Minimally Invasive Hepatopancreatobiliary Surgery at a Large Regional Health System: Assessing the Safety of Program Expansion

Abstract

Background

Complex, minimally invasive hepatopancreatobiliary surgery (MIS HPB) is safe at high-volume centers, yet outcomes during early implementation are unknown. We describe our experience during period of rapid growth in an MIS HPB program at a large regional health system.

Methods

During an increase in MIS HPB (60% greater from preceding year), hospital records of patients who underwent HPB surgery between 1/1/2019 and 12/31/2020 were reviewed. Operative time, estimated blood loss (EBL), conversion rates, length of stay (LOS), and perioperative outcomes were assessed.

Results

267 patients’ cases were reviewed. The population was 62 ± 13 years, 50% female, 90% white. MIS was more frequently performed for hepatic than pancreatic resections (59% vs 21%, P < .001). Open cases were more frequently performed for invasive malignancy in both pancreatic (70% vs 40%, P < .018) and hepatic (87% vs 70%, P = .046) resections. There was no difference in operative time between MIS and open surgery (293[218-355]min vs 296[199-399]min, P = .893). When compared to open, there was a shorter LOS (4[2-6]d vs 7[6-10]d, P < .001) and lower readmission rate (21% vs 37%, P = .005) following MIS. Estimated blood loss was lower in MIS liver resections, particularly when performed for benign disease (200[63-500]mL vs 600[200-1200]mL, P = .041). Overall 30-day mortality was similar between MIS and open surgery (1.0% vs 1.8%, P = 1.000).

Discussion

During a surgical expansion phase within our regional health system, MIS HPB offered improved perioperative outcomes when compared to open surgery. These data support the safety of implementation even during intervals of rapid programmatic growth.

Keywords

minimally invasive surgery hepatobiliary pancreas robotic surgery

Key Takeaways

• Minimally invasive hepatopancreatobiliary surgery (MIS HPB) is safe during the growth phase of implementation and show similar outcomes to those previously published.

• MIS HPB has comparable, if not improved, perioperative outcomes compared to open approaches at experienced HPB centers.

• Further studies are needed to elicit the full impact of an MIS HPB practice on patient outcomes.

Introduction

Minimally invasive surgery (MIS) is increasingly utilized as a standard of care for numerous conditions.^1-3 For many procedures, MIS has been shown to reduce postoperative pain, decrease blood loss, have fewer complications, and shorten hospital stay.^4-6 Initially, MIS was used exclusively for benign conditions due to concerns regarding perioperative risk and oncologic adequacy. Nonetheless, an extensive body of literature now supports the validity of MIS approaches in a number of malignancies.^4,6-8 However, due of the degree of technical skill required for safe hepatopancreatobiliary (HPB) surgery, the adoption of MIS techniques has lagged behind those for other organ sites.^9,10

Thus, the role of MIS in HPB is still evolving, even in large referral centers. The MIS HPB is becoming more frequently utilized as studies continue to demonstrate comparable complication rates and improved intraoperative metrics.^11-15 This is especially true in large referral centers with surgeons experienced in complex HPB surgery. There is evidence to support that high-volume HPB centers are associated with improved clinical outcomes due to experience gained from a hospital systems standpoint, as well as surgeon-specific experience.⁹ With increased use of the robotic platform, there has been a resulting increase in the complexity of cases treated using MIS techniques.^16,17 While previous studies have compared the outcomes of MIS to the outcomes of open approaches for HPB cases at these large referral centers, there is a scarcity of data describing perioperative outcomes during MIS adoption and growth.^12,14,18-21

As MIS techniques are becoming the standard of care for more pathologies and more complex MIS HPB surgeries are being performed, an evaluation of the safety during increased implementation is necessary. We assess the safety of MIS HPB during the growth phase of a program in our large regional health network.

