Minimally Invasive Distal Pancreatectomy: Review of the English Literature

Abstract

Background:

Recently, the superiority of the minimally invasive approach, which results in a better cosmetic result, faster recovery, and shorter length of hospital stay, is a technique that has been progressively recognized as it has developed. And the minimally invasive approach has been applied to distal pancreatectomy (DP), which is a standard method for the treatment of benign, borderline, and part of malignant lesions of the pancreatic body and tail. This article aims to analyze the types, postoperative recovery, and outcomes of laparoscopic distal pancreatectomy (LDP).

Materials and Methods:

A systematic search of the scientific literature was performed using PubMed, EMBASE, online journals, and the Internet for all publications on LDP. Articles were selected if the abstract contained patients who underwent LDP for pancreatic diseases. All selected articles were reviewed and analyzed.

Results:

If there were no contraindications for LDP, this operation is suitable for benign, borderline, or malignant tumors of the pancreatic body and tail, which should try to be performed with preservation of the spleen. LDP is safe and feasible under some conditions to experienced surgeon. Single-incision laparoscopic distal pancreatectomy (S-LDP) and robotic laparoscopic distal pancreatectomy (R-LDP) perioperative outcomes are similar with conventional multi-incision laparoscopic distal pancreatectomy (C-LDP). And the advantages of S-LDP and R-LDP require further exploration. With the application of enhanced recovery program (ERP), length of hospital stay and costs are reduced.

Conclusions:

LDP is safe and feasible under some conditions. Compared with open distal pancreatectomy, LDP has a lot of advantages; a trend was observed for LDP to replace traditional open surgery. LDP combined with ERP is expected to become standard in the treatment of pancreatic body and tail lesions.

Introduction

The minimally invasive surgical technique (MIST) is an important branch of surgery that is widely applied. The continuous development of MIST is beneficial to both patients and surgeons, in that it allows for improved visualization of the operative site, less blood loss, better prognosis, shorter hospital stay, faster recovery, excellent cosmetic results, and so on. Therefore, the MIST has gradually become a routine approach and is predicted to replace conventional surgery.^1,2 Minimally invasive surgery of the pancreas is more challenging and complex, mainly due to its deep anatomical location and high surgical risks of bleeding and pancreatic leakage.³ Thus, compared with other operations, the application of MIST in pancreatic surgery began late and developed slowly.

Distal pancreatectomy (DP) does not require complex digestive tract reconstruction, which creates conditions for the application and development of MIST. The feasibility of laparoscopic distal pancreatectomy (LDP) was initially shown by Soper et al. in a pig animal model in 1994.⁴ Subsequently, Cuschieri et al. performed the first LDP in 1996.⁵ With the improvement of surgical devices and technology, the operative approach to LDP is changing from conventional multi-incision laparoscopic distal pancreatectomy (C-LDP) to single-incision laparoscopic distal pancreatectomy (S-LDP) and robotic laparoscopic distal pancreatectomy (R-LDP). This article will review the application and development of various MISTs for DP.

Materials and Methods

A systematic search of the scientific literature was performed using PubMed, EMBASE, online journals, and the Internet for all publications on LDP. The search was restricted to publications in English, and search terms were “single-incision laparoscopic distal pancreatectomy,” “single-port laparoscopic distal pancreatectomy,” “single-site laparoscopic distal pancreatectomy,” “laparoscopic distal pancreatectomy,” “distal pancreatectomy,” and “robotic distal pancreatectomy.” All available major publications from the review period were considered. Articles were selected if the abstract contained patients who underwent LDP for pancreatic diseases in the form of case reports, case series, and controlled or comparative studies. Conference abstracts were included if they contained relevant data. The reference lists of these articles were also reviewed to find additional candidate studies. In the case of duplicate publications, the latest and most complete study was included. All selected articles were reviewed and analyzed.

Indications and Contraindications for LDP

Indications

The indications for LDP^5–11 are as follows: (1) benign, borderline, or malignant tumors of the pancreatic body and tail. The tumor should be relatively free of adhesions and easy to separate from the surrounding tissues, without distant metastasis; (2) pancreatic injury and chronic pancreatitis; and (3) pancreatitis with pseudocyst.

Contraindications

The contraindications for LDP are as follows¹²: (1) serious adhesions, where a malignant tumor is difficult to separate from surrounding tissues, risking injury to surrounding organs or critical vasculature; (2) preoperative examination revealed that the critical vasculature or surrounding organs may be involved, or distant metastasis is present; (3) acute pancreatitis; (4) history of laparotomy; (5) serious comorbidities that would preclude surgery.

