Summary
Numerous studies have demonstrated the advantages of anatomic resection. Nonetheless, whether anatomic resection can increase R0 resection rates remains controversial. Consequently, the present study describes an innovative procedure involving the en bloc concept combined with anatomic resection in laparoscopic hepatectomy, which can reduce postoperative recurrence and metastasis.
Abstract
Laparoscopic hepatectomy has been reported in many studies, and it is the mainstream method of liver resection. In some particular cases, such as when there are tumors adjacent to the cystic bed, surgeons cannot palpate the surgical margins through the laparoscopic approach, which leads to uncertainty about R0 resection. Conventionally, the gallbladder is resected first, and the hepatic lobes or segments are resected second. However, tumor tissues can be disseminated in the above cases. To address this issue, based on the recognition of the porta hepatis and intrahepatic anatomy, we propose a unique approach to hepatectomy combined with gallbladder resection by en bloc anatomic resection in situ. Firstly, after dissecting the cystic duct, without cutting the gallbladder primarily, the porta hepatis is pre-occluded by the single lumen ureter; secondly, the left hepatic pedicle is made free by the gap of the Laennec membrane and Hilar plate; thirdly, the assistant is asked to drag the fundus of the gallbladder, and the liver parenchyma tissue is resected using a harmonic scalpel along the ischemia line on the liver surface and intraoperative ultrasound. The whole middle hepatic vein (MHV) and its tributaries appear completely; lastly, the left hepatic vein (LHV) is disconnected, and the specimen is taken out from the abdominal cavity. The tumor, gallbladder, and other surrounding tissues are resected en bloc, which meets the tumor-free criterion, and a wide incisal margin and R0 resection are achieved. Therefore, the laparoscopic hepatectomy with the combination of the en bloc concept and anatomic resection is a safe, effective, and radical method with low postoperative recurrence and metastasis.
Introduction
Hepatocellular carcinoma is a common cancer; it is the sixth most common neoplasm in adults and the third leading cause of cancer death worldwide, and its incidence is predicted to rise in the future1. Surgical resection, ablative electrochemical therapy, transarterial chemoembolization, systemic therapy such as sorafenib, and transplantation have been reported to be effective treatment modalities for liver cancer2,3. Of these options, surgical resection of hepatocellular carcinoma (HCC) is considered the primary curative treatment since the tumor can be completely removed rather than limited4.
Laparoscopic surgery, a minimally invasive technique with fewer perioperative complications compared to open resection5, has made great progress worldwide and has steadily become an important surgical method for liver surgery6,7,8. However, in laparoscopic liver resection, the surgeon's inability to recognize the tumor margins under direct vision and the fear of not being able to ensure laparoscopic hemostasis have discouraged most liver surgeons from attempting this demanding procedure. In 1960, Lin et al. reported a case of right hepatic lobectomy with intrahepatic portal vein pedicle ligation9. In 1986, Takasaki also described Glisson's pedicle transect hepatectomy, named extrathecal dissection10. In 1991, Reich et al. applied laparoscopic resection of benign liver tumors and completed the world's first laparoscopic hepatectomy11. Since then, anatomical hepatectomy has gradually entered the public view while providing technical support for laparoscopic hepatectomy. However, in the case in the present study, the lower end of the tumor reached the cystic plate, and simple traditional anatomic resection could not guarantee an R0 resection, but the management of such cases has rarely been reported in detail. In 1999, Neuhaus et al. proposed the principle of total portal vein resection, which proved to be a good prognostic indicator, increasing the chance of R0 resection12. Accordingly, with a new understanding of liver anatomy, we advanced a new approach called "en bloc concept combined with anatomic resection", which is depicted in this video protocol.
