hr

Hot Keywords
non-alcoholic fatty liver disease epidemiology microenvironment nonalcoholic steatohepatitis transplantation cholangiocarcinoma direct-acting antiviral immunotherapy hepatitis B hepatitis C liver resection imaging cancer stem cell diagnosis gene cirrhosis biomarker recurrence

Top
Hepatoma Res 2021;7:26.10.20517/2394-5079.2020.111© The Author(s) 2021.
Open AccessReview

The evolution of minimally invasive surgery in liver transplantation for hepatocellular carcinoma

1School of Medicine, Democritus University of Thrace, Alexandroupolis 68100, Greece.

2First Department of Surgery, Papageorgiou University Hospital, Aristotle University of Thessaloniki, Thessaloniki 54622, Greece.

Correspondence to: Prof. Georgios Tsoulfas, First Department of Surgery, Aristotle University of Thessaloniki, 66 Tsimiski Street, Thessaloniki 54622, Greece. E-mail: tsoulfasg@gmail.com

    This article belongs to the Special Issue Minimally Invasive Surgery for HCC
    Views:428 | Downloads:83 | Cited:0 | Comments:0 | :1
    Academic Editor: Ho-Seong Han | Copy Editor: Cai-Hong Wang | Production Editor: Jing Yu
    ...

    © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, sharing, adaptation, distribution and reproduction in any medium or format, for any purpose, even commercially, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

    Abstract

    Hepatocellular carcinoma (HCC) is a malignant neoplasm associated with significant mortality worldwide. The most commonly applied curative options include liver resection and liver transplantation (LT). Advances in technology have led to the broader implementation of minimally invasive approaches for liver surgery, including laparoscopic, hybrid, hand-assisted, and robotic techniques. Laparoscopic liver resection for HCC or living donor hepatectomy in LT for HCC are considered to be feasible and safe. Furthermore, the combination of laparoscopy and LT is a recent impressive and promising achievement that requires further investigation. This review aims to describe the role of minimally invasive surgery techniques utilized in LT for HCC.

    INTRODUCTION

    Hepatocellular carcinoma (HCC) is a malignant neoplasm, typically arising in the setting of cirrhosis and chronic liver disease[1]. Globally, HCC leads to approximately 800,000 deaths every year[2], being the fifth most common malignant neoplasm and the third cause of death related to cancer worldwide[3]. It is usually diagnosed in advanced stages, with a median survival after diagnosis of 6-20 months[4]. Although locoregional therapy may lead to cure for small lesions in selected patients, complete surgical resection is the most commonly implemented curative option for patients diagnosed with HCC limited to the liver, with preserved liver function, and without portal hypertension.

    Laparoscopy can be used to diagnose, stage, and treat HCC[5]. According to the Louisville Statement (2008), the indications for laparoscopic liver resection (LLR) should be: solitary lesions ≤ 5 cm in diameter, in segments 2-6; laparoscopic left lateral sectionectomy should be standard practice; and major liver resections should be performed by experienced surgeons[5]. In 2014, the Second International Consensus Conference on Laparoscopic Liver Resection was held in Morioka, Japan, to establish further guidelines[6]. The experts concluded that LLR is not inferior in terms of overall survival, mortality, negative margins, and cost compared to the open approach, while they also concluded that it is probably superior regarding length of hospital stay and intraoperative transfusions[6].

    However, only approximately 15% of patients present with resectable tumors[7]. Since liver transplantation (LT) was established as the optimal treatment for end‐stage liver disease, its indications have expanded to include non-metastatic unresectable HCC (Milan criteria)[8,9]. Actually, among well-selected patients undergoing LT for HCC, the overall survival was found to be comparable to that of LT for non-malignant etiology[10,11]. Following resection, HCC patients may exhibit a recurrence rate of 40%-90%, especially in the case of underlying chronic liver disease, and in certain cases salvage LT can be a reasonable option[5,9,12]. As LT may be more complicated in the case of adhesions after previous abdominal surgery[13], LLR may have an additional advantage over its open counterpart in that scenario[14].

    Considering the benefits of laparoscopic approaches and the curative potential of LT, we aim to review the role of minimally invasive surgery in LT for HCC.

    LAPAROSCOPIC LIVER RESECTION FOR HEPATOCELLULAR CARCINOMA

    Technique and positioning for laparoscopic liver resection

    The most common position for the patient is the supine one[15]. The trocar for the laparoscope is inserted through an umbilical incision, while four additional trocars are usually used: at the epigastrium, abdomen bilaterally, and at the right hypochondrium[15,16]. Transthoracic or intercostal trocars are used when operating on the superior part of the liver[17]. Notably, single-incision LLR has also been described[18]. The Pringle maneuver is used to control intraoperative bleeding, and selective inflow occlusion is used to avoid ischemia-reperfusion injury during anatomical major LLR[19]. To reduce intraoperative bleeding, a low central venous and airway pressure should be maintained[15]. In addition, pneumoperitoneum should be ideally kept to 8-10 mmHg to reduce the risk of gas embolism[15].

