Journal Pre-proof

Pancreaticojejunostomy For Pancreatico-enteric Anastomosis After

Pancreaticoduodenectomy: One Procedure With Multiple
Techniques.

Rajesh S Shinde , Rajgopal Acharya , Vikram A Chaudhari ,

Manish S Bhandare , Shailesh V Shrikhande

PII: S2666-2620(20)30017-6
DOI: https://doi.org/10.1016/j.sipas.2020.100019
Reference: SIPAS 100019

To appear in: Surgery in Practice and Science

Received date: 3 August 2020

Revised date: 28 September 2020
Accepted date: 29 September 2020

Please cite this article as: Rajesh S Shinde , Rajgopal Acharya , Vikram A Chaudhari ,
Manish S Bhandare , Shailesh V Shrikhande , Pancreaticojejunostomy For Pancreatico-enteric
Anastomosis After Pancreaticoduodenectomy: One Procedure With Multiple Techniques., Surgery in
Practice and Science (2020), doi: https://doi.org/10.1016/j.sipas.2020.100019

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 1

Review Article
Pancreaticojejunostomy For Pancreatico-enteric Anastomosis After
Pancreaticoduodenectomy: One Procedure With Multiple Techniques.
Rajesh S Shinde*, Rajgopal Acharya**, Vikram A Chaudhari***, Manish S Bhandare***,
Shailesh V Shrikhande***.
*
Gastrointestinal Cancer Surgery, Department of Surgical Oncology, Apollo hospitals, Navi
Mumbai, India.
**
Centre for liver and biliary sciences, Max Hospital, Saket, New Delhi, India.
***
Gastrointestinal Cancer Surgery, Department of Surgical Oncology, Tata Memorial
Hospital, Homi Bhabha National Institute, Mumbai, India.
Correspondence and reprints:

Rajesh S Shinde (MCh)

Consultant Surgical Oncologist,

Gastrointestinal Cancer Surgery,

Apollo Hospitals, Navi Mumbai,

Maharashtra, 400614, India.

Ph: +91 22 33503350

E-mail: dr.rajeshinde@gmail.com

Running Head: Pancreatico-jejunostomy for pancreatico-enteric anastomosis.

Conflict of interest: None

Commercial/financial disclosures: None

Word count (excluding abstract, references, tables and figures): 2834

Key words: Pancreatico-jejunostomy, Pancreatico-enteric anastomosis,

Pancreaticoduodenectomy.
 2

Abstract
Pancreatico-enteric anastomoses after Pancreatico-duodenectomy (PD) has remained a true

Achilles' heel in this complex and technically demanding operation. Multiple techniques have

been described to achieve safe pancreatico-enteric drainage, however postoperative

pancreatic fistula (POPF), still remains the major cause of morbidity. Pancreatico-

jejunostomy (PJ) is commonly performed procedure for this purpose, however there are lot of

variations in PJ techniques. Herein, we intend to review the commonly practised PJ

techniques with emphasis on technical variations and reported outcomes. Literature review

suggest that, there is no single, universally accepted or gold standard technique for this

purpose. Pancreatic surgeons should be aware of technical aspects of different techniques, so

that they can choose the best suited technique as per the clinical scenario.
 3

1. 1. Introduction

Pancreatico-enteric anastomoses after Pancreatico-duodenectomy (PD) has remained a true

Achilles' heel in this complex and technically demanding operation even though it was first

described more than 7 decades ago in 1941 by Child et al [1]. Since then, multiple techniques

have been described in an effort to make this procedure safe, however postoperative

pancreatic fistula (POPF) still remains the major cause of morbidity after PD. In current era,

pancreatico-jejunostomy (PJ) and pancreatico-gastrostomy (PG) are the most commonly

performed anastomotic procedures for this purpose and literature is inconclusive to suggest

which method is better than the other. PJ is practiced more frequently and more than 80

different techniques of this anastomosis have been described in literature [2], pointing out the

intricacies involved in this procedure. These techniques have many similarities but they also

differ considerably from each other in many aspects. Herein, we intend to review the

common PJ techniques with emphasis on technical variations and outcomes.

2. 2. Methods

Literature search in MEDLINE (www.pubmed.com) was performed with the key words

pancreatic anastomosis, pancreatico-enteric anastomosis, pancreaticojejunostomy. All the

relevant articles published in English and involving human subjects were scrutinized. Articles

describing or comparing the various techniques of PJ were included. Commonly used PJ

techniques in different parts of the world were described with emphasis on the finer

differences amongst these techniques [3-10]. In all of the described techniques, the jejunal

limb is brought to the supracolic compartment in a retro colic fashion.

