COMPARATIVE STUDY BETWEEN PANCREATICOJEJUNOSTOMY AND PANCREATICOGASTROSTOMY FOLLOWING PANCREATICODUODENECTOMY

Document Type : Original Article

Authors

Department of General Surgery, Faculty of Medicine, Al-Azhar University

Abstract

Background: Pancreaticojejunostomy and pancreaticogastrostomy are the two techniques for pancreatic anastomosis that are widely established for the reconstruction after pancreaticoduodenectomy.
Aim: To study the effect of the type of pancreaticoenteric reconstruction pancreaticojejunostomy versus pancreaticogastrostomy (PJ versus PG) after pancreaticoduodenectomy regarding the post-operative mortality and morbidity particularly pancreatic fistula (PF).
Patients and Methods: A prospective cohort study included 40 patients with pancreatic or periampullary cancer who undergone pancreaticoduodenectomy. The patients divided randomizly into two groups; Group (A)included 20 patients who had undergone pancreaticojejunostomy reconstruction while group (B) included 20 patients who had undergone pancreaticogastrostomy reconstruction.
Results: Mean operative time in group A and B was 7.6 ± 2.2 and 7.2 ± 2.7, mean blood loss 984.7 ± 253.2 and 852.5 ± 152.6, in most of the cases there was a Drains in contact with anastomosis was 85% and 70%, respectively. Also, there is no significant difference between both groups regarding intraoperative data. Considering postoperative complications, there was significant difference between both groups regarding pancreatic fistula, bile leak, postoperative pancreatitis andpeptic ulcer.
Conclusion: This study observed that PG is associated with a lower risk for PF compared with PJ.

Keywords


COMPARATIVE STUDY BETWEEN PANCREATICOJEJUNOSTOMY AND PANCREATICOGASTROSTOMY FOLLOWING PANCREATICODUODENECTOMY

By

Salah Saber Mabrouk*, Essam El-Din Abd El-Azim El-Desouky and

Abd El-Fattah Morsy Saeid

Department of General Surgery, Faculty of Medicine, Al-Azhar University

*Corresponding Author: Salah Saber Mabrouk,

E-mail: 01000231689sasa@gmail.com

ABSTRACT

Background: Pancreaticojejunostomy and pancreaticogastrostomy are the two techniques for pancreatic anastomosis that are widely established for the reconstruction after pancreaticoduodenectomy.

Aim: To study the effect of the type of pancreaticoenteric reconstruction pancreaticojejunostomy versus pancreaticogastrostomy (PJ versus PG) after pancreaticoduodenectomy regarding the post-operative mortality and morbidity particularly pancreatic fistula (PF).

Patients and Methods: A prospective cohort study included 40 patients with pancreatic or periampullary cancer who undergone pancreaticoduodenectomy. The patients divided randomizly into two groups; Group (A)included 20 patients who had undergone pancreaticojejunostomy reconstruction while group (B) included 20 patients who had undergone pancreaticogastrostomy reconstruction.

Results: Mean operative time in group A and B was 7.6 ± 2.2 and 7.2 ± 2.7, mean blood loss 984.7 ± 253.2 and 852.5 ± 152.6, in most of the cases there was a Drains in contact with anastomosis was 85% and 70%, respectively. Also, there is no significant difference between both groups regarding intraoperative data. Considering postoperative complications, there was significant difference between both groups regarding pancreatic fistula, bile leak, postoperative pancreatitis andpeptic ulcer.

Conclusion: This study observed that PG is associated with a lower risk for PF compared with PJ.

Keywords: Pancreaticojejunostomy, Pancreaticogastrostomy, Pancreaticoduodenectomy.

 

 

INTRODUCTION

     Pancreatic surgery, in particular pancreatico-duodenectomy (PD), has been called a formidable operation. It is not only a technical challenge to surgeons, it is also demanding for patients, and it exerts a substantial logistical strain on healthcare resources (Ho et al., 2009).

