the effect of antecolic versus retrocolic reconstruction on delayed gastric emptying after classic...

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The effect of antecolic versus retrocolic reconstruction on delayed gastric emptying after classic non–pylorus-preserving pancreaticoduodenectomy Klaus Sahora, M.D., Vicente Morales-Oyarvide, M.D., Sarah P. Thayer, M.D., Ph.D., Christina R. Ferrone, M.D., Andrew L. Warshaw, M.D., Keith D. Lillemoe, M.D., Carlos Ferna ´ndez-del Castillo, M.D.* Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA KEYWORDS: Delayed gastric emptying; Pancreatico- duodenectomy; Antecolic; Retrocolic; Whipple resection; Reconstruction Abstract BACKGROUND: Delayed gastric emptying (DGE) after pancreaticoduodenectomy increases length of hospital stay and costs, and may be influenced by surgical techniques. METHODS: We retrospectively compared 400 patients with antecolic gastrojejunostomy with 400 patients with retrocolic gastrojejunostomy for the occurrence of DGE. RESULTS: The prevalence of DGE was 15% in the antecolic group and 21% in the retrocolic group (P 5 .021), and median length of stay was shorter for the former (8 vs 10 days, P 5 .001). The difference was statistically significant with grade A DGE (9% vs 14%, P 5 .038), but not B or C. In a multivariate anal- ysis, DGE was influenced by retrocolic reconstruction, as well as older age, chronic pancreatitis, preopera- tive bilirubin level, a history of previous upper abdominal surgery, and postoperative pancreatic fistula. CONCLUSIONS: An antecolic gastrojejunostomy for classic non–pylorus-preserving pancreatico- duodenectomy is associated with a lower incidence of mild DGE (grade A) and a shorter length of stay. Ó 2014 Elsevier Inc. All rights reserved. Within recent decades, pancreatic surgery has become safe in high-volume hospitals. A pancreaticoduodenectomy (PD), the standard procedure for pancreatic and periampul- lary tumors, should nowadays be performed with a periop- erative mortality below 3%. 1,2 Nevertheless, postoperative complications like pancreatic fistula, intra-abdominal abscess, hemorrhage, and delayed gastric emptying (DGE) are still seen in 20% to 45% of patients, with resul- tant longer length of stay and higher cost. 3 While DGE is generally not a threat to life and can be treated conserva- tively, interventions like the need for a central line or a percutaneous enteric feeding tube may be required to main- tain nutrition until oral alimentation is tolerated. Little is known about the pathophysiology of DGE. Some authors have reported that DGE is associated with other postoperative intra-abdominal complications such as hemorrhage, pancreatic fistula, and abdominal collec- tions. 3,4 Others have hypothesized that DGE may be caused * Corresponding author. Tel.: 11-617-726-5644; fax: 11-617-724- 3383. E-mail address: [email protected] Manuscript received January 27, 2014; revised manuscript April 12, 2014 0002-9610/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2014.04.015 The American Journal of Surgery (2014) -, --

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Page 1: The effect of antecolic versus retrocolic reconstruction on delayed gastric emptying after classic non–pylorus-preserving pancreaticoduodenectomy

The American Journal of Surgery (2014) -, -–-

The effect of antecolic versus retrocolicreconstruction on delayed gastric emptyingafter classic non–pylorus-preservingpancreaticoduodenectomy

Klaus Sahora, M.D., Vicente Morales-Oyarvide, M.D.,Sarah P. Thayer, M.D., Ph.D., Christina R. Ferrone, M.D.,Andrew L. Warshaw, M.D., Keith D. Lillemoe, M.D.,Carlos Fernandez-del Castillo, M.D.*

Department of Surgery, Massachusetts General Hospital, H

arvard Medical School, Boston, MA, USA

KEYWORDS:Delayed gastricemptying;Pancreatico-duodenectomy;Antecolic;Retrocolic;Whipple resection;Reconstruction

* Corresponding author. Tel.: 11-6

3383.