3. 3. Results

Eight commonly practiced PJ techniques are described (Figure 1- 4). Existing literature does

not suggest any clear advantage of one technique over the other, particularly in respect to

postoperative pancreatic fistula (POPF). There was no clear definition of POPF prior to 2005,
 4

and each author had their own interpretation of pancreatic leak. However, after

standardization of pancreatic fistula definition in 2005, the POPF rates have largely been

constant with each technique and across various techniques as well. One important factor in

this consistency is the surgeon's expertise with the technique, which has been proved beyond

doubt as a significant factor deciding POPF. It seems that, each technique described in this

review has its own advantages and when used in the appropriate scenario, is associated with

acceptable morbidity and POPF rates. Table 1 elaborates the various studies describing the

technical aspects of PJ and their outcomes [4, 6-8, 10-16]. Table 2 elaborates the salient

features of various studies comparing different techniques [17-22].

3.1) Blumgart Technique [3]

Outer layer is taken with interrupted, 4-8, through and through transpancreatic sutures using

Polyglactin (vicryl) suture. These sutures traverse the entire thickness of pancreas in a

downward fashion from anterior to posterior and then through the seromuscular layer of

jejunum along longitudinal axis, again returning back in pancreas from posterior to anterior

direction. These sutures include the pancreatic capsule both anteriorly and posteriorly.

Subsequent similar stitches are taken approximately 0.75 cm apart. The number of sutures

depends on the gland, but typically 4-8 such sutures are enough. Caution should be exercised

not to include the pancreatic duct in these stitches. Theses outer sutures are left untied, and

the needles should not be cut. A small enterotomy is then made in jejunum opposite the

pancreatic duct. Pancreatic duct - to- jejunal mucosa sutures are then placed using 5-0

Polydioxanone. These duct-to-mucosa sutures are placed following a clockwise orientation,

wherein 2 sutures each are placed at 12 O' clock and 6 O' clock position, and 1 suture each at

3 O' clock and 9 O' clock position. Use of pancreatic stents is on based on individual

preference. After all duct-to-mucosa sutures are placed, the pancreatic stump and the jejunum

are approximated and the duct-to-mucosa sutures are sequentially tied. Then, outer layer

Vicryl suture is used to take a bite of anterior jejunal seromuscular layer and then tied in such
 5

a manner that pancreas and jejunum are approximated but not too tight to cause ischemia of

gland. This imbricates the anterior seromuscular jejunum over the pancreas. When performed

correctly, the seromuscular edge of jejunum should roll over onto the pancreatic surface, both

anteriorly and posteriorly (Figure 1).

3.2. Modified Blumgart Technique [4]

In principle, this technique is similar to original Blumgart’s technique, however it uses

double-armed 4-0 polypropylene suture (instead of Vicryl) for taking the U-shaped stitch and

only 3 transpancreatic sutures (instead of 4-8). The duct-to-mucosa anastomoses is completed

as in original Blumgart technique. Transpancreatic sutures are then tied to approximate the

pancreas and the jejunum at the ventral wall of the jejunum rather than on the surface of the

pancreas to avoid laceration of the pancreas. This method also completely covers pancreatic

stump with jejunal serosa because of the modified lateral suture through the seromuscular

layer of the jejunum (Figure 1).

3.3. Heidelberg Technique [5]

In this technique, anastomosis starts with placement of pancreatic ductal sutures with 4-0 or

5-0 Polydioxanone (PDS). First, the anterior ductal sutures are taken at 10, 12 and 2 O' clock

position in an outside-to-inside manner, traversing the entire thickness of pancreatic

parenchyma from anterior pancreatic surface till needle comes out from the anterior ductal

wall. Similarly, the posterior ductal sutures are taken at 4, 6 and 8 O' clock position in an

inside-to-outside fashion, going in through the posterior ductal wall and traversing the full

thickness of pancreatic parenchyma before coming out from the posterior pancreatic surface.

