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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; Pancreaticoduodenectomy; 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 analysis, DGE was influenced by retrocolic reconstruction, as well as older age, chronic pancreatitis, preoperative bilirubin level, a history of previous upper abdominal surgery, and postoperative pancreatic fistula. CONCLUSIONS: An antecolic gastrojejunostomy for classic non–pylorus-preserving pancreaticoduodenectomy 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 periampullary tumors, should nowadays be performed with a perioperative mortality below 3%.1,2 Nevertheless, postoperative complications like pancreatic fistula, intra-abdominal * Corresponding author. Tel.: 11-617-726-5644; fax: 11-617-7243383. 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
abscess, hemorrhage, and delayed gastric emptying (DGE) are still seen in 20% to 45% of patients, with resultant longer length of stay and higher cost.3 While DGE is generally not a threat to life and can be treated conservatively, interventions like the need for a central line or a percutaneous enteric feeding tube may be required to maintain 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 collections.3,4 Others have hypothesized that DGE may be caused
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by postoperative local partial ischemia of the stomach, vagal dysfunction, the absence of motilin after duodenectomy, and/or pylorospasm related to devascularization of the pylorus after pylorus-preserving PD.5–7 Various surgical techniques, including the method of reconstruction 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 metaanalysis showed a significant reduction of DGE after preoperative biliary drainage (12% vs 17%) and for an antecolic gastrojejunostomy versus retrocolic reconstruction (10% vs 22%).4 Nonetheless, the authors concluded that the evidence did not permit definite conclusions and that larger series are needed. This study was conducted to compare the impact of the route of gastric drainage (antecolic vs retrocolic) on DGE after classic pancreatoduodenectomy with antrectomy in a large single-center series.
standardized 2-layer, end-to-side, duct-to-mucosa pancreaticojejunostomy was performed in the majority of cases (.95%) with an external transabdominal pancreatic stent. Distal to the pancreatic anastomosis an end-to-side hepaticojejunostomy was made. The jejunal loop was then fixed to the transverse mesocolon and an antecolic or retrocolic Hofmeister-type Billroth II gastrojejunostomy was performed. Soft closed-suction drains were placed anterior and posterior to the pancreatic and biliary anastomosis. A nasogastric tube was routinely placed intraoperatively.
Patients and Methods With the approval of the Institutional Review Board (IRBprotocol # 2012-P-000619/1), patients who underwent a classic PD with antrectomy at the Massachusetts General Hospital between 2000 and 2012 were identified from a prospective database. Patients were excluded if they had prior history of gastric surgery or subtotal colectomy (n 5 13). In addition, patients were excluded if a step-by-step return to a normal diet was not attempted because they were fasted and required parental nutrition to treat postoperative pancreatic fistula after surgery or if they required prolonged mechanical ventilation because of postoperative complications (n 5 38), including 11 fatal complications. After exclusion of these patients, 400 consecutive patients with antecolic reconstruction were compared with 400 consecutive contemporaneous patients with retrocolic reconstruction. All patients were operated upon by a team of specialized pancreatic surgeons. One surgeon (C.F.C.) routinely performed an antecolic reconstruction, whereas the others (A.L.W., S.P.T., and J.W.) used a retrocolic technique. Patient demographic and clinicopathologic characteristics were recorded. Variables included sex, age at the time of surgery, personal medical history, details on the surgical procedure and the postoperative course, and the final pathologic findings.
Surgery PD was performed with an antrectomy. If the tumor infiltrated into the portal vein or superior mesenteric vein, a segmental or lateral resection of the vein was performed to achieve negative margins. In malignant diseases, a standard lymphadenectomy was routinely performed. For reconstruction, the proximal jejunum was brought through the transverse mesocolon by a retrocolic route. A
Postoperative management Both groups followed the same postoperative care pathway: The nasogastric tube was typically discontinued on day 1 or 2 and clear liquids were given on day 2. The diet was then step-by-step advanced to low-fat soft solids in frequent small portions as tolerated by the patient. In the event sufficient oral intake was not possible by day 7 to 10, a gastrografin contrast upper gastrointestinal study was usually performed to rule out mechanical obstruction. In cases of severe DGE, measures such as replacement of the nasogastric tube, prokinetic agents, and parenteral nutrition via a central line were undertaken. Drains were individually removed after day 3 if no pancreatic or biliary fistula was apparent. The pancreatic stent (a 5-F pediatric feeding tube) was removed in the office after 3 weeks.
Definition of DGE DGE was diagnosed according to the definition proposed by the International Study Group of Pancreatic Surgery.13 The grades were defined as follows: A: need for nasogastric tube (NGT) intubation for 4 days or NGT reinsertion after postoperative day (POD) 3, or inability to tolerate a solid diet by POD 7; B: need for NGT intubation for 8 days or NGT reinsertion after POD 7, or inability to tolerate a solid diet by POD 14; C: need for NGT intubation for 15 days or NGT reinsertion after POD 14, or inability to tolerate a solid diet by POD 21.
Definitions of other complications Postoperative complications were classified according to the validated classification system by Clavien grade.14 Grade I and II (minor) complications describe deviations from a normal postoperative course that can be treated conservatively. Grade III complications require interventions under local (IIIa) or general anesthesia (IIIb). Grade IV complications require intensive care unit management because of single (IVa) or multiorgan failure (IVb). A grade V complication was defined as death during the hospital stay or within 30 days of surgery. Only the most severe complication was accounted. Pancreatic fistula was defined
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The impact of reconstruction on DGE
3
according to the International Study Group on Pancreatic fistula (ISGP) into grades A to C.15
There were no significant differences between the 2 groups regarding sex (P 5 .203), age (P 5 .108), and the type of pancreatic disease (malignant vs nonmalignant; P 5 .938). However, the following significant differences between both groups were observed: preoperative use of morphine or its derivatives (antecolic 13% vs retrocolic 7%; P 5 .006) and the number of patients undergoing neoadjuvant therapy (antecolic 11% vs retrocolic7%; P 5 .043; Table 2). The median operative time (antecolic 306 minutes vs retrocolic 396 minutes; P 5 .001) and mean postoperative length of stay were significantly longer in the retrocolic group (antecolic 8 days vs retrocolic 10 days; P 5 .001). No differences were observed in the rate of major postoperative complications (Clavien R 3), either in the overall rates of surgical or medical complications (Table 3). The rate of pancreatic fistulae (ISGPF grade B and C) was higher 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).