E-mail address: cfernandez@partner

Manuscript received January 27, 201

2014

0002-9610/$ - see front matter � 2014

http://dx.doi.org/10.1016/j.amjsurg.20

AbstractBACKGROUND: Delayed gastric emptying (DGE) after pancreaticoduodenectomy increases length

of hospital stay and costs, and may be influenced by surgical techniques.METHODS: We retrospectively compared 400 patients with antecolic gastrojejunostomy with 400

patients with retrocolic gastrojejunostomy for the occurrence of DGE.RESULTS: The prevalence of DGE was 15% in the antecolic group and 21% in the retrocolic group

(P 5 .021), and median length of stay was shorter for the former (8 vs 10 days, P 5 .001). The differencewas statistically significant with grade ADGE (9% vs 14%, P5 .038), but not B or C. In a multivariate anal-ysis, DGE was influenced by retrocolic reconstruction, as well as older age, chronic pancreatitis, preopera-tive bilirubin level, a history of previous upper abdominal surgery, and postoperative pancreatic fistula.

CONCLUSIONS: An antecolic gastrojejunostomy for classic non–pylorus-preserving pancreatico-duodenectomy is associated with a lower incidence of mild DGE (grade A) and a shorter length of stay.� 2014 Elsevier Inc. All rights reserved.

Within recent decades, pancreatic surgery has becomesafe in high-volume hospitals. A pancreaticoduodenectomy(PD), the standard procedure for pancreatic and periampul-lary tumors, should nowadays be performed with a periop-erative mortality below 3%.1,2 Nevertheless, postoperativecomplications like pancreatic fistula, intra-abdominal

17-726-5644; fax: 11-617-724-

s.org

4; revised manuscript April 12,

Elsevier Inc. All rights reserved.

14.04.015

abscess, hemorrhage, and delayed gastric emptying(DGE) are still seen in 20% to 45% of patients, with resul-tant longer length of stay and higher cost.3 While DGE isgenerally not a threat to life and can be treated conserva-tively, interventions like the need for a central line or apercutaneous enteric feeding tube may be required to main-tain nutrition until oral alimentation is tolerated.

Little is known about the pathophysiology of DGE.Some authors have reported that DGE is associated withother postoperative intra-abdominal complications such ashemorrhage, pancreatic fistula, and abdominal collec-tions.3,4 Others have hypothesized that DGE may be caused

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2 The American Journal of Surgery, Vol -, No -, - 2014

by postoperative local partial ischemia of the stomach,vagal dysfunction, the absence of motilin after duodenec-tomy, and/or pylorospasm related to devascularization ofthe pylorus after pylorus-preserving PD.5–7

Various surgical techniques, including the method ofreconstruction of the gastric outlet (antecolic vs retrocolic)and pylorus-preserving (with or without pylorus dilation)versus classic PD, have been compared.8–12 A recent meta-analysis showed a significant reduction of DGE after preop-erative biliary drainage (12% vs 17%) and for an antecolicgastrojejunostomy versus retrocolic reconstruction (10% vs22%).4 Nonetheless, the authors concluded that the evi-dence did not permit definite conclusions and that larger se-ries are needed.

This study was conducted to compare the impact of theroute of gastric drainage (antecolic vs retrocolic) on DGEafter classic pancreatoduodenectomy with antrectomy in alarge single-center series.

Patients and Methods

With the approval of the Institutional Review Board(IRBprotocol # 2012-P-000619/1), patients who underwenta classic PD with antrectomy at the Massachusetts GeneralHospital between 2000 and 2012 were identified from aprospective database. Patients were excluded if they hadprior history of gastric surgery or subtotal colectomy (n 513). In addition, patients were excluded if a step-by-step re-turn to a normal diet was not attempted because they werefasted and required parental nutrition to treat postoperativepancreatic fistula after surgery or if they required prolongedmechanical ventilation because of postoperative complica-tions (n 5 38), including 11 fatal complications. Afterexclusion of these patients, 400 consecutive patients withantecolic reconstruction were compared with 400 consecu-tive contemporaneous patients with retrocolic reconstruc-tion. All patients were operated upon by a team ofspecialized pancreatic surgeons. One surgeon (C.F.C.)routinely performed an antecolic reconstruction, whereasthe others (A.L.W., S.P.T., and J.W.) used a retrocolictechnique.

Patient demographic and clinicopathologic characteris-tics were recorded. Variables included sex, age at the timeof surgery, personal medical history, details on the surgicalprocedure and the postoperative course, and the finalpathologic findings.