These sutures are not tied and are left with their needles intact. Next, the 4th or the posterior

most interrupted sutures are taken between posterior pancreatic parenchyma and

seromuscular layer of jejunum. After taking adequate number of sutures (usually 4-6), these

sutures are tied and the needles cut. An enterotomy is then made in the jejunum such that the

jejunal opening is a little smaller to the superoinferior extent of pancreatic stump. Now, 1 or 2
 6

interrupted sutures are taken between the posterior cut margin of pancreas and full-thickness

of posterior wall of jejunum. As we proceed, previously placed posterior ductal sutures are

incorporated in this layer by passing the needle outside-in into the posterior jejunal wall

completing the 3rd layer. In a similar manner, the anterior pancreatic cut surface is

anastomosed to the anterior jejunal wall, incorporating the anterior ductal sutures, completing

the 2nd layer. Finally, interrupted sutures are taken beginning from the anterior pancreatic

surface and into the seromuscular layer of jejunum. At the end, the completed anastomosis is

an end to side duct to mucosa anastomosis with an outer seromuscular and inner full

thickness layer (Figure 2).

3.4. Modified Heidelberg Technique [6]

In principle, this technique is similar to original Heidelberg technique with few

modifications. Anterior and posterior ductal sutures are similar to original Heidelberg

technique. Following modifications are made to the original Heidelberg technique. First,

posterior most or the 4th layer is taken with running suture between the posterior pancreatic

surface and the seromuscular layer of jejunum (instead of interrupted). Second, enterotomy is

smaller than the original technique (approximate 0.5 cm). Third, a stent is always placed in

the pancreatic duct such that 15 cm of it is within the jejunal limb and 5 cm is in the duct.

Finally, the two stay/hemostatic sutures taken over the superior and inferior border of

pancreas are also used as a seromuscular layer and tied (Figure 2).

3.5. Peng's Binding Technique [7]

This technique was conceptualised based on the hypothesis that needle holes on the

anastomotic surface (jejunum/pancreas) and the anastomotic seam between jejunum and

pancreas can be a potential site for pancreatic enzyme leak. Using this technique needle holes

do not appear on the anastomotic surface, and the anastomotic seam is sealed by compression

from outside. To achieve this, the end of jejunum is everted for about 3 cm length. This can

be done by suturing the cut edge of jejunum to a point 6 cm on the jejunum; two such sutures
 7

would be enough to achieve eversion. Thus 3 cm of jejunum is everted with its mucosa

exposed; this mucosa is then destroyed using either electrocoagulation or carbolic acid. In

case carbolic acid is used it should be rinsed using 75% alcohol and saline. The pancreatic

stump is isolated for about 3 cm length. The pancreatic stump is then sutured to the mucosa

of everted jejunum in a continuous or intermittent manner, taking care to include the anterior

and posterior lip of pancreatic duct in these sutures. Sutures should involve only the mucosa

of jejunum and not the muscular or serosal layers. The two sutures taken to evert the jejunum

are then cut so that jejunum takes its normal position and wraps the pancreatic stump. The cut

end of jejunum is then fixed to pancreas with few sutures. An absorbable tie is then looped

circumferentially at 1.5-2 cm from the cut edge of jejunum. The blood supply to the distal

end of jejunum is ensured by passing this tie through a hole at jejunal mesentery between last

two groups of vessels at jejunal end. This tie should just be tight enough to allow a

haemostatic artery forceps to pass beneath it. Watertight closure is tested by passing saline

through a tube inserted from intended hepaticojejunostomy site (Figure 3).

3.6. Pair-Watch Technique [8]

A pancreatic duct stent is always used for two purposes, partial drainage of pancreatic juice

and it also serves as a probe to identify pancreatic duct and prevent accidental suturing of

both its anterior and posterior lips. Pancreatic duct stent is passed into the jejunum through a

small opening of 2-3 mm. This pancreaticojejunostomy technique is performed imagining

two watches lying face-to-face to each other, the jejunal hole corresponding to the left side

watch and the pancreatic stump corresponding to the right-side watch. Imagine the watches as

a mirror image of each other, such that posterior wall of pancreatic stump comprises of 6 O'

clock to 12 O' clock, while posterior wall of jejunal opening comprises of 12 O' clock to 6 O'

clock. A 6-0 PDS suture is used to take a stitch between the centre of posterior wall of either

side, i.e. between 9 O' clock on pancreas side and 3 O' clock on jejunal side. The pancreatic

ductal stitch should include the pancreatic parenchyma up to the edge. The second stitch is
 8

then placed caudal to the first stitch, i.e between 8 O' clock on pancreas side and 4 O' clock

on jejunal side. Similarly, stitches are continued further caudally till 6 O' clock on either side.

