Abstract
Objectives
This study was conducted to compare the incidences of delayed gastric emptying (DGE) following pylorus-resecting pancreaticoduodenectomy (PrPD) and pylorus-preserving pancreaticoduodenectomy (PpPD), respectively.
Methods
Data for 37 patients submitted to PrPD were compared with data for a matched number of patients submitted to PpPD during the same period. A meta-analysis of comparative studies of the two techniques was also carried out. The primary endpoint was the rate of DGE (grades A–C) defined according to the International Study Group of Pancreatic Surgery criteria.
Results
In the case-matched comparison, both overall DGE (six PrPD patients and 17 PpPD patients; P = 0.006) and clinically relevant DGE (one PrPD and eight PpPD patients; P = 0.013) occurred significantly less often in the PrPD group than in the PpPD group. Based on eight non-randomized clinical trials and two randomized clinical trials involving 804 subjects, the meta-analysis further confirmed a significant reduction in DGE with pooled odds ratios of 0.33 [95% confidence interval (CI) 0.17–0.63; P < 0.001] and 0.13 (95% CI 0.05–0.40; P < 0.001) for overall DGE and clinically relevant DGE, respectively. Other complications and mortality were similar in both groups.
Conclusions
Pylorus-resecting pancreaticoduodenectomy is a safe procedure associated with less severe and less frequent postoperative DGE than PpPD.
Introduction
Pylorus-preserving pancreaticoduodenectomy (PpPD) is the mainstay of treatment for periampullary lesions. Compared with classic Whipple resection with antrectomy, PpPD can facilitate a better nutritional status and more favourable quality of life without differences in mortality, morbidity or oncologic outcomes.1
Delayed gastric emptying (DGE) is one of the most common postoperative complications after PpPD with reported incidences of 14–61%.2 Although DGE is not life-threatening, it is associated with a longer duration of hospitalization and higher hospital costs.3 Pylorus-resecting pancreaticoduodenectomy (PrPD), a procedure that includes resection of the duodenum and pyloric ring, was introduced as an alternative to PpPD in Japan in the 1990s and is intended to maintain gastric pooling ability and reduce the incidence of DGE. However, studies comparing rates of DGE between PrPD and PpPD have been relatively limited and have yielded conflicting results.4–12 Therefore, the benefit of PrPD remains to be elucidated.
The aim of this study was to compare PrPD and PpPD in a case-matched comparison. In addition, in line with the PRISMA (preferred reporting items for systematic reviews and meta-analyses) guidelines,13 a meta-analysis of comparative studies of the two techniques was carried out to provide overall estimates of the incidences of DGE.
Materials and methods
Case-matched comparison
Pylorus-resecting pancreaticoduodenectomy was adopted in March 2011 at the First Affiliated Hospital of Xiamen University. To June 2014, 37 consecutive patients underwent PrPD for periampullary lesions at this institution. These 37 patients were matched with 37 patients submitted to PpPD during the same period. Patients were matched for baseline demographics, comorbidities, pancreatic texture, pancreatic duct size and pathology. The hospital records of these patients were reviewed retrospectively. The technique used for patients in the PpPD and PrPD groups was essentially similar to that described by Kawai et al.7 All operations were performed by the same surgeons. The technique for pancreaticoduodenectomy was not standardized, and the selection of PrPD or PpPD was based on the decision of the operating surgeon in this retrospective study. End-to-side pancreaticojejunostomy and end-to-side hepaticojejunostomy were performed on the same proximal jejunal, which was brought through the transverse mesocolon in a retrocolic position in all patients. Gastrojejunostomy in PrPD or duodenojejunostomy in PpPD were performed using a two-layer anastomosis in an antecolic position. Appropriate informed consent was obtained from all patients. The study was approved by the Human Ethics Review Board of the local institution.
The primary endpoint of this study was DGE characterized according to the definition of the International Study Group of Pancreatic Surgery (ISGPS); DGE of Grade B or C was regarded as clinically relevant.14 Primary DGE was defined as DGE occurring in the absence of other intra-abdominal complications.15 Secondary endpoints included other complications, mortality (defined as any death occurring within 30 days of the date of operation or during the same hospital admission) and hospital length of stay (LoS).
All statistical analyses were performed using spss Statistics for Windows Version 11.0 (SPSS, Inc., Chicago, IL, USA). In comparisons between the two groups, categorical variables were compared with Fisher's exact test, continuous variables with Student's t-test, and non-parametric variables with the Mann–Whitney U-test. A two-tailed P-value of <0.05 was considered to indicate statistical significance.