In this study, the patient was a 67-year-old female admitted to our hospital in August 2021 with mild upper abdominal pain for 1 month. Her medical history was notable for hypertension and diabetes. Abdominal contrast-enhanced computed tomography revealed a mass with heterogeneous enhancement located at segment 4 of the liver, with a size of 247 mm x 54 mm x 50 mm. The lower end of the mass had reached the cystic plate, and the possibility of gallbladder invasion could not be ruled out (Figure 1). The Child-Pugh liver function13 was grade A, and the ICG clearance rate14,15 R15 was 5.1% (<10%). The patient was classified as stage A according to the BCLC algorithm16 and stage IB according to the CNLC algorithm17. After a multidisciplinary meeting, it was decided that her treatment should be laparoscopic left lobe resection of the liver and cholecystectomy. The concept of en bloc resection combined with anatomic hepatic resection in laparoscopy was adopted to eliminate the enormous liver mass totally.
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Protocol
The procedure was reviewed and approved by the Clinical Research and Application Ethics Committee of the Second Affiliated Hospital of Guangzhou Medical University. The content and methods of the research are in line with medical ethics norms and requirements. The patient was informed of the purpose, background, process, risks, and benefits of the study prior to surgery. The patient understood that participation in this study was voluntary and signed informed consent.
1. Patient positioning, instruments, and port placement
- Place the patient in the supine and 30° reverse Trendelenburg position on the operating table, and subsequently tilt 30° to the right during the procedure, with the surgeon performing from the right side.
- Use the five-port technique during the procedure, with three 10 mm trocars, one 5 mm trocar, and one 12 mm trocar for retraction and specimen retrieval. Then, assemble the following hemostatic devices: 30° laparoscope, laparoscopic ultrasonography device, and basic laparoscopic instruments, including a single lumen catheter, a harmonic scalpel, a monopole electrocoagulator, a vascular clip, and a powered endoscopic cutter stapler (see Table of Materials).
- Administer the patient a combination of intravenous and inhalation anesthesia by giving propofol 150 mg, sufentanil 15 ug, and rocuronium bromide 50 mg intravenously, followed by endotracheal intubation 7.5 F after 90 s.
NOTE: The selection of the anesthetic agents and the application of intravenous and inhalation anesthesia are decided and performed by the anesthetist on a case-to-case basis.- During the parenchymal transection, lower the central venous pressure by 3-5 cm H2O to reduce hepatic venous bleeding while limiting the fluid replacement as much as possible. Place a lumen catheter and nasogastric tube (see Table of Materials) in the bladder and stomach for urinary volume recording and decompression.
- Routinely place a preoperative arterial line and a central venous (internal jugular vein) catheter. Use a 10 mm trocar for the observation port 2 cm below the umbilicus. Then, establish pneumoperitoneum by insufflating carbon dioxide, and maintain the intra-abdominal pressure at 12-14 mmHg (1 mmHg, 1/4 0.133 kPa).
- Place the other four trocars in the following locations: the 5 mm trocar in the right anterior axillary line, the 12 mm trocar in the right midclavicular line under the costal margin, the 10 mm trocar in the left anterior axillary line, and the 10 mm trocar in the left midclavicular line under the costal margin (Figure 2).
2. Surgical technique
- Pull the fundus of the gallbladder upward, and use a harmonic scalpel (see Table of Materials) for Calot's triangle18 dissociation. Take care to ligate the cystic duct and artery with medium-sized hemostatic clips, do not cut the gallbladder, and leave the gallbladder in situ primarily (Figure 3).
- Segment the round and falciform ligaments with the harmonic scalpel. Separate the left coronary and triangular ligaments carefully, avoiding injury to the adjacent phrenic vein branches (Figure 4). Then, incisethe hepatogastric ligaments medially 10 mm into the lesser sac.
- Access from left to right behind the hepatoduodenal ligament through a sling removed from the attached 14 F single-lumen catheter to prepare for hepatic inflow occlusion (Figure 5).
- After ligating the left hepatic artery with medium-sized vascular clips, ensure that the first porta hepatis has been blocked with the single-lumen catheter to prevent unexpected bleeding during the mobilization of the left hepatic pedicle.
