Since Whipple reported the first 1-stage pancreaticoduodenectomy (PD) in 1940,1 surgical resection is still the gold standard in the curative treatment of a wide range of periampullary neoplasms.2–4 The procedure was initially associated with a high incidence of perioperative morbidity and mortality, however, the surgical outcomes of PD have improved over the decades because of the continuous refinements in the surgical techniques and preoperative care.5 Analysis of surgical outcomes from high-volume centers revealed a decrease in hospital mortality to <3%, whereas the postoperative morbidity still ranges from 30% to 40%.6–10
Despite renovations in the surgical technique and technologies, pancreatic reconstruction remains an “Achilles heel.” Postoperative pancreatic fistula (POPF) always remained a major concern and is considered the most important cause of morbidity. POPF is linked to prolonged hospital stay, increased costs, and mortality, thus, remaining a challenge at high-volume centers for pancreatic surgery.4,5 The incidence POPF after PD among different series ranges from 5% to 30%.5–12
In the past 2 decades, the rise and development of laparoscopy as a minimally invasive substitute to open surgery has successfully gained the attraction of both surgeons and patients as it has the benefit of reduced postoperative pain, hospital stay, and better cosmosis.13 However, adoption of laparoscopy in PD was technically demanding as the anatomic position of the pancreatic head and its relationship with main vascular structures makes the procedure difficult and the reconstruction of the pancreatic stump challenging.14 These technical challenges made the progress of laparoscopic PD (LPD) slow although it was first introduced >20 years ago.15
Several retrospective studies in the literature reported encouraging results of LPD regarding blood loss, postoperative pain, and hospital stay.16–20 However, a comparative study in 2014 reported poorer oncological outcomes of LPD compared with open PD (OPD) regarding rates of R0 resections and the number of dissected lymph nodes (LNs).18 Because of the limited number of comparative studies, the value of LPD is still questionable.21–23 The aim of this study is to show the feasibility and surgical and oncological outcomes of LPD compared with conventional OPD in a tertiary referral hepato-pancreato-biliary center.
PATIENTS AND METHODS
This is a propensity score–matched analysis for patients with periampullary tumors who underwent PD in the period between June 2013 and April 2018 at our tertiary referral center (Gastrointestinal Surgery Center, Mansoura University, Egypt). Patients underwent complete LPD and matched group underwent OPD included in the study. The exclusion criteria included patients who underwent pancraticojejunostomy [because all cases performed by LPD reconstructed only by pancreaticogastrostomy (PG)], vascular resection, and PD with loupe. Data were retrieved from a prospectively maintained web-based hospital database for PD.
Written informed patient consent was routinely obtained from all cases describing and explaining the operative and postoperative details and complications of both approaches. Approval was taken from the institutional review board.
The enrolled patients divided into 2 groups: group A: patient who underwent OPD and group B: patient who underwent LPD.
Preoperative assessment for diagnosis and staging included complete history taking associated comorbidities, clinical examination, full laboratory investigation, tumor markers, radiologic investigations [ultrasound-magnetic resonance cholangiopancreatography, computerized tomography abdomen, computerized tomography portography, and angiography and endoscopic ultrasound if needed]. Preoperative endoscopic biliary drainage was done in cases associated with cholangitis or hepatic dysfunction.3,5,7
Operative Data Including
Technique of LPD
While placed in a supine position, the patient’s legs are abducted (French position). Creation of pneumoperitoneum was achieved by open technique through a 10-mm port above the umbilicus (optical trocar). Examination of the abdominal cavity was done to exclude visible signs of metastasis (liver secondaries, peritoneal nodules, or ascitis). Then 4 trocars were inserted in the upper quadrants (Fig. 1).
The lesser sac was accessed by dissection through the gastrocolic omentum. Colon mobilization was started from left to right, identifying the gastrocolic vessels and other tributaries of the trunk of Henle. Dissection was done in the lower border of the pancreas to expose superior mesenteric vein (SMV) and creating the tunnel behind the neck of the pancreas to assess the relationship of the tumor with SMV. Then kocherization of the duodenum was performed exposing inferior vena cava. The duodenum, pancreatic head, and uncinate process are completely mobilized from retroperitoneum.
Then dissection of the peritoneal covering of the hepatoduodenal ligament was done starting superiorly at the hepatic hilum extending caudally along the common bile duct (CBD). After dissection of around the CBD, the CBD was transected 1 cm below the bifurcation of the common hepatic duct. Then dissection of the lymphatics around the common hepatic artery was done craniocaudally till identification of the gastroduodenal artery, which was then clipped and divided.