Methods

This study was reviewed by the Allegheny Health Network (AHN) Institutional Review Board and deemed exempt (Protocol #2022-030). Corresponding with a 60% increase in HPB MIS cases from the year prior, we reviewed all cases of patients undergoing HPB surgery within AHN from January 1, 2019, through December 31, 2020. Basic patient demographics were recorded. If indicated, tumor characteristics were collected: primary tumor location, clinical T category, clinical N status, margin status, final pathologic stage according to the 8th edition of the American Joint Committee on Cancer (AJCC) staging manual, and histologic features. Treatment variables, including timing and use of chemotherapy (CT) or chemoradiotherapy (CRT), were recorded. The cases reviewed included any HPB surgery performed by any surgeon, and at any hospital within health system. This includes all laparoscopic, robotic, or open pancreas or liver resections. Primary gallbladder resections were excluded. A breakdown of types of procedures performed is noted in Table 1 below. Intraoperative metrics, such as operative time, estimated blood loss, and conversions rates, were compared. Estimated blood loss (EBL) was obtained from the anesthesia record and measured in milliliters. Perioperative outcomes, including hospital length of stay (LOS), 30-day, 60-day, and 90-day readmission rates, reoperations, intraoperative and postoperative transfusion requirements, surgical site infections, deep organ space infections, venous thromboembolism (VTE), the need for any invasive intervention, and overall mortality were compared. VTE was defined as pulmonary embolism, deep vein thrombosis, or portal vein thrombus. Invasive intervention was defined as any surgical, endoscopic, or radiographic intervention performed under local, regional, or general anesthesia within 30 days postoperatively.

Table 1.

Demographics of Patients That Underwent Hepatopancreaticobiliary Surgery, Procedures Performed, Minimally Invasive Surgery (MIS) vs Open Cases (n = 267).

	All	Pancreas (n = 158)			Liver (n = 109)
	All	Open (n = 125)	MIS (n = 33)	P-value	Open (n = 45)	MIS (n = 64)	P-value
Age, years	62 ± 14	66 ± 11	64 ± 12	.641	59 ± 13	56 ± 15	.302
Sex, female	134 (50%)	65 (52%)	14 (42%)	.328	20 (44%)	35 (55%)	.292
Race, white	240 (90%)	114 (91%)	28 (85%)	.282	39 (87%)	59 (92%)	.346
Body mass index		28 ± 6	30 ± 7	.121	31 ± 8	28 ± 5	.007
ASA class
I	0 (0%)	0 (0%)	0 (0%)	.420	0 (0%)	1 (2%)	.001
II	36 (14%)	15 (12%)	5 (15%)		0 (0%)	16 (25%)
III	175 (66%)	92 (74%)	26 (79%)		25 (56%)	32 (50%)
IV	55 (21%)	18 (14%)	2 (6%)		20 (44%)	15 (23%)
Tobacco use, current	29 ± 7	35 (28%)	7 (21%)	.438	6 (13%)	10 (16%)	.674
Neoadjuvent chemotherapy	58 (22%)	46 (37%)	4 (12%)	.024	30 (67%)	25 (39%)	.005
Neoadjuvent radiation	105 (40%)	3 (2%)	0 (0%)	.666	3 (7%)	6 (9%)	.613
Pathology
Malignant	188 (70%)	88 (70%)	16 (49%)	.018	39 (87%)	45 (70%)	.046
Benign	79 (30%)	37 (30%)	17 (52%)	.018	6 (13%)	19 (30%)	.046
Procedure
Whipple	107 (68%)	104 (83%)	3 (7%)	<.001
Distal pancreatectomy ± splenectomy	41 (26%)	13 (10%)	28 (86%)
Central pancreatectomy	2 (1%)	0 (0%)	2 (6%)
Total pancreatectomy + splenectomy	6 (4%)	6 (5%)	0 (0%)
Enucleation	2 (1%)	2 (2%)	0 (0%)
Non-anatomic partial hepatectomy	53 (49%)				16 (36%)	37 (58%)	.004
Segmentectomy	21 (19%)				7 (16%)	14 (22%)
Lobectomy	26 (24%)				14 (31%)	12 (19%)
Trisegmentectomy	9 (8%)				8 (18%)	1 (2%)

*Data reported as mean ± standard deviation or n (n%).

Abbreviation: ASA, American society of anesthesiologists.

Statistical Analysis

Data are reported as mean ± standard deviation if normally distributed, or median (interquartile range) if not. To test univariate associations, differences between treatment groups were compared using the Student t test for parametric data and the Mann-Whitney U test for nonparametric data. Categorical data were compared using Pearson chi-square; if cell counts were <5, the Fisher exact test was used. Statistical analyses were performed using SPSS version 28 (IBM Corporation; Armonk, NY).

Results

The full patient demographic breakdown is shown in Table 1. 267 patients’ cases were reviewed. Of the patients that underwent surgery, 97 (36%) underwent an MIS procedure, 15 (15%) laparoscopic and 82 (85%) robotic, and 170 (64%) underwent an open procedure. These patients were age 62 ± 13 years, 50% were male, and 90% were white. Of the entire cohort, 188 (70%) patients underwent resection for malignancy, and the remaining 79 (30%) were for benign indications.

Of the resections performed, 61 (32%) of malignant resections and 36 (46%) of benign diseases were performed via MIS, respectively. A breakdown of cases is shown in Table 1. MIS was more frequently performed for hepatic than pancreatic resections (59% vs 21%, P < .001). Of patients that underwent MIS, 64 (66%) underwent hepatectomy, 61 (63%) had invasive malignancy, 29 (30%) underwent neoadjuvant CT, 6 (6%) underwent neoadjuvant CRT, and 60 (62%) subsequently underwent an anatomical resection. Laparoscopic patients underwent mostly distal pancreatectomy and splenectomies (11, 73%), but also included central pancreatectomies (2, 13%), liver wedge resections (1, 6.7%), and segmentectomies (6.7%). Robotic patients underwent a wider variety of cases including whipples (3, 3.7%), distal pancreatectomies with or without splenectomy (17, 21%), and a full range of liver resections including wedge resections (36, 44%), segmentectomy (13, 15.9%), lobectomy (12, 12.6%), and trisegmentectomy (1, 1.2%). Of patients that underwent open surgery, 125 (74%) underwent pancreatectomy, 127 (75%) had invasive malignancy, 76 (45%) received neoadjuvant CT, 6 (4%) neoadjuvant CRT, and 152 (89%) underwent an anatomical resection. When compared to MIS, open cases were most frequently performed for invasive malignancies in both pancreatic (70% vs 40%, P < .018) and hepatic (87% vs 70%, P = .046) resections.

There was no significant difference in operative time between MIS and open procedures (293[218-355]min vs 296[199-399]min, P = .893). The EBL was lower in MIS liver resections, particularly when performed for benign disease (200[63-500]mL vs 600[200-1200]mL, P = .041). Overall, there were 26 MIS cases that required conversion to open including 30% of pancreatic MIS cases and 25% of MIS hepatic cases. All hepatic conversions occurred during resection for malignancies. Regarding reoperations, 5 MIS (5.2%) vs 16 (9.4%) open cases (P = .214) required reoperation. When compared to open surgeries, there was a shorter LOS (4[2-6]d vs 7[6-10]d, P < .001) and a lower overall readmission rate (21% vs 37%, P = .005) following MIS. When classified by organ site, LOS remained consistently shorter in MIS cases (see Table 2). Pancreatic fistulas were more common in MIS than open pancreatectomies (20 [61%] vs 26 [21%], P < .001). VTE were more frequent following open cases (25 [15%] vs 7 [7%], P = .070). Pleural effusions requiring intervention were more frequent in open hepatectomies (6 [13%] vs 1 [1.5%], P = .019), respectively. Open cases had higher 30-day readmission rates (41 [24%] vs 14 [14%], P = .060) and 60-day readmission rates (28 [16%] vs 6 [6.2%], P = .015). Patients undergoing MIS surgery were more likely to be discharged home compared to a secondary facility (91 [94%] vs 139 [82%], P = .006). Overall, 30-day mortality was similar between MIS and open procedures (1.0% vs 1.8%, P = 1.000).