- Gently lift the inferior edge of the liver, free the left Glissonean pedicles by the gap of the Laennec membrane19 and Hilar plate20 (Figure 6), and then prepare a tourniquet system to block the left hepatic inflow by inserting an 8 F single lumen catheter through the left Glissonean pedicle21 (Figure 7).
- After releasing the first porta hepatis, block the left hepatic pedicle by clamping the single lumen catheter with a hemostatic clip (Figure 8), which will be stapled after parenchyma transection. Determine the border between the left and right hepatic lobes by identifying ischemia of the left hepatic lobe.
- Following the dividing line, seek and mark the projection positions of the middle hepatic veins with laparoscopic ultrasonography. Pay attention to mapping the location and trajectories of the vital intrahepatic vessels, especially those located on the expected transverse plane of the liver parenchyma (Figure 9).
NOTE: In this study, the ultrasound was set to color Doppler flow image (CDFI) mode, and the thin-walled vessel flowing into the inferior vena cava in the same direction as the long axis of the ultrasound probe was judged to be the MHV. Moreover, it was also located near the dividing line.
- Following the dividing line, seek and mark the projection positions of the middle hepatic veins with laparoscopic ultrasonography. Pay attention to mapping the location and trajectories of the vital intrahepatic vessels, especially those located on the expected transverse plane of the liver parenchyma (Figure 9).
- Mark the parenchymal transection line with an electric hook along the demarcation line on the liver surface (Figure 10). Ask the assistant to drag the fundus of the gallbladder and transect the parenchyma from the foot side to the head side along the middle hepatic vein using an ultrasonic scalpel (Figure 11).
- Trigger the ultrasonic scalpel early to effectively reduce hepatic parenchymal bleeding, and do not clamp the tip of the scalpel to avoid vessel damage. Secure or suture the large intrahepatic vessels and bile ducts found during the parenchymal resection with 2-0 sutures if necessary.
- Expose the vascular pedicles inflowing into segments 4a/4b and the left hepatic vein further up in the cutting line (Figure 12). Then, expose the whole MHV and its tributaries fully, and dissect the roots of the LHV and MHV later (Figure 13). Lastly, staple the inflow and outflow vessels with the powered plus stapler when exposed.
- Once the liver specimens have been isolated from the remaining right hepatic lobe, conduct a hemostasis and bile leakage examination along the cut surface before suturing.
- Use monopole electrocoagulation (see Table of Materials) for hemostasis when bleeding spots are found on the cut surface (Figure 14). Wrap the resected left hepatic lobe (Figure 15) in a plastic bag, and take it out through a 4 cm long incision in the lower abdomen, followed by the placement of two drainage tubes.
3. Postoperative nursing
- On the first postoperative day, discontinue the nasogastric tube, and give the patient a liquid diet.
- Remove the Foley catheter on postoperative day 2, and assist the patient in getting out of bed for daily activities.
- Finally, when the drainage is less than 50 mL per day, remove the two drainage tubes on the fourth and fifth days, respectively. Ask the patient to return to the hospital for a follow-up examination 1 month later.
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Representative Results
The duration of the operation was 255 min, no complications were observed during the operation, and the estimated blood loss was less than 20 mL. The operation was not converted to open surgery, and no postoperative complications were seen. Liver segment 2, liver segment 3, and liver segment 4 (including the gallbladder) were resected anatomically, and the MHV as well as its tributaries (V5v, ventral branch of the fifth segment of the hepatic vein; V8v, ventral branch of the eigth segment of the hepatic vein) were completely exposed peripherally. The paraffin pathology22 of the tumor confirmed hepatocellular carcinoma, which was 2.2 cm from the negative liver resection margin (Figure 16). The CT re-examination results showed no abnormal heterogeneous enhancement in the remaining liver parenchyma (Figure 17, evaluated after 6 days; Figure 18, evaluated after 1 month).