The ligament of Treitz was divided. The first jejunal loop is transected with the stapler.
Division of the pancreatic neck was done using the harmonic scalpel and the duct was sharply divided with scissors. The pancreatic duct was easily seen because of the magnification of the laparoscopic camera.
Then the uncinate process was dissected free of the mesenteric vessels using the harmonic scalpel. The resected specimen was then placed in an extraction bag. The specimen was extracted either from the upper midline or from the pfannenstiel incision.
Regional lymphadenectomy was routinely performed in all patients, including the LNs within the outlines of the hepatoduodenal ligament, right side of the SMV, and inferior vena cava.
Three anastomoses needed to be created, with a fast intracorporeal knot. The pancreaticogastrostomy (PG) was done in 2 layers: an outer layer with interrupted 3-0 silk and an inner layer with 4-0 absorbable sutures placed, taking the duct to the gastric mucosa through the whole wall.
The hepaticojejunostomy (HJ) was done in an end to side, retrocolic manner with 1 layer of absorbable 3-0 continuous sutures starting posteriorly. The gastrojejunostomy (GJ) was done in a side to side, antecolic manner using a stapler. Drains were positioned below and above the anastomosis.
Technique of OPD
The abdomen was explored through a bilateral subcostal incision. Metastasis was first ruled out especially in liver, root of mesentery, meso-colon, and pelvis. Dissection and reconstruction were performed as described in the previous publications.5,24,25
Postoperative Assessment. All patients were admitted to the intensive care unit after the operation. Antibiotics and analgesics were given to all patients. Somatostatin analog was given to selected risky cases. Abdominal drains outputs were estimated daily.
Follow-up were scheduled at 1 week, 1 month, 3 months, and 6 months postoperatively, and then at 1 year.
POPF, biliary leak, delayed gastric emptying (DGE) were defined according to the international study group of pancreatic surgery.26,27
A primary outcome measure was the rate of total postoperative morbidities. Postoperative morbidities were graded according to Clavien and Dindo grading.28 Secondary outcome measures included the assessment of the following: total operative time, operative time of dissection, operative time of reconstruction, blood loss, blood transfusion, the need of deflation during the procedure, resection safety margin status, the number of dissected LNs, node positivity rate, POPF, DGE, BL, bleeding PG, bleeding GJ, internal hemorrhage, pulmonary complications, intraoperative and postoperative blood gases, pulse, blood pressure, postoperative pain postoperative pathology, re-exploration, and survival rate, recurrence, hospital stay.
Categorical variables are presented as frequency distributions and were compared using the χ2 test. Continuous data are expressed as medians and were compared using independent t test. All statistical tests were 2-sided, and the significance level was P-value ≤0.05. Statistical analyses were performed using SPSS version 17 (Chicago, IL). Survival analysis was done using life table test, Kaplan-Meier method, and log-rank test.
Age, sex, jaundice, diabetes, body mass index, blood sugar, preoperative hemoglobin level preoperative serum albumin, preoperative serum bilirubin, preoperative serum glutamic pyruvic transaminase, preoperative endoscopic retrograde cholangiopancreatography were introduced in a multivariate logistic regression to create propensity scores modeling the probability of a patient undergoing laparoscopic and OPD. Then, a propensity score–matched analysis, by using the nearest neighbor technique with match 1:2 and no caliper for optimal matching, was performed to generate matched couples.
In the period of study, 298 patients underwent PD, 133 patients were excluded from the study [89 patients (pancraticojejunostomy), 14 patients who underwent vascular resection, and 30 cases who underwent PD with a loupe]. A total of 165 patients entered in a propensity score–matched analysis and only 111 patients included in the study. Of them, 37 underwent LPD, whereas 74 patients underwent OPD (excluding 2 cases who underwent LPD and 52 cases who underwent OPD) (Fig. 2).
Both groups were well matched as regards demographics and preoperative characteristics (age, sex, body mass index, and preoperative comorbidities). Preoperative data are shown in Table 1.
Analysis of operative variables is shown in Table 2. The conversion rate was 4 cases (10.8%) (1 case because of uncontrolled bleeding from SMV, 1 case because of difficult dissection, 1 case because of adherence of uncinate process to underlying SMV, and 1 case because of anesthetic problem). Operative time was significantly longer in the LPD group (420 vs. 300 min; P<0.001). Regarding the time needed for reconstruction, pancreatic reconstruction took more time compared with the OPD group (P<0.001) and also when compared with laparoscopic HJ and GJ anastomosis. In all cases who underwent LPD, deflation was required during the procedure by anesthetic team because of CO2 retention. The median time for deflation was 20 minutes.