Statistical analysis A software packet (SPSS 18 software for Mac Os X; SPSS, Inc., Chicago, IL) was used for all analyses. The primary endpoint in this study was DGE incidence. Categorical variables were compared using a chi-square test. Continuous variables are expressed by median and range and compared by the Mann–Whitney U test, or, if they had a normal distribution, using a 2-sample Student t test. Logistic regressions were performed for multivariate analysis. P values of less than .05 were considered statistically significant.
Results The overall observed incidence of DGE in the 800 analyzed patients was 18%. There was a significant difference 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 (antecolic 9% vs retrocolic 14%; P 5 .038), which comprised 66% (95/143) of all DGE, but not for grades B and C (3% vs 4% and 3% vs 2%, respectively). Details of the antecolic and retrocolic group regarding management of the nasogastric tube, tolerability of solid diet, episodes of emesis, and nausea are listed in Table 1.
Table 1
Factors associated with DGE Univariate and multivariate analysis demonstrated that 59% of patients with DGE (84/143) had a retrocolic reconstruction, whereas 41% had had an antecolic one (P 5 .021; multivariate hazard ratio 1.496, 95% confidence interval 1.02 to 2.19). Additional significant factors were age, preoperative elevated total bilirubin, a history of pancreatitis, upper abdominal surgery or a second
Surgery, complications, and hospital stay Total (n 5 800)
Antecolic (n 5 400)
Retrocolic (n 5 400)
Variable
n
%
n
%
n
%
P value
Operative time (minutes) Blood loss R 1,000 mL Vascular resection ICU stay LOS (days) Readmission Surgical complications (any grade) Clavien Class (RIII) Intra-abdominal abscess Pancreatic fistula (ISGPF B or C) DGE (ISGPS) any grade A B C TPN NGT reinsert Emesis post-NGT Episode of nausea Tolerate solid diet (days after surgery)
352 186 46 84 9 120 225 122 64 68 143 95 28 22 54 69 117 141 6
188–970 23 6 10 65.2 15 28 15 8 8.5 18 12 3 3 7 9 15 18 4–49
306 87 19 28 8 58 106 56 28 24 59 38 11 12 23 48 69 72 6
188–570 22 5 7 64.7 14 26 14 7 6 14.8 9.5 2.8 3 6 12 17 18 4–49
396 99 27 56 10 62 119 66 36 44 84 57 17 10 31 21 48 68 7
230–970 25 7 14 65.5 15 30 16 9 11 21 14 4 2 8 5 12 17 5–32
.001 .315 .224 .001 .001 .692 .307 .325 .297 .011 .021 .038 .248 .665 .260 .001 .036 .781 .002
Data are expressed as median (range) or mean 6 standard deviation. DGE 5 delayed gastric emptying; ICU 5 intensive care unit; ISGPS 5 International Study Group of Pancreatic Surgery; LOS 5 length of stay; NGT 5 nasogastric tube; TPN 5 total parental nutrition.
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4 Table 2
Patient characteristics and preoperative variables Total (n 5 800)
Antecolic (n 5 400)
Retrocolic (n 5 400)
Variable
N
%
n
%
n
%
P value
Age (years) Sex Male Female BMI* Smoking† Diagnosis Malignancy Chronic pancreatitis Others Neoadjuvant therapy History of second malignant tumor Diabetes Bilirubin R 1.8 mg/dL Biliary stent History of upper abdominal surgery Prior morphine medication
65
21–92
64
21–91
67
26–92
.024
400 400 25 411
50 50 15–56 53
209 191 25 221
52 47.8 17–43 56
191 209 25 190
48 52 15–56 50
.203
561 69 170 68 113 153 131 390 76 77
70 9 21 8 14 19 16 49 9 10
280 31 89 42 52 86 57 202 40 50
70 7.8 22 10 13 21 14 50 10 12
281 38 81 26 61 67 74 188 36 27
70 9 20 6 15 17 18 47 9 7
.938 .378 .489 .043 .361 .088 .104 .322 .630 .006
.635 .105
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.
malignant tumor, and postoperative intra-abdominal abscess or pancreatic fistula (ISGPF grade B and C). A history of pancreatitis, upper abdominal surgery or a second malignant tumor, and postoperative pancreatic fistula (ISGPF grade B and C) were significant in the multivariate
Table 3
analysis (Table 3). After the exclusion of all patients with these significant co-etiological factors (344/800; 43%), we still observed a significant difference between the antecolic and retrocolic method of reconstruction (11% vs 19%; P 5 .010).
Risk factors for the development of DGE of any grade No DGE (n 5 657)
DGE all grades (n 5 143)
Univariate
Multivariate
Variable
n
%
n
%
P value
P value
HR
95% CI
Age (years) Sex (male) Diagnosis Malignancy Chronic pancreatitis Others History of second malignant tumor Diabetes Bilirubin R 1.8 mg/dL History of upper abdominal Surgery Antecolic reconstruction Retrocolic reconstruction Operative time (minutes) Blood loss R 1,000 mL Vascular resection Intra-abdominal abscess Pancreatic fistula (ISGPF B or C)
63 325
612 49
68 75
612 52
.001 .518
.006
1.024
1.01–1.04
460 65 132 83
70 10 20 13
101 4 38 30
71 3 27 21
.884 .006 .086 .009
.032
.560
.33–.95
123 117 55
19 18 8
30 14 21
21 10 15
.534 .019 .020
.012 .06
.463 1.746
.25–.85 .98–3.12
341 316 353 149 39 45 43
52 48 188–970 23 6 7 6
59 84 362 37 7 19 25
41 59 252–746 26 5 13 17
.021
.038
1.496
1.02–2.19
.518 .412 .628 .010 .001
.005
2.65
1.35–5.22
Data are expressed as mean 6 standard deviation. DGE 5 delayed gastric emptying; ISGPF 5 International Study Group of Pancreatic fistula.