    Apart from the standard method, hybrid or hand-assisted liver resection may also be used in challenging cases[20]. Additionally, technological advancement has led to the incorporation of the surgical robot in liver surgery. Robotic liver resection (RLR) has the advantage of more technically precise surgery because of its more flexible instrumentation and the 3D visualization of the operative field[21-23].

    Short-term outcomes

    The international consensus statement conclusions have been further validated by several systematic reviews and meta-analyses comparing LLR with open liver resection for patients with HCC. According to a recent one by Wang et al.[24], major LLR has the benefits of fewer postoperative complications, less blood loss, and shorter hospital length of stay with the potential drawback of longer operative time[24]. Long-term outcomes were comparable[24]. Another meta-analysis showed that LLR can lead to decreased intraoperative blood loss, need for transfusion, 30-day complication and mortality rate, and length of hospital stay[25]. According to the authors, LLR is a logical option even for recurrent HCC, with better short-term postoperative outcomes than the open approach[26]. Hybrid hepatectomy for HCC has also been associated with shorter length of hospital stay, same survival rates, and longer operation time when compared with open hepatectomy[27].

    A study by Chen et al.[28] showed that RLR for HCC is a feasible option for challenging major hepatectomies in cirrhotic patients. When compared to the open procedure, it resulted in shorter hospital stay, less postoperative pain, and similar survival outcomes, but longer operation time[28]. When compared with the open or the laparoscopic approach, it was found to be comparable in terms of margin-free resection rates[29]. Overall, LLR and RLR are considered to be equivalent in terms of safety and effectiveness for the management of liver neoplasms[30].

    ROLE OF MINIMALLY INVASIVE LIVING DONOR HEPATECTOMY FOR LIVER TRANSPLANTATION

    Technical details and learning curve of laparoscopic living donor hepatectomy

    Living donor LT was first reported in 1990[31,32]. The first laparoscopic donor hepatectomy in 2002 was a left lateral donor segmentectomy (LLDS) for a pediatric recipient[33]. Further minimal invasive surgical approaches have since been described[34].

    During laparoscopic donor hepatectomy, the Pringle maneuver is typically utilized to allow less blood loss in donors without affecting liver function[35]. For parenchymal transection, the high-pressure waterjet system or the ultrasonic surgical aspirator are used[36]. For hepatic and portal vein occlusion and division, surgical staplers are used. For the hepatic artery and the bile duct, Hem-o-lok clips are used to avoid shortening of vessel length[37]. Because precise bile duct transection is important, intraoperative cholangiography or indocyanine-green fluorescence cholangiography is often used[38]. After resection, the graft is retrieved through a Pfannenstiel incision in an endo-bag. The retrieval should be careful to avoid graft injury[39]. Furthermore, several innovations have been implemented for minimally invasive donor hepatectomy, either preoperatively (i.e., 3D imaging[40] and 3D printing[41]) or intraoperatively (i.e., surgical robot[42]).

    Donor hepatectomy is technically demanding. In particular, the learning curve for pure laparoscopic LLDS is 25 cases[43], while the more difficult right donor hepatectomy requires approximately 60 cases[44,45]. However, these numbers depend on other factors, such as prior experience on both open donor hepatectomy and minimally invasive surgery in general.

    Types and benefits of minimally invasive living donor hepatectomy

    According to a recent systematic review, open donor hepatectomy is superior to the laparoscopic approach in terms of hilar and parenchymal dissection and ischemic time. However, the laparoscopic approach has a superior cosmetic effect[39].

    Pure laparoscopic left and right hepatectomy for adult recipients

    To choose between left or right donor hepatectomy, the surgeon has to consider the size of the recipient to avoid small-for-size syndrome[46]. Pure laparoscopic donor left and right hepatectomies for adult recipients were first reported in 2013[47-50]. These procedures are complex and require a high level of surgical expertise. Despite this, some experienced teams have published successful reports with laparoscopic living donor hepatectomy[51-55]. Some experts support the use of right donor hepatectomy without specific selection criteria[38], while others have developed such criteria incorporating vascular anatomy and graft weight[56,57]. Several studies have described successful pure laparoscopic right hepatectomy for donors with variations in bile ducts[53,58,59], while anatomical reasons have been associated with high complication rates[45,60]. Laparoscopic right donor hepatectomy has been associated with a similar complication rate and shorter length of hospital stay compared to the open approach[45,60]. Suh et al.[38] showed that complication rates, hospital stay, and re-hospitalization were similar between donors undergoing either pure laparoscopic or open right donor hepatectomy.

