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Correspondence Marc G. Besselink, Department of Surgery, Academic Medical Center, PO Box 22660, 1105 AZ, Amsterdam, The Netherlands. Tel: +31 20 5669111.
Minimally invasive (MI) pancreatic surgery appears to be gaining popularity, but its implementation throughout Europe and the opinions regarding its use in pancreatic cancer patients are unknown.
Methods
A 30-question survey was sent between June and December 2014 to pancreatic surgeons of the European Pancreatic Club, European-African Hepato-Pancreato-Biliary Association and 5 European national pancreatic societies. Incomplete responses were excluded.
Results
In total, 237 pancreatic surgeons responded. After excluding 34 incomplete responses, 203 responses from 27 European countries were included. 164 (81%) surgeons were employed at a university hospital, 184 (91%) performed advanced MI surgery and 148 (73%) performed MI distal pancreatectomy. MI pancreatoduodenectomy was performed by 42 (21%) surgeons, whereas 9 (4.4%) surgeons had performed more than 10 procedures. Robot-assisted MI pancreatic surgery was performed by 28 (14%) surgeons. 63 (31%) surgeons expected MI distal pancreatectomy for cancer to be inferior to open distal pancreatectomy concerning oncological outcomes. 151 (74%) surgeons expected to benefit from training in MI distal pancreatectomy and 149 (73%) were willing to participate in a randomized trial on this topic.
Conclusions
MI distal pancreatectomy is a common procedure, although its use for cancer is still disputed. MI pancreatoduodenectomy is still an uncommon procedure. Specific training and a randomized trial regarding MI pancreatic cancer surgery are welcomed.
Introduction
Minimally invasive (MI) approaches to gastrointestinal diseases are on the rise worldwide, but evidence from randomized controlled trials, especially in cancer patients, is lacking.
Since the first publication on laparoscopic pancreatic surgery in 1994, its introduction into surgical practice has been rather slow. Although the popularity of laparoscopic pancreatic surgery seems to increase in recent years, there is no data available on the implementation of this approach.
Outcomes after distal pancreatectomy for malignant disease are still poor and it is unclear whether laparoscopy could improve postoperative outcomes.
Several recent systematic reviews have shown superior outcomes of laparoscopic distal pancreatectomy compared to open surgery concerning blood loss, spleen-preservation and length of hospital stay.
Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis.
A systematic review and meta-analysis of laparoscopic versus open distal pancreatectomy for benign and malignant lesions of the pancreas: it's time to randomize.
However, a recently published systematic review showed that only 5 comparative cohort studies on laparoscopic versus open distal pancreatectomy exclusively for cancer were available.
However, laparoscopic distal pancreatectomy is being increasingly utilized and, therefore, it is interesting to investigate the attitudes and future prospects of surgeons towards this procedure.
A systematic review and meta-analysis of laparoscopic versus open distal pancreatectomy for benign and malignant lesions of the pancreas: it's time to randomize.
What is the general opinion regarding laparoscopic distal pancreatectomy for pancreatic cancer? What is the incidence of this procedure and what do surgeons need to enable the implementation of the laparoscopic approach for cancer in their center? And how often is this procedure performed via a robot-assisted approach?
Similarly, comparative literature on laparoscopic versus open pancreatoduodenectomy is limited. A recently published matched case–control study showed that patient selection plays an important role.
Nevertheless, after case-matching, the laparoscopic approach was associated with a significantly shorter postoperative hospital stay, but at the detriment of longer operative time and possibly increased costs.
A recent systematic review of cohort studies concluded that laparoscopic pancreatoduodenectomy is feasible and safe in selected patients, when operated by expert surgeons trained in both laparoscopic and pancreatic surgery.
This MI approach to pancreatic surgery is evolving and is suggested to have some benefits as well as disadvantages compared with laparoscopic and open pancreatic surgery.
However, the utilization of robot-assisted pancreatic surgery in Europe is unknown.
The benefits of a MI pancreatic surgery are still unclear and it is unknown how many European surgeons perform this type of surgery, how many procedures they perform each year and whether these procedures are also performed in cancer patients. For this purpose, a specific survey was developed, with the aim to give insights in attitudes and prospects towards these procedures and its implementation, to investigate whether specific training on MI distal pancreatectomy is desired and to identify European pancreatic surgeons who would like to participate in a future randomized controlled trial focusing on MI pancreatic surgery in patients with pancreatic cancer.