Surgery

PD was performed with an antrectomy. If the tumorinfiltrated into the portal vein or superior mesenteric vein, asegmental or lateral resection of the vein was performed toachieve negative margins. In malignant diseases, a standardlymphadenectomy was routinely performed.

For reconstruction, the proximal jejunum was broughtthrough the transverse mesocolon by a retrocolic route. A

standardized 2-layer, end-to-side, duct-to-mucosa pancrea-ticojejunostomy was performed in the majority of cases(.95%) with an external transabdominal pancreatic stent.Distal to the pancreatic anastomosis an end-to-side hep-aticojejunostomy was made. The jejunal loop was thenfixed to the transverse mesocolon and an antecolic orretrocolic Hofmeister-type Billroth II gastrojejunostomywas performed. Soft closed-suction drains were placedanterior and posterior to the pancreatic and biliary anasto-mosis. A nasogastric tube was routinely placedintraoperatively.

Postoperative management

Both groups followed the same postoperative carepathway: The nasogastric tube was typically discontinuedon day 1 or 2 and clear liquids were given on day 2. Thediet was then step-by-step advanced to low-fat soft solids infrequent small portions as tolerated by the patient. In theevent sufficient oral intake was not possible by day 7 to 10,a gastrografin contrast upper gastrointestinal study wasusually performed to rule out mechanical obstruction. Incases of severe DGE, measures such as replacement of thenasogastric tube, prokinetic agents, and parenteral nutritionvia a central line were undertaken.

Drains were individually removed after day 3 if nopancreatic or biliary fistula was apparent. The pancreaticstent (a 5-F pediatric feeding tube) was removed in theoffice after 3 weeks.

Definition of DGE

DGE was diagnosed according to the definition pro-posed by the International Study Group of PancreaticSurgery.13 The grades were defined as follows: A: needfor nasogastric tube (NGT) intubation for 4 days or NGTreinsertion after postoperative day (POD) 3, or inabilityto tolerate a solid diet by POD 7; B: need for NGT intuba-tion for 8 days or NGT reinsertion after POD 7, or inabilityto tolerate a solid diet by POD 14; C: need for NGT intu-bation for 15 days or NGT reinsertion after POD 14, orinability to tolerate a solid diet by POD 21.

Definitions of other complications

Postoperative complications were classified according tothe validated classification system by Clavien grade.14

Grade I and II (minor) complications describe deviationsfrom a normal postoperative course that can be treatedconservatively. Grade III complications require interven-tions under local (IIIa) or general anesthesia (IIIb). GradeIV complications require intensive care unit managementbecause of single (IVa) or multiorgan failure (IVb). A gradeV complication was defined as death during the hospitalstay or within 30 days of surgery. Only the most severecomplication was accounted. Pancreatic fistula was defined

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K. Sahora et al. The impact of reconstruction on DGE 3

according to the International Study Group on Pancreaticfistula (ISGP) into grades A to C.15

Statistical analysis

A software packet (SPSS 18 software for Mac Os X;SPSS, Inc., Chicago, IL) was used for all analyses. Theprimary endpoint in this study was DGE incidence. Cate-gorical variables were compared using a chi-square test.Continuous variables are expressed by median and rangeand compared by the Mann–Whitney U test, or, if they hada normal distribution, using a 2-sample Student t test. Lo-gistic regressions were performed for multivariate analysis.P values of less than .05 were considered statisticallysignificant.

Results

The overall observed incidence of DGE in the 800analyzed patients was 18%. There was a significant differ-ence in the overall DGE rate between the antecolic (15%,n 5 59) and the retrocolic (21%, n 5 84) group (P 5 .021).The difference was significant for grade A DGE (antecolic9% vs retrocolic 14%; P 5 .038), which comprised 66%(95/143) of all DGE, but not for grades B and C (3% vs4% and 3% vs 2%, respectively). Details of the antecolicand retrocolic group regarding management of the nasogas-tric tube, tolerability of solid diet, episodes of emesis, andnausea are listed in Table 1.