    Right donor hepatectomy may be preferred for yielding a larger graft, yet studies have shown that laparoscopic left donor hepatectomy is also feasible[49]. Samstein et al.[61] compared laparoscopic to open or hybrid left donor hepatectomy. While the laparoscopic group required a longer time for graft procurement, it was associated with decreased blood loss, shorter hospital stay, and fewer days away from work. The one-year survival rates were similar between the two groups[61].

    Pure laparoscopic left lateral donor sectionectomy for pediatric recipients

    Laparoscopic LLDS is considered to be a safe alternative to the open approach. This method has been advocated to become the new standard of care for LLDS for pediatric recipients[57]. It has the benefit of acceptable recipient outcomes, less intraoperative bleeding, a shorter length of hospital stay, no wound complications, and similar biliary and vascular complications with the open approach, again with the potential drawback of long operative time[61-66]. Soubrane et al.[67] compared laparoscopic liver with kidney donors and found that, while liver donors had longer hospital stay and operation times, LLDS resulted in fewer minor complications[67].

    Hand-assisted and hybrid donor hepatectomy

    Hand-assisted or hybrid donor hepatectomy has the same principles as pure laparoscopic donor hepatectomy, but the hepatic hilum is dissected and the liver is transected through a small open upper midline or transverse incision[34,68]. Similarly, the muscle layer is not interrupted, and, as a result, patients feel less abdominal wall pain than with the open hepatectomy[69]. However, the small incision of these techniques has drawbacks for obese patients with deep body cavities, such as longer operative duration, postoperative complications, and longer hospital stay, as it is difficult for surgeons to manage vascular injuries in these deeper areas[68,70,71]. Recent meta-analyses associated laparoscopic-assisted hepatectomy with fewer complications, less blood loss and pain, no mortality, faster recovery, better cosmetic result, and longer operation time[70,72]. In other words, laparoscopic-assisted hepatectomy is a safe and feasible alternative to open hepatectomy for well-selected donors when performed by experienced teams[73] and can be gradually adopted by less-experienced groups[74,75]. In fact, hand-assisted or hybrid donor hepatectomy can be used by surgeons when transitioning from open to pure laparoscopic donor hepatectomy, because of the steep learning curve of the latter[76].

    Robotic donor hepatectomy

    The first robotic donor hepatectomy was a right hepatectomy reported by Giulianotti et al.[40] in 2012, and since then it has been implemented by several centers[40,77-79]. This technique offers the benefits of 3D vision, a stable and magnified field, and improved instrument precision compared to the laparoscopic technique. This helps the biliary and vascular dissection, and the decision of the point of transection, while the improved ability for suture ligation of venous bleeders can be helpful in minimizing blood loss[40]. The first series of 13 robotic right donor hepatectomies was published by Chen et al.[77] in 2016. The robotic group required no open conversion, the postoperative recovery was quicker, and the need for analgesics was decreased. Compared to the open group, the robotic one showed comparable results for complication rates, blood loss, and recovery of donor liver function. However, the robotic group had longer operation time, and one donor had bile leakage after discharge[77]. While some studies have shown the safety of robotic donor hepatectomy, they have not yet reported superiority in efficacy when compared to open and laparoscopic approaches[80,81]. A recent systematic review supports that the robotic approach is more beneficial regarding hilar dissection, while the laparoscopic is more beneficial for parenchymal dissection with no major difference in terms of ischemic time or cosmesis[39]. In 2018, the international consensus statement on RLR recommended that robotic donor hepatectomy can be an alternative option when performed by experienced surgeons[82].

    Laparoscopic living donor hepatectomy for recipients with hepatocellular carcinoma

    Lee et al.[45] compared pure laparoscopic vs. open donor right hepatectomy for living donor LT. The authors reported data from 115 donors and recipients, with HCC being the indication for LT in 67.8% of the patients. The study concluded that pure laparoscopic donor right hepatectomy is safe when performed by an experienced team[45]. A year later, Lee et al.[83] conducted a similar study of 33 donors and recipients, with HCC being the indication for LT in 21.2% of the patients. The incidence of postoperative complications among donors was similar between the open and laparoscopic groups, while the two approaches yielded similar results for most perioperative outcomes[83]. Further details about these two studies are shown in Table 1[45,83].