Then further stitches are taken cranial to the first stitch, i.e. between 10 O' clock on pancreas

side and 2 O' clock on jejunal side, and further continued cranially till 12 O' clock on either

side. Thus, a total of 7 posterior stitches are taken. These stitches are left untied. Further 5

anterior stitches from 1 O' clock to 5 O' clock are taken on the pancreatic side in advance.

The jejunum is then carefully approximated to the pancreas and the seven posterior wall

stitches are tied. Anterior wall anastomosis is then done by passing the already taken

pancreatic side sutures to their corresponding site on jejunal side. The second layer of

anastomoses is then done between pancreatic capsule and jejunal serosa in intermittent

manner using Vicryl 4-0 (Figure 3).

3.7. Invagination/Dunking Technique [9]

Posterior outer row of sutures is placed first in a horizontal mattress fashion using interrupted

sutures. These sutures incorporate substantial bites of the posterior pancreatic capsule and

underlying parenchyma, as well as seromuscular bites of the jejunum. After placement of all

stitches (typically 5-6 in number) these are sequentially tied. A full thickness jejunotomy is

then created, typically extending from the penultimate superior silk suture to the penultimate

inferior silk suture. All posterior outer row stitches except the corner ones are then cut. Two

sutures are placed at the inferior-most aspect of the jejunal opening at essentially the same

spot. Posterior inner row of suturing is then done in a running and locking manner proceeding

inferior to superior, taking substantial bites of pancreatic parenchyma and capsule and full

thickness of jejunum. A pancreatic duct stent is then placed across the PD and into the jejunal

lumen. The anterior inner row is then completed by running the second suture from inferior to

superior along the anterior aspect of the pancreas, again taking substantial bites of pancreatic

parenchyma and capsule and full thickness of jejunum. This allows "invagination" or

"dunking" of the entire pancreatic cut surface into the jejunal lumen, thereby allowing
 9

apposition of the pancreatic capsule to the jejunal serosa. The anterior outer layer of sutures is

then placed in an interrupted manner between the jejunal seromuscular layer and the

pancreatic capsule (Figure 4).

3.9. Cattell Warren Technique [10]

The posterior row of interrupted sutures is taken between the seromuscular layer of jejunum

and the posterior border of pancreatic stump. A small hole is then created in the jejunum

opposite the pancreatic duct. Posterior wall of pancreatic duct is then sutured to the posterior

layer of jejunal mucosa using interrupted sutures. In similar manner, anterior wall of

pancreatic duct is then sutured to the anterior layer of jejunal mucosa. After duct to mucosa

anastomoses is completed, the anterior border of pancreatic stump is approximated to the

anterior seromuscular wall of jejunum using interrupted sutures (Figure 4).

Discussion

Establishing a pancreatico-enteric drainage following pancreaticoduodenectomy has long

been established, even though it is associated with the risk of development of POPF. POPF is

directly related to the increase in hospital stay, morbidity and mortality following

pancreaticoduodenectomy. There has always been a debate regarding the best pancreatico-

enteric anastomoses technique. Worldwide, PJ is the most preferred technique of establishing

pancreatico-enteric drainage [23]. Several modifications of PJ have been proposed and are

being followed in different parts of the world, all in a pursuit of perfection and aiming to

achieve a "zero percent" rate of POPF. There is no conclusive evidence in literature regarding

the superiority of one technique over the other [24]. However, few authors believe that duct

to mucosa pancreaticojejunostomy technique is preferable for fibrotic firm pancreas with

dilated ducts whereas end-to-end invagination is advisable in a soft pancreas with non-dilated

ducts [25]. No defined limit for pancreatic duct dilatation has been established and 3 mm is

the general cut-off. It is assumed that a soft pancreas has higher chance of leakage and duct

stenosis so it blemishes the main advantage of performing a duct to mucosa

 10

pancreaticojejunostomy. One factor which all pancreatic surgeons agree to is performing a

successful technique which is in accordance to sound surgical principles. These principles

(according to Halstead) include a water-tight and tension-free anastomosis, preservation of

adequate blood supply for both organs involved in the anastomosis, and minimal trauma to

the pancreas gland [26]. Since PJ leak rates are related to the individual surgeon's experience,

the preferred PJ technique should be feasible and easily reproducible. It is absolutely essential

that pancreatic surgeons familiarise themselves with the various fistula mitigating strategies

which is likely to prove useful when faced with a difficult to manage pancreatic stump

requiring reconstruction [27].