Table 1 Surgery, complications, and hospital stay

Variable

Total (n 5 800) An

n % n

Operative time (minutes) 352 188–970 30Blood loss R 1,000 mL 186 23 87Vascular resection 46 6 19ICU stay 84 10 28LOS (days) 9 65.2 8Readmission 120 15 58Surgical complications (any grade) 225 28 10Clavien Class (RIII) 122 15 56Intra-abdominal abscess 64 8 28Pancreatic fistula (ISGPF B or C) 68 8.5 24DGE (ISGPS) any grade 143 18 59A 95 12 38B 28 3 11C 22 3 12

TPN 54 7 23NGT reinsert 69 9 48Emesis post-NGT 117 15 69Episode of nausea 141 18 72Tolerate solid diet (days after surgery) 6 4–49 6

Data are expressed as median (range) or mean 6 standard deviation.

DGE 5 delayed gastric emptying; ICU 5 intensive care unit; ISGPS 5 In

NGT 5 nasogastric tube; TPN 5 total parental nutrition.

There were no significant differences between the 2groups regarding sex (P 5 .203), age (P 5 .108), and thetype of pancreatic disease (malignant vs nonmalignant;P 5 .938). However, the following significant differencesbetween both groups were observed: preoperative use ofmorphine or its derivatives (antecolic 13% vs retrocolic7%; P 5 .006) and the number of patients undergoing neo-adjuvant therapy (antecolic 11% vs retrocolic7%; P 5 .043;Table 2).

The median operative time (antecolic 306 minutes vsretrocolic 396 minutes; P 5 .001) and mean postoperativelength of stay were significantly longer in the retrocolicgroup (antecolic 8 days vs retrocolic 10 days; P 5 .001).No differences were observed in the rate of major postop-erative complications (Clavien R 3), either in the overallrates of surgical or medical complications (Table 3). Therate of pancreatic fistulae (ISGPF grade B and C) washigher in the retrocolic group (11% vs 6%; P 5 .011).Two patients (1%) in the antecolic and 4 patients (1%)in the retrocolic group required re-laparotomy (P 5 .412).

Factors associated with DGE

Univariate and multivariate analysis demonstrated that59% of patients with DGE (84/143) had a retrocolicreconstruction, whereas 41% had had an antecolic one(P 5 .021; multivariate hazard ratio 1.496, 95% confi-dence interval 1.02 to 2.19). Additional significant factorswere age, preoperative elevated total bilirubin, a historyof pancreatitis, upper abdominal surgery or a second

tecolic (n 5 400) Retrocolic (n 5 400)

P value% n %

6 188–570 396 230–970 .00122 99 25 .3155 27 7 .2247 56 14 .00164.7 10 65.5 .00114 62 15 .692

6 26 119 30 .30714 66 16 .3257 36 9 .2976 44 11 .01114.8 84 21 .0219.5 57 14 .0382.8 17 4 .2483 10 2 .6656 31 8 .26012 21 5 .00117 48 12 .03618 68 17 .7814–49 7 5–32 .002

ternational Study Group of Pancreatic Surgery; LOS 5 length of stay;

Page 4: The effect of antecolic versus retrocolic reconstruction on delayed gastric emptying after classic non–pylorus-preserving pancreaticoduodenectomy

Table 2 Patient characteristics and preoperative variables

Variable

Total (n 5 800) Antecolic (n 5 400) Retrocolic (n 5 400)

P valueN % n % n %

Age (years) 65 21–92 64 21–91 67 26–92 .024SexMale 400 50 209 52 191 48 .203Female 400 50 191 47.8 209 52

BMI* 25 15–56 25 17–43 25 15–56 .635Smoking† 411 53 221 56 190 50 .105DiagnosisMalignancy 561 70 280 70 281 70 .938Chronic pancreatitis 69 9 31 7.8 38 9 .378Others 170 21 89 22 81 20 .489

Neoadjuvant therapy 68 8 42 10 26 6 .043History of second malignant tumor 113 14 52 13 61 15 .361Diabetes 153 19 86 21 67 17 .088Bilirubin R 1.8 mg/dL 131 16 57 14 74 18 .104Biliary stent 390 49 202 50 188 47 .322History of upper abdominal surgery 76 9 40 10 36 9 .630Prior morphine medication 77 10 50 12 27 7 .006

Data are expressed as median (range).