Methods
Survey target group
An online survey was sent to all surgeon members of the European Pancreatic Club, the European-African Hepato-Pancreato-Biliary Association and the national pancreatic societies of the United Kingdom, Italy, Spain, the Netherlands and Belgium using SurveyMonkey® (www.surveymonkey.com). Since the survey was sent by these associations and the membership lists are confidential and known to be partially overlapping, the total number of invitees could not be retrieved. The survey was conducted between June and December 2014 and consisted of 30 questions. Non-responders received up to two reminders. Incomplete responses were excluded.
Investigated parameters
Investigated parameters included hospital type, country of origin, details of surgical experience (surgery, open pancreatic surgery, MI pancreatic surgery), attitudes towards MI pancreatic surgery, essential elements of MI pancreatic surgery for cancer, views on training in laparoscopic pancreatic surgery and interest in future randomized trials on MI distal pancreatectomy for cancer.
Definitions
MI surgery was defined as laparoscopic or robot-assisted surgery. Advanced MI gastrointestinal surgery was defined as any MI procedure of the gastrointestinal tract beyond gallbladder surgery, appendectomy or inguinal hernia repair surgery.
Statistical analysis
Variables were processed and analysed using IBM SPSS Statistics for Microsoft Windows 22.0th Edition (SPSS, Armonk, NY, USA). Data were reported as number with percentage or as median with interquartile range (IQR). Sensitivity analyses were performed; 1) by excluding countries with > p75% relative response rate (defined as number responders per 5 million inhabitants) and 2) by excluding the 9 Western European countries as defined by the United Nations Statistical Commission (http://unstats.un.org/unsd/methods/m49/m49regin.htm, accessed March 15, 2015).
Results
Demographics
Responses were received from 237 pancreatic surgeons, of which 34 were excluded due to incompleteness, leaving 203 responses available for analysis. Responders originated from 27 European countries, as shown in Fig. 1. The majority of responders were from Spain (n = 29), the United Kingdom (n = 28), the Netherlands (n = 28), Italy (n = 23) and Germany (n = 13). Half of all responders (n = 100 (49%)) were employed at a center in which at least 40 pancreatic head resections are performed annually.
Overall, 154 (76%) surgeons had been practicing for longer than 10 years and 91% (n = 185) had experience with advanced MI gastrointestinal surgery. Of surgeons performing advanced MI gastrointestinal surgery, 44% of them (n = 90) personally performed more than 20 procedures per year. Procedures performed via a MI approach are listed in Table 1. Interestingly, 60 (30%) surgeons declared to perform MI pancreatic-, liver- and colorectal surgery. Most surgeons (n = 160 (79%)) performed 1 to 30 pancreatic resections annually and a minority of surgeons (n = 20 (10%)) performed more than 50 pancreatic resections annually, see Table 2. Of all responding surgeons, 68 (33%) pointed out to have a surgical robot system available, but only 28 (14%) surgeons used this robot for pancreatic surgery.
The majority of responding surgeons (n=148 (73%)) had some experience with MI distal pancreatectomy, but only 15 (7%) surgeons had experience with this procedure for more than 10 years. The total number of MI distal pancreatectomies performed per surgeon is shown in Table 3. The median proportion of distal pancreatectomies performed via a MI approach per surgeon was 30% (interquartile range 10%–70%). Of all distal pancreatectomies, surgeons declared to preserve the spleen in a median of 30% of patients (interquartile range 10%–50%).
Table 3Personal experience with distal pancreatectomy
Minimally invasive distal pancreatectomy
Number of surgeons
Total number of minimally invasive distal pancreatectomies performed personally
None
55 (27.1%)
1–10
71 (35.0%)
11–20
43 (21.2%)
21–50
22 (10.8%)
51–100
9 (4.4%)
>100
3 (1.5%)
Annual number of minimally invasive distal pancreatectomies performed for cancer
1–5
75 (36.9%)
6–10
20 (9.9%)
11–15
3 (1.5%)
Essential components of a oncological radical distal pancreatectomy
Feasibility of MI distal pancreatectomy for cancer
The average annual number of MI distal pancreatectomies for cancer and items which are considered essential for an oncological radical distal pancreatectomy are summarized in Table 3. In total, 63 (31%) of surgeons expected oncologic outcomes after MI distal pancreatectomy for cancer to be inferior to open distal pancreatectomy, mainly regarding lymphadenectomy, resection margins or survival. In addition, without asking for it, 11 (5%) surgeons stated in a free text box that a randomized trial on this subject is warranted before drawing any conclusions. Tumor involvement of at least one organ besides the pancreas was considered a contraindication for a MI approach by 121 (60%) surgeons, malignant disease by 40 (20%) surgeons, morbid adiposity by 34 (17%) surgeons and chronic pancreatitis by 30 (15%) surgeons.
