International Journal of Surgery 16 (2015) 1e6
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Original research
Comparative study between duct to mucosa and invagination pancreaticojejunostomy after pancreaticoduodenectomy: A prospective randomized study Ayman El Nakeeb*, Mohamed El Hemaly, Waleed Askr, Mohamed Abd Ellatif, Hosam Hamed, Ahmed Elghawalby, Mohamed Attia, Tallat Abdallah, Mohamed Abd ElWahab Gastroenterology Surgical Center, Mansoura University, Mansoura, Egypt
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 October 2014 Received in revised form 29 January 2015 Accepted 5 February 2015 Available online 13 February 2015
Background: The ideal technical pancreatic reconstruction following pancreaticoduodenectomy (PD) is still debated. The aim of the study was to assess the surgical outcomes of duct to mucosa pancreaticojejunostomy (PJ) (G1) and invagination PJ (G2) after PD. Methods: Consecutive patients treated by PD at our center were randomized into either group. The primary outcome measure was the rate of postoperative pancreatic fistula (POPF); secondary outcomes included; operative time, day to resume oral feeding, postoperative morbidity and mortality, exocrine and endocrine pancreatic functions. Results: One hundred and seven patients treated by PD were randomized. The median operative time for reconstruction was significantly longer in G1 (34 vs. 30 min, P ¼ 0.002). POPF developed in 11/53 patients in G1 and 8/54 patients in G 2, P ¼ 0.46 (6 vs. 2 patients had a POPF type B or C, P ¼ 0.4). Steatorrhea after one year was 21/50 in G1 and 11/50 in G2, respectively (P ¼ 0.04). Serum albumin level after one year was 3.4 gm% in G1 and 3.6 gm in G2 (P ¼ 0.03). There was no statistically significant difference regarding the incidence of DM preoperatively and one year postoperatively. Conclusion: Invagination PJ is easier to perform than duct to mucosa especially in small pancreatic duct. The soft friable pancreatic tissue can be problematic for invagination PJ due to parenchymal laceration. Invagination PJ was not associated with a lower rate of POPF, but it was associated with decreased severity of POPF and incidence of postoperative steatorrhea. Clinical Trials. gov ID: NCT02142517. © 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
Keywords: Pancreaticoduodenectomy Pancreaticojejunostomy Pancreatic fistula
Pancreaticoduodenectomy (PD) is a complex operative procedure and widely performed for various benign and malignant diseases of periampullary or pancreatic region [1e4]. With improvement in the operative techniques and the perioperative management, the operative mortality rate after PD has dramatically decreased to less than 5%, while the incidence of postoperative morbidity remains high, from 40% to 50% [1e6]. Postoperative pancreatic fistula (POPF) remains a challenge even at the specialized centers, and also affect significantly the surgical outcomes [2e6]. The incidence of POPF after PD among different studies, ranging from 5 to 30% [1e5].
* Corresponding author. E-mail address: [email protected] (A. El Nakeeb). http://dx.doi.org/10.1016/j.ijsu.2015.02.002 1743-9191/© 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
The morbidity and mortality after PD are usually related to the surgical management of the pancreatic stump [3e7]. Several methods and techniques of pancreatic anastomosis have been proposed after PD to reduce the rate of POPF including the usage of an external or an internal pancreatic stent, isolated loop pancreaticojejunostomy (IPJ), pancreaticogastrostomy, binding PJ, or an administration of postoperative somatostatin [4e13]. The safe pancreatic reconstruction after PD continues to be a challenge at the high volume centers. The variety of reconstruction is a reflection of the lack of the ideal one [4e9]. No pancreatic reconstruction technique after PD was found to be applicable to all kinds of pancreatic remnants. No consensus exists regarding the ideal PJ reconstruction to reduce POPF. Duct to mucosa and invagination are two classic PJ techniques. Many studies have compared both techniques, but their surgical outcomes are
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A. El Nakeeb et al. / International Journal of Surgery 16 (2015) 1e6
1. Patients and methods
and mucosa. The duct was taken posteriorly and anteriorly to jejunal mucosa. A pancreatic duct stent was inserted during anastomosis and removed at the end of taking the stitches. The reconstruction was completed by end to side hepaticojejunostomy (retrocolic) and gastrojejunostomy (GJ) (antecolic) end to side manually.
1.1. Patients
1.6. Data collected
Consecutive patients that were treated by PD at the Gastroenterology Surgical Center, Mansoura, Egypt, during the period from June 2011 to September 2013, were eligible for the study. The exclusion criteria included any patients with locally advanced periampullary tumor, metastases, patients received neoadjuvant chemoradiotherpy, patients underwent pancreaticogastrostomy (PG) and patients with advanced liver cirrhosis (Child B or C), malnutrition, or coagulopathy. Informed consent was obtained from all patients to be included in this study, after a careful explanation of the disease and the possible treatment options with its complications. The study was approved by the local ethical committee. All patients were subjected to careful history taking, clinical examination, routine laboratory investigation and tumor markers as CEA and CA19-9, an abdominal ultrasound, magnetic resonance cholangiopancreatography (MRCP), and an abdominal computerized tomography (CT).
Preoperative variables included; age, sex, body mass index, patients' symptoms and signs, laboratory tests, tumor markers and preoperative biliary drainage. Intraoperative variables included; liver status, tumor size, pancreatic duct diameter, texture of the pancreas, operative time, blood loss and blood transfusion. Postoperative variables included; postoperative complications, drain amylase, liver function, day to resume oral feeding, postoperative stay, re-exploration, hospital mortality, postoperative pathology, and surgical safety margins.
still unclear [8,14e21]. The aim of the study was to assess the effectiveness and the surgical outcomes of both techniques of PJ after PD.
1.2. Randomization The patients included in the study were randomized into two groups using the closed envelope method. The envelopes were drawn and opened by a nurse in the operating room after pancreatic resection. The patients were randomized into two groups: Group I: patients underwent duct to mucosa PJ. Group II: patients underwent invagination PJ. 1.3. Operative techniques Standard PD was performed in all patients. All patients underwent regional lymphadenectomy, which included resection of nodes within the outlines of the hepatoduodenal ligament, right side of the superior mesenteric vessels, and inferior vena cava. All anastomoses were performed by experienced surgeons.
1.7. Assessments The primary outcome was POPF rate. POPF was defined by the International Study Group of Pancreatic Fistula (ISGPF) as any measurable volume of fluid on or after POD 3 with amylase content greater than 3 times the serum amylase activity [22,23]. A pancreatic fistula (PF) was graded according to the ISGPF into Grade A, B and C according to the clinical course [22,23]. The secondary outcomes were operative time, operative time needed for reconstruction, length of postoperative hospital stay, postoperative morbidities including (delayed gastric emptying (DGE), pancreatitis and biliary leakage). Complications were graded according to their severity on a validated five point scale using Dindo-Clavien complication classification system into (grades I, II, IIIaeb, IVaeb, V) [24]. The complications which were higher than ClavieneDindo grade III were considered to be major complications [24]. The pancreatic exocrine function was evaluated clinically. It was assessed by the presence or the absence of the steatorrhea (passing stool more than three times per day, fecal output of >200 g/d for at least three days, pale or yellow stools, and appearance of stools as pasty or greasy), the need of pancreatic enzymes supplement and studied variation in the body weight pre and postoperative [25]. 1.8. Follow up
1.4. *Duct to mucosa PJ group (Group 1) The duct to mucosa PJ was performed by a two layer end to side PJ. The pancreatic capsule and the jejunal serosa were anastomosed by interrupted silk suture 3/0 to form the outer layer in both the anterior and posterior walls of the anastomosis. Jejunostomy was done matched to the pancreatic duct diameter. The inner layer duct to mucosa was performed in eight to twelve stitches with 5/0 prolene. A pancreatic duct stent was inserted during the anastomosis to allow an easy and accurate suture placement, ensure an adequate pancreatic duct exposure and protect the opposite wall from being inadvertently held by needles and then it was removed at the end of the anastomosis.
Follow-up was carried out one week postoperatively, 3 months, 6 months and then after one year. Statistical analysis in this study was performed using SPSS software, version 17. Descriptive statistics were calculated and described as median (range) for continuous variables. Categorical variables were represented using percentages. Student's t-test for paired samples was used to detect differences in the means of continuous variables and Chi-square test was used for categorical variables. P values 2 cm Pancreatic duct diameter (mm) Median (mm) 3 mm >3 mm Relation of pancreatic duct to the posterior border Median (mm) 3 mm >3 mm Pancreatic consistency Firm Soft Median total operative time (hours) Median operative time for PJ anastomosis (minute) Median blood loss (ml)
24 3 48 59
Duct to mucosa PJ Group 1
(22.4%) (0.5e12) (44.9%) (55.1%)
13 2.5 25 28
(24.5%) (0.5e6) (47.2%) (52.8%)
Invaginated PJ Group 2 11 3 23 31
(20.4%) (0.5e12) (42.6%) (57.4%)
P Values 0.17 0.19 0.69
3 (1e12) 55 (51.4%) 52 (48.6%)
3 (1e12) 30 (56.6%) 23 (43.4%)
3 (1e12) 25 (46.3%) 29 (53.7%)
0.49 0.33
3 (1e15) 54 (50.5%) 53 (49.5%)
3 (1e15) 30 (56.6%) 23 (43.4%)
3 (1e13) 24 (44.4%) 30 (55.6%)
0.91 0.25
55 (51.4%) 52 (78.6%) 5.5 (3e9) 31 (20e45) 500 (50e3000)
2.4.1. Pancreatic exocrine and endocrine function 21/50 (42%) patients presented with postoperative steatorrhea after one year in group 1 vs. 11/50 (22%) patients in group 2 (P ¼ 0.04). The median one year postoperative albumin was significantly more in group 1 than in group 2 (3.4 gm% vs 3.6 gm% respectively) (P ¼ 0.03) (Table 4). There was no statistically significant difference regarding preoperative and postoperative weight and BMI in both groups. There was no statistically significant difference regarding the incidence of DM preoperatively and one year postoperatively (Table 4).
28 25 5.5 34 500
(52.8%) (47.2%) (3e8) (20e42) (100e3000)
27 27 5 30 500
(50%) (50%) (4e9) (21e45) (50e2600)
0.85 0.90 0.002 0.92
3. Discussion The safe pancreatic anastomosis after PD continues to be a stump for the pancreatic surgeon even at the high volume centers. Several techniques and modifications of pancreatic anastomoses have been proposed [4e12]. Despite the lowering of the mortality rate to 5%, postoperative complications are still high up to 50% [2e7]. In most of published studies, morbidity and mortality after PD are related to pancreatic reconstruction [1e6]. POPF remains the most important cause of morbidity and also contributes significantly to prolonged hospital stay, increased costs
Table 3 Postoperative data. Variables
Total
Duct to mucosa PJ Group 1
Invaginated PJ Group 2
P alues
Hospital stay (days) Drain removal (days) Amount of draining (ml) Time starting oral (days) Total patients with complications Complications grade I II III IV V Severe complications (IIIb) Minor Major Drain amylase First day Third day POPF Pancreatic leakage Grade A Grade B Grade C Pancreatitis Biliary leakage Delayed gastric emptying Internal hemorrhage Wound infection Pulmonary complications Re-exploration Mortality Pulmonary embolism SIRS Liver insult
8 (4e41) 8 (4e35) 900 (70e18,000) 5 (4e28) 36 (33.6%)
8 (5e41) 8 (4e34) 1200 (70e18,000) 5 (4e28) 21 (39.6%)
8 (4e35) 8 (4e35) 800 (125e15,000) 5 (4e23) 15 (27.8%)
0.83 0.79 0.72 0.67 0.22
12 (11.2%) 7 (6.5%) 6 (5.6%) 1 (0.9%)
6 4 4 1
(11.3%) (7.5%) (7.5%) (1.9%)
6 (11.1%) 3 (5.6%) 2 (3.7%) 0
0.72
23 (21.5%) 4 (3.7%)
13 (24.5%) 3 (5.7%)
10 (18.5%) 1 (1.9%)
0.4
161 (6e44,000) 200 (10e22,180) 19 (17.8%) 12 (11.2%) 6 (5.6%) 2 (1.9%) 6 (5.6%) 13 (12.1%) 15 (14%) 5 (4.7%) 9 (8.4%) 4 (3.7%) 13 (12.1%) 7 (6.5%) 3 3 1
650 (20e44,000) 442 (10e22,180) 11 (20.8%) 6 (11.3%) 4 (7.5%) 2 (3.8%) 5 (7.5%) 7 (13.2%) 8 (15.1%) 3 (5.7%) 5 (9.4%) 1 (1.9%) 8 (15.1%) 3 (5.7%) 1 2 0
45 (6e8000) 120 (20e7500) 8 (14.8%) 6 (11.1%) 2 (3.7%) 0 1 (1.9%) 6 (11.1%) 7 (13%) 2 (3.7%) 4 (7.4%) 3 (5.6%) 5 (9.3%) 4 (7.4%) 2 1 0
0.48 0.49 0.46 0.4
0.08 0.78 0.79 0.68 0.72 0.62 0.39 0.72
A. El Nakeeb et al. / International Journal of Surgery 16 (2015) 1e6 Table 4 Functional changes. Variables
Duct to mucosa PJ Invaginated PJ P values Group 1 Group 2
Preoperative Steatorrhae Postoperative steatorrhae P* value
10/53 (18.9%) 21/50 (42%) 0.001
9/54 (16.7%) 11/50 (22%) 0.16
0.81 0.04
Preoperative albumin Postoperative albumin P* value
4 (3e5) 3.4 (3.1e4) 0.0001
4.05 (3e5) 3.6 (3e4.6) 0.0001
0.29 0.03
Preoperative weight Postoperative weight P* value
81 (60e125) 75 (58e99) 0.0001
75 (52e114) 0.16 74.5 (52e105) 0.96 0.0001
Preoperative fasting blood sugar 110 (71e410) Postoperative fasting blood sugar 136(71e450) P value* 0.0001
125 (79e231) 0.9 124 (75e233) 0.02 0.79
Preoperative DM Postoperative DM P value*
13/54 (24.1%) 15/50 (30%) 0.16
13/53 (24.5%) 19/50 (38%) 0.01
0.95 0.41
and mortality. Intra-abdominal abscess, bleeding and sepsis are common sequelae of POPF, which have been associated with a high mortality rate [2e8]. The development of POPF after PD appears to be a multifactorial. Many studies demonstrated that many factors significantly associated with POPF including; obesity, cirrhotic liver, soft pancreas, small pancreatic duct diameter, location of pancreatic duct within 3 mm distance from posterior edge, the technique and type of pancreatic reconstruction [2e7,25e27]. Ideally, the pancreatic reconstruction should not only decrease the risk of POPF, but it should decrease its severity if occurred and also, maintain pancreatic function [4e10]. Pancreaticojejunostomy (PJ) is the commonly preferred method of reconstruction after PD. In an effort to prevent POPF after PD, there have been many technical modifications for the pancreatic reconstruction [4e8]. Some retrospective studies showed that the duct to mucosa PJ was associated with a lower rate of POPF in the low risk patients with dilated pancreatic duct or firm pancreas, whereas the invagination PJ technique was safer in the high risk patients with small pancreatic duct or soft pancreas [9,19,28e32]. Several prospective randomized studies reported that a lower POPF in duct to mucosa PJ group than in the invagination PJ group. However the advantage