    Table 1

    Studies about pure laparoscopic donor hepatectomy for recipients with hepatocellular carcinoma

    DonorsRecipients
    Lee et al.[45] (2018) Lee et al.[83] (2019) Lee et al.[45] (2018) Lee et al.[83] (2019)
    CountryKoreaKoreaKoreaKorea
    Cases, n1153311533
    HCC, n (%)--78 (67.8)7 (21.2)
    Graft weight (g)715.4 ± 153.3750.0 ± 194.0--
    Estimated blood loss (mL)394.1 ± 197.6572.2 ± 438.9NA1650.0 ± 6082.7
    Operation time (min)321.5 ± 57.2433.7 ± 142.9NA597.5 ± 96.8
    Open Conversion, n (%)NA2 (6.1)--
    Complications, n (%)Overall10 (8.7)6 (18.2)26 (22.6)13 (39.4)
    Clavien-Dindo I-II7 (6.1)3 (9.1)NANA
    Clavien-Dindo III-IV3 (2.6)3 (9.1)NANA
    MortalityNANA2 (1.7)3 (9.1)
    Rejection--NA0 (0)
    Hospital stay (Day)7.8 ± 1.89.7 ± 4.417.8 ± 8.724.0 ± 3.9

    LAPAROSCOPIC-ASSISTED LIVER TRANSPLANTATION

    Nine cases of living donor LT with hand-assisted laparoscopic surgery were first reported in 2011 by Eguchi et al.[84]. The hand-assisted laparoscopic total hepatectomy was performed with an upper midline incision. Explantation and liver graft implantation were performed with an open approach after extending the incision[84]. In 2015, 29 selected cases of hybrid procedure for living donor LT were reported[85]. Liver recipients treated with the hybrid approach had no significant differences in blood loss, duration of surgery, vascular anastomosis, and survival, compared to those treated with the conventional open procedure[85]. Dokmak et al.[86] in 2020 published a hybrid LT case for neuroendocrine liver metastases with laparoscopic total hepatectomy and liver graft implantation through a preexisting incision. They showed that the laparoscopic approach for LT recipients may be safe and reasonable[86]. Details from these studies are summarized in Table 2[84-86]. That growing body of evidence, even in patients with cancer, suggests that the use of laparoscopy either for the donor or the recipient in LT for HCC will pave the way for further advancements in the field of minimally invasive surgery and its introduction in the field of LT.

    Table 2

    Studies on laparoscopic-assisted liver transplantation

    StudyCountrySurgery typePatients (n)ConditionsAge (years)Females (%)Blood loss (mL)Operation duration (min)Deaths (n)
    Eguchi et al.[84]JapanHA + midline incision9Cirrhosis, Caroli’s disease60 (44-69)55.63940 (1300-18400)741 (599-839)1
    Soyama et al.[85]JapanHA + midline incision29CirrhosisNANA7300 (1300-18400)761 (578-1057)0
    Dokmak et al.[86]FrancePLH + midline incision1Neuroendocrine liver metastases521004004000

    CONCLUSION

    The use of minimally invasive surgical approaches for LT appears to be feasible. Such approaches may be beneficial even for patients with recurrent HCC after resection requiring salvage LT. Regarding LLDS, laparoscopy is advocated to become the gold standard. Regarding living donor hepatectomy or LT itself, minimally invasive or hybrid laparoscopic approaches have been described. However, laparoscopic or even robotic donor hepatectomy is still rarely performed and only by experienced teams, and thus the need for an international registry or multicenter studies is apparent. In the future, the ongoing improvements in technology will probably further expand this rising surgical field.

    DECLARATIONS

    Authors’ contributions

    Study concept, data analysis and interpretation, critical revision of the manuscript, final approval of the manuscript: Sioutas GS, Tsoulfas G

    Data acquisition, drafting of the manuscript: Sioutas GS

    Availability of data and materials

    Not applicable.

    Financial support and sponsorship

    None.

    Conflicts of interest

    Both authors declared that there are no conflicts of interest.

    Ethical approval and consent to participate

    Not applicable.

    Consent for publication

    Not applicable.

    Copyright

    © The Author(s) 2021.

    References

    • 1. Ziogas IA, Tsoulfas G. Evolving role of Sorafenib in the management of hepatocellular carcinoma. World J Clin Oncol 2017;8:203-13.

      DOIPubMedPMC
    • 2. Akinyemiju T, Abera S, Ahmed M, et al. Global Burden of Disease Liver Cancer Collaboration. The burden of primary liver cancer and underlying etiologies from 1990 to 2015 at the global, regional, and national level: results from the global burden of disease study 2015. JAMA Oncol 2017;3:1683-91.

      DOIPubMedPMC
    • 3. Tejeda-Maldonado J, García-Juárez I, Aguirre-Valadez J, et al. Diagnosis and treatment of hepatocellular carcinoma: an update. World J Hepatol 2015;7:362-76.

      DOIPubMedPMC
    • 4. Cancer of the Liver Italian Program (Clip) Investigators. A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients: the Cancer of the Liver Italian Program (CLIP) investigators. Hepatology 1998;28:751-5.

      DOIPubMed
    • 5. Buell JF, Cherqui D, Geller DA, et al. World Consensus Conference on Laparoscopic Surgery. The international position on laparoscopic liver surgery: the Louisville Statement, 2008. Ann Surg 2009;250:825-30.

      DOIPubMed
    • 6. Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 2015;261:619-29.

