Laparoscopic Liver Resections: A Feasibility Study in 30 Patients
Abstract
Objective
To assess the feasibility and safety of laparoscopic liver resections.
Summary Background Data
The use of the laparoscopic approach for liver resections has remained limited for technical reasons. Progress in laparoscopic procedures and the development of dedicated technology have made it possible to consider laparoscopic resection in selected patients.
Methods
A prospective study of laparoscopic liver resections was undertaken in patients with preoperative diagnoses including benign lesion, hepatocellular carcinoma with compensated cirrhosis, and metastasis of noncolorectal origin. Hepatic involvement had to be limited and located in the left or peripheral right segments (segments 2–6), and the tumor had to be 5 cm or smaller. Surgical technique included CO2 pneumoperitoneum and liver transection with a harmonic scalpel, with or without portal triad clamping or hepatic vein control. Portal pedicles and large hepatic veins were stapled. Resected specimens were placed in a bag and removed through a separate incision, without fragmentation.
Results
From May 1996 to December 1999, 30 of 159 (19%) liver resections were included. There were 18 benign lesions and 12 malignant tumors, including 8 hepatocellular carcinomas in cirrhotic patients. Mean tumor size was 4.25 cm. There were two conversions to laparotomy (6.6%). The resections included 1 left hepatectomy, 8 bisegmentectomies (2 and 3), 9 segmentectomies, and 11 atypical resections. Mean blood loss was 300 mL. Mean surgical time was 214 minutes. There were no deaths. Complications occurred in six patients (20%). Only one cirrhotic patient developed postoperative ascites. No port-site metastases were observed in patients with malignant disease.
Conclusion
Laparoscopic resections are feasible and safe in selected patients with left-sided and right-peripheral lesions requiring limited resection. Young patients with benign disease clearly benefit from avoiding a major abdominal incision, and cirrhotic patients may have a reduced complication rate.
* Patients with atypical lesions and a suspected diagnosis of adenoma.
† Patients operated on with a suspected diagnosis of cystadenoma.
‡ Atypical symptomatic lesion.
§ Converted to laparotomy before resection.
Discussion
Prof. D. Jaeck (Strasbourg, France): First, Daniel, I congratulate you because I enjoyed your nice presentation. You showed that laparoscopic liver resection is feasible, and that in your hands it is safe! However, I would like to discuss the indications of this approach. It is clear that for benign lesions we are not allowed to have morbidity or any mortality. So we want to be sure to have at least the same results as in open surgery. For cancer, as you discussed particularly in the conclusion, you did not prove that it is as safe and as efficient as open surgery. So, which are the real advantages? Cost? Probably not, because we need more sophisticated instruments. Time? Certainly not, because you showed that hospital stay and duration of the procedure are the same as for open surgery. Blood loss is at least the same as with open surgery, perhaps even more. Morbidity seems to be the same, and your conclusion was that the potential benefit, if you do not consider the benign disease, could be obtained in case of hepatocellular carcinoma in cirrhotic patients. So I would like to ask if you could tell us more precisely for which type of tumor (location, stage) and in which kind (Child-Pugh stage) of cirrhotic patients you would propose a laparoscopic resection.
Prof. D. Cherqui (Créteil, France): Concerning benign lesions, I do not see that the risk has been increased in this study compared to open surgery. Indeed, there were no complications in patients with benign disease in this study. We did not perform these procedures until we were confident that we did not expose the patients to a higher risk. The operations were performed collaboratively by two surgeons, one expert in liver surgery and one expert in laparoscopic surgery. The patients were selected because they had a small and peripheral lesion. As soon as we felt that either exposure or minor bleeding was a problem, we converted to open surgery, and this occurred in two of the 30 cases.
