Pancreatic cancer is one of the most aggressive and lethal tumours in Western society (1). However, despite the advances in oncological therapy, the only chance of cure for patients with this disease is surgery to remove macroscopic and microscopic diseases (R0). Unfortunately, due to distant metastasis or locally invasive disease at the time of the diagnosis, only a few patients with pancreatic cancer are candidates for surgical therapy (2). The median disease-free survival time following complete resection and adjuvant chemotherapy is about 13–14 months (3). Approximately 19% of pancreatic cancer patients survive one year after diagnosis and 4% for five years, making this disease so lethal (4).
Nevertheless, surgery could be considered the cornerstone of multidisciplinary treatment that combines the benefit of surgery, chemotherapy, and radiotherapy to achieve the best results (2). Pancreatic surgery can be considered a challenge for open and laparoscopic surgeons, even if the accuracy of gland dissection, due to the close relationship between pancreas, the portal vein, and mesenteric vessels, besides the reconstructive phase (in pancreaticoduodenectomy), lead to significant difficulties for laparoscopic technique. Minimally invasive pancreatic surgery changed utterly with the development of robotic surgery, in particular since the introduction of the Da Vinci robotic platform (Intuitive Surgical, Sunnyvale, CA, USA). The robotic approach provides a three-dimensional stereoscopic view of the operating field; also, Endowrist instruments mimic the human hand’s movements with seven degrees of freedom, removing hand tremor and improving the precision of dissection and suturing (1,5). For these reasons, the literature suggests many reports on minimally invasive robotic-assisted pancreatic surgery in the last years. The safety and oncologic efficacy of this approach is still doubtful, as well as the knowledge of outcomes of patients who underwent robotic pancreatic surgery.
This review aims to summarize the current literature about robotic pancreatic surgery and underline which are the short-term and long-term morbidity comparing robotic surgery with the laparoscopic and open approach.
We present the following article in accordance with the PRISMA reporting checklist (available at http://dx.doi.org/10.21037/gs-21-64).
A systematic literature search was performed in PubMed, Cochrane Library, and Scopus to identify and analyze studies published from November 2011 to September 2020 concerning robotic pancreatic surgery. The following terms were used to perform the search: “long term morbidity robotic pancreatic surgery”.
The language of full-text articles was limited to English. All titles and abstracts were analyzed to select those concerning the long term morbidity of robotic pancreatic surgery. The research leads to 40 articles from PubMed, 32 from Scopus, and only one from Cochrane Library. 11 articles were excluded, matching PubMed results with Scopus because they were identical. Also, we excluded 26 studies on different topics or inappropriate. Some discussed only the laparoscopic approach. At last, we excluded meta-analysis, review, and book reports. Finally, we collect for our study 18 results (Figures 1,2).
Eighteen articles included in the study were published between November 2011 and September 2020 (Table 1). The review included 2041 patients who underwent robotic pancreatic surgery, mainly for a malignant tumour. The two most common robotic surgical procedures adopted were the robotic distal pancreatectomy RDP (6-10) and the robotic pancreaticoduodenectomy (RPD) (2,3,11-13). In two studies (13,14), patients were divided into groups, on the one hand, those who underwent a robotic pancreaticoduodenectomy (RPD), on the other hand, those who underwent robotic distal pancreatectomy (RDP). The remaining items included surgical approaches such as robotic middle pancreatectomy (RMP) (15,16), robotic distal pancreatectomy and splenectomy (17), robotic-assisted laparoscopic pancreatic dissection (RALPD) (18), robotic enucleation of pancreatic neuroendocrine tumors (19). At last, one study (20) evaluated outcomes of patients treated with modified robotic-assisted duodenum preserving pancreatic head resection (RA-DPPHR) and those treated with robotic-assisted pancreatoduodenectomy (RA-PD). All studies reported the median operative time (O.T.), except for Nassour et al. (14). The mean operative time ranged between 118 and 1,089 min; the O.T. was higher for robotic pancreatoduodenectomy than for distal pancreatectomy (PD 340–560 vs. DP 221–270 min). In a study (18) analyzing the learning curve of RLPD was reported a decreasing operative time from 2010 to 2013 (445 vs. 340 min). Blood loss was reported in 15 studies (3,6-8,10-13,15-21), with a range of 30–4,500 mL, more elevated for P.D. than for D.P. The case reported by Zhang et al. (15) concerning the use of RAMP in an elderly did not need blood transfusions. The conversion rate was analyzed in 12 studies (3,6,7,9-12,14,16,17,21). The overall conversion rate from the robotic approach to laparotomy varied between 0% to 18.2%, with rates higher in RPD than in laparoscopic pancreatoduodenectomy (OPD). Marino et al. (13) reported five conversions to open surgery (1 in D.P. and 4 in P.D.) for portal or superior mesenteric vein involvement, failure to progress with a high risk of inadequate oncologic resection, severe pancreatitis with massive disruption of pancreatic parenchyma on robotic touch and significant bleeding from the splenic artery (13). Massive bleeding was described in the case of Yusheng et al. (16), where five patients (5%) underwent digital subtraction angiography, and four (4%) underwent reoperation to stop the bleeding (16). All the articles reported less hospital stay than open surgery, with a range of 0 and 58 days. Nassour et al. (14) demonstrated a decreased hospital stay associated with robotic pancreatic surgery compared to the open approach, with a 20% and 50% reduction in risk of prolonged length of stay for RPD and RDP, respectively (14).