Although excess visceral fat can make surgery more challenging, some researchers believe that patients with high body mass index (BMI) are not contraindicated for LDP. This is because these patients may benefit from MIST, due to better access deep in the abdomen, less postoperative incisional pain, and reduced incidence of postoperative incisional hernia. Similarly, patients with cardiac and pulmonary disease are not contraindicated for LDP due to the potentially greater benefit from applying minimally invasive techniques in these scenarios, including faster recovery. However, randomized clinical trials with large sample sizes are required to support these conclusions.⁶

Surgical Technique

Operative procedures

The operative procedure was similar in C-LDP, S-LDP, and R-LDP. After induction of general anesthesia, a transumbilical incision was made to establish the pneumoperitoneum, which was maintained at a level of 13 mm Hg, after which an operating incision was established. A slight anti-Trendelenburg maneuver was obtained with a rotation of the bed to ∼30° to the right to expose the pancreas. Routine exploration of the abdominal organs was performed, followed by division of the gastrocolic ligament to expose the body and tail of the pancreas and confirm the location of the lesion. Loose connective tissue between the dorsal surface of the pancreas and the posterior abdominal wall was then carefully divided, and a tunnel was created behind the pancreatic body. A grasper was then inserted into the tunnel and maneuvers were performed to enlarge the visual fields behind the pancreas, while dividing the loose connective tissue toward the tail of the pancreas. The pancreas was then lifted and separated from the posterior abdominal wall, and divided with an endoscopic linear stapler. Finally, the specimen was placed into a retrieval bag and extracted, with an indwelling drainage tube placed as the final step.

With or without splenectomy

DP can be performed with or without preservation of the spleen. DP is usually combined with splenectomy due to the special anatomic relationship between the spleen and pancreas. Since the discovery of overwhelming postsplenectomy infection, and the continuous understanding of splenic function, the importance of the spleen as far as immune and hematopoietic function, as well as antitumor and anti-infection, has led surgeons to consider splenic preservation during DP.¹³ However, for malignant pancreatic lesions, splenectomy should be performed to ensure clear margins. Splenectomy should be performed if the lesions involve the spleen or serious adhesions are found in the splenic hilum, to avoid forced separation and bleeding.

There are two methods of LDP that include conservation of the spleen, the Kimura method¹⁴ and the Warshaw method.¹⁵ The Kimura approach requires preserving the splenic artery and vein, which fully maintains the blood supply of the spleen and prevents postoperative splenic infarction. This method is indicated in benign diseases or borderline tumors of the body and tail of the pancreas, which do not involve the splenic artery and vein.^14,16

In the Warshaw technique, the splenic artery and vein are ligated and the short gastric artery and the left gastroepiploic artery are preserved to spare the blood supply to the spleen. This method does not require dissection of the splenic artery and vein, thus decreasing the operative risk. However, the rates of postoperative splenic infarction are increased correspondingly, due to ligation of the splenic vessels. This technique is used for tumors of the pancreatic body and tail adjacent to the splenic artery or vein.^15,16 However, for patients with splenomegaly, retention of the short gastric artery and the left gastroepiploic artery alone may be difficult to ensure sufficient blood supply to the spleen. Therefore, the Warshaw method is contraindicated in patients with splenomegaly.

Jain et al. showed that, compared with the Kimura method, postoperative spleen-related complications were significantly increased in the Warshaw method.¹⁷ Therefore, the Kimura method should first be attempted to preserve the spleen and the short gastric artery should be conserved.¹⁶

In DP with preservation of the spleen, blood flow to the spleen should be always examined until the operation is completed. Splenectomy should be performed if there are obvious signs of splenic ischemia, as enlargement of the ischemic region may occur in 10% of patients.^16,18 Another study showed that, compared to open surgery, the spleen preserving rate may be higher in LDP, which may be associated with enlarged vision and improved visual field exposure in laparoscopic surgery.^19,20

Types and Outcomes of LDP

Conventional multi-incision laparoscopic distal pancreatectomy

C-LDP surgery was first performed using four or five ports. The impact of the learning curve gave birth to hand-assisted LDP. The potential advantages to the hand-assisted technique include preservation of the surgeon's ability to directly palpate the viscera, tumor, and surrounding structures, helping to expose the organs and preventing hemorrhage. This method allows for flexibility and tactile feedback of the surgeon's hand, which may lead to a lower conversion rate.^21–23 Although the need to apply this approach lessens with the effects of the learning curve, it still plays an important role in more challenging resections of larger tumors, tumors with surrounding inflammation, and in obese patients.²³