K. Sahora et al. Table 4
The impact of reconstruction on DGE
5
Risk factors for the development of DGE grade B and C No DGE grade B, C (n 5 657)
DGE grade B, C (n 5 50)
Univariate
Multivariate
Variable
n
%
n
%
P value
P value
HR
95% CI
Age (years) Sex (male) Diagnosis Malignancy Chronic pancreatitis Others History of second malignant tumor Diabetes Bilirubin R 1.8 mg/dL History of upper abdominal surgery Retrocolic reconstruction Operative time (minutes) Blood loss R 1,000 mL Vascular resection Intra-abdominal abscess Pancreatic fistula (ISGPF B or C)
64 371
612 49
67 29
612 58
.154 .243
527 68 155 103
70 9 21 14
34 1 15 10
68 2 30 20
.735 .085 .118 .218
142 127 66
19 17 9
11 4 10
22 8 20
.593 .098 .009
.013
2.587
1.22–5.47
373 353 174 43 54 59
50 188–970 23 6 7 8
27 348 12 3 10 9
54 252–746 24 6 20 18
.559 .884 .897 .937 .001 .013
.035
2.786
1.08–7.21
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.
Analyzing DGE grade B and C only, a history of upper abdominal surgery, postoperative intra-abdominal abscess, or pancreatic fistula (ISGPF grade B and C) was significant by univariate analysis, and a history of upper abdominal surgery and postoperative intra-abdominal abscess in the multivariate one (Table 4).
DGE and abdominal inflammatory complications Overall, 22% (31/143) of patients with DGE had a postoperative 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 abdominal abscess were observed in 17% of patients with DGE in the antecolic group compared with 25% in the retrocolic group (P 5 .25), and 34% of all patients with pancreatic fistula and/or abdominal abscess had DGE. Analyzing exclusively patients 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 patients with major complications (Clavien R 3), the occurrence of DGE was still significantly different between the antecolic and retrocolic group (7% vs 13%; P 5 .007).
Comments Following the report of DGE in patients undergoing pylorus-preserving PD by Warshaw et al in 1985,16 several studies 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 spasm of the pylorus, pancreatic leak, ischemic distress, and mechanical factors, like torsion or angulation, have been described as possible promoters of postoperative gastroparesis, gastric stasis, and DGE.10,17–21 Pharmacologic agents such as erythromycin or metoclopramide have been used to enhance postoperative gastric motility with varying results.7,17,22 In addition, several modifications of resection and reconstruction methods have been described to lower DGE incidence. Performing an antecolic gastrojejunostomy instead of a retrocolic reconstruction is one of the most commonly advocated techniques to decrease the incidence of DGE.4,10,23,24 The antecolic reconstruction has several theoretical advantages: less angulation, location of the gastrojejunostomy further away from the pancreaticojejunostomy (which reduces the potential negative effect of small pancreatic anastomotic leaks), and a more mobile jejunal loop. However, retrospective analysis as well as prospective randomized trials comparing antecolic versus classic retrocolic reconstruction have provided controversial results, and the influence of the chosen route of reconstruction is still a matter of discussion.25–28 In this large retrospective single-center study, we confirm that an antecolic gastrojejunostomy for classic PD with antrectomy is associated with a significantly lower incidence of DGE (15% vs 21%; P 5 .021) and a shorter length of stay (8 days vs 10 days; P 5 .001). Among all 800 patients, we found that a retrocolic reconstruction, age, a history of pancreatitis, upper abdominal surgery or a second malignant tumor, and postoperative pancreatic
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fistula were independent risk factors of the occurrence of any type of DGE. Severe DGE (grade B and C), in contrast, was only associated with a history of upper abdominal surgery and postoperative intra-abdominal abscess. The positive effect of the antecolic gastrojejunostomy was only noticeable in lowering the incidence of mild DGE (grade A), defined as requirement of an NGT required between post operative day 4 and 7, or reinsertion of the NGT because of nausea and vomiting after removal by POD 3 or the inability to tolerate a solid diet on POD 7. Paradoxically, episodes of emesis and reinsertion of the NGT were recorded more frequently in the antecolic arm, but a more detailed analysis shows that in 35% of patients of the retrocolic group who required an NGT after POD 3, the NGT was never discontinued after surgery because of high output compared with only 4% in the antecolic group. As observed by others, DGE was clearly associated with the occurrence of other postoperative complications in this study. It has been suggested that gastroparesis as a consequence of local inflammation may be the main cause of DGE in these cases.19,29,30 We elected to exclude from the study patients with severe complications in whom a step-by-step return to a normal diet was not attempted because of a prolonged nil per os (NPO) status (eg, patients with a grade C pancreatic fistula requiring nothing per os and parental nutrition or those with continuing mechanical ventilation). According to the International Study Group of Pancreatic Surgery definition of DGE, most of these patients would falsely be classified as having DGE, and we believe their exclusion enabled us to assess the true incidence of DGE. Other authors, who included such patients by definition, described a DGE rate of 90% in patients with prolonged intensive care unit stay.9 Among all patients in our series with DGE, 23% had a pancreatic fistula (ISGPF grade B and C) or an abdominal collection. Even though we observed a higher rate of pancreatic fistula in the retrocolic cohort, both pancreatic fistula and retrocolic reconstruction remained independent risk factors for DGE in multivariate analysis. Moreover, after exclusion of all patients with major complications (Clavien R 3), pancreatic fistula or abdominal abscess, the occurrence of DGE was still significantly lower in the antecolic group. The overall DGE rate in this study was low and comparable with others reporting a DGE incidence ranging from 6% to 57%.16,31–33 As it is the institutional preference, all patients in this series underwent