Concerning patients with malignant lesions, who represent the majority of indications of liver resections, there is a concern about the possibility of tumor seeding. We chose to use laparoscopic resections in patients with hepatocellular carcinoma and cirrhosis with the aim of reducing morbidity, which is high in these patients. There is evidence that part of the morbidity is related to the abdominal wall incision, with division of collateral circulation. We anticipated that there would be less postoperative ascites, and indeed, although this is not controlled data, only one patient developed ascites. Ascites is usually reported in 30% to 50% of the cases, even after small resections by open surgery in cirrhotic patients. We excluded patients with colorectal metastases from this study because the use of laparoscopy is presently a controversial issue in colorectal cancer, even for the resection of the primary tumor. Patients with small colorectal metastases are operated on for cure, so at the present time we are waiting for the results of controlled studies in progress for laparoscopic resection of the primary colorectal tumors. However, patients with primary colorectal tumors may have peritoneal invasion, which has a higher risk of dissemination, while liver metastases are very rarely associated with peritoneal invasion. For patients with breast metastases, we used laparoscopy because these patients often have very small lesions that one cannot detect on preoperative imaging. Initial laparoscopy permitted us to avoid unnecessary laparotomy in such cases and to proceed with laparoscopic resection in other cases.
Prof. A. Johnson (Sheffield, United Kingdom): This is an interesting paper on technique, but the indications in about half the cases might be questioned (e.g., FNH with good MRI scans and secondary breast tumors). You state that the benefit is clear in young people, but I still think you have to prove that for the indications that would be generally agreed. The particular group in which this technique might be helpful are cirrhotic patients, but as you were only operating on grade A liver tissue, you would not expect much postoperative ascites. I wonder if you measured the metabolic response, because studies in gallbladder surgery show that the pneumoperitoneum itself produces a tremendous increase in antidiuretic and other hormones. The laparoscopic approach could actually be increasing, rather than decreasing, the problem of ascites. It is a very long operation, unnecessarily long for benign disease, and if you add up the length of all your incisions there is quite significant damage to the abdominal wall, 9 or 10 cm perhaps. One question about technique: you said you put a sling around the right hepatic and middle hepatic veins. If you did make a hole there, there is a real risk of a gas embolus with the pneumoperitoneum. Did you always do that, or was it only used on certain occasions? Two final questions: did you do any comparative costings, compared with the open procedure, and why did the patients stay in for so long after the laparoscopic resection?
Prof. D. Cherqui (Closing Discussion): Concerning the indications, I did not have time to show them to you here, but in our institution, many patients with benign lesions found incidentally at ultrasound are referred for diagnosis, and these include mainly young women. We see about 60 new cases of focal nodular hyperplasia (FNH) every year. Presently, noninvasive diagnosis is obtained in 80% of these patients just by CT and MRI scans. In the remaining 20%, diagnosis cannot be obtained by these means and a biopsy is required. Our previously reported policy is to undertake laparoscopic biopsy. The reason is that we get a large specimen for histologic diagnosis. In more than half of the cases, frozen-section study gives us the diagnosis. If it says FNH, we do not resect and the procedure is limited to laparoscopy, with the patient out of hospital the day after. So it is only a very small percentage of the patients with FNH that undergo resection, including the rare patients with symptoms and those in whom the pathologist cannot diagnose FNH. The latter are atypical FNHs that can only be diagnosed on the full specimen, therefore requiring resection for diagnosis.
For breast tumor metastases, there is no consensus so far as to the benefit of liver resection. However, in selected patients, the prognosis seems related to the liver lesions, and there are several articles in the literature advocating liver resection of isolated and limited breast metastases. Several cases are proposed every year. Only a few are operated on, but occasional long-term survival is observed. Indeed, we only operated on Child A patients because this is, for us, the only indication. In Child B patients with small hepatocellular carcinoma, we never consider resection and we would rather do transplantation. In Child A patients, there are several options. When the tumor is superficial, we believe that it is not an indication for percutaneous treatment because this would open the tumor in the peritoneum. So we propose resection of superficial tumors and do it by laparoscopy when feasible. The sling around the middle and left hepatic vein must be placed cautiously, and we did not observe any case of gas embolus. It is true that numerous port sites are required to perform this procedure, plus an extraction incision. However, this is the case for most complex laparoscopic procedures. I do not think that you can sum up all small incisions and say it is equal to one large laparotomy with fascia and muscle division. Finally, laparoscopic liver resection is certainly more expensive at the present time, but the primary goal is to be less invasive, and hopefully costs will be reduced in the future.
Footnotes
Correspondence: Daniel Cherqui, MD, Service de Chirurgie Générale et Digestive, Hôpital Henri Mondor, 94010 Créteil, France.