      DOIPubMed
    • 7. Coon C, Berger N, Eastwood D, et al. Primary liver cancer: an NCDB analysis of overall survival and margins after hepatectomy. Ann Surg Oncol 2020;27:1156-63.

      DOIPubMed
    • 8. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet 2012;379:1245-55.

      DOIPubMed
    • 9. Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996;334:693-9.

      DOIPubMed
    • 10. Wong SN, Reddy KR, Keeffe EB, et al. Comparison of clinical outcomes in chronic hepatitis B liver transplant candidates with and without hepatocellular carcinoma. Liver Transpl 2007;13:334-42.

      DOIPubMed
    • 11. Yoo HY, Patt CH, Geschwind JF, Thuluvath PJ. The outcome of liver transplantation in patients with hepatocellular carcinoma in the United States between 1988 and 2001: 5-year survival has improved significantly with time. J Clin Oncol 2003;21:4329-35.

      DOIPubMed
    • 12. Felli E, Cillo U, Pinna AD, et al. Salvage liver transplantation after laparoscopic resection for hepatocellular carcinoma: a multicenter experience. Updates Surg 2015;67:215-22.

      DOIPubMed
    • 13. Adam R, Azoulay D. Is primary resection and salvage transplantation for hepatocellular carcinoma a reasonable strategy? Ann Surg 2005;241:671-2.

      DOIPubMedPMC
    • 14. Laurent A, Tayar C, Andréoletti M, Lauzet JY, Merle JC, Cherqui D. Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 2009;16:310-4.

      DOIPubMed
    • 15. Yoshida H, Taniai N, Yoshioka M, et al. Current status of laparoscopic hepatectomy. J Nippon Med Sch 2019;86:201-6.

      DOIPubMed
    • 16. Otsuka Y, Tsuchiya M, Maeda T, et al. Laparoscopic hepatectomy for liver tumors: proposals for standardization. J Hepatobiliary Pancreat Surg 2009;16:720-5.

      DOIPubMed
    • 17. Ishizawa T, Gumbs AA, Kokudo N, Gayet B. Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 2012;256:959-64.

      DOIPubMed
    • 18. Gaujoux S, Kingham TP, Jarnagin WR, D’Angelica MI, Allen PJ, Fong Y. Single-incision laparoscopic liver resection. Surg Endosc 2011;25:1489-94.

      DOIPubMed
    • 19. Cai XJ, Wang YF, Liang YL, Yu H, Liang X. Laparoscopic left hemihepatectomy: a safety and feasibility study of 19 cases. Surg Endosc 2009;23:2556-62.

      DOIPubMed
    • 20. Koffron AJ, Kung RD, Auffenberg GB, Abecassis MM. Laparoscopic liver surgery for everyone: the hybrid method. Surgery 2007;142:463-8; discussion 468.e1.

      DOIPubMed
    • 21. Ho CM, Wakabayashi G, Nitta H, Ito N, Hasegawa Y, Takahara T. Systematic review of robotic liver resection. Surg Endosc 2013;27:732-9.

      DOIPubMedPMC
    • 22. Panaro F, Piardi T, Cag M, Cinqualbre J, Wolf P, Audet M. Robotic liver resection as a bridge to liver transplantation. JSLS 2011;15:86-9.

      DOIPubMedPMC
    • 23. Lai EC, Tang CN, Yang GP, Li MK. Multimodality laparoscopic liver resection for hepatic malignancy--from conventional total laparoscopic approach to robot-assisted laparoscopic approach. Int J Surg 2011;9:324-8.

      DOIPubMed
    • 24. Wang ZY, Chen QL, Sun LL, et al. Laparoscopic versus open major liver resection for hepatocellular carcinoma: systematic review and meta-analysis of comparative cohort studies. BMC Cancer 2019;19:1047.

      DOIPubMedPMC
    • 25. Xiangfei M, Yinzhe X, Yingwei P, Shichun L, Weidong D. Open versus laparoscopic hepatic resection for hepatocellular carcinoma: a systematic review and meta-analysis. Surg Endosc 2019;33:2396-418.

      DOIPubMed
    • 26. Cai W, Liu Z, Xiao Y, et al. Comparison of clinical outcomes of laparoscopic versus open surgery for recurrent hepatocellular carcinoma: a meta-analysis. Surg Endosc 2019;33:3550-7.

      DOIPubMed
    • 27. Kobayashi S, Nagano H, Marubashi S, et al. Hepatectomy based on the tumor hemodynamics for hepatocellular carcinoma: a comparison among the hybrid and pure laparoscopic procedures and open surgery. Surg Endosc 2013;27:610-7.

      DOIPubMed
    • 28. Chen PD, Wu CY, Hu RH, et al. Robotic versus open hepatectomy for hepatocellular carcinoma: a matched comparison. Ann Surg Oncol 2017;24:1021-8.