     Pancreaticojejunostomy and pancreaticogastrostomy are the two techniques for pancreatic anastomosis that are widely established for the reconstruction after pancreaticoduodenectomy. Pancreaticogastrostomy is the most recent and to date less frequently performed method (Tittelbach et al., 2017).

     Since postoperative complications contribute to the overall mortality (Bakkevoid and Kambestad, 2001), efforts to reduce morbidity rates are now turned to the four most frequent procedure-related complications following pancreatic resection, namely pancreatic fistula, delayed gastric emptying (DGE), septic complications in particular intra-abdominal abscess, and abdominal hemorrhage. The major complications after pancreatic surgery such as intra-abdominal abscesses, anastomotic leakage and postoperative bleeding are responsible for most of the postoperative mortality (Buchler et al., 2005).

     We aimed to study the effect of the type of pancreaticoenteric reconstruction pancreaticojejunostomy versus pancreaticogastrostomy (PJ versus PG) after pancreaticoduodenectomy regarding the post-operative mortality and morbidity particularly pancreatic fistula (PF).

PATIENTS AND METHODS

     A prospective cohort study conducted at General Surgery Department, Al Azhar University during the period from 1 September 2017 to 1 March 2021.

This study included 40 patients with pancreatic or periampullary cancer who undergone pancreaticoduodenectomy. The patients divided randomized into two groups:

  • Group (A) patients: included 20 patients who had undergone pancreaticojejunostomy reconstruction for pancreatic duct after PD. Pancreatic duct had been anastomosed with proximal jejunum (end to side) with interrupted duct to mucosa method in two layers.
  • Group (B) patients: included 20 patients who had undergone pancreaticogastrostomy reconstruction for pancreatic duct after PD. Pancreatic duct had been anastomosed with the posterior wall of the stomach with invagination technique in two layers.

     Then the sequence of reconstruction had been completed by end to side hepatico-jejunostomy and gastrojejunostomy.

  • Inclusion criteria:

     The study included forty patients in the period of study with suspected pancreatic or periampullary cancer that was assumed to be resectable, according to preoperative clinical examination and work up.

  • Exclusion criteria:

     Patients with locally advanced and metastatic tumors had been excluded from the study, as indicated by clinical examination, preoperative workup and intraoperative findings.

  • Methods:

     The design of this study had been consisted of a pretreatment evaluation and treatment with either a PJ or PG reconstruction of the pancreatic duct after PD.

     All patients subjected to full history talking, clinical assessment and investigation which involved CBC, coagulation profile, liver function tests, renal function tests, tumor markers, electrolytes level, ECG, ECHO, computerized tomography (CT) pancreatic protocol, MRI, endoscopic retrograde cholangio-panereatography (ERCP) and endoscopic U/S.

     The postoperative morbidity (especially the Pancreatic fistula), mortality and the postoperative hospital stay had been evaluated.

Statistical Analysis of Data:

     The collected data organized, tabulated and statistically analyzed using statistical package for social sciences (SPSS) version 22 (SPSS Inc, Chicago, USA). For qualitative data, frequency and percent distributions was calculated. For quantitative data, mean, standard Error (SE), minimum and maximum was calculated. Statistical significance was defined as P value < 0.05.

The following tests were done:

  • Independent-samples t-test of significance was used when comparing between two means.
  • Chi-square test of significance was used when comparing between frequencies.
  • P-value <0.05 was considered significant.

 

RESULTS

 

 

     A total of 40 patients enrolled in this study, the mean of age in group A and B was 60.7±25.3 and 62.1±28.6, respectively.There is no significant difference between both groups regarding age, sex, BMI and indication of surgery (Table 1).

     There is no significant difference between both groups regarding Hematocrit (%), White blood cell count, Creatinine, Total bilirubin and Albumin levels (Table 2).

     Mean operative time in group A and B was 7.6 ± 2.2and 7.2 ± 2.7, mean blood loss 984.7 ± 253.2 and 852.5 ± 152.6, in most of the cases there was a Drains in contact with anastomosis was 85% and 70%, respectively. Also, there is no significant difference between both groups regarding intraoperative data (Table 3).