Analysis of Postoperative Outcomes
As shown in Table 3, the median hospital stay was significantly shorter in the LPD group (P=0.004). Patients who underwent LPD resumed oral intake earlier than the OPD group (3 vs. 5 d; P=0.001). Both groups were comparable regarding the incidence of overall complications. The incidence of clinically relevant POPF was the same in both groups. Although grade C POPF occurred more in the LPD group, this was statistically insignificant when compared with the OPD group.
Four patients were re-explored in the early postoperative period in LPD group because 1 case had bleeding PG, 1 case had GJ leakage, and 2 cases had POPF grade C. One hospital mortality occurred because of systemic inflammatory response syndrome secondary to POPF grade C. In OPD group, 7 cases were re-explored because 1 case had bleeding PG and 2 cases had bleeding GJ, 1 case had GJ leakage, 1 case had biliary peritonitis, and 2 cases had POPF grade C. Three deaths occurred in this group, 2 cases because of systemic inflammatory response syndrome secondary to POPF grade C and 1 case because of pulmonary embolism.
Analysis of haemodynamic and metabolic changes during and after surgery is demonstrated in Table 4. Postoperative pain and the need for analgesia was significantly less in the LPD group where only 5 patients required analgesia on postoperative day 3 in the LPD group compared with 29 patients in the OPD group (P=0.006).
Analysis of Pathologic and Oncological Outcomes
There was no difference between both groups regarding the tumor site and size (median size 3 cm in each group; P=0.33). The most frequent pathology in both groups was pancreatic head adenocarcinoma (83.8% for LPD and 81.1% for OPD; P=0.65). The rates of R0 resections were similar among both groups (P=0.6). Also, there was no statistically significant difference between both groups regarding the number of LNs harvested (15 for LPD vs. 14 for OPD; P=0.21) (Table 5).
Since its introduction in 1994, LPD has slowly progressed over the past few decades as it is a complex and challenging procedure even for experienced surgeons. It includes extensive dissection along mesenteric vessels, portal vein, and celiac trunk branches with 3 difficult laparoscopic reconstructions.10,29
Several studies reported that LPD is associated with higher morbidity, less number of resected LNs, and fewer rates of R0 resection compared with OPD.16,30 However, other comparative retrospective studies and few randomized studies encouraged LPD. These studies have reported that LPD is better than OPD for blood loss, hospital stay, more number of dissected LNs, and longer free survival.31–34 Because of the limited number of comparative studies, it is still difficult to assess the feasibility and oncologic outcomes of LPD.
In the current propensity score–matched study, LPD provided shorter hospital stay, less blood loss, less postoperative pain, early oral intake, and better cosmosis. However, the operative time needed for dissection and reconstruction was significantly longer in the LPD group. Both groups were comparable as regards lymph node retrieved and R0 rate. No significant differences were found between both groups as regards POPF, DGE, bile leak, postpancreatectomy hemorrhage, postoperative collection, re-exploration, readmission, recurrence rate, and survival rate. Also, this study demonstrated that there was the reversible impact of CO2 insufflation on intraoperative and postoperative heart rate and blood gases, which were controlled by the team of anesthesia by repeated request of deflation of the abdomen during the operation.
In most of the literature, the conversion rate from LPD to OPD ranged from 0% to 16%.11,16,23,31–33 Croome et al22 reported that 7 patients (6.5%) in the LPD group underwent conversion to OPD for anticipated venous involvement or complex pancreatic reconstruction. Stauffer et al31 reported that the conversion from LPD to OPD was needed in 14 (24.1%) patients. All conversions were required for venous involvement for vein resection in 11 patients or adherence to underlying vasculature because of desmoplastic reaction or pancreatitis in 3 patients. Palanivelu et al33 reported that the conversion rate was 1 case (3.1%) because of concomitant vascular resection required venous graft. In this study, the conversion rate was 4 cases (10.8%) (1 case because of uncontrolled bleeding from SMV, 1 case because of difficult dissection, 1 case because of adherence of uncinate process to underlying SMV, and 1 case because of anesthetic problem). In this study, no conversion because of vascular involvement because preoperative angiography and portography were performed for all cases that underwent LPD.