Postoperative pancreatic fistula (POPF), based on the International Study Group for Pancreatic Fistula (ISGPF), represents one of D.P’s most frequent complications. Except for Nassour et al. (14), all the authors reported the rate of POPF B and C with a variable range of 0% and 41.2%. In line with literature values, POPF rates were higher in patients treated with RPD than those who underwent RDP. Although the high value of POPF showed by Jiang et al. (20), in their review, there were no significant differences between RA-DPPHR and RA-PD groups in terms of frequencies of POPFs and biliary fistula (11.8% vs. 8.8%) (20). Postoperative complications were analyzed almost in all the reports through the Clavien-Dindo scoring system (CDC). The most important postoperative complication, besides POPF, were: wound infection, delayed gastric emptying, hemorrhagic lesions, bile leakage (22). Because the most robotic pancreatic resections were performed for malignant diseases, almost all the studies (3,6,10,12-14,16-19,21,22) reported the rate of R0 resection. The oncological safety of the robotic approach in pancreatic surgery is not yet clear because long term follow-up and data about that are not available. Many studies figured out a rate of 100% of R0 resection, in line with the literature. In contrast with these data, Zureikat et al. (12) reported a higher rate of microscopically positive surgical margins and a greater lymph node harvesting for RPD as compared with OPD. The multivariate analysis took in evidence that the operative approach was not independently associated with positive resection margin or tumor under staging (12). Ten articles (2,6-9,13,17,18,20,21) reported data relating to morbidity and 14 (2,6,8-10,12-14,16-18,20,22) about incidence of mortality. Nassour et al. (14) and Marino et al. (10) reported a reduction of the overall postoperative mortality rate in the robotic groups compared to the open one (10,14). In Marino et al.’s report, the median overall survival was nearly 35.3 months for RDP and 24.9 months for ODP. The analysis showed that intending to evaluate patients’ safety and outcome underwent robotic pancreatic surgery, a reoperation rate of 6%, and 30-day postoperative mortality of 4%. The study evidenced a rate of R0 resection for patients treated with P.D. of 90.5% and 86.7% for the D.P. With a morbidity rate of 30% and a pancreatic fistula rate of 16%, and they did not found any differences between robotic and open surgery (13). Qu et al. (17) in the score-matched study described a median Overall Survival (O.S.) rate and a median disease-free survival (DFS) of 27 and 16 months, respectively for patients treated with RDP, demonstrating, besides, a similar result for the LDP group (17). In order to identify strong indicators of morbidity after DP, Xourafas et al. (9) found those in a higher Body max index (BMI >25), preoperative system sepsis, a preoperative hematocrit of less than 35%, the use of drains, and contaminated wound presence. Short-term postoperative morbidity was significantly lower when a vascular resection was not required or when patients were discharged to rehabilitation. Patients older than 62 years old, those who did not require a pancreatic reconstruction, those with a length of stay of more than 5 days and those discharged to rehabilitation had a odds of death within 30 days significantly reduced (9). As the morbidity rate so the mortality was lower than open surgery, the range was of 1–4% at 30 day and of 0–1.9% a 90 day. Benizri et al. (7) evaluated an overall morbidity rate of 50% in patients underwent robotic and laparoscopic distal pancreatectomy and a mortality rate of 0%. No significant differences were found between the two groups (7) (Tables 2-5).