Presented at the Seventh Annual Meeting of the European Surgical Association, Amstel Intercontinental Hotel, Amsterdam, The Netherlands, April 14–15, 2000.
E-mail: daniel.cherqui@hmn.ap-hop-paris.fr
Accepted for publication July 2000.
References
- 1. John TG, Greig JD, Crosbie JL, Miles WF, Garden OJ. Superior staging of liver tumors with laparoscopy and laparoscopic ultrasound. Ann Surg 1994; 220: 711–719.
- 2. Rahusen F, Cuesta MA, Borgstein PJ, et al. Selection of patients for resection of colorectal metastases to the liver using diagnostic laparoscopy and laparoscopic ultrasonography. Ann Surg 1999; 230: 31–37.
- 3. Morino M, De Giuli M, Festa V, Garrone C. Laparoscopic management of symptomatic nonparasitic cysts of the liver. Ann Surg 1994; 219: 157–164.
- 4. Hashizume M, Takenaka K, Yanaga K, et al. Laparoscopic hepatic resection for hepatocellular carcinoma. Surg Endosc 1995; 9: 1289–1291. [[PubMed]
- 5. Gugenheim J, Mazza D, Katkhouda N, Goubaux B, Mouiel J. Laparoscopic resection of solid liver tumours. Br J Surg 1996; 83: 334–335. [[PubMed]
- 6. Kaneko H, Takagi S, Shiba T. Laparoscopic partial hepatectomy and left lateral segmentectomy: technique and results of a clinical series. Surgery 1996; 120: 468–475. [[PubMed]
- 7. Azagra JS, Goergen M, Gilbert E, Jacobs D. Laparoscopic anatomical hepatic left lateral segmentectomy: technical aspects. Surg Endosc 1996; 7: 758–761. [[PubMed]
- 8. Watanabe Y, Sato M, Ueda S, et al. Laparoscopic hepatic resection: A new and safe procedure by abdominal wall lifting method. Hepato-Gastroenterology 1997; 44: 143–147. [[PubMed]
- 9. Rau HG, Buttler E, Meyer G, Schardey HM, Schildberg FW. Laparoscopic liver resection compared with conventional partial hepatectomy: a prospective analysis. Hepato-Gastroenterology 1998; 45: 2333–2338. [[PubMed]
- 10. Huscher C, Lirici MM, Chiodini S. Laparoscopic liver resections. Sem Laparosc Surg 1998; 5: 204–210. [[PubMed]
- 11. Samama G, Chiche L, Bréfort JL, Le Roux Y. Laparoscopic anatomical hepatic resection. Surg Endosc 1998; 12: 76–78. [[PubMed]
- 12. Abdel-Atty MY, Farges O, Jagot P, Belghiti J. Laparoscopy extends the indications for liver resections in patients with cirrhosis. Br J Surg 1999; 86: 1397–1400 [[PubMed]
- 13. Katkhouda N, Hurwitz M, Gugenheim J, et al. Laparoscopic management of benign solid and cystic lesions of the liver. Ann Surg 1999; 229: 460–466.
- 14. Gagner M, Pomp A, Henford BT, Pharand D, Lacroix A. Laparoscopic adrenalectomy: lessons learned from 100 consecutive procedures. Ann Surg 1997; 226: 238–247.
- 15. Elias D, Desruennes E, Lasser P. Prolonged intermittent clamping of the portal triad during hepatectomy. Br J Surg 1991; 78: 42–44. [[PubMed]
- 16. Wu CC, Hwang CR, Liu TJ, P’eng FK. Effects and limitations of prolonged intermittent ischemia for hepatic resection on the cirrhotic liver. Br J Surg 1996; 83: 121–124. [[PubMed]
- 17. Belghiti J, Noun R, Malafosse R, et al. Continuous versus intermittent portal triad clamping for liver resection. A controlled study. Ann Surg 1999; 229: 369–375.
- 18. Cherqui D, Malassagne B, Colau PI, et al. Hepatic vascular exclusion with preservation of the caval flow for liver resections. Ann Surg 1999; 230: 24–30.