In a study reported by Dokmak et al,16 comparing the outcomes of 46 LPD cases with 311 OPD cases, the authors found that LPD is feasible, with low mortality rate but associated with high complications rate. In their series, the incidence of POPF was 44%, postoperative bleeding was 24%, and re-exploration was needed in 24% of LPD cases. The blood loss with LPD was similar to that with OPD. The operative time was significantly longer in LPD than OPD (342 vs. 264 min), and the reduction in postoperative hospital stay was not observed in his study. So, the study concluded that no improvement in the surgical outcomes of LPD and should not be routinely performed in a risky patient of POPF.
Dokmak et al16 also found that although the overall incidence of POPF was not significantly different between LPD and OPD, the incidence of grade C POPF was significantly more frequent in the LPD group (P=0.007). The authors’ hypothesis to explain this high incidence included the following: the more frequent soft pancreas and small pancreatic duct diameter (because of the selection of early cases for laparoscopy), difficult less effective laparoscopic pancreatic reconstruction compared with OPD, and fewer adhesions. However, some studies reported a low POPF after LPD (6% to 26%), a high rate of the abdominal collection (19%) or readmission (30%) were also noted.30–32
Palanivelu et al33 performed a randomized study to compare LPD versus OPD on 64 patients and randomized into 2 groups. The median postoperative hospital stay was significantly longer for OPD than LPD (13 vs. 7 d). The operative time was significantly longer in LPD (359 vs. 320 min). The blood loss was significantly less in LPD than OPD (250 VS. 401 mL). As regards oncologic outcomes, both groups were comparable as regards lymph node retrieved (18.9 vs. 17 LN) and R0 rate (31 vs. 30). The overall morbidities were the same in both groups. No significant difference between both groups as regards POPF, DGE, bile leak, postpancreatectomy hemorrhage, postoperative collection, re-exploration, and readmission. The mortality rate was 1 death in each group. The limitations of his study were small sample size, the long-term outcomes not studied including recurrence and survival rate, finally his cases of relatively nonobese patients and the cases performed by expertise in advanced laparoscopic surgery. The study recommends an urgent need for standardization, international guidelines, and further randomized studies with large sample size and multicentric.
Four large series on LPD were available. The first study was from the Mayo clinic, where 108 patients who underwent LPD were compared with 214 patients who underwent OPD with pancreatic adenocarcinoma regarding the oncological results. In this study, they concluded that LPD is possible in pancreatic ductal adenocarcinoma. It provides shorter hospital stay, faster recovery, less DGE, the same postoperative morbidity, and better survival rate than OPD.23 The second study from Pittsburgh Medical Center on 132 robotic LPD for all indications. They reported that the postoperative morbidity was (21%), readmission was (28%), hospital stay was 10 days (4 to 87 d).34 The third noncomparative study from China analyzed 233 patients who underwent LPD by a single surgical group. The study reported that the LPD is a routinely safe operation under skilled hands in selected patients. The postoperative morbidity rate was 33.5%, with 6.9% of grade B or C POPF and 9.9% of bleeding. The re-exploration rate was 5.6%. The mortality rate was 0.9%. The LNs dissected were 21.3±11.9.35 The fourth study from India on 130 patients by Senthilnathan et al11 reported that the mean operative time was 310 minutes. POPF was presented in 8.5%. R0 was 90.8% and the harvested lymph node was 18.15. The overall 5-year survival was 29.4% and the median survival was 33 months. They concluded that LPD has evolved over a period of 2 decades and may become the standard approach for selected periampullary tumors with satisfactory oncological outcomes, particularly in high-volume hospitals.
Many recent studies showed the progress of LPD and recommended it as an alternative of OPD with different approaches.36–40
Our propensity score–matched analysis had many limitations including its retrospective study but the data are a prospectively recorded in our center and the small sample size. However, with the progress of laparoscopic skills and in high-volume centers, the LPD program should be increased. To improve the surgical outcomes of LPD it needs along learning curve, high-volume centers, and required 2 surgical teams, one for dissection and other one for reconstruction.
LPD in the presence of the required laparoscopic skills and pancreatic surgery experience is feasible in selected cases; it provided a shorter hospital stay, less blood loss, earlier oral intake, and better cosmosis than OPD. It had the same postoperative complications and oncological outcomes as OPD. It should be a routine for periampullary tumors candidate for PD in high-volume centers and required 2 teams of surgeons, one for dissection and other one for reconstruction. However, its application as the standard of care needs more multicentric prospective randomized controlled trials.
The authors acknowledge all staff in archive in gastrointestinal surgery and Mr Mahmoud El Sokary for their effort and help.
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