgical field when bleeding^12,13. During the operation, the primary surgeon uses the CUSA to fragment and aspirate the liver parenchyma, while the secondary surgeon directly transects residual ducts (small blood vessels and bile ducts) with an ultrasonic dissector, or first ligates the ducts (large blood vessels and bile ducts) with Hem-o-lok before using an ultrasonic dissector to cut them off. This significantly accelerates the speed of surgery. The ultrasonic dissector can also be used to stop bleeding on the cut surface of the liver at any time, ensuring a dry operation field. Thorough sharing of roles between two surgeons enables rapid transection of liver parenchyma. The key to successful implementation of this two-surgeon technique is teamwork, with both senior surgeons keeping in mind the transition between transection and hemostasis.

Massive intraoperative bleeding is associated with a high risk of postoperative mortality and a recurrence of liver cancer^26,27. Many techniques have been reported to control hepatic inflow and outflow during liver resection^16,28, among which the Pringle maneuver and maintenance of low CVP are the most effective and most commonly used techniques nowadays. Previous studies have proposed different kinds of intra- or extra-corporeal Pringle maneuver approaches in laparoscopic hepatectomy. However, the occluding instrumentation and components of each device have not always been consistent^16,21,29,30. The occlusion tapes include umbilical tape, cotton tape, tetron tape, and polyester tape. However, each approach has its drawbacks, such as complex manipulation or inadequate blocking of the hepatic pedicle. For example, umbilical or tetron material may lack the elasticity to provide homogeneous power while tightening the hepatoduodenal ligament, resulting in the incomplete occlusion of hepatic inflow. Thus, controlling intraoperative bleeding may not be satisfactory. In addition, some materials may cause a "cutting effect" and damage to the hepatoduodenal ligament.

Herein, we improved the extracorporeal Pringle maneuver by replacing the occluding instrumentation with acotton rope and using a special plastic tube (known as a Lumir device) as an occlusion tube. The cotton rope is soft, elastic, and stronger than single cotton tape. Therefore, it can tighten the hepatoduodenal ligament with homogeneous power to achieve better hepatic inflow occlusion without potentially cutting the portal triad. Moreover, compared with the intracorporeal Pringle maneuver, we can easily block or unblock hepatic inflow by pushing the Lumir device inside or outside. This significantly shortens the processing time and avoids causing unexpected damage when performing the Pringle maneuver during "blind bleeding" periods. We adopted a strategy of 15 min of occlusion followed by 5 min of reperfusion, which has been proven safe for long hepatectomies. The transection surface is carefully checked during every clamp-free interval³¹. The key step for performing the extracorporeal Pringle maneuver is to horizontally pass the cotton rope, carried by a laparoscopic grasper through Winslow's foramen, while avoiding injury to the portal vein or vena cava. There should be no resistance when passing tools through Winslow's foramen, which requires minimal adhesion around the hepatoduodenal ligament. Therefore, one should be cautious with patients who have a history of upper abdominal surgery.

In addition, anesthesiologists must strictly maintain low CVP during hepatectomy, which has been proven fairly effective in controlling and minimizing intraoperative bleeding^10,32. The regulation of CVP requires active communication and cooperation between anesthesiologists and surgeons based on the intraoperative situation. Risks associated with low CVP, such as air embolism and insufficient perfusion of vital organs, should also be considered when maintaining low CVP.

However, centers without a laparoscopic CUSA cannot follow the protocol of this new combination technique. Two senior hepatobiliary surgeons familiar with liver anatomy and surgical procedure are required for this technique. Another limitation is that the occlusion instrument requires additional incisions and is fixed extracorporeally, which sometimes hinders manipulation.

In conclusion, this technique is both safe and feasible. It is easier to achieve a dry and clean operative field, so the bile ducts and blood vessels can be ligated and dissected accurately. Postoperative complications, such as hemorrhage and biliary leakage, are effectively reduced. A wide surgical margin can also be guaranteed with this technique. This method is expected to be a promising surgical technique for patients who receive LAH.

Materials

Name	Company	Catalog Number	Comments
1.0 absorbable suture	Ethicon Inc	SN2210023642	Sterile, radiation sterilization, disposable
1.0 non-absorbable suture	Ethicon Inc	SF1AN	Sterile, radiation sterilization, disposable
10-mm trocar	Hangzhou Optoelectronic Equipment Medical Co., LTD	121-01715	Sterile, ethylene oxide sterilized, disposable
12-mm trocar	Hangzhou Optoelectronic Equipment Medical Co., LTD	121-01715	Sterile, ethylene oxide sterilized, disposable
5-mm trocar	Hangzhou Optoelectronic Equipment Medical Co., LTD	121-01715	Sterile, ethylene oxide sterilized, disposable
7.0 non-absorbable suture	Ethicon Inc	SF7AN	Sterile, radiation sterilization, disposable
Aspirator	Hangzhou Kangji Medical Instrument Co., LTD	20172080644	Sterile,dry heat sterilized, reusable
Cordless Ultrasonic dissector	Covidien llc	SCD396	Sterile, ethylene oxide sterilized, disposable
CUSA	INTEGRA	HDA1902805IE	Sterile,dry heat sterilized, reusable
Electric coagulation hook	Zhejiang Shuyou Instrument Equipment Co., LTD	IIIA-D003-SG842	Sterile, ethylene oxide sterilized, disposable
Endo-GIA stapler	Jiangsu Guanchuang Medical Technology Co., LTD	GCJQB-160	Sterile, ethylene oxide sterilized, disposable
Endoscopic specimen bag	Qingdao Huaren Medical Product Co., LTD	20192060113	Sterile, ethylene oxide sterilized, disposable
Hem-o-lok	Zhejiang Wedu Medical Instrument Co., LTD	JY1004-2012003	Sterile, ethylene oxide sterilized, disposable
Laparoscopic ultrasound	BK medical	flex Focus 800	Sterile,dry heat sterilized, reusable
Lumir device (modified Pringle maneuver)	Shanghai Chester Medical Technology Co., LTD	016651477	Sterile,dry heat sterilized, reusable
Surgicel(absorbable hemostat)	Ethicon Inc	LAB0011179V3	Sterile, radiation sterilization, disposable
Veress needle	Hangzhou Kangji Medical Instrument Co., LTD	20172080644	Sterile, ethylene oxide sterilized, disposable