BMI 5 body mass index.

*BMI data available in 94% of patients.†Smoking history available in 97% of patients.

4 The American Journal of Surgery, Vol -, No -, - 2014

malignant tumor, and postoperative intra-abdominal ab-scess or pancreatic fistula (ISGPF grade B and C). A his-tory of pancreatitis, upper abdominal surgery or a secondmalignant tumor, and postoperative pancreatic fistula(ISGPF grade B and C) were significant in the multivariate

Table 3 Risk factors for the development of DGE of any grade

Variable

No DGE (n 5 657) DGE all grades

n % n %

Age (years) 63 612 68 6Sex (male) 325 49 75 5DiagnosisMalignancy 460 70 101 7Chronic pancreatitis 65 10 4 3Others 132 20 38 2

History ofsecond malignant tumor

83 13 30 2

Diabetes 123 19 30 2Bilirubin R 1.8 mg/dL 117 18 14 1History ofupper abdominal Surgery

55 8 21 1

Antecolic reconstruction 341 52 59 4Retrocolic reconstruction 316 48 84 5Operative time (minutes) 353 188–970 362 2Blood loss R 1,000 mL 149 23 37 2Vascular resection 39 6 7 5Intra-abdominal abscess 45 7 19 1Pancreaticfistula (ISGPF B or C)

43 6 25 1

Data are expressed as mean 6 standard deviation.

DGE 5 delayed gastric emptying; ISGPF 5 International Study Group of Pa

analysis (Table 3). After the exclusion of all patients withthese significant co-etiological factors (344/800; 43%), westill observed a significant difference between the ante-colic and retrocolic method of reconstruction (11% vs19%; P 5 .010).

(n 5 143) Univariate Multivariate

HR 95% CIP value P value

12 .001 .006 1.024 1.01–1.042 .518

1 .884.006 .032 .560 .33–.95

7 .0861 .009

1 .5340 .019 .012 .463 .25–.855 .020 .06 1.746 .98–3.12

1 .021 .038 1.496 1.02–2.19952–746 .5186 .412

.6283 .0107 .001 .005 2.65 1.35–5.22

ncreatic fistula.

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Table 4 Risk factors for the development of DGE grade B and C

Variable

No DGE grade B, C(n 5 657)

DGE grade B, C(n 5 50) Univariate Multivariate

HR 95% CIn % n % P value P value

Age (years) 64 612 67 612 .154Sex (male) 371 49 29 58 .243DiagnosisMalignancy 527 70 34 68 .735Chronic pancreatitis 68 9 1 2 .085Others 155 21 15 30 .118

History of secondmalignant tumor

103 14 10 20 .218

Diabetes 142 19 11 22 .593Bilirubin R 1.8 mg/dL 127 17 4 8 .098History of upperabdominal surgery

66 9 10 20 .009 .013 2.587 1.22–5.47

Retrocolic reconstruction 373 50 27 54 .559Operative time (minutes) 353 188–970 348 252–746 .884Blood loss R 1,000 mL 174 23 12 24 .897Vascular resection 43 6 3 6 .937Intra-abdominal abscess 54 7 10 20 .001 .035 2.786 1.08–7.21Pancreatic fistula (ISGPF B or C) 59 8 9 18 .013

Data are expressed as median (range) or mean 6 standard deviation.

CI 5 confidence interval; DGE 5 delayed gastric emptying; HR 5 hazard ratio; ISGPF 5 International Study Group of Pancreatic fistula.

K. Sahora et al. The impact of reconstruction on DGE 5

Analyzing DGE grade B and C only, a history of upperabdominal surgery, postoperative intra-abdominal abscess,or pancreatic fistula (ISGPF grade B and C) was significantby univariate analysis, and a history of upper abdominalsurgery and postoperative intra-abdominal abscess in themultivariate one (Table 4).