Table 2.

Intraoperative and Post-Operative Outcomes by Organ (n = 267).

Pancreas (n = 158)	Open (n = 125)	MIS (n = 33)	P-value
Operative time (min, mean ± SD)	289 ± 107	297 ± 106	.687
EBL* (ml, mdn [IQR])	375 (200-600)	350 (175-650)	.884
LOS** (days, mdn [IQR])	8 (6-11)	6 (5-8)	.004
Intraoperative transfusion (n, %)	24 (19%)	7 (21%)	.812
Postoperative transfusion (n, %)	10 (22%)	7 (11%)	.603
30-day readmissions (n, %)	33 (26%)	9 (27%)	.920
30-day unplanned return to OR (n, %)	12 (10%)	3 (9%)	.929
30-day mortality (n, %)	2 (2%)	1 (3%)	.592

Liver (n = 109)	Open (n = 45)	MIS (n = 64)	P-value
Operative time (min, mean ± SD)	306 ± 134	295 ± 154	.680
EBL* (ml, mdn [IQR])	600 (200-1150)	400 (100-950)	.019
LOS** (days, mdn [IQR])	6 (4-8)	3 (1-4)	.001
Intraoperative transfusion (n, %)	15 (33%)	15 (24%)	.276
Postoperative transfusion (n, %)	11 (9%)	2 (6%)	.118
30-day readmissions (n, %)	8 (18%)	5 (8%)	.114
30-day unplanned return to OR (n, %)	4 (9%)	2 (3%)	.194
30-day mortality (n, %)	1 (2%)	0 (0%)	.231

*EBL: estimated blood loss, **LOS: length of stay.

Discussion

With comparable perioperative outcomes, our analysis demonstrates safety during a phase of increased implementation of MIS HPB within a large regional health network.

The complexity of HPB surgeries has made surgeons cautious about adopting MIS approaches for these HPB cases. With increased coalescence of HPB surgery to high-volume centers and the increased use of the robotic platform, the adoption of MIS for HPB pathology has been proven to be safe. Overall, our center had a comparable performance to those previously studied. An important factor in evaluating expertise in MIS is conversion rate. Our conversion rate for pancreatic cases was 30%; other high-volume centers have reported conversion rates from 10-30% for laparoscopic cases and 0-10% for robotic cases.^22-27 The conversion rate for hepatic cases was 25%, exclusively occurring during oncologic resections. This rate is higher than other studies, which have reported conversion rates of 0-12% for laparoscopic and 0-20% for robotic hepatic resections.^28-34 It should be noted that several of the studies listed did not specify the indication for resection, only laparoscopic vs robotic, when comparing conversion rates. Conversion to open resection typically occurs due to uncontrolled hemorrhage, difficulty achieving adequate oncologic resection, or general lack of progress in performing the procedure. In our early implementation, it is likely that patient selection and surgeon comfortability with specific procedures, such as whipples and lobectomies or trisegmentectomies, contributed to an increased overall conversion rate compared to more experienced centers.

Other studies have reported a learning curve of approximately 60 cases for laparoscopic liver resections.²⁸ In our experience, we were able to demonstrate comparable complication rates and significantly shorter hospital stays for the 64 cases reviewed. These results are similar to those previously reported at other high-volume centers.^18,28-30,32 Given the anticipated further learning curve, we would expect these metrics to continue to improve. We did not observe the changes in MIS for pancreatic cases, as these cases are likely more technically challenging and potentially involve a greater learning curve than the 33 cases reported here. Braga et al. demonstrated a reduction in conversion rate, operative time, and operative blood loss after their first 10 procedures yet did not report significant differences in blood loss after 30 consecutive MIS pancreas cases.¹⁵ It is unclear how this change with the continued use of laparoscopic and robotic surgery at our institution and improved proficiency with these techniques. Though not abundant, there are randomized trials that have already begun to demonstrate noninferiority of MIS HPB.^35,36