With the increasing use of minimally invasive (MIS) PD, reconstructive options for

pancreatico-enteric anastomosis have also been described with some modification from open

techniques. Most described PJ techniques have been used during MIS PD. Simpler techniques

involving less number of sutures or layers, use of continuous or barbed sutures are frequently

employed to overcome the difficulties faced in achieving / replicating the technical quality of

PJ which can be achieved while performing open PJ. Many high-volume centers have

published MIS PJ techniques and proposed their outcomes to be similar to open PD.

Blumgart’s techniques and its modification/s remain common PJ technique employed during

MIS PJ due to its simplicity [28-31].

Edil BH et al [29], have described a running barbed suture (V-Loc™; Covidien, Mansfield,

MA) to perform the PJ over a stent placed in the pancreatic duct and a small enterotomy in

the jejunum for a laparoscopic PD. Pastena et al [30], have described a modified Blumgart

end-to-side PJ with 4 large needles (3/0) barbed trans-pancreatic sutures and 4 to 6, duct-to-

mucosa sutures using 5/0 absorbable multifilament combined with a 12 cm, 6 or 8 Fr internal

stent for laparoscopic PJ. Liu et al [31], have described a single layer Robotic PJ technique

which involves trans pancreatic sutures and single layer continuous PJ over a pancreatic stent

and no duct to mucosa sutures. Robotic approach provides a relatively easier intra corporeal
 11

suturing as compared to laparoscopic PJ and therefore theoretically surgeons can imitate open

PJ techniques more comfortably while performing robotic PJ. [32].

Conclusion

There seems to be no difference in terms of the POPF rates amongst the various PJ

techniques, except in high-risk anastomoses where invagination technique has been debatably

shown to be superior. Adhering to the basic surgical principles of Halstead and performing a

safe and reproducible anastomoses appears the only way to achieve best outcomes. The

pancreatic surgeon should be wise enough and aware of the various surgical techniques

which can be appropriately applied in cases where high-risk anastomoses is anticipated.

 12

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Figure 1: Blumgart (A-F) and modified Blumgart (G-L) technique.

Figure 2: Heidelberg (A-F) and modified Heidelberg (G-L) technique.

Figure 3: Peng’s binding (A-D) and Pair watch (E-H) technique.

Figure 4: Invagination (A-F) and Cattell Warren (G-L) technique.

Table 1: Studies describing PJ techniques.

PJ technique Study Year No. of Overall POPF Overall
patie POPF grade B mortality
nts (%) or C (%) (%)

Blumgart Kleespies et al [12] 2009 92 - 4 3.26

Grobmyer et al 2010 187 20.3 6.9 1.6
[13] 2011 98 15.6 7.1 3.06
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Mishra et al [14]
Modified Blumgart Fuji et al [4] 2014 120 26 2.5 0
Heidelberg Buchler et al [15] 2000 331 2.1 - 0
Modified Heidelberg Torres et al [6] 2017 17 23.5 0 0
Peng's binding Peng et al [7] 2004 227 0 - 2.2
technique
Pair-watch technique Yoshinori et al [8] 2010 29 10 0 0
Invagination Lampe et al [11] 2015 104 1.9 1.9
technique
Cattell Warren Warren et al [10]
Bassi C et al [16] 2003 72 13 - 2

PJ- Pancreatico-jejunostomy, POPF- Postoperative pancreatic fistula.

Table 2: Studies comparing various PJ techniques.

Study Arms Author Type of Year Results p
study value
 18

Duct to Berger et al RCT 2009 Higher PF rate with duct-to- 0.04

mucosa v/s [17] mucosa technique
Invagination
Bai et al [18] RCT 2016 Similar overall POPF but higher 0.004
rate of clinically relevant POPF in
invagination group

Zhang et al Meta- 2017 No significant difference 0.13

[19] analysis
Cattell-Warren Lee et al [20] Before- 2018 No significant difference in POPF 0.11
v/s Blumgart after rates
Binding versus Peng et al [21] RCT 2007 POPF rate lower with binding 0.014
Invagination technique

Maggiori et al Case- 2010 No significant difference 0.33

[22] Control
PJ- Pancreatico-jejunostomy, POPF- Postoperative pancreatic fistula, RCT- Randomised control trial.
 19

Declaration of interests

☒ The authors declare that they have no known competing financial interests or personal
relationships that could have appeared to influence the work reported in this paper.

☐The authors declare the following financial interests/personal relationships which may be
considered as potential competing interests: