Trends in Robotic Pancreaticoduodenectomy and Distal Pancreatectomy

Abstract

Background:

Pancreatic surgery remains a challenge even to the most experienced surgeons. Despite significant advances in the field, morbidity and mortality continue to have elevated rates even in specialized, high-volume centers. The rise of laparoscopy in the past decades has improved outcomes for patients, but remains unused due to the technical complexities involved.

Methods:

A literature search was performed using PubMed and Google Scholar databases. Key words used in the search include: “robotic surgery,” “robotic pancreas surgery,” “pancreas surgery,” “minimally invasive pancreas surgery,” “robotic pancreaticoduodenectomy,” and “robotic distal pancreatectomy.” The studies included in our review were summarized in a patient intervention comparison and outcome table.

Results:

The use of a robotic platform has emerged to counteract the more challenging aspects of laparoscopic pancreatic surgery, but incurs a high cost. Data, however, show a trend toward ever improving outcomes such as operative time, estimated blood loss, and length of stay, while still offering the benefits of minimally invasive surgery.

Conclusion:

There is no question that the use of robots in surgery will continue to expand, and with this, appropriate measures must be taken to ensure patient safety in the form of standardized education and certification for the future generation of surgeons considering robotic surgery. As robotic pancreatic surgery grows, encouraging data have emerged—as surgeons become more skilled and programs gain experience, patients are being benefited by this expanding technology. Larger, prospective cohorts will also provide more definitive evidence of the benefits of robotic surgery.

Introduction

Pancreatic surgery is one of the most challenging fields a surgeon can face due to the complexity of the anatomical region, which is characterized by the presence of critical vessels and important visceral structures, as well as the nature of the procedure itself, which requires the construction of several high-risk anastomoses. As our knowledge of pancreatic pathology increases, the indications for pancreatic surgery expand with more patients being offered a surgical procedure. Advances in surgical techniques and equipment have also contributed to the progress of the field.¹ Major developments have contributed to the reduction of morbidity and mortality rates, but even high-volume centers still experience ∼40% rate of morbidity and up to 6% mortality.²

Minimally invasive surgery (MIS) has emerged in the 1990s as an alternative to the traditional open approach. Laparoscopic pancreaticoduodenectomy (PD) was first introduced in 1994 by Gagner and Pomp, but proved to be technically difficult and did not enjoy widespread use.^2,3 Robotic surgery has opened new possibilities to address the more challenging features of MIS. Initially developed to assist cardiac surgery, the daVinci robot (Intuitive Surgical, Inc.) was applied in the difficult radical prostatectomies performed by urologists and has now been adapted to many other surgical specialties such as gynecology and general surgery. The daVinci system provides 7 degrees of freedom, 3D binocular visualization, and fine tremor reducing technology. In addition, the sitting position that the surgeon must assume at the console is surely an ergonomic advantage, especially when confronted by lengthy procedures such as a PD.^4,5 Disadvantages include the loss of haptic feedback, reduced ability to position the patient, and the fact that the surgeon must operate away from the table at a separate console.

Despite this, the feasibility of robotic PD is well established.^6,7 Cost-effectiveness, on the contrary, remains a matter of an ongoing debate.

In the case of distal pancreatectomy (DP), according to a review of the Nationwide Inpatient Sample (NIS) database, the proportion of minimally invasive distal pancreatectomies (MIDP) tripled in a span of 12 years, from 2.4% in 1998 to 7.3% in 2009.⁸ Despite reported technical difficulties in the laparoscopic approach, MIDP has enjoyed increasing popularity due to improved outcomes.^9,10 With the advent of robotic DP, the technical challenges related to laparoscopy can be offset, while retaining or even improving outcomes.

Methodology

An online literature search on English language was performed to identify published data on robotic pancreas surgery. Studies that presented data on pre-, intra-, and postoperative patient outcomes were selected for review. Databases consulted for the search included PubMed and Google Scholar. Terms used in the search include the following: “robotic surgery,” “robotic pancreas surgery,” “pancreas surgery,” “minimally invasive pancreas surgery,” “robotic pancreaticoduodenectomy,” and “robotic distal pancreatectomy.” While PD and DP are the most common surgeries performed on the pancreas, studies exploring all kinds of pancreatic procedures were included. The studies included in our review were summarized in a patient intervention comparison and outcome (PICO) table (Table 1).

Table 1.

Patient Intervention Comparison and Outcome Table of Pancreatic Robotic Surgery

Author (year)	n	Operation	Approach	LoS (days)	Blood loss, mL (mean)	Operative time, minutes (mean)	Complications	Conversion rate	Type of study
Giulianotti (2010)³⁰	134	Robotic pancreas surgery	RPD	9.3	394	331	26%	10.4%	Retrospective cohort
	60 PD
	46 DP
	28 other
Zhou (2011)²⁹	16	PD	RPD vs. OPD	16.4 vs. 24.3 (P = .04)	153 vs. 210 (P = .045)	718 vs. 420 (P = .011)	25% vs. 75% (P = .05)	N/A	Retrospective cohort
	8 RPD
	8 OPD
Chalikonda (2012)¹³	60	PD	RPD vs. OPD	9.79 vs. 13.26 (P = .043)	485.5 vs. 775 (P = .13)	476.2 vs. 366.4 (P = .0005)	30% LRPD vs. 44% OPD	12%	Retrospective cohort
	30 RPD
	30 OPD
Lai (2012)¹²	87	PD	RPD vs. OPD	13.7 vs. 25.8	247 vs. 774.8	491.5 vs. 264.9	50% vs. 49.3%	5%	Retrospective cohort
	20 RPD
	67 OPD
Zeh (2012)¹⁷	50	PD	RPD	10	350	568	30% major	16%	Retrospective cohort
Boggi (2013)⁶	34	PD	RPD	23	220	597	55%	0%	Retrospective cohort
Daouadi (2013)³²	124	DP	RDP vs. LDP	7.1 vs. 6.1	150 vs. 150	293 vs. 371 (P ≤ .01)	14% vs. 20% (major)	0% vs. 16%	Retrospective cohort
	30 RDP
	94 LDP
Zureikat (2013)⁷	250	Robotic pancreas surgery	Robotic vs. Open	PD 10 DP 6	50–300 range for all cohort	PD 529 DP 257	PD 14% DP 6% (major)	6%	Retrospective cohort
	132 PD
	83 DP
	35 Other
Bao (2014)¹⁵	56	PD	RPD vs. OPD	8 vs. 8	100 vs. 300 (P ≤ .001)	431 vs. 410 (P = .04)	21% vs. 21% (pancreatic fistula)	14%	Retrospective cohort
	28 RPD
	28 OPD
Chen (2015)¹¹	180	PD	RPD vs. OPD	20 vs. 25 (P = .002)	400 vs. 500 (P = .005)	410 vs. 323 (P ≤ .001)	35% vs. 40% (P = .51)	1.7%	Retrospective cohort
	60 RPD
	120 OPD
Lee (2015)²²	805	DP	RDP vs. LDP vs. ODP	5 vs. 5 vs. 7	193 vs. 262 vs. 596 (P = .05)	213 vs. 193 vs. 185 (P = .05)	60% vs. 53% vs. 74% (P ≤ .05)	14% vs. 43%	Retrospective cohort
	37 RDP
	131 LDP
	637 ODP
Shi (2016)³³	43	Enucleation	Robotic vs. open enucleation	22.6 vs. 23.9	76 vs. 157.1	124.6 vs. 198.5	46.2% vs. 47.1%	0%	Retrospective cohort
	26 robotic
	17 open
Zureikat (2016)²⁸	1028	PD	RPD vs. OPD	8 vs. 8	200 vs. 300 (P ≤ .001)	402 vs. 300 (P ≤ .001)	23.87% vs. 23.7% (major)	4.7%	Retrospective cohort
	211 RPD
	817 OPD
Xourafas (2017)²⁰	1815	DP	RDP vs. LDP vs. ODP	5 vs. 5 vs. 7 (P ≤ .001)	N/A	243 vs. 205 vs. 222 (P ≤ .0001)	37% vs. 36% vs. 45% (P = .047)	8% vs. 16% (P = .0068)	Retrospective cohort
	200 RDP
	694 LDP
	921 ODP
Liu (2017)²³	204	DP	RDP vs. LDP	7.67 vs. 8.58 (P = .032)	100 vs. 100 (P = .69)	207 vs. 199 (P = .41)	41% vs. 45% (P = .57)	3% vs. 10% (P = .7)	Case–control propensity-matched study
	102 RDP
	102 LDP

P-scores listed when available. Overall complications listed unless specified otherwise. Major complications refer to Clavien–Dindo grades 3–4.

DP, distal pancreatectomy; LDP, laparoscopic DP; LoS, length of stay; LPD, laparoscopic PD; LRPD, laparoscopic-robotic pancreaticoduodenectomy; ODP, open DP; OPD, open PD; PD, pancreaticoduodenectomy; RDP, robotic DP; RPD, robotic PD.

Results

Robotic PD and DP

Published literature regarding robotic pancreatic surgery has increased in the last few years from a few small case series to robust cohorts in high-volume centers. The first series to appear was the one by Giulianotti et al. They described a cohort of 134 patients who underwent robotic surgery for pancreatic disease. Sixty patients underwent PD, 23 spleen-preserving DP, 3 middle pancreatectomies, 1 total pancreatectomy, and 3 enucleations. They reported an overall morbidity of 26% and a mortality of 2.23%. Fourteen surgeries had to be converted to open procedures. This series stimulated interest to replicate robotic pancreatic surgery and to further establish its feasibility compared with laparoscopic and open techniques. The largest series published to date is by Zureikat et al. composed of 250 patients undergoing pancreatic surgery; the majority of patients (132) had a PD. The authors reported 90-day morbidity (Clavien–Dindo grade 3–4) of 21% for PD and 13% for DP. Interestingly, complication rates were significantly different in the first 100 procedures than on the last 150, suggesting that with increased experience, complication rates improved.⁷ One of the most encouraging findings in this article is the observation that establishing a learning curve results in improved outcomes over time, justifying the notion that training and educational programs in pancreatic robotic surgery are needed.

Several studies have found that length of hospital stay was shorter in minimally invasive (including robotic) procedures, as well as lower intraoperative blood loss.^4,11–15 Others, such as the study published by Bao et al., found no significant difference in length of stay between the two approaches.¹⁵ Two meta-analysis, however, favor a shorter length of stay for MIS.^2,16 One of the principal concerns of robotic surgery is the longer operative time required. Earlier series of robotic PD showed a comparatively higher operation time,^6,13,17 but there is evidence that operation time is inversely related to number of cases performed by the surgeon, suggesting that increased experience also improves outcomes.^7,18 There are some recent series that report operative times similar to open surgeries.^19,20 However, there are still concerns that increased costs associated with robotic surgery are not offset by these advantages.²¹ Conversion rates for MIS range from 0% to 43%.^6,20,22,23 A recent study by Beane et al. addressed surgical outcomes for MIS that was converted to open, compared with planned open procedures. In general, conversions were associated with higher 30-day mortality, transfusions, and need for percutaneous drain placement.²⁴

As most PDs and a significant number of DPs are performed for the treatment of pancreatic cancer, oncologic outcomes are a major concern when evaluating the safety and feasibility of robotic PD. Negative margin (R0) resections in published robotic PD series range from 74% to 87%.^2,17,25 Large studies comparing the two techniques have found comparable R0 rates between open versus robotic approaches.²⁶ One comparative study that used data from the NCDB found significantly improved R0 resection rates in patients undergoing minimally invasive PD.¹⁴ Another important oncologic factor possibly affected by operative technique is the number of harvested lymph nodes. The American Joint Committee on Cancer (AJCC) requires at least 12 lymph nodes resected for adequate staging of pancreatic cancer. Various studies have addressed this potential problem, with a systematic review showing a trend in favor of robotic PD as to number of lymph nodes resected and a higher rate of margin-negative resection.²⁷ A recent multicenter review of oncologic outcomes comparing robotic versus open techniques reported a significant increase of lymph nodes harvested in the robotic approach (27.5 versus 19, P ≤ .001) and a significantly reduced rate of positive margins (31% versus 50%, P = .002).²⁸

Postoperative pancreatic fistula (POPF) is one of the most feared complications of pancreatic surgery. POPF has been classified by the International Study Group of Pancreatic Fistula (ISGPF) as grade A, B, or C. PF grade B and C are considered to be clinically relevant-POPF (CR-POPF). An early report of 16 patients undergoing robotic versus open PD reported similar outcomes in terms of CR-POPF (2 versus 3 patients, P = .05).²⁹ More recent literature also suggests that CR-POPF rates are comparable between robotic and open PD, ranging from 8.6% to 35%.^{11,12,15,30,31} Again, the evidence shows that morbidity rates (including CR-POPF) decrease after the surgeon has performed a certain number of cases. Boone et al. report that POPF rates were significantly decreased after 40 cases (27.5% versus 14.4%, P = .04).¹⁸

One of the most recent studies by Liu et al.,²³ with a well-matched propensity score analysis from recent robotic experience in DP (2011–2015), compared robotic versus laparoscopic technique. The variables analyzed in this study showed a reduced rate of conversion to laparotomy particularly in larger tumors, improved spleen, and vessel preservation in selected patients and most importantly reduced postoperative stay.

The studies addressing robotic pancreatic surgery, while hampered by heterogeneity in population and outcomes analyzed, demonstrate a constant trend in the benefits in regard to hospital length of stay, blood loss, and oncologic outcomes. A PICO table (Table 1) shows a comparison of the most impactful studies and allows for a quick review of the evolution of robotic pancreatic surgery and its outcomes.

Training and Credentialing

The opportunity to perform complex pancreatic operations with robotic assistance resulted in a wide range of educational challenges, which had been addressed partially in multiple articles. The proper training and set up of programs have been the keys for the larger series success in their reported outcomes.

A study conducted at the University of Pittsburgh to assess the learning curve associated with robotic PD concluded that surgeons needed to complete at least 80 cases for outcomes optimization. Parameters such as conversion rates and blood loss were the first to reach optimization at 20 cases, followed by incidence of pancreatic fistulas at 40 cases, and finally operative time was made to be comparable (mean of 417 minutes) to open procedures after 80 cases.¹⁸ However, Andolfi and Umanskiy have found that the transition of skills from open or laparoscopy to robotic surgery is not a linear process. Surgeons experienced in open or laparoscopic procedures may have an easier time transferring skills to a robotic platform, but they must still get used to the degree of freedom and articulation afforded by the robot, as well as to the spatial separation of the surgeon from the surgical field. As such, credentialing pathways are being developed to standardize the performance of surgeons coming to robotic surgery, along with curricular activities designed to meet the requirements defined by such pathways.^34–36 In the University of Pittsburgh Medical Center, a proficiency-based robotic training curriculum has been developed and consists of five steps: (1) virtual reality simulation, (2) inanimate biotissue, (3) video review, (4) operative coaching, and (5) outcomes scrutiny with ongoing quality assurance.^37–39

Conclusion

In this article, we have reviewed some of the trends and data compiled from multiple studies since pancreatic robotic surgery emerged and its benefits have been a matter of controversy.

The studies reviewed clearly demonstrate encouraging outcomes, but education and training is absolutely paramount for surgeons interested in adopting robotic technology for pancreatic surgery. It is anticipated that this technology will become more affordable in the near future, as new competitive systems arrive on the market.

As in many emerging procedures, larger prospective cohorts are still needed to fully resolve the questions regarding the benefits of robotic surgery in the field of pancreatic surgery. However, one cannot ignore the growing body of positive data available as surgeons become more skilled, programs gain experience, and institutions increase funding of technological advances in surgical fields.

Footnotes

Disclosure Statement

No competing financial interests exist.

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