The primary limitations of this study stem from the retrospective design that was undertaken. We recognize there was significant selection bias in patients undergoing MIS compared to open techniques. Surgical approaches were tailored based on case complexity and surgeon preference. Overall, operative techniques are still surgeon-dependent, considering that the National Comprehensive Cancer Network (NCCN) and other organizations have been slow to address the role of MIS in HPB cancer surgery. Decisions regarding surgical approach are dependent on a number of factors, including tumor-related variables, patient preference, patient financial or logistical factors, physician preference, and other reasons that could not be captured via retrospective data collection. Therefore, substantial differences between patients who underwent MIS and those who underwent open HPB surgery are likely. The immeasurable confounders and vastly different patient populations, including the surgeries performed, thus could not be accounted for utilizing a multivariate analysis. We were also unable to utilize propensity score matching due to this variability and our small sample size. Additionally, treatment regimens, including perioperative management strategies, were not standardized, and likely impacted outcomes between groups.

Lastly, this study does not represent the immediate commencement of MIS HPB surgery in our institution. However, due to the low number of cases performed prior to the dates of this analysis, we feel this study is more indicative of the true transition to a high-volume MIS program. Throughout the course of this study, we were unable to account for the sudden increase in MIS cases during this time period or the preparations, if any, that were made by the health system to handle the increase in cases. We did not incorporate the cost of implementing the MIS program within our health system as this study looks at cases performed by multiple surgeons at multiple hospitals. The focus of this study was the safety of the program, though these questions are important to address and would be worthwhile to investigate in a future study. Due to our small sample size, our analysis combines laparoscopic and robotic approaches into the aggregate of MIS and, although there are likely differences in outcome measures within these populations, they are unlikely to affect the conclusions within the context of our study. This would be a valuable area for a future study looking at the program several years out from inception and comparing the outcomes and case complexity as the program has evolved, as well as how the health system has been affected.

In the context of these limitations, these data support the safety of implementation of MIS HPB. With appropriate expertise, we expect reproducibility of these outcomes at other centers.

Footnotes

Author’s Note

Portions of these data were presented at the 2022 American College of Surgeons Quality and Safety Conference, Chicago, IL, July 15-18, 2022.

Acknowledgments

The authors thank Sarah Carey, MS, Jade Chang, and Jacalyn Newman, PhD, of Allegheny Health Network’s Health System Publication Support Office (HSPSO) for their assistance in editing and formatting the manuscript. The HSPSO is funded by Highmark Health (Pittsburgh, PA, United States of America) and all work was done in accordance with Good Publication Practice (GPP3) guidelines ().

Author Contributions

SJF was directly responsible for all aspects of the study. She participated in the collection, analysis, and interpretation of data and drafting and revision of the manuscript, figures, and tables. CM, DK, and SD participated in the analysis and interpretation of data and drafting and revision of the manuscript, figures, and tables. PR, SCS, PLW, and DLB participated in the review and revision of the manuscript, figures, and tables. CJA had overall responsibility for the study, including conception and experimental design, analysis and interpretation of data, drafting and revision of the manuscript, obtaining funding for the project, and supervision.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

References

Peng

Hochwald

. Minimally invasive esophagectomy—standard of care. J Thorac Dis. 2019;11(S9):S1387-S1388. doi:10.21037/jtd.2019.03.43

Van Praet

Stamm

Sündermann

, et al. minimally invasive surgical mitral valve repair: State of the art review. Interv Cardiol Rev. 2017;13(01):14. doi:10.15420/icr.2017:30:1

A prospective analysis of 1518 laparoscopic cholecystectomies. N Engl J Med. 1991;324(16):1073-1078. doi:10.1056/nejm199104183241601

Chang

Rattner

. History of minimally invasive surgical oncology. Surg Oncol Clin N Am. 2019;28(1):1-9. doi:10.1016/j.soc.2018.07.001

Yibulayin

Abulizi

Sun

. Minimally invasive oesophagectomy versus open esophagectomy for resectable esophageal cancer: A meta-analysis. World J Surg Oncol. 2016;14(1):304. doi:10.1186/s12957-016-1062-7

Friedant

Handorf

Scott

. Minimally invasive versus open thymectomy for thymic malignancies: Systematic review and meta-analysis. J Thorac Oncol. 2016;11(1):30-38. doi:10.1016/j.jtho.2015.08.004

Luketich

Pennathur

Awais

, et al. Outcomes after minimally invasive esophagectomy: Review of over 1000 patients. Ann Surg. 2012;256(1):95-103. doi:10.1097/SLA.0b013e3182590603

Clinical Outcomes of Surgical Therapy Study G, Nelson

Sargent

, et al. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350(20):2050-2059. doi:10.1056/NEJMoa032651

Cleary

. Minimally invasive liver surgery: Has it achieved the standard of care? Ann Surg Oncol. 2018;25(5):1105-1107. doi:10.1245/s10434-018-6380-2

10.

Spiegelberg

Iken

Diener

Fichtner-Feigl

. Robotic-assisted surgery for primary hepatobiliary tumors—possibilities and limitations. Cancers. 2022;14(2):265. doi:10.3390/cancers14020265

11.

van der Poel

Besselink

Cipriani

, et al. Outcome and learning curve in 159 consecutive patients undergoing total laparoscopic hemihepatectomy. JAMA Surg. 2016;151(10):923-928. doi:10.1001/jamasurg.2016.1655

12.

Kendrick

Cusati

. Total laparoscopic pancreaticoduodenectomy: Feasibility and outcome in an early experience. Arch Surg. 2010;145(1):19-23. doi:10.1001/archsurg.2009.243

13.

de Rooij

Jilesen

Boerma

, et al. A nationwide comparison of laparoscopic and open distal pancreatectomy for benign and malignant disease. J Am Coll Surg. 2015;220(3):263-270.e1. doi:10.1016/j.jamcollsurg.2014.11.010

14.

Croome

Farnell

Que

, et al. Pancreaticoduodenectomy with major vascular resection: a comparison of laparoscopic versus open approaches. J Gastrointest Surg. 2015;19(1):189-194; discussion 194. doi:10.1007/s11605-014-2644-8

15.

Braga

Ridolfi

Balzano

Castoldi

Pecorelli

Di Carlo

. Learning curve for laparoscopic distal pancreatectomy in a high-volume hospital. Updates Surg. Sep 2012;64(3):179-183. doi:10.1007/s13304-012-0163-2

16.

Shaw

Wright

Taylor

, et al. Robotic colorectal surgery learning curve and case complexity. J Laparoendosc Adv Surg Tech A. 2018;28(10):1163-1168. doi:10.1089/lap.2016.0411

17.

Muller

Laengle

Riss

Bergmann

Bachleitner-Hofmann

. Surgical complexity and outcome during the implementation phase of a robotic colorectal surgery program-a retrospective cohort study. Front Oncol. 2020;10:603216. doi:10.3389/fonc.2020.603216

18.

Nguyen

Laurent

Dagher

, et al. Minimally invasive liver resection for metastatic colorectal cancer: a multi-institutional, international report of safety, feasibility, and early outcomes. Ann Surg. 2009;250(5):842-848. doi:10.1097/SLA.0b013e3181bc789c

19.

Ito

Are

, et al. Laparoscopic versus open liver resection: A matched-pair case control study. J Gastrointest Surg. 2009;13(12):2276-2283. doi:10.1007/s11605-009-0993-5

20.

Croome

Farnell

Que

, et al.

Total laparoscopic pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: Oncologic advantages over open approaches?

Ann Surg. 2014;260(4):633-638; discussion 638-40. doi:10.1097/SLA.0000000000000937

21.

Buell

Thomas

Rudich

, et al. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg. 2008;248(3):475-486. doi:10.1097/SLA.0b013e318185e647

22.

Jayaraman

Gonen

Brennan

, et al. Laparoscopic distal pancreatectomy: Evolution of a technique at a single institution. J Am Coll Surg. Oct 2010;211(4):503-509. doi:10.1016/j.jamcollsurg.2010.06.010

23.

DiNorcia

Schrope

Lee

, et al. Laparoscopic distal pancreatectomy offers shorter hospital stays with fewer complications. J Gastrointest Surg. 2010;14(11):1804-1812. doi:10.1007/s11605-010-1264-1

24.

Magge

Zenati

Hamad

, et al. Comprehensive comparative analysis of cost-effectiveness and perioperative outcomes between open, laparoscopic, and robotic distal pancreatectomy. HPB (Oxford). 2018;20(12):1172-1180. doi:10.1016/j.hpb.2018.05.014

25.

van Hilst

de Rooij

Bosscha

, et al. Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours (LEOPARD-2): a multicentre, patient-blinded, randomised controlled phase 2/3 trial. Lancet Gastroenterol Hepatol. 2019;4(3):199-207. doi:10.1016/S2468-1253(19)30004-4

26.

Klompmaker

van Hilst

Wellner

, et al. Outcomes after minimally-invasive versus open pancreatoduodenectomy: a pan-european propensity score matched study. Ann Surg. 2020;271(2):356-363. doi:10.1097/SLA.0000000000002850

27.

Raoof

Nota

Melstrom

, et al. Oncologic outcomes after robot-assisted versus laparoscopic distal pancreatectomy: analysis of the national cancer database. J Surg Oncol. 2018;118(4):651-656. doi:10.1002/jso.25170

28.

Vigano

Laurent

Tayar

Tomatis

Ponti

Cherqui

. The learning curve in laparoscopic liver resection: Improved feasibility and reproducibility. Ann Surg. 2009;250(5):772-782. doi:10.1097/SLA.0b013e3181bd93b2

29.

Topal

Fieuws

Aerts

Vandeweyer

Penninckx

. Laparoscopic versus open liver resection of hepatic neoplasms: Comparative analysis of short-term results. Surg Endosc. 2008;22(10):2208-2213. doi:10.1007/s00464-008-0023-9

30.

Simillis

Constantinides

Tekkis

, et al. Laparoscopic versus open hepatic resections for benign and malignant neoplasms--a meta-analysis. Surgery. 2007;141(2):203-211. doi:10.1016/j.surg.2006.06.035

31.

Mala

Edwin

Rosseland

Gladhaug

Fosse

Mathisen

. Laparoscopic liver resection: Experience of 53 procedures at a single center. J Hepatobiliary Pancreat Surg. 2005;12(4):298-303. doi:10.1007/s00534-005-0974-3

32.

Dagher

Proske

Carloni

Richa

Tranchart

Franco

. Laparoscopic liver resection: Results for 70 patients. Surg Endosc. 2007;21(4):619-624. doi:10.1007/s00464-006-9137-0

33.

Kamarajah

Bundred

Manas

Jiao

Hilal

White

. Robotic versus conventional laparoscopic liver resections: A systematic review and meta-analysis. Scand J Surg. 2021;110(3):290-300. doi:10.1177/1457496920925637

34.

Aboudou

Zhang

, et al. Laparoscopic versus Robotic Hepatectomy: A systematic review and meta-analysis. J Clin Med. 2022;30(19):11. doi:10.3390/jcm11195831

35.

de Rooij

van Hilst

van Santvoort

, et al. Minimally Invasive Versus Open Distal Pancreatectomy (LEOPARD): A multicenter patient-blinded randomized controlled trial. Ann Surg. 2019;269(1):2-9. doi:10.1097/SLA.0000000000002979

36.

Bjornsson

Larsson

Hjalmarsson

Gasslander

Sandstrom

. Comparison of the duration of hospital stay after laparoscopic or open distal pancreatectomy: randomized controlled trial. Br J Surg. 2020;107(10):1281-1288. doi:10.1002/bjs.11554