Over the past decade, minimally invasive surgery has been introduced as a means to allow manipulation of delicate tissues with outstanding visualization of the surgical field. The purpose of this article is to review the available literature regarding early postoperative outcomes and the technical challenges of minimally invasive pancreaticoduodenectomy, including robotic techniques. Herein, we provide a retrospective review of all published studies in the English literature in which a minimally invasive pancreaticoduodenectomy was performed. The reported advantages of minimally invasive pancreaticoduodenectomy include better visualization, faster recovery time, and decreased length of hospital stay. In cases of robotic approaches, some of the proposed advantages include increased dexterity and a superior ergonomic position for the operating surgeon. To our knowledge, few studies have reported results comparable to open techniques in oncologic outcomes with regard to the number of lymph nodes resected and clear margins obtained. An increasing number of pancreatic resections are being performed using minimally invasive approaches. It remains to be determined if the benefits of this technique outweigh its longer operative times and higher costs.
A pancreaticoduodenectomy (PD) has been universally accepted as the only chance for cure for patients with cancerous tumors on the head of the pancreas, distal common bile duct tumors, and periampullary malignant tumors. Since first described by Alessandro Codivilla in 18981 and later popularized by Whipple et al2 in 1935, significant improvements have been achieved in the preoperative, intraoperative, and postoperative management of patients with pancreatic cancers, resulting in decreased morbidity and mortality rates when surgical procedures are performed at high-volume institutions.3 These advances have allowed surgeons to explore less invasive alternative techniques with the intention of obtaining faster recovery times while maintaining sound oncologic outcomes.4- 6 Over the last several years, the introduction of minimally invasive techniques and robotic systems to the field of surgical oncology has allowed for improved visualization of the surgical field with precise manipulation of delicate tissues. For patients with pancreatic cancer, this is of paramount importance because an increasing number of patients undergo neoadjuvant therapy prior to surgical resection, which makes the distinction of normal dissection planes challenging. To date, only a handful of institutions have retrospectively reported their experience with laparoscopic and robotic PD (Table), with conflicting results. With this background, the purpose of our study is to review the current data available on minimally invasive PD.
Laparoscopic PD was first reported in 1994 by Gagner and Pomp4 in a young patient with chronic pancreatitis from pancreas divisum. Since then, a growing number of surgeons have published their early experience with these procedures.5,6,11- 13 These early studies mainly focused on the feasibility of the technique and on early postoperative outcomes. In general, early data show outcomes similar to those with open techniques, with faster recovery times as evidenced by shorter intensive care unit and overall hospital stays. A recent review by Gumbs et al14 published in 2011 found 27 articles comprising 285 cases of laparoscopic PD, including 13% of hand-assisted cases. In this extensive review,14 the rate of conversion to an open approach was 9%, with a weighted average length of stay of 12 days and a morbidity rate of 48%. Based on these findings, Gumbs et al14 concluded that laparoscopic pancreatic head resections are not only feasible but also safe, with low mortality rates and acceptable complication rates. The authors further emphasized the lack of long-term follow-up data and the relatively small number of studies comparing minimally invasive techniques with open techniques.14
With the increasing number of surgeons rapidly gaining experience in complex laparoscopic pancreatic techniques, the first reports of comparative studies have recently been published.9,11,15 In a retrospective review of 51 consecutive patients who underwent either an open or a laparoscopic PD, Kuroki and colleagues15 found decreased blood loss in the laparoscopy-assisted PD group compared with the open PD group. Furthermore, these investigators found no significant differences in the occurrence of postoperative complications between the 2 groups.15 To our knowledge, Asburn and Stauffer11 recently published the largest comparative study of more than 260 patients, 53 of whom underwent a laparoscopic PD. Intraoperative and postoperative factors in favor of a laparoscopic approach included decreased blood loss, shorter lengths of hospital stay and intensive care unit stay, transfusion requirements, and greater number of lymph nodes retrieved at the time of the operation. Importantly, no differences were noted in the rate of early postoperative morbidity or mortality. As expected, operative times were significantly longer for laparoscopic cases, with a mean (SD) time per case of 541 (88) minutes (9 hours).
It is generally accepted that the use of robotic systems provides improved visualization with 3-dimensional imaging and improved movement of instrumentation in limited spaces and ensures better ergonomics for the operating surgeon16 (Box). These observations arose from a series of retrospective studies describing the first experiences using robotics for PD. Giulianotti and colleagues7 reported in 2010 the first series of 50 patients who underwent robotic-assisted PD in Italy and the United States. In this retrospective study, the median operative time was 421 minutes (range, 240-660 minutes), with a median blood loss of 394 cm3 (range, 80-1500 cm3). The length of stay significantly varied depending on the location. In the Italian group, the mean length of stay was 28.7 days, whereas in the US group, the mean length of stay was 12.5 days. In this series,7 6 patients had a grade A fistula postoperatively, 5 patients had a grade B fistula postoperatively, and 1 patient had a grade C fistula postoperatively. More recently, in a single-institution retrospective review, Zureikat and colleagues17 reported on 24 patients who underwent a robotic-assisted nonpylorus-preserving PD at the University of Pittsburgh in Pennsylvania. The median operative time in this study17 was 512 minutes (range, 327-848 minutes), with a median blood loss of 320 cm3 (range, 50-1000 cm3) and a median length of stay of 9 days (range, 4-87 days). The overall pancreatic fistula rate was 27% (n = 8). Clavien grade III and grade IV complications occurred in 7 patients (23%), whereas Clavien grade I and grade II complications occurred in 27% of patients.