Implementation of MI distal pancreatectomy
Reported barriers for the implementation of MI distal pancreatectomy were insufficient training, concerns about oncological efficiency, higher costs and a low indication frequency. Even more surgeons saw barriers of performing MI distal pancreatectomy for cancer, mostly because of the technical difficulty and the lack of experience. 92 (45%) of all surgeons noted that they did not have sufficient training in laparoscopic distal pancreatectomy for all indications and 151 (74%) surgeons declared that they would benefit from expert training in laparoscopic distal pancreatectomy for cancer, preferably in a combined training program that includes video training, central training and proctoring on-site. Despite the need for training in laparoscopic distal pancreatectomy, 149 (73%) surgeons declared to be willing to participate in a randomized controlled trial on MI versus open distal pancreatectomy for cancer.
MI pancreatoduodenectomy
In total, 42 (21%) surgeons reported experience with MI pancreatoduodenectomy (see Table 4). Furthermore, 35 (17%) surgeons had 1–5 years of experience with this technique. The total number of MI pancreatoduodenectomies performed per surgeon is summarized in Table 4. These surgeons declared to perform a median of 5% (interquartile range 0–13) of pancreatoduodenectomies via a MI approach. Finally, 132 (65%) surgeons pointed out that a laparoscopic approach to pancreatoduodenectomy is a technical problem.
Table 4Total personal experience with minimally invasive pancreatoduodenectomy
Excluding countries with > p75% relative response rate did not change the main study outcomes (75/95 (79%) experience with MI distal pancreatectomy, 25/95 (26%) experience with MI pancreatoduodenectomy and 35/95 (37%) concerns with MI pancreatic surgery for cancer). Likewise, the sensitivity analyses excluding 9 Western European countries also did not change the main study results (45/61 (74%) experience with MI distal pancreatectomy, 12/61 (20%) experience with MI pancreatoduodenectomy and 24/61 (39%) concerns with MI pancreatic surgery for cancer).
Discussion
This pan-European survey showed that the majority of responding European pancreatic surgeons has experience with MI distal pancreatectomy but only a minority is experienced with MI pancreatoduodenectomy. A minority of surgeons utilizes robot-assisted MI pancreatic surgery. The feasibility and safety of MI distal pancreatectomy for cancer was questioned by about a third of pancreatic surgeons. The majority of surgeons indicate that training in MI pancreatic cancer surgery and a randomized controlled trial on MI versus open distal pancreatectomy for cancer would be welcomed.
There are no comparable studies which focussed on the implementation of MI pancreatic surgery in an entire continent. Most surgeons participating in this survey had rather extensive experience with both pancreatic surgery and advanced MI gastrointestinal surgery, and most surgeons already got acquainted with MI distal pancreatectomy. The relatively low proportion (30%) of distal pancreatectomy performed via a MI approach may be considered surprising, especially when expert centers report use of MI pancreatic surgery in 60–80% of procedures.
Nevertheless, this outcome is comparable to those of recent nationwide studies that found a proportion of MI approaches to pancreatic surgery of 10%, 28% and 15% in the Netherlands, Italy and the United States respectively.
Robot-assisted MI surgery was introduced in the late ‘90s, but the first publications on robot-assisted MI pancreatic surgery appeared 5–10 years later.
As of these days, robot-assisted MI pancreatic surgery is gaining popularity. The benefits and disadvantages of robot-assisted pancreatic surgery over laparoscopic pancreatic surgery regarding costs are not clear yet, as some studies suggested superiority
Referring to these publications, one would expect that the robot-assisted approach would have become quite common. Interestingly, this survey shows that this is neither the case for laparoscopic nor robot-assisted MI pancreatic surgery. This is even more interesting when considering that the results of this survey could be biased, as surgeons with a positive attitude towards MI pancreatic surgery are probably more likely to have completed the survey. The slow rate by which MI pancreatic surgery is implemented may be due to the low-volume and high-risk nature of pancreatic surgery. In this survey, the majority of medical centers reported to perform only 5–10 distal pancreatectomies annually. These low-volume characteristics were also shown in a multicenter survey on the technique and variability of perioperative pathways of distal pancreatectomy.