Meta-analysis
A literature search was performed in PubMed for relevant publications from the time of the inception of the database to May 2014. The medical subject heading (MeSH) search terms were ‘pylorus-resecting pancreaticoduodenectomy’, ‘pylorus-preserving pancreaticoduodenectomy’, ‘subtotal stomach-preserving pancreaticoduodenectomy’ and ‘delayed gastric emptying’. Only studies conducted in humans and published in English were considered for inclusion. The reference lists of all retrieved articles were manually searched for additional studies. Animal studies, case reports, reviews, studies including patients who underwent total pancreatectomy and central pancreatectomy or distal pancreatectomy, and those lacking control groups were excluded.
Two reviewers (BL and LW) independently extracted data on the following parameters from each study: first author; year of publication; study population characteristics; number of patients submitted to each procedure, and endpoints. All relevant text, tables and figures were reviewed for data extraction. Any discrepancies in inclusion were resolved by discussion between the reviewers.
The meta-analysis was performed using RevMan Version 5.1 (Cochrane Collaboration, Oxford, UK). Estimated effect measures were the odds ratio (OR) for dichotomous variables and the weighted mean difference (WMD) for continuous variables. Pooled estimates were presented with 95% confidence intervals (95% CI). The pooled effect was calculated using either the fixed-effects model or the random-effects model. Heterogeneity was evaluated using the I2 statistic, with values over 50% indicating considerable heterogeneity. Publication bias was assessed visually using a funnel plot, based on the DGE result.
Results
Case-matched comparison
Perioperative variables across the two groups are shown in Table 1.
Table 1.
Patient characteristics and surgical outcomes in the two groups
| Variable | PrPD group (n = 37) | PpPD group (n = 37) | P-value |
|---|---|---|---|
| Male gender, n | 23 | 23 | 0.999 |
| Age, years, median (range) | 61 (34–77) | 63 (31–73) | 0.944 |
| Comorbidity, n | |||
| Diabetes mellitus | 7 | 9 | 0.572 |
| Hypertension | 11 | 10 | 0.797 |
| Chronic pulmonary disease | 2 | 3 | 0.643 |
| Jaundice, n | 26 | 22 | 0.330 |
| Preoperative biliary drainage, n | 7 | 5 | 0.528 |
| Pathology, n | |||
| Malignancy/benign | 28/9 | 28/9 | 0.999 |
| Pancreatic adenocarcinoma | 18 | 15 | |
| Other disease | 19 | 22 | |
| Intraoperative parameters | |||
| Soft pancreas, n | 12 | 14 | 0.626 |
| Pancreatic duct size, mm, median (range) | 4 (2–9) | 4 (2–8) | 0.746 |
| Operating time, min, median (range) | 290 (210–420) | 305 (195–480) | 0.524 |
| Blood loss, ml, median (range) | 580 (200–1300) | 610 (150–1600) | 0.317 |
| Blood transfusion, n | 14 | 11 | 0.461 |
| Vascular resection, n | 6 | 4 | 0.496 |
| Morbidity, n | |||
| DGE grade (A/B/C) | (5/0/1) | (9/3/5) | 0.006 |
| DGE grade (B/C) | 1 | 8 | 0.013 |
| Primary DGE | 2 | 8 | 0.041 |
| Pancreatic fistula grade (A/B/C) | (5/1/0) | (7/0/1) | 0.553 |
| Intra-abdominal abscess | 3 | 5 | 0.454 |
| Biliary leakage | 0 | 1 | 0.314 |
| Haemorrhage | 1 | 2 | 0.556 |
| Wound infection | 4 | 3 | 0.691 |
| Ileus | 1 | 3 | 0.304 |
| Re-exploration | 0 | 1 | 0.314 |
| Length of hospital stay, days, median (range) | 16 (11–43) | 28 (10–75) | 0.017 |
DGE, delayed gastric emptying; PpPD, pylorus-preserving pancreaticoduodenectomy; PrPD, pylorus-resecting pancreaticoduodenectomy.
There was no postoperative in-hospital mortality in either group.
Both overall DGE (six PrPD patients and 17 PpPD patients; P = 0.006) and clinically relevant DGE (one PrPD and eight PpPD patients; P = 0.013) occurred significantly less often in the PrPD group than in the PpPD group. Primary DGE was recorded in two patients in the PrPD group and in eight in the PpPD group, which represents a significant difference (P = 0.041). No significant differences were observed in incidences of other postoperative complications between the two groups. One patient in the PpPD group underwent a reoperation as a result of intra-abdominal haemorrhage secondary to pancreatic fistula on postoperative day 12. Hospital LoS was significantly shorter after PrPD than after PpPD (P = 0.017).
Meta-analysis
A total of nine publications published between 2007 and 2014 matched the criteria for inclusion in the present meta-analysis and were therefore reviewed.4–12 Fig. 1 demonstrates a flow diagram of the selection process. The characteristics of the studies included in the meta-analysis are summarized in Table 2. A total of 804 patients were included in the meta-analysis, of whom 433 (53.9%) underwent PrPD and 371 (46.1%) underwent PpPD. Table 3 shows the results by operation type for the outcome variables.