The effects of the learning curve on C-LDP are described in detail in the study conducted by Kneuertz et al.²¹ As experience increased, tumor diameter gradually increased, and the use of the hand-assisted technique was significantly lower. Despite the increased acuity of patients and complexity of tumor location, there were no significant differences in perioperative outcomes. Recent studies showed that in selected patients, there were no significant differences in perioperative outcomes between the C-LDP and open distal pancreatectomy (ODP) groups, such as negative margin rate, operative time, and pancreatic fistula.^19,22,24 Compared with ODP, estimated blood loss, postoperative complications, and length of hospital stay were less during C-LDP. In the multivariate analysis, C-LDP may be an independent influencing factor on shorter hospital stay.

Early experiments in the treatment of malignant pancreatic tumors by C-LDP were rare. As some scholars believe that C-LDP may not suitable for malignant tumors of the pancreas, oncological outcomes data of C-LDP are scarce, including surgical margin and lymph node harvesting, among other factors. Therefore, the application of MIST in malignant tumors of the distal pancreas is few.

With the development of laparoscopic technology and increased surgical experience, increasing evidence has shown no significant difference between ODP and C-LDP in the complications, mortality, and short- and long-term oncologic outcomes in the treatment of some malignant tumors.^10,24–28 There is controversy regarding the negative margin that results in an R0 resection in the present study. Some authors argue that it is easier to achieve an R0 resection with C-LDP,^22,29–31 while others argue that there is no significant difference in R0 resection rates between C-LDP and ODP.^10,24,28,32 There is evidence that the number of lymph nodes resected is higher in the ODP group, although there is no significant difference in the detection rate of positive lymph nodes between the two groups.²² Multivariable regression analysis for lymph node assessment greater than the median of 12 reported by Sharpe et al. was age, lymph node positivity, and treatment in an academic institution compared with a community cancer program. Surgical approach was not associated with achieving a lymph node count greater than 12. Higher stages, when compared with Stage I, predicted positive margins in the multivariable regression model, and there was a trend for positive margins with lymph node positivity. C-LDP was associated with a decreased risk of having positive margins. The only factor that predicted an increased risk of a 30-day unplanned readmission was older age, and surgical approach was not an associated factor. There were no factors associated with increased perioperative mortality, including surgical approach.²⁶ Therefore, laparoscopic resection of lesions in the body and tail of the pancreas in an unselected patient series was safe and feasible.³³

C-LDP was therefore found to be safe and feasible compared with open surgery, with most patients benefitting from C-LDP due to the advantages of MIST. However, most studies were retrospective and therefore may include a more significant selection bias. The advantages of C-LDP, especially for malignant tumors of the pancreas, remain to be confirmed by large-sample randomized controlled trials.³⁴

Single-incision laparoscopic distal pancreatectomy

S-LDP is an innovative development of LDP with transumbilical single-incision LDP (TUSI-LDP) mostly performed. TUSI-LDP involves the insertion of multiple trocars via separate fascial punctures through the same incision at the umbilicus. However, a recent report described that the pneumoperitoneum leaks from the side of each port and intraperitoneal pressure cannot be maintained.^35,36 One of the advantages of the single-trocar approach is reduced loss of pneumoperitoneum due to high airtightness.^36,37

Limited by a single incision and number of trocars, S-LDP is actually performed by 1 person, which makes surgery more difficult in many aspects, due to a number of factors—collision of instruments as well as exposure of the operative field and the lesions.

As experience increased, researchers found the utilization of gravity in single-incision laparoscopic operations to be very important. During operations on the pancreas, it is essential to rotate or position the patient in the anti-Trendelenburg position, allowing gravity to pull the pancreas and spleen close to the umbilicus and to help achieve good exposure.³⁸ In addition, a similar stomach-hanging method and lasso technique were used to expose the operative field in some reports, which obtained favorable results.^11,39–43 Furthermore, a balloon retractor was also useful for retracting the stomach, spleen, and pancreas. In the pig model, a hook retractor was used to pull the pancreas to expose the operative field, as reported by Wang et al.⁴⁴ In the study conducted by Yao et al., neither the stomach-hanging method nor the balloon retractor was used, although those operations were also performed smoothly.^38,45 Certainly, with the accumulation of operator experience, these methods may be gradually omitted.