Box Section Ref ID
Decreased blood loss, resulting in less transfusions
Shorter hospital stays
Shorter intensive care unit stays
Improved 3-dimensional imaging
Better visualization, increased magnification
Other investigators have compared robotic-assisted PD with open PD. Zhou et al8 reported on 16 patients who had no significant difference in negative margin rates but had lower rates of blood loss, lower complications rates, and decreased lengths of stay with robotic-assisted PD. The low number of patients in this study8 prohibits any meaningful statistical analysis. A larger study by Chalikonda and colleagues9 compared 30 patients undergoing robotic-assisted PD with 30 patients undergoing open PD; both groups had similar demographic characteristics and surgical indications. Operative times were significantly longer in the robotic-assisted group, but their overall blood loss was lower. The mean lengths of stay were significantly different between groups (9.79 days for the robotic-assisted group vs 13.26 days for the open group; P = .04). Based on these limited data, both studies8,9 concluded that robotic-assisted PD might be associated with faster recovery times but longer operative times.
With regard to immediate oncologic outcomes, Zeh et al18 reported on 50 consecutives patients who underwent a robotic-assisted PD (36 underwent a classic PD, and 14 underwent a pylorus-preserving PD). The median tumor size was 2.5 cm, with a mean (SD) of 17 (7) lymph nodes retrieved. For these patients, the overall margin-negative (R0) resection rate was 89%. Importantly, 11 of the 15 patients who met the criteria for adjuvant therapy were treated at a mean follow-up of 11.5 weeks postoperatively.
The main limitations of robotic procedures are related to the high costs associated with the purchase of the robotic system and disposable equipment19 and the steep learning curve associated with the technique. To date, studies comparing the cost-effectiveness of robotic-assisted PD or minimally invasive PD with the cost-effectiveness of open PD have not been conducted.
As with other complex operations, there is a lack of data regarding the recommended number of procedures a surgeon should perform before attempting robotic-assisted PD. Undoubtedly, prior extensive experience in hepatopancreatobiliary surgery is mandatory, and training in minimally invasive PD is typically recommended. Proctored testing tailored to the curriculum is often required by credentialing departments before establishing a new program.20
Minimally invasive techniques provide some benefits to patients requiring a PD. The robotic systems currently available are not hindered by some of the limitations that plague laparoscopic techniques, such as a limited range of motion, a 2-dimensional visualization of the surgical field, and poor ergonomics for surgeons. For example, the ability of the system to compensate for natural tremors may allow for a more precise technique when a delicate anastomosis is constructed.10 However, it is intriguing that the available data on minimally invasive techniques have failed to demonstrate improvements in outcomes, such as leak rates and conversion rates, compared with the outcomes associated with laparoscopic techniques. The need for a longer learning curve might serve to explain some of these issues.
Currently, data on oncologic outcomes have been limited to a few retrospective reports, and there is a lack of literature investigating the financial implications of this approach. The need for cost-effective approaches that could potentially provide similar or better early and late results is essential in times of financial difficulties. Although shorter hospital stays are certainly appealing, based on currently available data, the faster recovery times associated with minimally invasive approaches have not resulted in adjuvant chemotherapy being initiated sooner. From the perspective of general surgery residents, it is imperative to understand that only after rigorous unbiased examination could minimally invasive PD potentially become a valid tool in the armamentarium of surgeons for treating pancreatic cancer.
Accepted for Publication: February 15, 2013.
Corresponding Author: Sebastian G. de la Fuente, MD, Department of Surgical Oncology, Florida Hospital Orlando, 2415 N Orange Ave, Ste 400, Orlando, FL 32804 (firstname.lastname@example.org).
Published Online: October 23, 2013. doi:10.1001/jamasurg.2013.366.
Author Contributions: Arnoletti and de la Fuente had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Zenoni, de la Fuente.
Acquisition of data: Zenoni, de la Fuente.
Analysis and interpretation of data: All authors.
Drafting of the manuscript: All authors.
Critical revision of the manuscript for important intellectual content: Zenoni, de la Fuente.
Conflict of Interest Disclosures: None reported.
Thank you for submitting a comment on this article. It will be reviewed by JAMA Surgery editors. You will be notified when your comment has been published. Comments should not exceed 500 words of text and 10 references.
Do not submit personal medical questions or information that could identify a specific patient, questions about a particular case, or general inquiries to an author. Only content that has not been published, posted, or submitted elsewhere should be submitted. By submitting this Comment, you and any coauthors transfer copyright to the journal if your Comment is posted.
* = Required Field
Disclosure of Any Conflicts of Interest*
Indicate all relevant conflicts of interest of each author below, including all relevant financial interests, activities, and relationships within the past 3 years including, but not limited to, employment, affiliation, grants or funding, consultancies, honoraria or payment, speakers’ bureaus, stock ownership or options, expert testimony, royalties, donation of medical equipment, or patents planned, pending, or issued. If all authors have none, check "No potential conflicts or relevant financial interests" in the box below. Please also indicate any funding received in support of this work. The information will be posted with your response.
Some tools below are only available to our subscribers or users with an online account.
Download citation file:
Web of Science® Times Cited: 3
Customize your page view by dragging & repositioning the boxes below.
Enter your username and email address. We'll send you a link to reset your password.
Enter your username and email address. We'll send instructions on how to reset your password to the email address we have on record.
Athens and Shibboleth are access management services that provide single sign-on to protected resources. They replace the multiple user names and passwords necessary to access subscription-based content with a single user name and password that can be entered once per session. It operates independently of a user's location or IP address. If your institution uses Athens or Shibboleth authentication, please contact your site administrator to receive your user name and password.