- 19. Moskop RJ, Lubarsky DA. Carbon dioxide embolism during laparoscopic cholecystectomy. South Med J 1994; 84: 414–415. [[PubMed]
- 20. Yacoub OF, Cardona I, Coveler LA, Dodson MG. Carbon dioxide embolism during laparoscopy. Anesthesiology 1982; 57: 533–535. [[PubMed]
- 21. Delaunay L, Bonnet F, Cherqui D, et al. Laparoscopic surgery minimally impairs postoperative cardiorespiratory and muscle performance. Br J Surg 1995; 82: 373–376. [[PubMed]
- 22. Schwenk W, Bohm B, Witt C, et al. Pulmonary function following laparoscopic or conventional colorectal resection. A randomized controlled evaluation. Arch Surg 1999; 134: 6–12. [[PubMed]
- 23. Cherqui D, Rahmouni A, Charlotte F, et al. Management of focal nodular hyperplasia and hepatocellular adenoma in young women. A series of 41 patients with clinical, radiologic and pathologic correlations. Hepatology 1995; 22: 1674–1681. [[PubMed]
- 24. Mathieu D, Kobeiter H, Cherqui D, Rahmouni A, Dhumeaux D. Oral contraceptive intake in women with focal nodular hyperplasia of the liver. Lancet 1998; 352: 1679–1680. [[PubMed]
- 25. Johnstone PAS, Rohde DC, Swartz SE, Fetter JE, Wexner SD. Port-site recurrences after laparoscopic and thoracoscopic procedures in malignacy. J Clin Oncol 1996; 14: 1950–1956. [[PubMed]
- 26. Cook TA, Dehn TC. Port-site metastases in patients undergoing laparoscopy for gastrointestinal malignancy. Br J Surg 1996; 83: 1419–1420. [[PubMed]
- 27. Neuhaus SJ, Texler M, Hewett PJ, Watson DI. Port-site metastases following laparoscopic surgery. Br J Surg 1998; 85: 735–741. [[PubMed]
- 28. Jacquet P, Averbach AM, Stephens AD, Sugarbaker PH. Cancer recurrence following laparoscopic colectomy. Report of two patients treated with intraperitoneal heated chemotherapy. Dis Colon Rectum 1995; 38: 1110–1114. [[PubMed]
- 29. Poulin EC, Mamazza J, Schlachta CM, Gregoire R, Roy N. Laparoscopic resection does not adversely affect early survival curves in patients undergoing surgery for colorectal adenocarcinoma. Ann Surg 1995; 229: 487–492.
- 30. Beart RW. Laparoscopy: to inflate or to lift? Cancer 1999; 86: 747–748. [[PubMed]
- 31. Vittimberga FJ, Foley DP, Meyers WC, Callery MP. Laparoscopic surgery and the systemic immune response. Ann Surg 1998; 227: 226–234.
- 32. Bismuth H, Houssin D, Ornowski J, Meriggi F. Liver resections in cirrhotic patients: a Western experience. World J Surg 1986; 10: 311–317. [[PubMed]
- 33. Franco D, Capussotti L, Smadja C, et al. Resection of hepatocellular carcinomas. Results in 72 European patients with cirrhosis. Gastroenterology 1990; 98: 733–738. [[PubMed]
- 34. Nagasue N, Kohno H, Chang YC, et al. Liver resection for hepatocellular carcinoma: results of 229 consecutive patients during 11 years. Ann Surg 1993; 217: 375–384.
- 35. Bismuth H, Chiche L, Adam R, et al. Liver resection versus transplantation for hepatocellular carcinoma in cirrhotic patients. Ann Surg 1993; 218: 145–151.
- 36. Bruix J, Castells A, Bosch J, et al. Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology 1996; 111: 1018–1022. [[PubMed]
- 37. Elias D, Cavalcanti de Albuquerque A, Eggenspieler P, et al. Resection of liver metastases from a noncolorectal primary: indications and results based on 147 monocentric patients. J Am Coll Surg 1998; 187: 4874–4893. [[PubMed]
- 38. Harrison LE, Murray FB, Newman, et al. Hepatic resection for noncolorectal, nonendocrine metastases: a fifteen-year experience with ninety-six patients. Surgery 1997; 121: 625–632. [[PubMed]
- 39. Geoghegan JG, Scheele J. Treatment of colorectal liver metastases. Br J Surg 1999; 86: 158–169. [[PubMed]