a classic PD with antrectomy, which is positively reflected in the overall low incidence of DGE compared with other series of pyloruspreserving PD.8,20,34 In a retrospective series, Nikfarjam et al report a DGE rate of 14% in patients with an antecolic reconstruction with a retrogastric omental patch compared with 40% DGE in the retrocolic group. Of note, however, most patients with retrocolic reconstruction in that series underwent pylorus-preserving PD and were compared with a classic PD with antecolic reconstruction.35 The DGE rate of 14% in the antecolic group undergoing a classic 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 preservation. Hartel et al10 (not using the ISGPF-DGE definition) reported a DGE rate of 5% vs 24%, also favoring an antecolic reconstruction. Similarly, Murakami et al36 observed only 10% DGE rate after antecolic Roux-en-Y reconstruction. A recent randomized controlled trial comparing the occurrence of DGE between an antecolic Billroth II and retrocolic Billroth I reconstruction after PD with antrectomy and pancreaticogastrostomy found a lower prevalence in the antecolic method.37 A reduction of the postoperative DGE rate after an antecolic reconstruction was also described in a recently published meta-analysis.4,24 In contrast, 2 prospective randomized controlled trails, conducted by Gangavatiker et al,28 who mainly performed a classic pancreatoduodenectomy with antrectomy resection, and Imamura et al,38 who included only patients after pylorus-preserving PD, did not find a correlation between the method of reconstruction and the DGE incidence (antecolic 34% vs retrocolic 28%; P 5 .06) and (antecolic 12% vs retrocolic 21%; P5 .31). Those results were confirmed by a currently published randomized controlled multicenter study of 246 patients, of whom most underwent a pyloruspreserving PD (antecolic 34% [n 5 121] vs retrocolic 36% [n 5 125]).11 Additional studies investigating gastric emptying by 13C-acetate breath test or paracetamol absorption test were likewise unable to show a significant difference between the antecolic and the retrocolic methods of reconstruction.27,39 In addition to its retrospective nature, limitations of this study include the potential bias from the fact that all the antecolic reconstructions were done by a single surgeon, and therefore the differences between antecolic and retrocolic gastrojejunostomy could be related to the surgeon’s experience that is not accounted in the study. Nonetheless, the technique of performing the PD was identical in both groups, including standard lymphadenectomy and the placement of a transabdominal external pancreatic drain, and we also show that the results remained significant even after the exclusion of a coincidental pancreatic leak, which is a major potential confounder. On the other hand, the 800 patients evaluated represent the largest cohort of exclusively non–pylorus-preserving PD patients addressing DGE as a function of the route of reconstruction. Because the pylorus-preserving operation seems to be inherently associated to a higher degree of gastric emptying, it becomes a confounding factor when analyzing the type of reconstruction, and having series that include both non–pyloruspreserving PD and pylorus preserving pancreatic duodenectomy (PPPD) are therefore more difficult to analyze. In conclusion, the results of this large series show that an antecolic gastrojejunostomy after classic non–pylorus-preserving PD is associated with an overall lower incidence of DGE, and that this type of reconstruction is also associated to a significantly shorter length of stay. This observation, together with several prior studies and meta-analyses that have shown similar advantages of the gastrojejunal
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antecolic anastomosis, suggests that this method of reconstruction should be the preferred one after a classic non– pylorus-preserving pancreatoduodenectomy.
7
18. 19.
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35.
36.
placebo-controlled trial. Ann Surg 1993;218:229–37; discussion 237–8. Tanaka M, Sarr MG. Role of the duodenum in the control of canine gastrointestinal motility. Gastroenterology 1988;94:622–9. Park YC, Kim SW, Jang JY, et al. Factors influencing delayed gastric emptying after pylorus-preserving pancreatoduodenectomy. J Am Coll Surg 2003;196:859–65. Kim DK, Hindenburg AA, Sharma SK, et al. Is pylorospasm a cause of delayed gastric emptying after pylorus-preserving pancreaticoduodenectomy? Ann Surg Oncol 2005;12:222–7. Kurosaki I, Hatakeyama K. Clinical and surgical factors influencing delayed gastric emptying after pyloric-preserving pancreaticoduodenectomy. Hepatogastroenterology 2005;52:143–8. Nguyen NQ, Chapman MJ, Fraser RJ, et al. Erythromycin is more effective than metoclopramide in the treatment of feed intolerance in critical illness. Crit Care Med 2007;35:483–9. Nikfarjam M, Houli N, Tufail F, et al. Reduction in delayed gastric emptying following non-pylorus preserving pancreaticoduodenectomy by addition of a Braun enteroenterostomy. JOP 2012;13:488–96. Su AP, Cao SS, Zhang Y, et al. Does antecolic reconstruction for duodenojejunostomy improve delayed gastric emptying after pyloruspreserving pancreaticoduodenectomy? A systematic review and meta-analysis. World J Gastroenterol 2012;18:6315–23. Oida T, Mimatsu K, Kano H, et al. Antecolic and retrocolic route on delayed gastric emptying after MSSPPD. Hepatogastroenterology 2012;59:1274–6. Chijiiwa K, Ohuchida J, Hiyoshi M, et al. Vertical retrocolic duodenojejunostomy decreases delayed gastric emptying after pyloruspreserving pancreatoduodenectomy. Hepatogastroenterology 2007; 54:1874–7. Chijiiwa K, Imamura N, Ohuchida J, et al. Prospective randomized controlled study of gastric emptying assessed by (13)C-acetate breath test after pylorus-preserving pancreaticoduodenectomy: comparison between antecolic and vertical retrocolic duodenojejunostomy. J Hepatobiliary Pancreat Surg 2009;16:49–55. Gangavatiker R, Pal S, Javed A, et al. Effect of antecolic or retrocolic reconstruction of the gastro/duodenojejunostomy on delayed gastric emptying after pancreaticoduodenectomy: a randomized controlled trial. J Gastrointest Surg 2011;15:843–52. van Berge Henegouwen MI, van Gulik TM, DeWit LT, et al. Delayed gastric emptying after standard pancreaticoduodenectomy versus pylorus-preserving pancreaticoduodenectomy: an analysis of 200 consecutive patients. J Am Coll Surg 1997;185:373–9. Riediger H, Makowiec F, Schareck WD, et al. Delayed gastric emptying after pylorus-preserving pancreatoduodenectomy is strongly related to other postoperative complications. J Gastrointest Surg 2003; 7:758–65. Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997;226:248–57; discussion, 257–60. JH 4th Balcom, Rattner DW, Warshaw AL, et al. Ten-year experience with 733 pancreatic resections: changing indications, older patients, and decreasing length of hospitalization. Arch Surg 2001;136:391–8. Park JS, Hwang HK, Kim JK, et al. Clinical validation and risk factors for delayed gastric emptying based on the International Study Group of Pancreatic Surgery (ISGPS) Classification. Surgery 2009;146: 882–7. Kawai M, Tani M, Hirono S, et al. Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: a prospective, randomized, controlled trial of pylorusresecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg 2011;253:495–501. Nikfarjam M, Kimchi ET, Gusani NJ, et al. A reduction in delayed gastric emptying by classic pancreaticoduodenectomy with an antecolic gastrojejunal anastomosis and a retrogastric omental patch. J Gastrointest Surg 2009;13:1674–82. Murakami H, Suzuki H, Nakamura T. Pancreatic fibrosis correlates with delayed gastric emptying after pylorus-preserving
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pancreaticoduodenectomy with pancreaticogastrostomy. Ann Surg 2002;235:240–5. 37. Kurahara H, Shinchi H, Maemura K, et al. Delayed gastric emptying after pancreatoduodenectomy. J Surg Res 2011;171: e187–92. 38. Imamura N, Chijiiwa K, Ohuchida J, et al. Prospective randomized clinical trial of a change in gastric emptying and nutritional status after
a pylorus-preserving pancreaticoduodenectomy: comparison between an antecolic and a vertical retrocolic duodenojejunostomy. HPB (Oxford) 2014;16:384–94. 39. Tamandl D, Sahora K, Prucker J, et al. Impact of the reconstruction method on delayed gastric emptying after pylorus-preserving pancreaticoduodenectomy: a prospective randomized study. World J Surg 2014;38:465–75.
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; Pancreaticoduodenectomy; 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 analysis, DGE was influenced by retrocolic reconstruction, as well as older age, chronic pancreatitis, preoperative bilirubin level, a history of previous upper abdominal surgery, and postoperative pancreatic fistula. CONCLUSIONS: An antecolic gastrojejunostomy for classic non–pylorus-preserving pancreaticoduodenectomy 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 periampullary tumors, should nowadays be performed with a perioperative mortality below 3%.1,2 Nevertheless, postoperative complications like pancreatic fistula, intra-abdominal * Corresponding author. Tel.: 11-617-726-5644; fax: 11-617-7243383. 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
abscess, hemorrhage, and delayed gastric emptying (DGE) are still seen in 20% to 45% of patients, with resultant longer length of stay and higher cost.3 While DGE is generally not a threat to life and can be treated conservatively, interventions like the need for a central line or a percutaneous enteric feeding tube may be required to maintain 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 collections.3,4 Others have hypothesized that DGE may be caused
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by postoperative local partial ischemia of the stomach, vagal dysfunction, the absence of motilin after duodenectomy, and/or pylorospasm related to devascularization of the pylorus after pylorus-preserving PD.5–7 Various surgical techniques, including the method of reconstruction 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 metaanalysis showed a significant reduction of DGE after preoperative biliary drainage (12% vs 17%) and for an antecolic gastrojejunostomy versus retrocolic reconstruction (10% vs 22%).4 Nonetheless, the authors concluded that the evidence did not permit definite conclusions and that larger series are needed. This study was conducted to compare the impact of the route of gastric drainage (antecolic vs retrocolic) on DGE after classic pancreatoduodenectomy with antrectomy in a large single-center series.
standardized 2-layer, end-to-side, duct-to-mucosa pancreaticojejunostomy was performed in the majority of cases (.95%) with an external transabdominal pancreatic stent. Distal to the pancreatic anastomosis an end-to-side hepaticojejunostomy was made. The jejunal loop was then fixed to the transverse mesocolon and an antecolic or retrocolic Hofmeister-type Billroth II gastrojejunostomy was performed. Soft closed-suction drains were placed anterior and posterior to the pancreatic and biliary anastomosis. A nasogastric tube was routinely placed intraoperatively.
Patients and Methods With the approval of the Institutional Review Board (IRBprotocol # 2012-P-000619/1), patients who underwent a classic PD with antrectomy at the Massachusetts General Hospital between 2000 and 2012 were identified from a prospective database. Patients were excluded if they had prior history of gastric surgery or subtotal colectomy (n 5 13). In addition, patients were excluded if a step-by-step return to a normal diet was not attempted because they were fasted and required parental nutrition to treat postoperative pancreatic fistula after surgery or if they required prolonged mechanical ventilation because of postoperative complications (n 5 38), including 11 fatal complications. After exclusion of these patients, 400 consecutive patients with antecolic reconstruction were compared with 400 consecutive contemporaneous patients with retrocolic reconstruction. All patients were operated upon by a team of specialized pancreatic surgeons. One surgeon (C.F.C.) routinely performed an antecolic reconstruction, whereas the others (A.L.W., S.P.T., and J.W.) used a retrocolic technique. Patient demographic and clinicopathologic characteristics were recorded. Variables included sex, age at the time of surgery, personal medical history, details on the surgical procedure and the postoperative course, and the final pathologic findings.
Surgery PD was performed with an antrectomy. If the tumor infiltrated into the portal vein or superior mesenteric vein, a segmental or lateral resection of the vein was performed to achieve negative margins. In malignant diseases, a standard lymphadenectomy was routinely performed. For reconstruction, the proximal jejunum was brought through the transverse mesocolon by a retrocolic route. A
Postoperative management Both groups followed the same postoperative care pathway: The nasogastric tube was typically discontinued on day 1 or 2 and clear liquids were given on day 2. The diet was then step-by-step advanced to low-fat soft solids in frequent small portions as tolerated by the patient. In the event sufficient oral intake was not possible by day 7 to 10, a gastrografin contrast upper gastrointestinal study was usually performed to rule out mechanical obstruction. In cases of severe DGE, measures such as replacement of the nasogastric tube, prokinetic agents, and parenteral nutrition via a central line were undertaken. Drains were individually removed after day 3 if no pancreatic or biliary fistula was apparent. The pancreatic stent (a 5-F pediatric feeding tube) was removed in the office after 3 weeks.
Definition of DGE DGE was diagnosed according to the definition proposed by the International Study Group of Pancreatic Surgery.13 The grades were defined as follows: A: need for nasogastric tube (NGT) intubation for 4 days or NGT reinsertion after postoperative day (POD) 3, or inability to tolerate a solid diet by POD 7; B: need for NGT intubation for 8 days or NGT reinsertion after POD 7, or inability to tolerate a solid diet by POD 14; C: need for NGT intubation for 15 days or NGT reinsertion after POD 14, or inability to tolerate a solid diet by POD 21.
Definitions of other complications Postoperative complications were classified according to the validated classification system by Clavien grade.14 Grade I and II (minor) complications describe deviations from a normal postoperative course that can be treated conservatively. Grade III complications require interventions under local (IIIa) or general anesthesia (IIIb). Grade IV complications require intensive care unit management because of single (IVa) or multiorgan failure (IVb). A grade V complication was defined as death during the hospital stay or within 30 days of surgery. Only the most severe complication was accounted. Pancreatic fistula was defined
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The impact of reconstruction on DGE
3
according to the International Study Group on Pancreatic fistula (ISGP) into grades A to C.15
There were no significant differences between the 2 groups regarding sex (P 5 .203), age (P 5 .108), and the type of pancreatic disease (malignant vs nonmalignant; P 5 .938). However, the following significant differences between both groups were observed: preoperative use of morphine or its derivatives (antecolic 13% vs retrocolic 7%; P 5 .006) and the number of patients undergoing neoadjuvant therapy (antecolic 11% vs retrocolic7%; P 5 .043; Table 2). The median operative time (antecolic 306 minutes vs retrocolic 396 minutes; P 5 .001) and mean postoperative length of stay were significantly longer in the retrocolic group (antecolic 8 days vs retrocolic 10 days; P 5 .001). No differences were observed in the rate of major postoperative complications (Clavien R 3), either in the overall rates of surgical or medical complications (Table 3). The rate of pancreatic fistulae (ISGPF grade B and C) was higher 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).
Statistical analysis A software packet (SPSS 18 software for Mac Os X; SPSS, Inc., Chicago, IL) was used for all analyses. The primary endpoint in this study was DGE incidence. Categorical variables were compared using a chi-square test. Continuous variables are expressed by median and range and compared by the Mann–Whitney U test, or, if they had a normal distribution, using a 2-sample Student t test. Logistic regressions were performed for multivariate analysis. P values of less than .05 were considered statistically significant.
Results The overall observed incidence of DGE in the 800 analyzed patients was 18%. There was a significant difference 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 (antecolic 9% vs retrocolic 14%; P 5 .038), which comprised 66% (95/143) of all DGE, but not for grades B and C (3% vs 4% and 3% vs 2%, respectively). Details of the antecolic and retrocolic group regarding management of the nasogastric tube, tolerability of solid diet, episodes of emesis, and nausea are listed in Table 1.
Table 1
Factors associated with DGE Univariate and multivariate analysis demonstrated that 59% of patients with DGE (84/143) had a retrocolic reconstruction, whereas 41% had had an antecolic one (P 5 .021; multivariate hazard ratio 1.496, 95% confidence interval 1.02 to 2.19). Additional significant factors were age, preoperative elevated total bilirubin, a history of pancreatitis, upper abdominal surgery or a second
Surgery, complications, and hospital stay Total (n 5 800)
Antecolic (n 5 400)
Retrocolic (n 5 400)
Variable
n
%
n
%
n
%
P value
Operative time (minutes) Blood loss R 1,000 mL Vascular resection ICU stay LOS (days) Readmission Surgical complications (any grade) Clavien Class (RIII) Intra-abdominal abscess Pancreatic fistula (ISGPF B or C) DGE (ISGPS) any grade A B C TPN NGT reinsert Emesis post-NGT Episode of nausea Tolerate solid diet (days after surgery)
352 186 46 84 9 120 225 122 64 68 143 95 28 22 54 69 117 141 6
188–970 23 6 10 65.2 15 28 15 8 8.5 18 12 3 3 7 9 15 18 4–49
306 87 19 28 8 58 106 56 28 24 59 38 11 12 23 48 69 72 6
188–570 22 5 7 64.7 14 26 14 7 6 14.8 9.5 2.8 3 6 12 17 18 4–49
396 99 27 56 10 62 119 66 36 44 84 57 17 10 31 21 48 68 7
230–970 25 7 14 65.5 15 30 16 9 11 21 14 4 2 8 5 12 17 5–32
.001 .315 .224 .001 .001 .692 .307 .325 .297 .011 .021 .038 .248 .665 .260 .001 .036 .781 .002
Data are expressed as median (range) or mean 6 standard deviation. DGE 5 delayed gastric emptying; ICU 5 intensive care unit; ISGPS 5 International Study Group of Pancreatic Surgery; LOS 5 length of stay; NGT 5 nasogastric tube; TPN 5 total parental nutrition.