was not found in patients with soft pancreatic stump [19,33,34]. The meta-analysis studies showed that the rate of POPF was not statistically different between duct to mucosa PJ group and the invagination PJ group [8,16,35]. In the current study no significant difference as regards POPF in both groups. The severity of POPF was noticed more in duct to mucosa PJ with no significant differences. No pancreatic reconstruction technique after PD was found to be applicable to all types of pancreatic stumps. Tailored pancreatic reconstruction is the best way to overcome the complications related to the type of reconstruction. Pancreatic reconstruction is difficult in pancreases with small duct and a soft fragile pancreas even in experienced hand [2e10]. Soft friable pancreatic tissue can be problematic for invagination PJ as the parenchymal laceration and ischemia of the stump can occur because of extensive sutures and compression which lead to POPF [2,8,16,36]. The small pancreatic duct makes duct to mucosa PJ difficult and liable to inaccurate suture placement and obstruction. In duct to mucosa PJ, the jejunal folds and edema formed around the opening of the pancreatic duct make it liable to the obstruction and development of the pancreatitis and anastomotic stenosis [36]. In contrast to, the invagination PJ is easier to perform and all of the pancreatic juice is drained into the jejunum [8,36]. In this study, postoperative steatorrhea after one year was
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noticed more significantly in duct to mucosa than in the invagination PJ group (P ¼ 0.04). Also, the median one year postoperative albumin was significantly less in the duct to mucosa group than in the invagination PJ group (3.4 gm% vs. 3.6 gm% respectively) (P ¼ 0.03). Several published studies found that pancreatic exocrine function after PD depends on many complex variables including; preexisting pancreatitis, the degree of fibrosis in pancreatic remnant, the volume of resected pancreatic tissue, the impairment of the pancreatic secretion flow due to the anastomotic stricture or by swelling of the jejunal mucosa and may be the type of pancreatic reconstruction [37e39]. There is however no evidence that impaired pancreatic endocrine function would be associated more often with a certain type of reconstruction [38]. PG could cause more morphological and functional derangement because the reflux of gastric juice causes inactivation of the pancreatic enzymes and early pancreatic insufficiency [40,41]. In duct to mucosa PJ, the jejunal folds and edema formed around the opening of pancreatic duct make it liable to a development of pancreatitis and an anastomotic stricture which may lead to a pancreatic exocrine dysfunction [36e38]. Additional studies are needed to recognize the tailored pancreatic reconstruction after PD. Soft friable pancreatic tissue can be problematic for the invagination PJ due to parenchymal laceration. Small pancreatic duct makes duct to mucosa PJ difficult and liable to inaccurate suture placement and obstruction. 4. Conclusion Invagination PJ is easier to perform than duct to mucosa especially in the small pancreatic duct. All of the pancreatic juice is drained into the jejunum in the invagination PJ. The soft and friable pancreatic tissue can be problematic for the invagination PJ due to parenchymal laceration. POPF was not statistically different between the duct to mucosa PJ group and the invagination PJ group. The severity of POPF was noticed more in duct to mucosa PJ with no significant differences. Postoperative steatorrhea was noticed more significantly in duct to mucosa than in invagination PJ group. Postoperative serum albumin level was significantly more in the invagination PJ group than in the duct to mucosa group. Ethical approval The study was approved by the local ethical committee. Financial support None. Conflicts of interest None. Author contribution Ayman El Nakeeb designed research. Ayman El Nakeeb, Mohamed El Hemaly, Waleed Askr, Mohamed Abd Ellatif, Hosam Hamed, Mohamed Attia, Tallat Abdallah, Mohamed Abd ElWahab performed research. Ayman El Nakeeb, Mohamed Said analyzed data. Ayman El Nakeeb wrote the paper. Guarantor Name: Ayman El Nakeeb. E-Mail: [email protected].