      DOIPubMed
    • 29. Magistri P, Tarantino G, Assirati G, et al. Robotic liver resection for hepatocellular carcinoma: a systematic review. Int J Med Robot 2019;15:e2004.

      DOIPubMed
    • 30. Qiu J, Chen S, Chengyou D. A systematic review of robotic-assisted liver resection and meta-analysis of robotic versus laparoscopic hepatectomy for hepatic neoplasms. Surg Endosc 2016;30:862-75.

      DOIPubMed
    • 31. Strong RW, Lynch SV, Ong TH, Matsunami H, Koido Y, Balderson GA. Successful liver transplantation from a living donor to her son. N Engl J Med 1990;322:1505-7.

      DOIPubMed
    • 32. Broelsch CE, Emond JC, Whitington PF, Thistlethwaite JR, Baker AL, Lichtor JL. Application of reduced-size liver transplants as split grafts, auxiliary orthotopic grafts, and living related segmental transplants. Ann Surg 1990;212:368-75; discussion 375.

      DOIPubMedPMC
    • 33. Cherqui D, Soubrane O, Husson E, et al. Laparoscopic living donor hepatectomy for liver transplantation in children. Lancet 2002;359:392-6.

      DOIPubMed
    • 34. Koffron AJ, Kung R, Baker T, Fryer J, Clark L, Abecassis M. Laparoscopic-assisted right lobe donor hepatectomy. Am J Transplant 2006;6:2522-5.

      DOIPubMed
    • 35. Park JB, Joh JW, Kim SJ, et al. Effect of intermittent hepatic inflow occlusion with the Pringle maneuver during donor hepatectomy in adult living donor liver transplantation with right hemiliver grafts: a prospective, randomized controlled study. Liver Transpl 2012;18:129-37.

      DOIPubMed
    • 36. Poon RT. Current techniques of liver transection. HPB (Oxford) 2007;9:166-73.

      DOIPubMedPMC
    • 37. Liu Y, Huang Z, Chen Y, et al. Staplers or clips? Medicine (Baltimore) 2018;97:e13116.

      DOIPubMedPMC
    • 38. Suh KS, Hong SK, Lee KW, et al. Pure laparoscopic living donor hepatectomy: Focus on 55 donors undergoing right hepatectomy. Am J Transplant 2018;18:434-43.

      DOIPubMed
    • 39. Cho HD, Samstein B, Chaundry S, Kim KH. Minimally invasive donor hepatectomy, systemic review. Int J Surg 2020;82S:187-91.

      DOIPubMed
    • 40. Giulianotti PC, Tzvetanov I, Jeon H, et al. Robot-assisted right lobe donor hepatectomy. Transpl Int 2012;25:e5-9.

      DOIPubMed
    • 41. Ziogas IA, Zein NN, Quintini C, Miller CM, Tsoulfas G. . Chapter 7 - Three-dimensional (3D) printing and liver transplantation. In: Tsoulfas G, Bangeas PI, Suri JSBT-3D PA in M and S, editors. St. Louis: Elsevier; 2020. pp. 97-116.

    • 42. Suh KS, Hong SK, Yi NJ, et al. Pure 3-dimensional laparoscopic extended right hepatectomy in a living donor. Liver Transpl 2016;22:1431-6.

      DOIPubMed
    • 43. Broering DC, Berardi G, El Sheikh Y, Spagnoli A, Troisi RI. Learning curve under proctorship of pure laparoscopic living donor left lateral sectionectomy for pediatric transplantation. Ann Surg 2020;271:542-8.

      DOIPubMed
    • 44. Hong SK, Suh KS, Yoon KC, et al. The learning curve in pure laparoscopic donor right hepatectomy: a cumulative sum analysis. Surg Endosc 2019;33:3741-8.

      DOIPubMed
    • 45. Lee KW, Hong SK, Suh KS, et al. One hundred fifteen cases of pure laparoscopic living donor right hepatectomy at a single center. Transplantation 2018;102:1878-84.

      DOIPubMed
    • 46. Goldaracena N, Echeverri J, Selzner M. Small-for-size syndrome in live donor liver transplantation-Pathways of injury and therapeutic strategies. Clin Transplant 2017;31:e12885.

      DOIPubMed
    • 47. Soubrane O, Perdigao Cotta F, Scatton O. Pure laparoscopic right hepatectomy in a living donor. Am J Transplant 2013;13:2467-71.

      DOIPubMed
    • 48. Rotellar F, Pardo F, Benito A, et al. Totally laparoscopic right-lobe hepatectomy for adult living donor liver transplantation: useful strategies to enhance safety. Am J Transplant 2013;13:3269-73.

      DOIPubMed
    • 49. Troisi RI, Wojcicki M, Tomassini F, et al. Pure laparoscopic full-left living donor hepatectomy for calculated small-for-size LDLT in adults: proof of concept. Am J Transplant 2013;13:2472-8.

      DOIPubMed
    • 50. Samstein B, Cherqui D, Rotellar F, et al. Totally laparoscopic full left hepatectomy for living donor liver transplantation in adolescents and adults. Am J Transplant 2013;13:2462-6.

      DOIPubMed
    • 51. Han HS, Cho JY, Yoon YS, et al. Total laparoscopic living donor right hepatectomy. Surg Endosc 2015;29:184.

      DOIPubMed
    • 52. Takahara T, Wakabayashi G, Hasegawa Y, Nitta H. Minimally invasive donor hepatectomy: evolution from hybrid to pure laparoscopic techniques. Ann Surg 2015;261:e3-4.

      DOIPubMed
    • 53. Chen KH, Huang CC, Siow TF, et al. Totally laparoscopic living donor right hepatectomy in a donor with trifurcation of bile duct. Asian J Surg 2016;39:51-5.

      DOIPubMed
    • 54. Li H, Wei Y, Li B. Total laparoscopic living donor right hemihepatectomy: first case in China mainland and literature review. Surg Endosc 2016;30:4622-3.

      DOIPubMed
    • 55. Rotellar F, Pardo F, Benito A, et al. Totally laparoscopic right hepatectomy for living donor liver transplantation: analysis of a preliminary experience on 5 consecutive cases. Transplantation 2017;101:548-54.

      DOIPubMed
    • 56. Kim KH, Kang SH, Jung DH, et al. Initial outcomes of pure laparoscopic living donor right hepatectomy in an experienced adult living donor liver transplant center. Transplantation 2017;101:1106-10.

      DOIPubMed
    • 57. Han HS, Cho JY, Kaneko H, et al. Expert panel statement on laparoscopic living donor hepatectomy. Dig Surg 2018;35:284-8.

      DOIPubMed
    • 58. Han YS, Ha H, Kwon HJ, Chun JM. Pure laparoscopic donor right hepatectomy in a living donor with type 3a biliary variation: a case report. Medicine (Baltimore) 2017;96:e8076.

      DOIPubMedPMC
    • 59. Hong SK, Suh KS, Kim HS, et al. Pure 3D laparoscopic living donor right hemihepatectomy in a donor with separate right posterior and right anterior hepatic ducts and portal veins. Surg Endosc 2017;31:4834-5.

      DOIPubMed
    • 60. Park J, Kwon DCH, Choi GS, et al. Safety and risk factors of pure laparoscopic living donor right hepatectomy: comparison to open technique in propensity score-matched analysis. Transplantation 2019;103:e308-16.

      DOIPubMed
    • 61. Samstein B, Griesemer A, Cherqui D, et al. Fully laparoscopic left-sided donor hepatectomy is safe and associated with shorter hospital stay and earlier return to work: a comparative study. Liver Transpl 2015;21:768-73.

      DOIPubMed
    • 62. Broering DC, Elsheikh Y, Shagrani M, Abaalkhail F, Troisi RI. Pure laparoscopic living donor left lateral sectionectomy in pediatric transplantation: a propensity score analysis on 220 consecutive patients. Liver Transpl 2018;24:1019-30.

      DOIPubMed
    • 63. Soubrane O, Cherqui D, Scatton O, et al. Laparoscopic left lateral sectionectomy in living donors: safety and reproducibility of the technique in a single center. Ann Surg 2006;244:815-20.

      DOIPubMedPMC
    • 64. Kim KH, Jung DH, Park KM, et al. Comparison of open and laparoscopic live donor left lateral sectionectomy. Br J Surg 2011;98:1302-8.

      DOIPubMed
    • 65. Scatton O, Katsanos G, Boillot O, et al. Pure laparoscopic left lateral sectionectomy in living donors: from innovation to development in France. Ann Surg 2015;261:506-12.

      DOIPubMed
    • 66. Gautier S, Monakhov A, Gallyamov E, et al. Laparoscopic left lateral section procurement in living liver donors: a single center propensity score-matched study. Clin Transplant 2018;32:e13374.

      DOIPubMed
    • 67. Soubrane O, de Rougemont O, Kim KH, et al. Laparoscopic living donor left lateral sectionectomy: a new standard practice for donor hepatectomy. Ann Surg 2015;262:757-61; discussion 761.

      DOIPubMed
    • 68. Nagai S, Brown L, Yoshida A, Kim D, Kazimi M, Abouljoud MS. Mini-incision right hepatic lobectomy with or without laparoscopic assistance for living donor hepatectomy. Liver Transpl 2012;18:1188-97.

      DOIPubMed
    • 69. Kitajima T, Kaido T, Iida T, et al. Short-term outcomes of laparoscopy-assisted hybrid living donor hepatectomy: a comparison with the conventional open procedure. Surg Endosc 2017;31:5101-10.