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4 Table 2
Patient characteristics and preoperative variables Total (n 5 800)
Antecolic (n 5 400)
Retrocolic (n 5 400)
Variable
N
%
n
%
n
%
P value
Age (years) Sex Male Female BMI* Smoking† Diagnosis Malignancy Chronic pancreatitis Others Neoadjuvant therapy History of second malignant tumor Diabetes Bilirubin R 1.8 mg/dL Biliary stent History of upper abdominal surgery Prior morphine medication
65
21–92
64
21–91
67
26–92
.024
400 400 25 411
50 50 15–56 53
209 191 25 221
52 47.8 17–43 56
191 209 25 190
48 52 15–56 50
.203
561 69 170 68 113 153 131 390 76 77
70 9 21 8 14 19 16 49 9 10
280 31 89 42 52 86 57 202 40 50
70 7.8 22 10 13 21 14 50 10 12
281 38 81 26 61 67 74 188 36 27
70 9 20 6 15 17 18 47 9 7
.938 .378 .489 .043 .361 .088 .104 .322 .630 .006
.635 .105
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.
malignant tumor, and postoperative intra-abdominal abscess or pancreatic fistula (ISGPF grade B and C). A history of pancreatitis, upper abdominal surgery or a second malignant tumor, and postoperative pancreatic fistula (ISGPF grade B and C) were significant in the multivariate
Table 3
analysis (Table 3). After the exclusion of all patients with these significant co-etiological factors (344/800; 43%), we still observed a significant difference between the antecolic and retrocolic method of reconstruction (11% vs 19%; P 5 .010).
Risk factors for the development of DGE of any grade No DGE (n 5 657)
DGE all grades (n 5 143)
Univariate
Multivariate
Variable
n
%
n
%
P value
P value
HR
95% CI
Age (years) Sex (male) Diagnosis Malignancy Chronic pancreatitis Others History of second malignant tumor Diabetes Bilirubin R 1.8 mg/dL History of upper abdominal Surgery Antecolic reconstruction Retrocolic reconstruction Operative time (minutes) Blood loss R 1,000 mL Vascular resection Intra-abdominal abscess Pancreatic fistula (ISGPF B or C)
63 325
612 49
68 75
612 52
.001 .518
.006
1.024
1.01–1.04
460 65 132 83
70 10 20 13
101 4 38 30
71 3 27 21
.884 .006 .086 .009
.032
.560
.33–.95
123 117 55
19 18 8
30 14 21
21 10 15
.534 .019 .020
.012 .06
.463 1.746
.25–.85 .98–3.12
341 316 353 149 39 45 43
52 48 188–970 23 6 7 6
59 84 362 37 7 19 25
41 59 252–746 26 5 13 17
.021
.038
1.496
1.02–2.19
.518 .412 .628 .010 .001
.005
2.65
1.35–5.22
Data are expressed as mean 6 standard deviation. DGE 5 delayed gastric emptying; ISGPF 5 International Study Group of Pancreatic fistula.
K. Sahora et al. Table 4
The impact of reconstruction on DGE
5
Risk factors for the development of DGE grade B and C No DGE grade B, C (n 5 657)
DGE grade B, C (n 5 50)
Univariate
Multivariate
Variable
n
%
n
%
P value
P value
HR
95% CI
Age (years) Sex (male) Diagnosis Malignancy Chronic pancreatitis Others History of second malignant tumor Diabetes Bilirubin R 1.8 mg/dL History of upper abdominal surgery Retrocolic reconstruction Operative time (minutes) Blood loss R 1,000 mL Vascular resection Intra-abdominal abscess Pancreatic fistula (ISGPF B or C)
64 371
612 49
67 29
612 58
.154 .243
527 68 155 103
70 9 21 14
34 1 15 10
68 2 30 20
.735 .085 .118 .218
142 127 66
19 17 9
11 4 10
22 8 20
.593 .098 .009
.013
2.587
1.22–5.47
373 353 174 43 54 59
50 188–970 23 6 7 8
27 348 12 3 10 9
54 252–746 24 6 20 18
.559 .884 .897 .937 .001 .013
.035
2.786
1.08–7.21
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.
Analyzing DGE grade B and C only, a history of upper abdominal surgery, postoperative intra-abdominal abscess, or pancreatic fistula (ISGPF grade B and C) was significant by univariate analysis, and a history of upper abdominal surgery and postoperative intra-abdominal abscess in the multivariate one (Table 4).
DGE and abdominal inflammatory complications Overall, 22% (31/143) of patients with DGE had a postoperative 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 abdominal abscess were observed in 17% of patients with DGE in the antecolic group compared with 25% in the retrocolic group (P 5 .25), and 34% of all patients with pancreatic fistula and/or abdominal abscess had DGE. Analyzing exclusively patients 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 patients with major complications (Clavien R 3), the occurrence of DGE was still significantly different between the antecolic and retrocolic group (7% vs 13%; P 5 .007).