Figure 1: Preoperative CT images. CT images 3 days before surgery. Please click here to view a larger version of this figure.
Figure 2: Trocar positions. The trocar positions for the present study are shown here. Please click here to view a larger version of this figure.
Figure 3: Handling the gallbladder. The cystic duct was dissected carefully without cutting the gallbladder primarily. Please click here to view a larger version of this figure.
Figure 4: Mobilization of the left hepatic lobe. The round ligament, the falciform ligament, the left coronary ligament, and the triangular ligament were separated. Please click here to view a larger version of this figure.
Figure 5: First porta hepatis blocking. The first porta hepatis was occluded by a single-lumen catheter. Please click here to view a larger version of this figure.
Figure 6: Isolation of the left hepatic pedicle. The left hepatic pedicle by the gap of the Laennec membrane and Hilar plate was isolated. Please click here to view a larger version of this figure.
Figure 7: Preparation of the tourniquet system. A tourniquet system was prepared using a single-lumen catheter. Please click here to view a larger version of this figure.
Figure 8: Left hepatic inflow blocking. The same method was used to block the left hepatic inflow. Please click here to view a larger version of this figure.
Figure 9: Laparoscopic ultrasonography. Laparoscopic ultrasonography was used to seek the MHV. Please click here to view a larger version of this figure.
Figure 10: Marking the excision boundary. The parenchymal transection was planned along the ischemia line on the liver surface. Please click here to view a larger version of this figure.
Figure 11: Liver parenchyma resection. The liver parenchyma tissue was resected by a harmonic scalpel. Please click here to view a larger version of this figure.
Figure 12: Exposure of the vascular pedicles. The ventral branch of the fifth segment of the hepatic vein (V5v) and the intersegmental vein were exposed completely. Please click here to view a larger version of this figure.
Figure 13: Exposure of the hepatic vein. The middle hepatic vein (MHV), the ventral branch of the eighth segment of the hepatic vein (V8v), and the left hepatic vein (LHV) were exposed completely. Please click here to view a larger version of this figure.
Figure 14: Cut surface. Liver dissection surface and the apparent whole MHV and its tributaries. Please click here to view a larger version of this figure.
Figure 15: The resected specimen. Please click here to view a larger version of this figure.
Figure 16: Results of the paraffin pathology. (A) A liver tissue specimen with a gallbladder attached. (B,C) The microscopic examination showed that the tumor cells were arranged adenoidally. Please click here to view a larger version of this figure.
Figure 17: Re-examination result at 6 days post surgery. The CT re-examination result (6 days later). Please click here to view a larger version of this figure.
Figure 18: Re-examination result at 1 month post surgery. The CT re-examination result (1 month later). Please click here to view a larger version of this figure.
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Discussion
Anatomic hepatectomy is a procedure that can simultaneously remove the lesion and the liver segments along with the corresponding veins and has been considered an ideal method for treating liver cancer23,24,25,26. With technological innovation, anatomic liver resection with laparoscopic technology has developed rapidly as an alternative to conventional open liver resection and is now widely accepted27. This technology can reduce intraoperative blood loss, preserve the functional liver volume to the maximum extent, reduce the occurrence of complications in patients, help them recover faster, and achieve better long-term clinical efficacy. In particular, it has a positive effect on prolonging the postoperative survival time and tumor-free survival time in patients with liver tumors28,29. However, in patients with large hepatocellular carcinoma with potential gallbladder invasion, laparoscopic anatomical hepatectomy is highly demanding, though there have been numerous reports30,31. One of the reasons for this procedure being demanding is that surgeons cannot palpate the tumor through the laparoscopic approach, which may affect the surgical margins and tumor prognosis. It is generally believed that the most favorable long-term survival rate for liver cancer is brought about by R0 resection32,33,34. However, the patient shown in this study had a lesion at segment 4 adjacent to the gallbladder. In this case, if only the traditional anatomical resection method was used, the gallbladder would be removed first, and then the hepatic lobe or segment would be dissected, and it would potentially not be possible to ensure a sufficient resection margin and improve the R0 resection rate. Leaving the gallbladder in situ avoids destroying the integrity of the mass, but it also makes it more difficult to expose the Hilar of the liver. Peter Neuhaus' group has proposed a surgical technique called "hilar en-bloc" resection, which consists of non-contact resection of the tumor and adjacent tissue35. This technique is beneficial for radical tumor resection and has been widely performed in patients with hilar cholangiocarcinoma and portal vein tumor thrombosis36,37. By re-understanding the anatomy of the hepatic hilar region, the combination of the en bloc resection concept provides a new option for the surgical approach in this type of patient. Therefore, in this case, the treatment measures used were left hepatectomy and the later resection of the adjacent gallbladder.