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Wu, Combined invagination and ductto-mucosa techniques with modifications: a new method of pancreaticojejunal anastomosis, Hepatobiliary Pancreat. Dis. Int. 10 (4) (2011 Aug) 422e427. [37] T.C.K. Tran, G. Kazemier, C. Pek, A.W. van Toorenenbergen, H. van Dekken, C.H.J. van Eijck, Pancreatic fibrosis correlates with exocrine pancreatic insufficiency after pancreatoduodenectomy, Dig. Surg. 25 (2008) 311e318. €ty, J. Sand, Obstructed pan[38] I. Nodback, M. Parviainen, A. Piironen, S. Ra creaticojejunostomy partly explains exocrine insufficiency after pancreatic head resection, Scand. J. Gastroenterol. 42 (2007) 263e270. [39] H. Nakamura, Y. Murakami, K. Uemura, Y. Hayashidani, T. Sudo, H. Ohge, Predictive factors for exocrine pancreatic insufficiency after pancreatoduodenectomy with pancreaticogastrostomy, J. Gastrointest. Surg. 13 (7) (2009 Jul) 1321e1327. [40] W.L. Fang, C.H. Su, Y.M. Shyr, T.H. Chen, R.C. Lee, L.C. Tai, et al., Functional and morphological changes in pancreatic remnant after pancreaticoduodenectomy, Pancreas. Nov. 35 (4) (2007) 361e365. [41] E. Lemaire, D. O'Toole, A. Sauvanet, P. Hammel, J. Belghiti, P. Ruszniewski, Functional and morphological changes in the pancreatic remnant following pancreaticoduodenectomy with pancreaticogastric anastomosis, Br. J. Surg. 87 (4) (2000 Apr) 434e438.
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Original research
Comparative study between duct to mucosa and invagination pancreaticojejunostomy after pancreaticoduodenectomy: A prospective randomized study Ayman El Nakeeb*, Mohamed El Hemaly, Waleed Askr, Mohamed Abd Ellatif, Hosam Hamed, Ahmed Elghawalby, Mohamed Attia, Tallat Abdallah, Mohamed Abd ElWahab Gastroenterology Surgical Center, Mansoura University, Mansoura, Egypt
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 October 2014 Received in revised form 29 January 2015 Accepted 5 February 2015 Available online 13 February 2015
Background: The ideal technical pancreatic reconstruction following pancreaticoduodenectomy (PD) is still debated. The aim of the study was to assess the surgical outcomes of duct to mucosa pancreaticojejunostomy (PJ) (G1) and invagination PJ (G2) after PD. Methods: Consecutive patients treated by PD at our center were randomized into either group. The primary outcome measure was the rate of postoperative pancreatic fistula (POPF); secondary outcomes included; operative time, day to resume oral feeding, postoperative morbidity and mortality, exocrine and endocrine pancreatic functions. Results: One hundred and seven patients treated by PD were randomized. The median operative time for reconstruction was significantly longer in G1 (34 vs. 30 min, P ¼ 0.002). POPF developed in 11/53 patients in G1 and 8/54 patients in G 2, P ¼ 0.46 (6 vs. 2 patients had a POPF type B or C, P ¼ 0.4). Steatorrhea after one year was 21/50 in G1 and 11/50 in G2, respectively (P ¼ 0.04). Serum albumin level after one year was 3.4 gm% in G1 and 3.6 gm in G2 (P ¼ 0.03). There was no statistically significant difference regarding the incidence of DM preoperatively and one year postoperatively. Conclusion: Invagination PJ is easier to perform than duct to mucosa especially in small pancreatic duct. The soft friable pancreatic tissue can be problematic for invagination PJ due to parenchymal laceration. Invagination PJ was not associated with a lower rate of POPF, but it was associated with decreased severity of POPF and incidence of postoperative steatorrhea. Clinical Trials. gov ID: NCT02142517. © 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
Keywords: Pancreaticoduodenectomy Pancreaticojejunostomy Pancreatic fistula
Pancreaticoduodenectomy (PD) is a complex operative procedure and widely performed for various benign and malignant diseases of periampullary or pancreatic region [1e4]. With improvement in the operative techniques and the perioperative management, the operative mortality rate after PD has dramatically decreased to less than 5%, while the incidence of postoperative morbidity remains high, from 40% to 50% [1e6]. Postoperative pancreatic fistula (POPF) remains a challenge even at the specialized centers, and also affect significantly the surgical outcomes [2e6]. The incidence of POPF after PD among different studies, ranging from 5 to 30% [1e5].
* Corresponding author. E-mail address: [email protected] (A. El Nakeeb). http://dx.doi.org/10.1016/j.ijsu.2015.02.002 1743-9191/© 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
The morbidity and mortality after PD are usually related to the surgical management of the pancreatic stump [3e7]. Several methods and techniques of pancreatic anastomosis have been proposed after PD to reduce the rate of POPF including the usage of an external or an internal pancreatic stent, isolated loop pancreaticojejunostomy (IPJ), pancreaticogastrostomy, binding PJ, or an administration of postoperative somatostatin [4e13]. The safe pancreatic reconstruction after PD continues to be a challenge at the high volume centers. The variety of reconstruction is a reflection of the lack of the ideal one [4e9]. No pancreatic reconstruction technique after PD was found to be applicable to all kinds of pancreatic remnants. No consensus exists regarding the ideal PJ reconstruction to reduce POPF. Duct to mucosa and invagination are two classic PJ techniques. Many studies have compared both techniques, but their surgical outcomes are
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A. El Nakeeb et al. / International Journal of Surgery 16 (2015) 1e6
1. Patients and methods
and mucosa. The duct was taken posteriorly and anteriorly to jejunal mucosa. A pancreatic duct stent was inserted during anastomosis and removed at the end of taking the stitches. The reconstruction was completed by end to side hepaticojejunostomy (retrocolic) and gastrojejunostomy (GJ) (antecolic) end to side manually.