Pancreatic cancer is the fourth most common cause of adult cancer-related death, with 10.9–11.8 new cases per year (23). According to the National Cancer Institute (NCI), the mortality rates for pancreatic cancer in the USA is the same in the last two decades (24). Pancreatic resection was introduced between the 19th and 20th centuries by surgical innovators such as Billroth and Codivilla (25). With the development of advanced technology, minimally invasive techniques have increasingly been used in pancreatic surgery. Several studies reported that minimally invasive surgery improved perioperative pain control and led to postoperative morbidity rates and shorter postoperative hospital stay (26). However, laparoscopic surgery has limitations such as the restricted range of motion and two-dimensional vision; these restrictions could be overcome by robotic surgery. The Da Vinci robotic platform (Intuitive Surgical, Sunnyvale, CA, USA) provides a three-dimensional magnification of the camera system, articulated instrumentation, and increased freedom of movement for the surgical instruments (21). Da Vinci Si platform is an older system comparing with the Xi one; its main advantage is the use of a larger (12 mm) robotic camera with improved definition over the 8 mm camera (e.g., Xi) (3). The different configuration of the robot, with the Xi platform, reduces conflicts between the arms. Besides the possibility of switching the camera from a trocar to another, the table-motion feature makes it possible to change the configuration of the arms during the procedure.
On the contrary, the Si platform has only one arm dedicated to the camera, which does not allow the table’s movement when it is docked to the patient. Another advantage of the Xi platform is the ability to approach larger surgical fields than the Si one (19). Since surgical system development, many reports have been published concerning minimally invasive robotic-assisted pancreatic surgery (5). With the growing expansion of robotic surgery, Melvin (27) and Giulianotti (28) described the first robotic distal pancreatectomy and pancreaticoduodenectomy, despite though the wide acceptance of this approach for pancreatic surgery is still low.
On the one hand, in the literature, several studies demonstrated that the robotic approach reduced the length of postoperative stay, giving a lower intraoperative blood loss, overall complication rate, and R0 resection margin rate similar to open surgery. On the other hand, robotic surgery still presents drawbacks regarding its high costs and unclear oncological results (13). Alfieri et al. showed a recurrence rate, after RADP, of 6.9% in a mean time of 23.4 months represented by pulmonary metastases and hepatic metastases. In contrast, reports like the one of Boggi et al. (29) and Lai et al. (8) found less positive margin in the minimally invasive group than in the open approach (8,29). Positive margin and lymph nodes (LN) harvested are two important malignancy prognosis factors for pancreatic cancer, and the ability of surgeons could influence them. According to this hypothesis, Zhang et al. (22) analyzed the R0 resection rate and the number of lymph nodes harvested in the first 40 patients who underwent RPD compared to the later 60 patients who underwent the same operation. The results suggested a similar R0 resection rate, a similar rate of postoperative complications but an increased rate of lymph nodes harvested (22). Adequate LN sampling is a significant cancer surgery component that provides an accurate staging and risk stratification. A multi-institutional study (12) confirmed the association between RPD and the increased number of harvested LNs, suggesting the advantages of these findings mainly around the superior mesenteric artery. At the same time, it is essential to add that a significant part of robotic cases in this analysis was performed at high-volume centres where high-volume surgeons and specialized pathologists may lead to higher LN yield (14). As demonstrated by several authors (13,30,31), the gentle and meticulous dissection around large vessels allows a high rate of spleen-preserving procedures. Also, 7 degrees of freedom instruments help obtain good oncologic adequacy reaching difficult anatomic zones as the celiac nerve plexus, which is often a recurrence site (13,30,31).