DGE and abdominal inflammatory complications

Overall, 22% (31/143) of patients with DGE had apostoperative abdominal inflammatory complication(pancreatic fistula and/or abdominal abscess). Of them,55% had DGE grade A, 29% grade B, and 16% grade C.Concurrent DGE and pancreatic fistula and/or abdominalabscess were observed in 17% of patients with DGE in theantecolic group compared with 25% in the retrocolic group(P 5 .25), and 34% of all patients with pancreatic fistulaand/or abdominal abscess had DGE. Analyzing exclusivelypatients without pancreatic fistula, the DGE rate was 14%after antecolic reconstruction and 19% after retrocolic(P 5 .049). Finally, after the additional exclusion of all pa-tients with major complications (Clavien R 3), the occur-rence of DGE was still significantly different between theantecolic and retrocolic group (7% vs 13%; P 5 .007).

Comments

Following the report of DGE in patients undergoingpylorus-preserving PD by Warshaw et al in 1985,16 severalstudies have focused on its possible cause and on surgical

as well as pharmacologic strategies to lower its incidence.Lower motilin levels, vagal disruption resulting in spasmof the pylorus, pancreatic leak, ischemic distress, and me-chanical factors, like torsion or angulation, have beendescribed as possible promoters of postoperative gastropa-resis, gastric stasis, and DGE.10,17–21 Pharmacologic agentssuch as erythromycin or metoclopramide have been used toenhance postoperative gastric motility with varying re-sults.7,17,22 In addition, several modifications of resectionand reconstruction methods have been described to lowerDGE incidence. Performing an antecolic gastrojejunostomyinstead of a retrocolic reconstruction is one of the mostcommonly advocated techniques to decrease the incidenceof DGE.4,10,23,24 The antecolic reconstruction has severaltheoretical advantages: less angulation, location of the gas-trojejunostomy further away from the pancreaticojejunos-tomy (which reduces the potential negative effect ofsmall pancreatic anastomotic leaks), and a more mobile je-junal loop. However, retrospective analysis as well as pro-spective randomized trials comparing antecolic versusclassic retrocolic reconstruction have provided controver-sial results, and the influence of the chosen route of recon-struction is still a matter of discussion.25–28

In this large retrospective single-center study, weconfirm that an antecolic gastrojejunostomy for classicPD with antrectomy is associated with a significantly lowerincidence of DGE (15% vs 21%; P 5 .021) and a shorterlength of stay (8 days vs 10 days; P 5 .001). Among all800 patients, we found that a retrocolic reconstruction,age, a history of pancreatitis, upper abdominal surgery ora second malignant tumor, and postoperative pancreatic

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6 The American Journal of Surgery, Vol -, No -, - 2014

fistula were independent risk factors of the occurrence ofany type of DGE. Severe DGE (grade B and C), in contrast,was only associated with a history of upper abdominal sur-gery and postoperative intra-abdominal abscess.

The positive effect of the antecolic gastrojejunostomywas only noticeable in lowering the incidence of mild DGE(grade A), defined as requirement of an NGT requiredbetween post operative day 4 and 7, or reinsertion of theNGT because of nausea and vomiting after removal byPOD 3 or the inability to tolerate a solid diet on POD 7.Paradoxically, episodes of emesis and reinsertion of theNGT were recorded more frequently in the antecolic arm,but a more detailed analysis shows that in 35% of patientsof the retrocolic group who required an NGT after POD 3,the NGT was never discontinued after surgery because ofhigh output compared with only 4% in the antecolic group.

As observed by others, DGE was clearly associated withthe occurrence of other postoperative complications in thisstudy. It has been suggested that gastroparesis as aconsequence of local inflammation may be the main causeof DGE in these cases.19,29,30 We elected to exclude fromthe study patients with severe complications in whom astep-by-step return to a normal diet was not attemptedbecause of a prolonged nil per os (NPO) status (eg, patientswith a grade C pancreatic fistula requiring nothing per osand parental nutrition or those with continuing mechanicalventilation). According to the International Study Group ofPancreatic Surgery definition of DGE, most of these pa-tients would falsely be classified as having DGE, and webelieve their exclusion enabled us to assess the true inci-dence of DGE. Other authors, who included such patientsby definition, described a DGE rate of 90% in patientswith prolonged intensive care unit stay.9 Among all patientsin our series with DGE, 23% had a pancreatic fistula(ISGPF grade B and C) or an abdominal collection. Eventhough we observed a higher rate of pancreatic fistula inthe retrocolic cohort, both pancreatic fistula and retrocolicreconstruction remained independent risk factors for DGEin multivariate analysis. Moreover, after exclusion of all pa-tients with major complications (Clavien R 3), pancreaticfistula or abdominal abscess, the occurrence of DGE wasstill significantly lower in the antecolic group.

The overall DGE rate in this study was low andcomparable with others reporting a DGE incidence rangingfrom 6% to 57%.16,31–33 As it is the institutional preference,all patients in this series underwent a classic PD with an-trectomy, which is positively reflected in the overall lowincidence of DGE compared with other series of pylorus-preserving PD.8,20,34 In a retrospective series, Nikfarjamet al report a DGE rate of 14% in patients with an antecolicreconstruction with a retrogastric omental patch comparedwith 40% DGE in the retrocolic group. Of note, however,most patients with retrocolic reconstruction in that seriesunderwent pylorus-preserving PD and were comparedwith a classic PD with antecolic reconstruction.35 TheDGE rate of 14% in the antecolic group undergoing aclassic antrectomy is identical to the DGE rate in this study,

while the DGE rates in the retrocolic group (21% vs 40%)were much higher, most likely because of pylorus preserva-tion. Hartel et al10 (not using the ISGPF-DGE definition)reported a DGE rate of 5% vs 24%, also favoring an ante-colic reconstruction. Similarly, Murakami et al36 observedonly 10% DGE rate after antecolic Roux-en-Y reconstruc-tion. A recent randomized controlled trial comparing theoccurrence of DGE between an antecolic Billroth II and ret-rocolic Billroth I reconstruction after PD with antrectomyand pancreaticogastrostomy found a lower prevalence inthe antecolic method.37 A reduction of the postoperativeDGE rate after an antecolic reconstruction was alsodescribed in a recently published meta-analysis.4,24 Incontrast, 2 prospective randomized controlled trails, con-ducted by Gangavatiker et al,28 who mainly performed aclassic pancreatoduodenectomy with antrectomy resection,and Imamura et al,38 who included only patients afterpylorus-preserving PD, did not find a correlation betweenthe method of reconstruction and the DGE incidence (ante-colic 34% vs retrocolic 28%; P 5 .06) and (antecolic 12%vs retrocolic 21%; P5 .31). Those results were confirmedby a currently published randomized controlled multicenterstudy of 246 patients, of whom most underwent a pylorus-preserving PD (antecolic 34% [n 5 121] vs retrocolic 36%[n 5 125]).11 Additional studies investigating gastricemptying by 13C-acetate breath test or paracetamol absorp-tion test were likewise unable to show a significant differ-ence between the antecolic and the retrocolic methods ofreconstruction.27,39

In addition to its retrospective nature, limitations of thisstudy include the potential bias from the fact that all theantecolic reconstructions were done by a single surgeon,and therefore the differences between antecolic and retro-colic gastrojejunostomy could be related to the surgeon’sexperience that is not accounted in the study. Nonetheless,the technique of performing the PD was identical in bothgroups, including standard lymphadenectomy and theplacement of a transabdominal external pancreatic drain,and we also show that the results remained significant evenafter the exclusion of a coincidental pancreatic leak, whichis a major potential confounder. On the other hand, the 800patients evaluated represent the largest cohort of exclu-sively non–pylorus-preserving PD patients addressing DGEas a function of the route of reconstruction. Because thepylorus-preserving operation seems to be inherently asso-ciated to a higher degree of gastric emptying, it becomes aconfounding factor when analyzing the type of reconstruc-tion, and having series that include both non–pylorus-preserving PD and pylorus preserving pancreatic duode-nectomy (PPPD) are therefore more difficult to analyze.

In conclusion, the results of this large series show that anantecolic gastrojejunostomy after classic non–pylorus-pre-serving PD is associated with an overall lower incidence ofDGE, and that this type of reconstruction is also associatedto a significantly shorter length of stay. This observation,together with several prior studies and meta-analyses thathave shown similar advantages of the gastrojejunal

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K. Sahora et al. The impact of reconstruction on DGE 7

antecolic anastomosis, suggests that this method of recon-struction should be the preferred one after a classic non–pylorus-preserving pancreatoduodenectomy.

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