1.1. Patients
1.6. Data collected
Consecutive patients that were treated by PD at the Gastroenterology Surgical Center, Mansoura, Egypt, during the period from June 2011 to September 2013, were eligible for the study. The exclusion criteria included any patients with locally advanced periampullary tumor, metastases, patients received neoadjuvant chemoradiotherpy, patients underwent pancreaticogastrostomy (PG) and patients with advanced liver cirrhosis (Child B or C), malnutrition, or coagulopathy. Informed consent was obtained from all patients to be included in this study, after a careful explanation of the disease and the possible treatment options with its complications. The study was approved by the local ethical committee. All patients were subjected to careful history taking, clinical examination, routine laboratory investigation and tumor markers as CEA and CA19-9, an abdominal ultrasound, magnetic resonance cholangiopancreatography (MRCP), and an abdominal computerized tomography (CT).
Preoperative variables included; age, sex, body mass index, patients' symptoms and signs, laboratory tests, tumor markers and preoperative biliary drainage. Intraoperative variables included; liver status, tumor size, pancreatic duct diameter, texture of the pancreas, operative time, blood loss and blood transfusion. Postoperative variables included; postoperative complications, drain amylase, liver function, day to resume oral feeding, postoperative stay, re-exploration, hospital mortality, postoperative pathology, and surgical safety margins.
still unclear [8,14e21]. The aim of the study was to assess the effectiveness and the surgical outcomes of both techniques of PJ after PD.
1.2. Randomization The patients included in the study were randomized into two groups using the closed envelope method. The envelopes were drawn and opened by a nurse in the operating room after pancreatic resection. The patients were randomized into two groups: Group I: patients underwent duct to mucosa PJ. Group II: patients underwent invagination PJ. 1.3. Operative techniques Standard PD was performed in all patients. All patients underwent regional lymphadenectomy, which included resection of nodes within the outlines of the hepatoduodenal ligament, right side of the superior mesenteric vessels, and inferior vena cava. All anastomoses were performed by experienced surgeons.
1.7. Assessments The primary outcome was POPF rate. POPF was defined by the International Study Group of Pancreatic Fistula (ISGPF) as any measurable volume of fluid on or after POD 3 with amylase content greater than 3 times the serum amylase activity [22,23]. A pancreatic fistula (PF) was graded according to the ISGPF into Grade A, B and C according to the clinical course [22,23]. The secondary outcomes were operative time, operative time needed for reconstruction, length of postoperative hospital stay, postoperative morbidities including (delayed gastric emptying (DGE), pancreatitis and biliary leakage). Complications were graded according to their severity on a validated five point scale using Dindo-Clavien complication classification system into (grades I, II, IIIaeb, IVaeb, V) [24]. The complications which were higher than ClavieneDindo grade III were considered to be major complications [24]. The pancreatic exocrine function was evaluated clinically. It was assessed by the presence or the absence of the steatorrhea (passing stool more than three times per day, fecal output of >200 g/d for at least three days, pale or yellow stools, and appearance of stools as pasty or greasy), the need of pancreatic enzymes supplement and studied variation in the body weight pre and postoperative [25]. 1.8. Follow up
1.4. *Duct to mucosa PJ group (Group 1) The duct to mucosa PJ was performed by a two layer end to side PJ. The pancreatic capsule and the jejunal serosa were anastomosed by interrupted silk suture 3/0 to form the outer layer in both the anterior and posterior walls of the anastomosis. Jejunostomy was done matched to the pancreatic duct diameter. The inner layer duct to mucosa was performed in eight to twelve stitches with 5/0 prolene. A pancreatic duct stent was inserted during the anastomosis to allow an easy and accurate suture placement, ensure an adequate pancreatic duct exposure and protect the opposite wall from being inadvertently held by needles and then it was removed at the end of the anastomosis.
Follow-up was carried out one week postoperatively, 3 months, 6 months and then after one year. Statistical analysis in this study was performed using SPSS software, version 17. Descriptive statistics were calculated and described as median (range) for continuous variables. Categorical variables were represented using percentages. Student's t-test for paired samples was used to detect differences in the means of continuous variables and Chi-square test was used for categorical variables. P values 2 cm Pancreatic duct diameter (mm) Median (mm) 3 mm >3 mm Relation of pancreatic duct to the posterior border Median (mm) 3 mm >3 mm Pancreatic consistency Firm Soft Median total operative time (hours) Median operative time for PJ anastomosis (minute) Median blood loss (ml)
24 3 48 59
Duct to mucosa PJ Group 1
(22.4%) (0.5e12) (44.9%) (55.1%)
13 2.5 25 28
(24.5%) (0.5e6) (47.2%) (52.8%)
Invaginated PJ Group 2 11 3 23 31
(20.4%) (0.5e12) (42.6%) (57.4%)
P Values 0.17 0.19 0.69
3 (1e12) 55 (51.4%) 52 (48.6%)
3 (1e12) 30 (56.6%) 23 (43.4%)
3 (1e12) 25 (46.3%) 29 (53.7%)
0.49 0.33
3 (1e15) 54 (50.5%) 53 (49.5%)
3 (1e15) 30 (56.6%) 23 (43.4%)
3 (1e13) 24 (44.4%) 30 (55.6%)
0.91 0.25
55 (51.4%) 52 (78.6%) 5.5 (3e9) 31 (20e45) 500 (50e3000)
2.4.1. Pancreatic exocrine and endocrine function 21/50 (42%) patients presented with postoperative steatorrhea after one year in group 1 vs. 11/50 (22%) patients in group 2 (P ¼ 0.04). The median one year postoperative albumin was significantly more in group 1 than in group 2 (3.4 gm% vs 3.6 gm% respectively) (P ¼ 0.03) (Table 4). There was no statistically significant difference regarding preoperative and postoperative weight and BMI in both groups. There was no statistically significant difference regarding the incidence of DM preoperatively and one year postoperatively (Table 4).