For many years only benign and low-grade malignant pancreatic tumors have been treated by laparoscopic surgery; however, recent studies suggest as laparoscopy could be feasible and effective in treating pancreatic cancer. The using of Yonsei Criteria (tumor confined to the pancreas, intact fascia layer between the distal pancreas and the left adrenal gland and kidney, and tumor located more than 1–2 cm from the celiac axis) for evaluating if treatment with laparoscopic radical distal pancreatectomy is indicated, makes minimally invasive techniques highly safe and effective for achieving bloodless and margin-negative resection during the treatment of left-sided pancreatic cancer. Furthermore, studies demonstrated more also favorable long-term oncologic outcomes for patients with tumor that meet all three criteria (32). NCCN guideline version 1. 2020 pancreatic adenocarcinoma recommended surgical treatment by laparotomy or minimally invasive surgery as a treatment for resectable pancreatic cancer. Considering the oncologic significance of retroperitoneal margin in treating pancreatic cancer, to secure them during LPD, Rho et al. (33) introduced the potential application of indocyanine green to facilitate the securement of the SMA (superior mesenteric artery) lateral margin in laparoscopic PD (33). With the same aim, Kuroki et al. (34) introduced the concept of the pancreas-hanging maneuver by Penrose drain in managing SMA margin during LDP (34).
For advanced pancreatic cancer, only a few case reports and case series have been reported on the technical feasibility and safety of LPD with combined venous vascular resection. Several authors (35,36) demonstrated no statistical significance between LPD and OPD in terms of overall survival. These studies confirmed that there was no significant difference in the 5-year overall survival. In addition, LPD resulted in a higher rate of R0 resection, more harvested lymph nodes, shorter hospital stays and less estimated blood loss, so LPD is not inferior to OPD respect to long term oncologic outcomes as well as better short term surgical outcomes in patients with pancreatic cancer (35,36). Sharpe et al. (37) showed that patients who underwent LPD for pancreatic cancer in high volume centers had equivalent outcomes than OPD patients concerning on length stay, R0 resection, lymph node count and readmission rate (37). Furthermore, Kantor et al. (38) found comparable short term and long-term overall survival outcomes with OPD and LPD (38). On the basis of the last study recently performed by Van Hilst et al. (39) nine surgeons demonstrated the safety concerns with LPD. They recognized that technical feasibility, procedural safety and surgical extent for margin negative resection should be considered in defining potential indication of LPD (36,39). According to the literature, LPD could be a good alternative strategy in managing well-selected resectable pancreatic cancer.
In addition, concerning the oncological safety of the robotic technique, in literature, some studies confirm the reduction of hospital stay of robotic more than laparoscopy and open. This characteristic and its potential benefit with a less immunological response and faster adjuvant chemotherapy could lead to better survival (29). Besides, Anderson et al. (40) demonstrated that patients who underwent minimally invasive distal pancreatectomy were more likely to receive adjuvant chemotherapy, which may explain the survival difference (40).
An important factor affecting the robotic approach is the operative time. Alfieri et al. (6) found a more prolonged operative time for RDP than LDP due to the docking time and the learning curve. On the one hand, the robotic set-up took a meantime, representing 8% of all the procedure duration; on the other hand, the surgeon’s progressive experience in this new technique led to a reduction of the operative duration. Also, the propensity to use the Warshaw technique (splenic preservation during a distal pancreatectomy performed with splenic vessel ligation), for its complexity, leads to more prolonged operative time (6,41). The robotic approach seems to improve haemorrhage control better than the laparoscopic approach; thanks to using a 3D vision and the rapid switch from monopolar to bipolar energy, surgeons could control bleeding. Simultaneously, the capability to perform hand-sewn ligation during gastroduodenal artery control provides a low risk of postoperative pseudoaneurysm (13,42,43). Chen et al. (18) demonstrated that blood loss from RLPD decreased during the “learning curve”, and the large degree of freedom enables the surgeons to complete complex vessel reconstruction. They suggested that venous involvement may not be an absolute contraindication to robotic surgery; prosthetic graft reconstruction can be completed using the robotic surgery approach. Even if the robotic approach seems to improve different aspects of pancreatic surgery, the occurrence and severity of POPF did not reduce with robotic assistance (18).