Figure 1.
Flow diagram of the selection and screening process for eligible studies
Table 2.
Baseline characteristics of studies included in the meta-analysis
| Study | Design | Definition of DGE | EI (Region) | PA | n | PrPD/PpPD |
|---|---|---|---|---|---|---|
| Hayashibe et al. (2007)4 | NRCT | NGT ≥ PoD 10 or DGE 14a | 1999–2005 (Japan) | ES-PJ | 33 | 21/12 |
| Akizuki et al. (2008)5 | NRCT | NGT ≥ PoD 10 or DGE 14a | 2003–2007 (Japan) | ES-PJ | 64 | 30/34 |
| Kurahara et al. (2010)6 | NRCT | ISGPS definition | 2000–2010 (Japan) | ES-PG | 112 | 64/48 |
| Kawai et al. (2011)7 | RCT | ISGPS definition | 2005–2009 (Japan) | ES-PJ | 130 | 66/64 |
| Oida et al. (2011)8 | NRCT | ISGPS definition | 1999–2008 (Japan) | ES-PG | 67 | 42/25 |
| Fujii et al. (2012)9 | NRCT | ISGPS definition | 2000–2010 (Japan) | ES-PJ | 89 | 56/33 |
| Hackert et al. (2013)10 | NRCT | ISGPS definition | – (Germany) | ES-PJ | 80 | 40/40 |
| Nanashima et al. (2013)11 | NRCT | ISGPS definition | 2000–2009 (Japan) | ES-PJ | 55 | 27/28 |
| Matsumoto et al. (2014)12 | RCT | ISGPS definition | 2003–2009 (Japan) | ES-PJ | 100 | 50/50 |
| Current study | NRCT | ISGPS definition | 2011–2014 (China) | ES-PJ | 74 | 37/37 |
Inability to tolerate a regular diet on PoD 14.
DGE, delayed gastric emptying; EI, enrolment interval; ES, end-to-side; ISGPS, International Study Group of Pancreatic Surgery; NGT, nasogastric tube; NRCT, non-RCT; PA, pancreatic anastomosis; PG, pancreaticogastrostomy; PJ, pancreatojejunostomy; PpPD, pylorus-preserving pancreaticoduodenectomy; PrPD, pylorus-resecting pancreaticoduodenectomy; PoD, postoperative day; RCT, randomized controlled trial.
Table 3.
Results of a meta-analysis
| Outcome of interest | Studies, n | Patients, n | Results | OR/WMD | 95% CI | P-value | I2 (%) | |
|---|---|---|---|---|---|---|---|---|
| PrPD, n (%) | PpPD, n (%) | |||||||
| DGE | 10 | 804 | 133/433 (31%) | 156/371 (42%) | 0.33 | 0.17–0.63 | <0.001 | 58% |
| ISGPS B + C DGE | 8 | 707 | 30/382 (8%) | 101/325 (31%) | 0.13 | 0.05–0.40 | <0.001 | 76% |
| Pancreatic fistula | 9 | 724 | 76/393 (19%) | 73/331 (22%) | 0.87 | 0.60–1.26 | 0.45 | 0% |
| Intra-abdominal abscess | 6 | 535 | 21/264 (8%) | 23/251 (9%) | 0.87 | 0.48–1.60 | 0.66 | 0% |
| Haemorrhage | 6 | 535 | 7/264 (3%) | 4/251 (2%) | 1.46 | 0.51–4.18 | 0.48 | 0% |
| Bile leak | 2 | 174 | 0/77 (0%) | 4/77 (5%) | 0.17 | 0.02–1.49 | 0.13 | 0% |
| Wound infection | 5 | 404 | 13/206 (7%) | 12/178 (6%) | 1.01 | 0.46–2.24 | 0.97 | 0% |
| Reoperation | 5 | 448 | 7/213 (3%) | 2/215 (1%) | 2.56 | 0.73–8.99 | 0.14 | 0% |
| Mortality | 10 | 804 | 4/433 (1%) | 1/371 (0%) | 2.25 | 0.48–10.65 | 0.31 | 0% |
| Length of hospital stay, days | 9 | 692 | – | – | −3.53 | −7.18 to 0.05 | 0.05 | 74% |
95% CI, 95% confidence interval; DGE, delayed gastric emptying; ISGPS International Study Group of Pancreatic Surgery; OR, odds ratio; PpPD, pylorus-preserving pancreaticoduodenectomy; PrPD, pylorus-resecting pancreaticoduodenectomy; WMD, weighted mean difference.
Pooled analysis showed there to be a significant reduction in the overall incidence and clinically relevant incidence of DGE in the PrPD group (Figs 2 and 3).