28 25 5.5 34 500
(52.8%) (47.2%) (3e8) (20e42) (100e3000)
27 27 5 30 500
(50%) (50%) (4e9) (21e45) (50e2600)
0.85 0.90 0.002 0.92
3. Discussion The safe pancreatic anastomosis after PD continues to be a stump for the pancreatic surgeon even at the high volume centers. Several techniques and modifications of pancreatic anastomoses have been proposed [4e12]. Despite the lowering of the mortality rate to 5%, postoperative complications are still high up to 50% [2e7]. In most of published studies, morbidity and mortality after PD are related to pancreatic reconstruction [1e6]. POPF remains the most important cause of morbidity and also contributes significantly to prolonged hospital stay, increased costs
Table 3 Postoperative data. Variables
Total
Duct to mucosa PJ Group 1
Invaginated PJ Group 2
P alues
Hospital stay (days) Drain removal (days) Amount of draining (ml) Time starting oral (days) Total patients with complications Complications grade I II III IV V Severe complications (IIIb) Minor Major Drain amylase First day Third day POPF Pancreatic leakage Grade A Grade B Grade C Pancreatitis Biliary leakage Delayed gastric emptying Internal hemorrhage Wound infection Pulmonary complications Re-exploration Mortality Pulmonary embolism SIRS Liver insult
8 (4e41) 8 (4e35) 900 (70e18,000) 5 (4e28) 36 (33.6%)
8 (5e41) 8 (4e34) 1200 (70e18,000) 5 (4e28) 21 (39.6%)
8 (4e35) 8 (4e35) 800 (125e15,000) 5 (4e23) 15 (27.8%)
0.83 0.79 0.72 0.67 0.22
12 (11.2%) 7 (6.5%) 6 (5.6%) 1 (0.9%)
6 4 4 1
(11.3%) (7.5%) (7.5%) (1.9%)
6 (11.1%) 3 (5.6%) 2 (3.7%) 0
0.72
23 (21.5%) 4 (3.7%)
13 (24.5%) 3 (5.7%)
10 (18.5%) 1 (1.9%)
0.4
161 (6e44,000) 200 (10e22,180) 19 (17.8%) 12 (11.2%) 6 (5.6%) 2 (1.9%) 6 (5.6%) 13 (12.1%) 15 (14%) 5 (4.7%) 9 (8.4%) 4 (3.7%) 13 (12.1%) 7 (6.5%) 3 3 1
650 (20e44,000) 442 (10e22,180) 11 (20.8%) 6 (11.3%) 4 (7.5%) 2 (3.8%) 5 (7.5%) 7 (13.2%) 8 (15.1%) 3 (5.7%) 5 (9.4%) 1 (1.9%) 8 (15.1%) 3 (5.7%) 1 2 0
45 (6e8000) 120 (20e7500) 8 (14.8%) 6 (11.1%) 2 (3.7%) 0 1 (1.9%) 6 (11.1%) 7 (13%) 2 (3.7%) 4 (7.4%) 3 (5.6%) 5 (9.3%) 4 (7.4%) 2 1 0
0.48 0.49 0.46 0.4
0.08 0.78 0.79 0.68 0.72 0.62 0.39 0.72
A. El Nakeeb et al. / International Journal of Surgery 16 (2015) 1e6 Table 4 Functional changes. Variables
Duct to mucosa PJ Invaginated PJ P values Group 1 Group 2
Preoperative Steatorrhae Postoperative steatorrhae P* value
10/53 (18.9%) 21/50 (42%) 0.001
9/54 (16.7%) 11/50 (22%) 0.16
0.81 0.04
Preoperative albumin Postoperative albumin P* value
4 (3e5) 3.4 (3.1e4) 0.0001
4.05 (3e5) 3.6 (3e4.6) 0.0001
0.29 0.03
Preoperative weight Postoperative weight P* value
81 (60e125) 75 (58e99) 0.0001
75 (52e114) 0.16 74.5 (52e105) 0.96 0.0001
Preoperative fasting blood sugar 110 (71e410) Postoperative fasting blood sugar 136(71e450) P value* 0.0001
125 (79e231) 0.9 124 (75e233) 0.02 0.79
Preoperative DM Postoperative DM P value*
13/54 (24.1%) 15/50 (30%) 0.16
13/53 (24.5%) 19/50 (38%) 0.01
0.95 0.41
and mortality. Intra-abdominal abscess, bleeding and sepsis are common sequelae of POPF, which have been associated with a high mortality rate [2e8]. The development of POPF after PD appears to be a multifactorial. Many studies demonstrated that many factors significantly associated with POPF including; obesity, cirrhotic liver, soft pancreas, small pancreatic duct diameter, location of pancreatic duct within 3 mm distance from posterior edge, the technique and type of pancreatic reconstruction [2e7,25e27]. Ideally, the pancreatic reconstruction should not only decrease the risk of POPF, but it should decrease its severity if occurred and also, maintain pancreatic function [4e10]. Pancreaticojejunostomy (PJ) is the commonly preferred method of reconstruction after PD. In an effort to prevent POPF after PD, there have been many technical modifications for the pancreatic reconstruction [4e8]. Some retrospective studies showed that the duct to mucosa PJ was associated with a lower rate of POPF in the low risk patients with dilated pancreatic duct or firm pancreas, whereas the invagination PJ technique was safer in the high risk patients with small pancreatic duct or soft pancreas [9,19,28e32]. Several prospective randomized studies reported that a lower POPF in duct to mucosa PJ group than in the invagination PJ group. However the advantage