Comments Following the report of DGE in patients undergoing pylorus-preserving PD by Warshaw et al in 1985,16 several studies 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 spasm of the pylorus, pancreatic leak, ischemic distress, and mechanical factors, like torsion or angulation, have been described as possible promoters of postoperative gastroparesis, gastric stasis, and DGE.10,17–21 Pharmacologic agents such as erythromycin or metoclopramide have been used to enhance postoperative gastric motility with varying results.7,17,22 In addition, several modifications of resection and reconstruction methods have been described to lower DGE incidence. Performing an antecolic gastrojejunostomy instead of a retrocolic reconstruction is one of the most commonly advocated techniques to decrease the incidence of DGE.4,10,23,24 The antecolic reconstruction has several theoretical advantages: less angulation, location of the gastrojejunostomy further away from the pancreaticojejunostomy (which reduces the potential negative effect of small pancreatic anastomotic leaks), and a more mobile jejunal loop. However, retrospective analysis as well as prospective randomized trials comparing antecolic versus classic retrocolic reconstruction have provided controversial results, and the influence of the chosen route of reconstruction is still a matter of discussion.25–28 In this large retrospective single-center study, we confirm that an antecolic gastrojejunostomy for classic PD with antrectomy is associated with a significantly lower incidence of DGE (15% vs 21%; P 5 .021) and a shorter length of stay (8 days vs 10 days; P 5 .001). Among all 800 patients, we found that a retrocolic reconstruction, age, a history of pancreatitis, upper abdominal surgery or a second malignant tumor, and postoperative pancreatic
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fistula were independent risk factors of the occurrence of any type of DGE. Severe DGE (grade B and C), in contrast, was only associated with a history of upper abdominal surgery and postoperative intra-abdominal abscess. The positive effect of the antecolic gastrojejunostomy was only noticeable in lowering the incidence of mild DGE (grade A), defined as requirement of an NGT required between post operative day 4 and 7, or reinsertion of the NGT because of nausea and vomiting after removal by POD 3 or the inability to tolerate a solid diet on POD 7. Paradoxically, episodes of emesis and reinsertion of the NGT were recorded more frequently in the antecolic arm, but a more detailed analysis shows that in 35% of patients of the retrocolic group who required an NGT after POD 3, the NGT was never discontinued after surgery because of high output compared with only 4% in the antecolic group. As observed by others, DGE was clearly associated with the occurrence of other postoperative complications in this study. It has been suggested that gastroparesis as a consequence of local inflammation may be the main cause of DGE in these cases.19,29,30 We elected to exclude from the study patients with severe complications in whom a step-by-step return to a normal diet was not attempted because of a prolonged nil per os (NPO) status (eg, patients with a grade C pancreatic fistula requiring nothing per os and parental nutrition or those with continuing mechanical ventilation). According to the International Study Group of Pancreatic Surgery definition of DGE, most of these patients would falsely be classified as having DGE, and we believe their exclusion enabled us to assess the true incidence of DGE. Other authors, who included such patients by definition, described a DGE rate of 90% in patients with prolonged intensive care unit stay.9 Among all patients in our series with DGE, 23% had a pancreatic fistula (ISGPF grade B and C) or an abdominal collection. Even though we observed a higher rate of pancreatic fistula in the retrocolic cohort, both pancreatic fistula and retrocolic reconstruction remained independent risk factors for DGE in multivariate analysis. Moreover, after exclusion of all patients with major complications (Clavien R 3), pancreatic fistula or abdominal abscess, the occurrence of DGE was still significantly lower in the antecolic group. The overall DGE rate in this study was low and comparable with others reporting a DGE incidence ranging from 6% to 57%.16,31–33 As it is the institutional preference, all patients in this series underwent a classic PD with antrectomy, which is positively reflected in the overall low incidence of DGE compared with other series of pyloruspreserving PD.8,20,34 In a retrospective series, Nikfarjam et al report a DGE rate of 14% in patients with an antecolic reconstruction with a retrogastric omental patch compared with 40% DGE in the retrocolic group. Of note, however, most patients with retrocolic reconstruction in that series underwent pylorus-preserving PD and were compared with a classic PD with antecolic reconstruction.35 The DGE rate of 14% in the antecolic group undergoing a classic 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 preservation. Hartel et al10 (not using the ISGPF-DGE definition) reported a DGE rate of 5% vs 24%, also favoring an antecolic reconstruction. Similarly, Murakami et al36 observed only 10% DGE rate after antecolic Roux-en-Y reconstruction. A recent randomized controlled trial comparing the occurrence of DGE between an antecolic Billroth II and retrocolic Billroth I reconstruction after PD with antrectomy and pancreaticogastrostomy found a lower prevalence in the antecolic method.37 A reduction of the postoperative DGE rate after an antecolic reconstruction was also described in a recently published meta-analysis.4,24 In contrast, 2 prospective randomized controlled trails, conducted by Gangavatiker et al,28 who mainly performed a classic pancreatoduodenectomy with antrectomy resection, and Imamura et al,38 who included only patients after pylorus-preserving PD, did not find a correlation between the method of reconstruction and the DGE incidence (antecolic 34% vs retrocolic 28%; P 5 .06) and (antecolic 12% vs retrocolic 21%; P5 .31). Those results were confirmed by a currently published randomized controlled multicenter study of 246 patients, of whom most underwent a pyloruspreserving PD (antecolic 34% [n 5 121] vs retrocolic 36% [n 5 125]).11 Additional studies investigating gastric emptying by 13C-acetate breath test or paracetamol absorption test were likewise unable to show a significant difference between the antecolic and the retrocolic methods of reconstruction.27,39 In addition to its retrospective nature, limitations of this study include the potential bias from the fact that all the antecolic reconstructions were done by a single surgeon, and therefore the differences between antecolic and retrocolic gastrojejunostomy could be related to the surgeon’s experience that is not accounted in the study. Nonetheless, the technique of performing the PD was identical in both groups, including standard lymphadenectomy and the placement of a transabdominal external pancreatic drain, and we also show that the results remained significant even after the exclusion of a coincidental pancreatic leak, which is a major potential confounder. On the other hand, the 800 patients evaluated represent the largest cohort of exclusively non–pylorus-preserving PD patients addressing DGE as a function of the route of reconstruction. Because the pylorus-preserving operation seems to be inherently associated to a higher degree of gastric emptying, it becomes a confounding factor when analyzing the type of reconstruction, and having series that include both non–pyloruspreserving PD and pylorus preserving pancreatic duodenectomy (PPPD) are therefore more difficult to analyze. In conclusion, the results of this large series show that an antecolic gastrojejunostomy after classic non–pylorus-preserving PD is associated with an overall lower incidence of DGE, and that this type of reconstruction is also associated to a significantly shorter length of stay. This observation, together with several prior studies and meta-analyses that have shown similar advantages of the gastrojejunal
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antecolic anastomosis, suggests that this method of reconstruction should be the preferred one after a classic non– pylorus-preserving pancreatoduodenectomy.
7
18. 19.
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