Figure 2.
Result of the meta-analysis of data on overall delayed gastric emptying. 95% CI, 95% confidence interval; M-H, Mantel–Haenszel test; PpPD, pylorus-preserving pancreaticoduodenectomy; PrPD, pylorus-resecting pancreaticoduodenectomy
Figure 3.
Result of the meta-analysis of data on clinically relevant delayed gastric emptying. 95% CI, 95% confidence interval; M-H, Mantel–Haenszel test; PpPD, pylorus-preserving pancreaticoduodenectomy; PrPD, pylorus-resecting pancreaticoduodenectomy
Other postoperative complications, mortality and hospital LoS were similar between the two groups (Table 3).
The funnel plot for DGE was asymmetric, indicating the presence of publication bias (Fig. 4).
Figure 4.
Funnel plot analysis of publication bias. The outcome was delayed gastric emptying
Discussion
As a result of advances in perioperative management and operative techniques in recent years, operative mortality after PpPD has decreased to <5% in high-volume centres, but morbidity remains high.2,3 Delayed gastric emptying is one of the most common postoperative complications after PpPD and may contribute to longer hospital stay and higher costs. Incidences of DGE range from 14% to 61% in most series, but the extent of this range reflects the use of different definitions of DGE throughout the literature.2 The 45.9% incidence of DGE in the PpPD group in the present study may seem high, but probably relates to the use of the strict definition criteria of the ISGPS.14 In fact, this result was comparable with those in previous reports.10,15
Among the pathophysiological mechanisms responsible for the occurrence of DGE are ischaemic injury and intraoperative trauma of the antrum and pylorus. This claim is supported by the fact that the use of prokinetic drugs such as erythromycin can improve gastric emptying and thereby reduce the incidence of DGE after pancreaticoduodenectomy.16 In the light of this, removing the pylorus seems to be a reasonable and causal prophylactic strategy to prevent the occurrence of DGE and its attendant complications. The results from the present case-matched comparison show that PrPD is associated with a less severe and lower rate of postoperative DGE than PpPD. Rates of other complications and mortality were similar in both groups. These findings were further confirmed by a meta-analysis of 10 trials.
An argument against PrPD is that resection of the pylorus ring may result in the more frequent occurrence of dumping syndrome after this procedure than after PpPD. Dumping syndrome is a serious late postoperative complication affecting quality of life, body weight change, and nutritional status. However, more than 95% of the stomach is preserved in PrPD, and the stomach pooling ability is preserved in PrPD in the same way as in PpPD.7 In a randomized controlled trial (RCT) by Kawai et al.,17 during the 2-year follow-up period, only one of 66 patients (1.5%) with PrPD had dumping syndrome, and PrPD and PpPD were shown to be equivalent with regard to nutritional status and the incidence of new-onset or worsening diabetes. Similarly, in another RCT by Matsumoto et al.,12 there were no significant differences between patients submitted to either of the two procedures on postoperative serum albumin levels, serum total cholesterol levels, and body mass index during the 3-year follow-up period.
In the current series, hospital stay was significantly shorter after PrPD than after PpPD, which is mainly a consequence of the difference in postoperative DGE. However, this finding was inconsistent with that derived from the meta-analysis. Variability in health care systems among countries may explain the diversity of this outcome.
With reference to longterm survival, most studies, including the current series, did not provide relevant information because the duration of postoperative follow-up was short. Only Fujii et al.9 and Matsumoto et al.12 reported that longterm survival did not differ significantly between the two procedures.
Two reconstruction routes are usually used for gastrojejunostomy or duodenojejunostomy: the antecolic route, and the retrocolic route. The former is the present authors' preference. A 2006 RCT with 40 patients conducted by Tani et al.18 found the antecolic route to be better than the retrocolic route in terms of DGE. However, four RCTs15,19–21 showed similar rates of DGE between the two reconstruction routes. A large multicentre trial should be considered for further conclusive evidence.
The present study has some limitations. Publication bias was detected on funnel plot analysis in the meta-analysis. This may relate to the inclusion of only studies published in English. As a result, the efficacy of PrPD may not have been fully estimated. Most operations were conducted in Japanese patients, which limits the generalizability of the findings. The number of patients in the current series and the available studies is small. It is also important to note that only two of the studies included in this meta-analysis were of RCT design. This implies that current evidence is too weak to provide a definitive basis for clinical decision making.
In conclusion, the findings of this study suggest that PrPD is a safe procedure associated with a less severe and lower rate of postoperative DGE than PpPD. Further large RCTs are warranted to confirm this finding and to assess longterm survival.
Acknowledgments
The authors thank Yanfang Zhao, Department of Health Statistics, Second Military Medical University, Shanghai, China, for her critical revision of the section on statistical analyses.
Conflicts of interest
None declared.
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