was not found in patients with soft pancreatic stump [19,33,34]. The meta-analysis studies showed that the rate of POPF was not statistically different between duct to mucosa PJ group and the invagination PJ group [8,16,35]. In the current study no significant difference as regards POPF in both groups. The severity of POPF was noticed more in duct to mucosa PJ with no significant differences. No pancreatic reconstruction technique after PD was found to be applicable to all types of pancreatic stumps. Tailored pancreatic reconstruction is the best way to overcome the complications related to the type of reconstruction. Pancreatic reconstruction is difficult in pancreases with small duct and a soft fragile pancreas even in experienced hand [2e10]. Soft friable pancreatic tissue can be problematic for invagination PJ as the parenchymal laceration and ischemia of the stump can occur because of extensive sutures and compression which lead to POPF [2,8,16,36]. The small pancreatic duct makes duct to mucosa PJ difficult and liable to inaccurate suture placement and obstruction. In duct to mucosa PJ, the jejunal folds and edema formed around the opening of the pancreatic duct make it liable to the obstruction and development of the pancreatitis and anastomotic stenosis [36]. In contrast to, the invagination PJ is easier to perform and all of the pancreatic juice is drained into the jejunum [8,36]. In this study, postoperative steatorrhea after one year was
5
noticed more significantly in duct to mucosa than in the invagination PJ group (P ¼ 0.04). Also, the median one year postoperative albumin was significantly less in the duct to mucosa group than in the invagination PJ group (3.4 gm% vs. 3.6 gm% respectively) (P ¼ 0.03). Several published studies found that pancreatic exocrine function after PD depends on many complex variables including; preexisting pancreatitis, the degree of fibrosis in pancreatic remnant, the volume of resected pancreatic tissue, the impairment of the pancreatic secretion flow due to the anastomotic stricture or by swelling of the jejunal mucosa and may be the type of pancreatic reconstruction [37e39]. There is however no evidence that impaired pancreatic endocrine function would be associated more often with a certain type of reconstruction [38]. PG could cause more morphological and functional derangement because the reflux of gastric juice causes inactivation of the pancreatic enzymes and early pancreatic insufficiency [40,41]. In duct to mucosa PJ, the jejunal folds and edema formed around the opening of pancreatic duct make it liable to a development of pancreatitis and an anastomotic stricture which may lead to a pancreatic exocrine dysfunction [36e38]. Additional studies are needed to recognize the tailored pancreatic reconstruction after PD. Soft friable pancreatic tissue can be problematic for the invagination PJ due to parenchymal laceration. Small pancreatic duct makes duct to mucosa PJ difficult and liable to inaccurate suture placement and obstruction. 4. Conclusion Invagination PJ is easier to perform than duct to mucosa especially in the small pancreatic duct. All of the pancreatic juice is drained into the jejunum in the invagination PJ. The soft and friable pancreatic tissue can be problematic for the invagination PJ due to parenchymal laceration. POPF was not statistically different between the duct to mucosa PJ group and the invagination PJ group. The severity of POPF was noticed more in duct to mucosa PJ with no significant differences. Postoperative steatorrhea was noticed more significantly in duct to mucosa than in invagination PJ group. Postoperative serum albumin level was significantly more in the invagination PJ group than in the duct to mucosa group. Ethical approval The study was approved by the local ethical committee. Financial support None. Conflicts of interest None. Author contribution Ayman El Nakeeb designed research. Ayman El Nakeeb, Mohamed El Hemaly, Waleed Askr, Mohamed Abd Ellatif, Hosam Hamed, Mohamed Attia, Tallat Abdallah, Mohamed Abd ElWahab performed research. Ayman El Nakeeb, Mohamed Said analyzed data. Ayman El Nakeeb wrote the paper. Guarantor Name: Ayman El Nakeeb. E-Mail: [email protected].
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