Pancreatic surgery is more challenging, due to the anatomic and physiologic characteristics of the pancreas; therefore, the study of LDP is less challenging, especially for S-LDP. At present, most studies suggest that S-LDP is safe and feasible.^{11,38,45–48} Han reported that the mean operative time and mean duration of hospital stay in the S-LDP group were significantly longer than in the LDP group. The spleen was preserved more in the C-LDP group than in the S-LDP group, but this difference was not found to be significant. There were no significant differences in intraoperative blood loss, tumor size, conversion rate, or postoperative complications between the two groups.⁴⁸ However, Yao et al. and Haugvik et al. reported that there were no significant differences in operative time, estimated blood loss, postoperative pain, and the length of postoperative hospital stay, even more so in the S-LDP group.^45,47 Most of the current research include retrospective studies or case reports; thus, the advantages of S-LDP require further exploration.

Robotic laparoscopic distal pancreatectomy

Robotic surgery is a recently developed minimally invasive procedure. Compared with traditional laparoscopic surgery, it has obvious advantages, such as restoration of hand–eye coordination, reduction of natural tremors with no fulcrum effect, three- instead of bi-dimensional vision, more precise movement, and an improvement in ergonomics for the surgeon with a more comfortable position. In some conditions, robotic surgery can even accomplish some movements similar to open surgery.⁶

R-LDP was first performed in 2003 and has been increasingly used.⁴⁹ In the present study, operative times of R-LDP were significantly longer than that of LDP.^50–52 However, there was no significant difference in intraoperative blood loss, conversion to open surgery, spleen preserving, postoperative complications, and length of postoperative hospital stay between the two groups.^50–55 For malignant tumors, the rates of negative surgical margins and the number of lymph nodes harvested were higher in R-LDP.⁵⁴ However, some other studies reported that there were no significant differences between the two groups.^52,55 This difference may be caused by the selective bias of the study.

With the popularity of robotic surgery, its shortcomings are gradually exposed, such as lack of tactile feedback, high consumption, and longer operating times.²² Operative time may be affected by the learning curve; those shortcomings may be compensated by increasing experience and advantages of the 3D vision field of robotic surgery.

Postoperative Pancreatic Fistula

Pancreatic fistula is one of the most common complications after pancreatic surgery, which can cause serious consequences, such as secondary abdominal infection, incisional infection, and postoperative bleeding. According to the International Study Group on Pancreatic Fistula (ISGPF), the definition of postoperative pancreatic fistula is drain output of any volume on or after postoperative day 3 with an amylase greater than three times the upper limit of normal. It can be divided into three levels: no clinically significant pancreatic fistula (grade A) and clinically significant pancreatic fistula (grade B and grade C).

At present, it is considered that pancreatic fistula after DP is primarily caused by incomplete closure of the pancreatic ductal system. Many factors influence postoperative pancreatic fistula, including patient-related risk factors (age, sex, and BMI), disease-related risk factors (pancreatic gland texture and pancreatic duct size), procedure-related risk factors (operative time, transection, technique, closure technique, and intraoperative blood loss), and surgeon experience.^56–58 Although postoperative outcomes of LDP are better than ODP, it is reported that MIST does not reduce the incidence of pancreatic fistula after DP.^59,60

With the progress of technology and increased experience, there are some methods to prevent pancreatic fistula after DP, such as transection and closure using a stapling device, oversewing the staple line, pancreatic transection using various energy devices, staple line reinforcement, reinforcement of the pancreatic stump with a jejunal loop, gastric anastomosis or falciform ligament patch, sealing with fibrin sealant patches, pancreatic sphincterotomy, and administration of somatostatin analogues.¹⁶ Most of these techniques can be applied during LDP.

Perioperative endoscopic intervention

Perioperative endoscopic pancreatic sphincterotomy has been proposed to prevent pancreatic fistula, mainly after DP.^61,62 This technique is highly feasible and is usually well tolerated by patients.⁶³ Recent randomized controlled trials showed that prophylactic pancreatic stenting does not reduce postoperative pancreatic fistula after DP.⁶⁴ In fact, it increases bacterial seeding in the stent, leading to formation of abscesses. As to the true value of this technology, it needs to be confirmed by randomized clinical trials with large sample sizes.

Transection and closure techniques

Hand-sewn closure and stapled closure represent the most common techniques of pancreatic remnant management, both of which can be performed during LDP. Evidence has shown that there are no significant differences in postoperative pancreatic fistula rates between hand-sewn closure and stapled closure.^65–67 Furthermore, gradual closing of the stapler over the course of about 2–3 minutes could reduce postoperative pancreatic fistula rates, as reported by Asbun and Stauffer.⁶⁸ In recent years, increasing evidence has shown that staple line reinforcement after DP significantly reduces postoperative pancreatic fistula rate.^69,70 Thus, stapled closure may be preferable in LDP.