      DOIPubMed
    • 70. Zhang B, Pan Y, Chen K, et al. Laparoscopy-assisted versus open hepatectomy for live liver donor: systematic review and meta-analysis. Can J Gastroenterol Hepatol 2017;2017:2956749.

      DOIPubMedPMC
    • 71. Safwan M, Nagai S, Collins K, Rizzari M, Yoshida A, Abouljoud M. Impact of abdominal shape on living liver donor outcomes in mini-incision right hepatic lobectomy: Comparison among 3 techniques. Liver Transpl 2018;24:516-27.

      DOIPubMed
    • 72. Coelho FF, Bernardo WM, Kruger JAP, et al. Laparoscopy-assisted versus open and pure laparoscopic approach for liver resection and living donor hepatectomy: a systematic review and meta-analysis. HPB (Oxford) 2018;20:687-94.

      DOIPubMed
    • 73. Park JI, Kim KH, Lee SG. Laparoscopic living donor hepatectomy: a review of current status. J Hepatobiliary Pancreat Sci 2015;22:779-88.

      DOIPubMed
    • 74. Hori T, Kaido T, Iida T, Yagi S, Uemoto S. Comprehensive guide to laparoscope-assisted graft harvesting in live donors for living-donor liver transplantation: perspective of laparoscopic vision. Ann Gastroenterol 2017;30:118-26.

      DOIPubMedPMC
    • 75. Eguchi S, Soyama A, Hara T, et al. Standardized hybrid living donor hemihepatectomy in adult-to-adult living donor liver transplantation. Liver Transpl 2018;24:363-8.

      DOIPubMed
    • 76. Abu Hilal M, Aldrighetti L, Dagher I, et al. The southampton consensus guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg 2018;268:11-8.

      DOIPubMed
    • 77. Chen PD, Wu CY, Hu RH, et al. Robotic liver donor right hepatectomy: a pure, minimally invasive approach. Liver Transpl 2016;22:1509-18.

      DOIPubMed
    • 78. Choi GH, Chong JU, Han DH, Choi JS, Lee WJ. Robotic hepatectomy: the Korean experience and perspective. Hepatobiliary Surg Nutr 2017;6:230-8.

      DOIPubMedPMC
    • 79. Liao MH, Yang JY, Wu H, Zeng Y. Robot-assisted living-donor left lateral sectionectomy. Chin Med J (Engl) 2017;130:874-6.

      DOIPubMedPMC
    • 80. Magistri P, Tarantino G, Ballarin R, Coratti A, Di Benedetto F. Robotic liver donor right hepatectomy: a pure, minimally invasive approach. Liver Transpl 2017;23:857-8.

      DOIPubMed
    • 81. Chen PD, Wu CY, Wu YM. Use of robotics in liver donor right hepatectomy. Hepatobiliary Surg Nutr 2017;6:292-6.

      DOIPubMedPMC
    • 82. Liu R, Wakabayashi G, Kim HJ, et al. International consensus statement on robotic hepatectomy surgery in 2018. World J Gastroenterol 2019;25:1432-44.

      DOIPubMedPMC
    • 83. Lee B, Choi Y, Han HS, et al. Comparison of pure laparoscopic and open living donor right hepatectomy after a learning curve. Clin Transplant 2019;33:e13683.

      DOIPubMed
    • 84. Eguchi S, Takatsuki M, Soyama A, et al. Elective living donor liver transplantation by hybrid hand-assisted laparoscopic surgery and short upper midline laparotomy. Surgery 2011;150:1002-5.

      DOIPubMed
    • 85. Soyama A, Takatsuki M, Hidaka M, et al. Hybrid procedure in living donor liver transplantation. Transplant Proc 2015;47:679-82.

      DOIPubMed
    • 86. Dokmak S, Cauchy F, Sepulveda A, et al. Laparoscopic liver transplantation: dream or reality? Ann Surg 2020;272:889-93.

      DOIPubMed

    Cite This Article

    Sioutas GS, Tsoulfas G. The evolution of minimally invasive surgery in liver transplantation for hepatocellular carcinoma. Hepatoma Res 2021;7:26. http://dx.doi.org/10.20517/2394-5079.2020.111

    Views
    428
    Downloads
    83
    Citations
     0
    Comments
    0

    1

    Download and Bookmark

    Download

    Download PDF Add to Bookmark

    Share This Article

    Article Access Statistics

    Full-Text Views Each Month

    PDF Downloads Each Month

    Comments

    Comments must be written in English. Spam, offensive content, impersonation, and private information will not be permitted. If any comment is reported and identified as inappropriate content by OAE staff, the comment will be removed without notice. If you have any queries or need any help, please contact us at support@oaepublish.com.

    Article Access Statistics

    • Viewed: 428
    • Downloaded: 83
    • Cited: Crossref0

    Share This Article

    See Updates

    © 2016-2021 OAE Publishing Inc., except certain content provided by third parties