The surgical technique results in a significant reduction of postoperative complications and improving patient’s quality of life. Hence, Beger (44) in 1972 described the duodenum-preserving pancreatic head resection (DPPHR) for patients with severe pancreatitis to preserve the digestive tract’s integrity while cutting off the head of the pancreas. Since that, DPPHR has become an effective surgical option for benign and premalignant pancreatic head lesions (44). Jiang et al. (20) analyzing the short and long-term outcomes of modified RA-DPPHR and RA-PD (robotic-assisted pancreatoduodenectomy), did not observe P.G. (pancreaticogastrostomy) fistulas. It suggested that the orig]in of pancreatic leakage could be from the proximal pancreatic stump rather than from the P.G.
Another great aspect of the surgery technique useful for avoiding the incidence of exocrine and endocrine insufficiency is that the use of a pancreaticogastrostomy could preserve the digestive tract’s continuity and integrity. It is easier to perform a P.G. in robotic-assisted operations, such as in open technique, thanks to the short distance between pancreatic stumps and the stomach’s posterior wall (45). It seems that P.G. led to a lower cumulative incidence of exocrine failure but a similar incidence of endocrine insufficiency and pancreatic fistula (46). Besides, as a complication, afferent loop obstruction was statistically frequent in the robotic approach, more than in OPD. It occurs in 0.3% of patients undergoing gastroenterostomy due to intestinal adhesion and angulation, internal hernia, anastomotic structure, and tumor recurrence (47,48).
In light of the propensity of pancreatic cancer to be metastatic at the time of the diagnosis, adjuvant chemotherapy could improve morbidity and substantially affect survival. Trials demonstrated an improved 10-year overall and disease-free survival rates with adjuvant gemcitabine in resected patients. The morbidity associated with pancreatic resection has a role in the ability of patients to receive adjuvant treatment. Complications are associated with a delay in the initiation of adjuvant treatment. Also, it seems that patients without postoperative complications had a significantly longer median survival than those with complications (19.5 vs. 16.1) (49). In high volume centres, the minimally invasive pancreatic resections demonstrate the potential benefit of minimizing the morbidities that hinder patient access to adjuvant therapy (50). Lee et al. (51) reported a significant survival benefit of mini-invasive surgery compared to the open group for disease-free and overall survival. Besides, patients without lymph node metastasis had a 5-year survival rate of 77.8%, suggesting a role of this group in the category of early pancreatic cancer (51). Nassour et al. (14) found no difference in 30 and 90-day mortality between RPD and OPD. On the contrary, the robotic approach was associated with lower postoperative mortality. The most significant finding of this analysis was the superior long-term survival associated with the use of the robotic platform for R.D. (14), the same results that Sulpice et al. (52) found comparing LDP to ODP (52). Quality of life (QOL) for pancreatic cancer is a crucial studied metric. Some studies demonstrated that pancreatic cancer patients undergoing resection are less likely to enrol in hospice and more likely to receive aggressive care at the end of life, so the intensity of care in the final month of life has increased in the last years (53). Also, RLPD patients presented a significantly faster nutritional status recovery thanks to the earlier resumption of oral intake, less incisional pain, and more relaxed psychological status (54).
Robotic surgery also allows some integrations, such as using U.S. scan and FireFly fluorescence technology to provide a precise localize of the lesion, the main pancreatic duct, and the vessels overcoming the absence of tactile sense and avoiding surgical injuries (19).
Comparison between robotic surgery and open surgery lead to evidence of different advantages of the robotic approach. A multidisciplinary team and a surgical center at high volume are essential for better postoperative morbidity and mortality. It is still doubtful if oncological results and cost-effectiveness are really adequate for the use of robotic pancreatic surgery. The robotic platform may contribute to additional costs regarding one procedure. However, it is the overall cost reduction of performing a wide range of procedures in a minimally invasive way that must be evaluated. As an expensive investment, the overall cost-effectiveness should be calculated on the total number of cost reductions deriving from all robotic-assisted procedures that would have been otherwise performed open or laparoscopically. Other aspects that are often overlooked concerning the advantages of minimally invasive surgery in the long term. Furthermore, the robotic platform will eventually become more affordable over time, especially when competitors share the market, which is currently a monopoly. Pancreatic surgery represents one of the most successful fields of applying the robotic platform, and its use is growing at an astonishing pace.
Like a randomized clinical trial, further research is necessary to confirm the evidence reported in this review.
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