     Considering postoperative complications, there was significant difference between both groups regarding pancreatic fistula (group A 20%, group B 10%), bile leak (group A 5%, group B 15%), postoperative pancreatitis (group A 5%, group B 15%), peptic ulcer (group A 10%, group B 0%) (Table 4).

 

 

Table (1):   Demographic and clinical data of studied groups

 

Group A

(N=20)

Group B

(N=20)

P value

Age (year)

⁃          Mean +SD

⁃          Range

 

60.7±25.3

(56-71)

 

62.1±28.6

(59-75)

0.517

Sex

⁃          Male

⁃          Female

 

12 (60%)

8 (40%)

 

9 (45%)

11 (55%)

0.352

BMI (kg/m2)

24.7±5.8

23.8±6.3

0.583

Indication of operation:

⁃          Pancreatic cancer

⁃          Ampullary cancer

⁃          Cancer of distal bile ducts

 

15 (75%)

3(15%)

2 (10%)

 

13 (65%)

4 (20%)

3(15%)

0.316

 

Table (2):   Comparison between both groups regarding preoperative laboratory

 

Group A

(N=20)

Group B

(N=20)

P value

Hematocrit (%)

37.5 ±15.6

36.4±18.2

0.335

White blood cell count (103 cells/mm3)

9.3 ± 2.5

9.1 ± 2.8

0.128

Creatinine (mg/dL)

1.1 ±0.1

1.0 ±0.1

0.831

Total bilirubin (mg/dL)

7.6 ± 2.4

5.7 ± 1.9

0.182

Albumin (g/dL)

3.5 ± 1.3

3.7 ± 1.5

0.311

 

Table (3):   Comparison between both groups regarding intraoperative data

 

Group A

(N=20)

Group B

(N=20)

P value

Operative time (hr)

7.6 ± 2.2

7.2 ± 2.7

0.461

Blood loss (mL)

984.7 ± 253.2

852.5 ± 152.6

0.274

Texture at transected neck

⁃                      Hard

⁃                      Intermediate

⁃                      Soft

 

3 (15%)

12 (60%)

5 (25%)

 

7 (35%)

9 (45%)

4 (20%)

0.115

Mean length of remnant mobilized (cm)

3.1 ± 0.1

3.0 ± 0.2

0.624

Mean diameter of pancreatic duct at

transected neck (mm)

3.2 ± 1.2

2.7 ± 1.4

0.258

Pancreatic duct in inner layer of

anastomosis (%)

17 (85%)

15 (75%)

0.424

Drains in contact with anastomosis (%)

17 (85%)

14 (70%)

0.217

 

Table (4):   Comparison between both groups regarding postoperative complications

 

Group A

(N=20)

Group B

(N=20)

P value

Delayed gastric emptying1

5 (25%)

4 (20%)

0.181

Wound infection

4 (20%)

5 (25%)

0.374

Pancreatic fistula2

4 (20%)

2 (10%)

< 0.001*

Cholangitis

2 (10%)

3 (15%)

0.265

Pneumonia

1 (5%)

2 (10%)

0.113

Intra-abdominal abscess

3 (15%)

2 (10%)

0.253

Cardiac arrhythmia

1 (5%)

1 (5%)

1.0

Bile leak

1 (5%)

3 (15%)

< 0.001*

Urinary tract infection

4 (20%)

3 (15%)

0.218

Postoperative pancreatitis

1 (5%)

3 (15%)

< 0.001*

Peptic ulcer

2 (10%)

0 (0%)

< 0.001*

1Defined as follows: (1) nasogastric tube in place ≥10 days plus one of the following: (a) emesis after nasogastric tube removed, (b) reinsertion of nasogastric tube, or (c) failure to progress with diet; or (2) nasogastric tube in place < 10 days plus two of (a) to (c) above.

2Defined as follows: (1) drainage of > 50 mL of amylase-rich fluid (greater than threefold elevation above upper limit of normal in serum) via the operatively placed drains on or after postoperative day 10 or (2) pancreatic anastomotic disruption demonstrated radiographically.

*p value significant

 

 

 

 

DISCUSSION

     Pancreatic reconstruction is particularly demanding; a variety of methods and techniques have been proposed to maintain the continuity of the anastomosis and diminish rates of leak. The conventional anastomosis described for this operation is pancreaticojejunostomy (PJ), Pancreaticogastrostomy (PG) has been described and studied as an alternative to jejunal anastomosis in both observational studies and randomized controlled trials (RCTs) with inconsistent results (Topal et al., 2013).

     Most common indication of surgery of our study was Pancreatic cancer, this also was confirmed by many studies, in the study of (El Nakeeb et al., 2019) to evaluate Laparoscopic Pancreaticodudenectomy, most of operated cases had Pancreatic head mass (55%).

    In the study of (Karim et al., 2018), concerning the indications behind this procedure for our patients, 16.33% of patients had benign tumors, whereas, the commonest malignant tumors were periampullary (43.88%), followed by pancreatic cancer (16.33%), and the least indications were ampullary carcinoma (9.18%).

     Regarding intraoperative data, there was no statistically significant difference between both groups regarding intraoperative data. Mean operative time in our study was (7.6 ± 2.2, 7.2 ± 2.7) in both groups, mean blood loss (984.7 ± 253.2, 852.5 ± 152.6), in most of the cases there was a Drains in contact with anastomosis (85%, 70%). These results were near results of (El Nakeeb et al., 2019), (Senthilnathanet al., 2015), (Topal et al., 2013).

     Operative time relies on surgical skills and technical feasibility, in the study of (Romano et al., 2015), the The mean operative time was 4.9 min (±55 min). The mean blood loss was 450 ml and median blood transfusion was 1 unit.

     Also, in the study of (El Nakeeb et al., 2019), the mean operative time was 5 hours for method and 7 hours for laparoscopic one, while blood loss was 450 ml for open and 250 for laparoscopic methods.

     In the study of (Wang et al., 2016), there was no significant difference in operative time between PG (7 (3–16)) and PJ (7 (3–13)). This indicates similar technical and operative similarities between both techniques.

     Regarding Comparison between both groups regarding postoperative complications, there was statistically significant difference between both groups regarding Pancreatic fistula (group A 20%, group B 10%), Bile leak (group A 5%, group B 15%), Postoperative pancreatitis (group A 5%, group B 15%), Peptic ulcer            group A 10%, group B 0%), Duodenojejunostomy leak (group A 0%, group B 15%).

     PG has been claimed to be a better pancreatic reconstruction in reducing the incidence and severity of POPF. Four recent meta-analyses based on 8 randomized control trials (RCTs) conclude that POPF rate is significantly lower in PG than that in PJ (Wang et al., 2016), (Hallet et al., 2015), (Que et al., 2015).

     PG has been proposed as an alternative to PJ. A number of theoretical advantages of PG have been suggested including: pancreatic enzyme inactivation due to gastric secretions and absence of enterokinase, tension-free anastomosis due to anatomical co-location, excellent blood supply and the thick stomach wall is less likely to dehisce, early detection of bleeding from the pancreatic remnant by routine postoperative gastric decompression, direct examination of the anastomosis by endoscopy if necessary; and easy exploration of the anastomosis without disassembling the pancreatic anastomosis by opening the anterior wall of stomach if bleeding occur (Kleespies et al., 2008). This explains the lower incidence of peptic ulcer and leake in PG group.

     However, in the study of (Hallet J et al., 2015) PF occurred in 8% of PG cases, while 20% in PJ (P <0.001). they concluded that, this study systematically reviewed and pooled data from four RCTs investigating the impacts of PG compared with PJ on PF. Based on evidence of moderate quality, PG is associated with a lower occurrence of PF (RR 0.41, 95% CI 0.27–0.62), but no significant differences emerged in biliary leak, DGE, postoperative bleeding, major morbidity, mortality or LoS. When only high- or low-risk pancreas groups were considered, there was no difference in RR.

     The proposed technical and physiological advantages of PG over PJ have been discussed in several studies reporting the technique. The anastomosis may be facilitated by a thick gastric wall, can rely on an excellent gastric blood supply, and is subject to less tension as a result of the anatomic proximity of the pancreatic remnant to the posterior gastric wall. Lack of enterokinase in the gastric remnant may prevent the activation of pancreatic enzymes, thereby avoiding both damage to the anastomosis itself and the repercussions associated with potential PF (He et al., 2008).

CONCLUSION

     This study observed that PG is associated with a lower risk for PF compared with PJ. This benefit appeared to be greater in high-risk patients. Surgeons should consider reconstructing the pancreatic remnant following PD with PG, particularly in patients at high risk for PF.

REFERENCES

  1. Bakkevotd KE, Kambcstad B (2001): Morbidity and mortality after radical and palliative pancreatic cancer surgery. Risk factors influencing the short-term results. Ann Surg; 217:356-68.
  2. Buchler MW, Wagner M, Schmied BM, (2005): Changes in morbidity after pancreatic resection: toward the end of completion pancreatectomy. Arch Surg; 138: 1310-1314.
  3. El Nakeeb A, El Sorogy M, Hamed H, Said R, Elrefai M, Ezzat H, et al. (2019): Biliary leakage following pancreaticoduodenectomy: Prevalence, risk factors and management. Hepatobiliary& Pancreatic Diseases International. 18(1):67-72.
  4. Hallet J, Zih FS, Deobald RG, Scheer AS, Law CH, Coburn NG et al. (2015): The impact of pancreaticojejunostomy versus pancreaticogastrostomy reconstruction on pancreatic fistula after pancreaticoduodenectomy: meta-analysis of randomized controlled trials. HPB 17:113–122.
  5. He T, Zhao Y, Chen Q, Wang X, Lin H, Han W. (2013): Pancreaticojejunostomy versus pancreaticogastrostomy after pancreaticoduodenectomy: a systematic review and meta-analysis. Dig Surg 30:56–69.
  6. Ho C, KleefJ, FriessH, Buchler MW (2009): Complications of pancreatic surgery. HPB; 7: 99-108.
  7. Karim SA, Abdulla KS, Abdulkarim QH, Rahim FH. (2018): The outcomes and complications of pancreaticoduodenectomy (Whipple procedure): Cross sectional study. International Journal of Surgery. 52:383-7.
  8. Kleespies A, Albertsmeier M, Obeidat F, Seeliger H, Jauch KW, Bruns CJ. (2008): The challenge of pancreatic anastomosis. Langenbeck’s Archives of Surgery;393(4):459-471.
  9. Que W, Fang H, Yan B, Li J, Guo W, Zhai W et al. (2015): Pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy: a meta-analysis of randomized controlled trials. Am J Surg 209:1074–1082.
  10. Senthilnathan P, Srivatsan, Gurumurthy S, (2015): Long-term results of laparoscopic pancreaticoduodenectomy for pancreatic and periampullary cancer-experience of 130 cases from a tertiary-care center in South India. J LaparoendoscAdvSurg Tech A. 25:295–300.
  11. Tittelbach-Helmrich D, Keck T, Wellner UF (2017): The challenges of improving survival following pancreaticoduodenectomy for pancreatic ductal adenocarcinoma Chirurg. 88(1):11-17.
  12. Topal B, Fieuws S, Aerts R, Weerts J, Feryn T, Roeyen G et al. (2013): Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after pancreaticoduodenectomy for pancreatic or periampullarytumours a multicentre randomized trial. Lancet Oncol. 14:655–662.
  13. Wang M, Meng L, Cai Y, Li Y, Wang X, Zhang Z, Peng B. (2016): Learning curve for laparoscopic pancreaticoduodenectomy: A CUSUM analysis. Journal of Gastrointestinal Surgery.;20(5):924-935.



دراسة مقارنة بين نتائج توصيل البنكرياس بالأمعاء الدقيقة وتوصيله بالمعدة بعد استئصال البنكرياس والاثني عشر فى حالات الأورام الخبيثة

صلاح صابر مبروك ابراهيم*، عصام الدين عبد العظيم الدسوقى زايد،

عبد الفتاح مرسي سعيد محمد قلموش

E-mail: 01000231689sasa@gmail.com

خلفية البحث: توصيل  البنكرياس بالأمعاء الدقيقة وتوصيل البنكرياس بالمعدة هما طريقتان توصيل البنكرياس بالجهاز الهضمى  اللتان تم تأسيسهما على نطاق واسع لإعادة الإعمار بعد استئصال البنكرياس والاثني عشر. توصيل البنكرياس بالمعدة هو أحدث الطرق وأقلها استخدامًا حتى الآن.

         نظرًا لأن مضاعفات ما بعد الجراحة تساهم فى إجمالى نتائج الإجراءات الجراحية، فقد تحولت الجهود المبذولة لتقليل معدلات مضاعافات مابعد الجراحة حيث أن المضاعفات الأربعة الأكثر شيوعًا المتعلقة بالإجراء بعد استئصال البنكرياس، وهي ناسور البنكرياس، وتأخر إفراغ المعدة (DGE)، ومضاعفات الإنتان فى خراج داخل البطن بشكل خاص، و نزيف في البطن. يذكر أن المضاعفات الرئيسية بعد جراحة البنكرياس مثل الخراجات داخل البطن والتسرب من التوصيل بين البنكرياس والجهاز الهضمى والنزيف بعد الجراحة هي المسؤولة عن معظم الوفيات بعد الجراحة.

الهدف: من هذا العمل هو دراسة تأثير نوع إعادة بناء البنكرياس بالأمعاء الدقيقة مقابل توصيل البنكرياس بالمعدة (PJ مقابل PG) بعد استئصال البنكرياس والاثنى عشر فيما يتعلق بالوفيات والمراضة بعد الجراحة وخاصة ناسور البنكرياس (PF).

المرضى وطرق البحث: تضمنت هذه الدراسة 40 مريضا يعانون من سرطان البنكرياس أو ماحول فتحة القناة المرارية داخل الإثنى عشر والذين خضعوا لعملية استئصال البنكرياس و الاثناعشر.

قسم المرضى إلى مجموعتين:

  • مرضى المجموعة (أ): تضمنت 20 مريضًا خضعوا لتوصيل البنكرياس بالأمعاء الدقيقة. حيث تم توصيل قناة البنكرياس مع الأمعاء الدقيقة (من طرف إلى جانب) بطريقة القناة إلى الغشاء المخاطى فى طبقتين.
  • مرضى المجموعة (ب): تضمنت 20 مريضًا خضعوا لإعادة توصيل البنكرياس بالمعدة. حيث تم توصيل الجزء المتبقى من البنكرياس بالجدار الخلفي للمعدة بطريقة الإنغماس أو الإنغماد فى طبقتين.

         ثم تم الانتهاء من تسلسل إعادة الإعمار بتوصيل القناة المرارية الكبدية بالأمعاء الدقيقة وكذلك توصيل المعدة بالأمعاء الدقيقة.

         أظهرت نتيجتنا أنه لا يوجد فرق معتد به إحصائيًا بين المجموعتين فيما يتعلق بالبيانات أثناء العملية.

         فيما يتعلق بالمقارنة بين المجموعتين فيما يتعلق بمضاعفات ما بعد الجراحة ، كان هناك فرق معتد به إحصائيًا بين المجموعتين فيما يتعلق بناسور البنكرياس) المجموعة أ 20٪، المجموعة ب 10٪، (P <0.001، تسرب الصفراء) المجموعة أ 5٪، المجموعة ب 15٪، (P <0.001، التهاب البنكرياس بعد الجراحة) المجموعة أ 5٪، المجموعة ب 15٪، (P <0.001، مجموعة القرحة الهضمية أ 10٪، المجموعة ب 0٪، ف < 0.001).

استنتاج: يمكننا أن نستنتج أن هذه الدراسة لاحظت أن توصيل الجزء المتبقى من النكرياس PG يرتبط بانخفاض خطر الإصابة بـ PF مقارنة بـتوصيل الجزء المتبقى من البنكرياس بالأمعاء الدقيقة PJ. ويبدو أن هذه الفائدة تكون أكبر في المرضى المعرضين لمخاطر عالية. لذا يجب على الجراحين التفكير في إعادة بناء بقايا البنكرياس بعداستئصال البنكرياس والإثنى عشر PD مع المعدة PG، خاصة في المرضى المعرضين لخطر كبير للإصابة بـناسور البنكرياس PF.

  1. REFERENCES

    1. Bakkevotd KE, Kambcstad B (2001): Morbidity and mortality after radical and palliative pancreatic cancer surgery. Risk factors influencing the short-term results. Ann Surg; 217:356-68.
    2. Buchler MW, Wagner M, Schmied BM, (2005): Changes in morbidity after pancreatic resection: toward the end of completion pancreatectomy. Arch Surg; 138: 1310-1314.
    3. El Nakeeb A, El Sorogy M, Hamed H, Said R, Elrefai M, Ezzat H, et al. (2019): Biliary leakage following pancreaticoduodenectomy: Prevalence, risk factors and management. Hepatobiliary& Pancreatic Diseases International. 18(1):67-72.
    4. Hallet J, Zih FS, Deobald RG, Scheer AS, Law CH, Coburn NG et al. (2015): The impact of pancreaticojejunostomy versus pancreaticogastrostomy reconstruction on pancreatic fistula after pancreaticoduodenectomy: meta-analysis of randomized controlled trials. HPB 17:113–122.
    5. He T, Zhao Y, Chen Q, Wang X, Lin H, Han W. (2013): Pancreaticojejunostomy versus pancreaticogastrostomy after pancreaticoduodenectomy: a systematic review and meta-analysis. Dig Surg 30:56–69.
    6. Ho C, KleefJ, FriessH, Buchler MW (2009): Complications of pancreatic surgery. HPB; 7: 99-108.
    7. Karim SA, Abdulla KS, Abdulkarim QH, Rahim FH. (2018): The outcomes and complications of pancreaticoduodenectomy (Whipple procedure): Cross sectional study. International Journal of Surgery. 52:383-7.
    8. Kleespies A, Albertsmeier M, Obeidat F, Seeliger H, Jauch KW, Bruns CJ. (2008): The challenge of pancreatic anastomosis. Langenbeck’s Archives of Surgery;393(4):459-471.
    9. Que W, Fang H, Yan B, Li J, Guo W, Zhai W et al. (2015): Pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy: a meta-analysis of randomized controlled trials. Am J Surg 209:1074–1082.
    10. Senthilnathan P, Srivatsan, Gurumurthy S, (2015): Long-term results of laparoscopic pancreaticoduodenectomy for pancreatic and periampullary cancer-experience of 130 cases from a tertiary-care center in South India. J LaparoendoscAdvSurg Tech A. 25:295–300.
    11. Tittelbach-Helmrich D, Keck T, Wellner UF (2017): The challenges of improving survival following pancreaticoduodenectomy for pancreatic ductal adenocarcinoma Chirurg. 88(1):11-17.
    12. Topal B, Fieuws S, Aerts R, Weerts J, Feryn T, Roeyen G et al. (2013): Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after pancreaticoduodenectomy for pancreatic or periampullarytumours a multicentre randomized trial. Lancet Oncol. 14:655–662.
    13. Wang M, Meng L, Cai Y, Li Y, Wang X, Zhang Z, Peng B. (2016): Learning curve for laparoscopic pancreaticoduodenectomy: A CUSUM analysis. Journal of Gastrointestinal Surgery.;20(5):924-935.