An apparently important barrier for the widespread introduction of MI pancreatic surgery are concerns regarding oncological safety. The general poor postoperative prognosis of patients with pancreatic cancer makes it hard to measure differences between surgical approaches. The absence of sufficient training, such as dedicated courses, fellowships or mentoring programs, might also be a barrier in the introduction of MI pancreatic surgery.
Surgeons pointed out that structured training, including video training, central training and proctoring on-site, would be welcomed. Before starting a training program on laparoscopic pancreatic surgery, research on the effectiveness of possible training methods is needed. Such training programs might be easiest to organize on a regional or national level, but preparations for a pan-European fellowship on MI hepato-pancreato-biliary surgery are also underway. Another barrier could be the lack of evidence on the benefits of MI pancreatic surgery, especially when focusing on cancer treatment. Randomized controlled trials on this subject could improve clarity regarding potential benefits and hereby also accelerate further implementation. Ideally, a randomized trial on MI versus open distal pancreatectomy for cancer would primarily focus on the non-inferiority of the MI approach concerning postoperative survival. Given the small number of pancreatic cancer cases per center per year, such a trial would necessitate collaboration of many high-volume pancreatic centers, as even in a non-inferiority setting over 1000 patients are needed and would seem unlikely. Alternatively, based on outcomes of a recent systematic review by Ricci et al.,
a randomized non-inferiority trial primarily focusing on radical resection rates and secondarily on postoperative survival would be feasible and is currently being prepared by the authors.
In this survey, no consensus was seen on the details of MI distal pancreatectomy for pancreatic cancer. For instance, only a minority of surgeons (19%) considered the key elements of a radical antegrade modular pancreatosplenectomy (RAMPS), as described by Strasberg et al.,
essential in order to achieve radical resection margins. This procedure is frequently recommended in the literature and there is some evidence on its superiority compared to conventional distal pancreatectomy for cancer.
Outcomes after distal pancreatectomy for pancreatic cancer are still poor and it would be interesting to assess the effect of further implementation of the RAMPS in Europe.
Surprisingly, only two-thirds of pancreatic surgeons considered splenectomy during distal pancreatectomy for cancer essential for oncological radical resection, despite the recommendations of the International Study Group on Pancreatic Surgery (ISGPS).
Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS).
A strength of this survey is its circulation through several societies involved in pancreatic surgery in Europe. A limitation is the unknown denominator. Due to the confidentiality of membership lists, the response rate of this survey is unfortunately unknown. Nevertheless, a large group of pancreatic surgeons from 27 countries replied. There did appear to be some misbalance between country size and the number of responses. However, a sensitivity analysis failed to detect a clear impact of this imbalance on the main study outcomes, as the main study outcomes did not change after excluding countries with the relatively highest rate of responses and after excluding the 9 Western European countries. Importantly, outcomes of this pan-European survey are probably biased, as surgeons performing MI pancreatic surgery will be more likely to respond.
In conclusion, MI distal pancreatectomy is performed by the majority of European pancreatic surgeons, although its benefits for cancer are still under debate. MI pancreatoduodenectomy is still an uncommon procedure in Europe. Specific training in MI pancreatic cancer surgery is welcomed, as well as future randomized controlled trials on MI surgery for pancreatic cancer. Future studies should also assess these items and other areas of controversy in all regions of the world. This will be explored during the upcoming first international state-of-the-art conference on MI pancreatic resection staged by the International Hepato-Pancreato-Biliary-Association, which will be held on April 20, 2016 in São Paulo, Brazil (http://www.ihpba2016.com/scientificprogram/consensus.html).
Conflicts of interest
None declared.
References
Clinical Outcomes of Surgical Therapy Study Group
A comparison of laparoscopically assisted and open colectomy for colon cancer.
Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis.
A systematic review and meta-analysis of laparoscopic versus open distal pancreatectomy for benign and malignant lesions of the pancreas: it's time to randomize.
Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS).
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