Compared with traditional non-anatomical hepatectomy methods, this en bloc way is more convenient and effective. Firstly, laparoscopic liver resection is a minimally invasive method that can reduce the intraoperative blood loss, relieve patient pain, and shorten hospital stays and has a low incidence of postoperative complications. Secondly, anatomical liver resection can remove the blood vessels of the hepatic segment where the tumor is located, preserve the normal liver tissue, avoid postoperative residual liver congestion, and reduce the occurrence of biliary fistula. Thirdly, the Laennec capsule approach is simple and intuitive, making it especially suitable for laparoscopy and other minimally invasive liver surgery, and using this approach can avoid the destruction of the liver parenchyma, reduce bleeding, simplify the surgical steps, and shorten the time of hepatic portal occlusion and surgery. Finally, by applying the en bloc concept, it is easier to obtain wide negative margins and avoid the dissemination of tumor tissues while achieving better long-term outcomes. The results of "hilar en bloc" resection are still controversial, and some think this resection is excessive. However, in the absence of extended resection, the en bloc resection technique is consistent with the basic principle of oncological surgery and prevents tumor metastasis.
Although the patient received good benefits in the case mentioned, the follow-up time was short, the sample size was too small, and the selection of a target patient lacks universality. A longer follow-up and more examples of the above methods being applied are needed. In addition, it should be noted that this technique may increase the difficulty of the operation because the gallbladder can block the view of the Hilar plate, so experienced surgeons need to judge the complexity of the hepatic portal structure and decide whether to perform the above surgical method. Next, temporary retention of the gallbladder may lead to the potential disadvantage of difficult access to intraoperative bleeding points.
In summary, the technical aspects and preliminary results of laparoscopic hepatectomy in combination with the en bloc concept and anatomic resection are presented. This procedure provides easier access to wide negative margins, increasing the chance of R0 resection and achieving better outcomes later on. This method can help surgeons perform this type of challenging procedure.
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Disclosures
The authors have no conflicts of interest or financial ties to disclose.
Acknowledgments
This work was supported by grants from the Science and Technology Project of Guangzhou City (202102010090) and the Guangzhou Municipal Health and Family Planning Commission (grant No.20201A001086 to Dr. Tang).
Materials
| Name | Company | Catalog Number | Comments |
| 30° Laparoscopy | Olympus Corporation | CV-190 | |
| Harmonic Ace Ultrasonic Surgical Devices | Ethicon Endo-Surgery, LLC | HAR36 | |
| Laparoscopic ultrasonography | Hitachi | Arietta 60 | |
| Monopole electrocoagulation | Kangji Medical | / | |
| Nasogastric tube | Pacific Hospital Supply Co. Ltd | I02705 | |
| Powered plus stapler | Ethicon Endo-Surgery, LLC | PSEE60A | |
| Single lumen ureter | Well Lead Medical CO, LTD | 14F,8F | |
| Trocar | Surgaid Medical | NPCM-100-1-10 | |
| Vascular clips | Teleflex Medical | 544243 |
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