Glue and patches

At present, the effects of fibrin glue and sealant patches remain controversial. There have been reports using gastric and jejunal patches to cover the pancreatic stump. Moriura et al. reported that pancreas-related complications decreased when using a seromuscular patch.⁷¹ However, these results have not been confirmed in the randomized controlled trial by Olah et al., in which grade B/C postoperative pancreatic fistulas after stapled transection and stapled transection combined with a seromuscular patch were found to be similar.⁷² In addition, the application of a falciform ligament patch and fibrin glue to standard stapled or sutured remnant closure did not reduce the rate of postoperative pancreatic fistula in patients undergoing DP.⁷³ To date, it is unclear whether these kind of interventions will decrease postoperative pancreatic fistula rates significantly after LDP or not, and remains to be proven by further studies.

Somatostatin analogues

Somatostatin is an inhibitor of endocrine and exocrine pancreatic activity. The use of somatostatin analogues for preventing postoperative pancreatic fistula remains controversial. However, a meta-analysis conducted by Gurusamy et al. showed reduction of complications and postoperative pancreatic fistula rates using somatostatin analogues, without decreasing clinically relevant postoperative pancreatic fistula rates.⁷⁴ The efficacy of prophylactic somatostatin analogues was reported to be improved, by selective administration of high-risk patients, including patients with a soft pancreatic gland, a small pancreatic duct, or patients in whom intraoperative blood loss was excessive.⁷⁵ Interestingly, the newest results from a trial by Allen et al. showed that the use of pasireotide (a long half-life somatostatin analogue) in the perioperative period significantly reduced the risk of clinically relevant postoperative pancreatic fistula after DP.⁷⁶

Complication Risk Score

In 2009, a complication risk score (CRS) was previously established with data from nine academic centers by Weber et al. This study revealed that when cases that were completed laparoscopically were included, only higher BMI, longer resected pancreatic length, and greater estimated blood loss predicted an increased risk for major complications (BMI >27: OR 3.22, 95% CI 0.97–10.70, P = .056; pancreatic length >8 cm: OR 4.64, 95% CI 1.38–15.53, P = .013; estimated blood loss >150 mL: OR 3.59, 95% CI 1.15–11.23, P = .028). Because BMI, pancreatic length, and estimated blood loss were associated with major complications, these three factors were incorporated into a CRS. The CRS, which consisted of 1 point each for BMI >27, pancreatic specimen length >8 cm, or estimated blood loss >150 mL, predicted an increased risk of any complication, major complication, any pancreatic fistula, and clinically important pancreatic fistula.⁷⁷ Therefore, the CRS system can be used to quantitatively analyze the risk of postoperative complications after LDP.

Application of an Enhanced Recovery Program for LDP

The concept of an enhanced recovery program (ERP) was initially introduced by Moiniche et al.,⁷⁸ with the primary aim to reduce surgical stress, maintain physiological functional capacity, and optimize postoperative recovery.⁷⁹ In recent years, ERP has been gradually applied in various surgical procedures. The application of ERP for LDP include the following: (1) preoperative use of a phosphate enema for bowel preparation; (2) patient-controlled analgesia (PCA) administered on the day of surgery and the first day after surgery, and PCA discontinued on the second day after surgery; (3) resumption of water consumption on the day of surgery. On the first postoperative day, patients can consume a light diet and energy drinks and the urinary catheter is removed. On the second postoperative day, patients can consume a normal diet and energy drinks and the nasogastric tube is removed; (4) 4 hours postoperatively, patients ambulate; on postoperative days 1 and 2, patients ambulated 200 m/day; and (5) metoclopramide and physiotherapy are given to patients from the first postoperative day. If there is no evidence of pancreatic fistula, the drain is removed on the second postoperative day.

This study revealed that there were no significant differences in readmission or complication rate. Also, implementation of ERP optimizes outcomes for LDP with a significantly earlier return to normal gut function, reduced length of stay, and cost savings.⁸⁰ Therefore, it is safe and feasible to use the ERP method in perioperative management of patients undergoing LDP.

Conclusions

LDP is safe and feasible under some conditions. With increasing surgeon experience and technological development, the application of LDP is increasing. Compared with ODP, LDP has the advantages of rapid postoperative recovery and fewer postoperative complications; a trend was observed for LDP to replace traditional open surgery. With the application of ERP, length of hospital stay and costs are reduced. Therefore, LDP combined with ERP is expected to become standard in the treatment of pancreatic body and tail lesions.

Footnotes

Disclosure Statement

No competing financial interests exist.

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