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10.1245/s10434-006-9330-3
Annals of Surgical Oncology 14:1825-1834 (2007)
© 2007 Society of Surgical Oncology
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Original Article

The Pylorus: Take It or Leave It? Systematic Review and Meta-Analysis of Pylorus-Preserving versus Standard Whipple Pancreaticoduodenectomy for Pancreatic or Periampullary Cancer

Paul J. Karanicolas, MD1,3, Edward Davies, MD3, Regina Kunz, MD, MSc4, Matthias Briel, MD1,4, H. Pavan Koka, MD1,3, Darrin M. Payne, MD1,3, Shona E. Smith, MD3, Hui-Ping Hsu, MD5, Pin-Wen Lin, MD5, Christian Bloechle, MD6, Karl-Joseph Paquet, MD7 and Gordon H. Guyatt, MD, MSc1,2

1 Department of Clinical Epidemiology and Biostatistics, McMaster University, 1200 Main St. W, Hamilton, Ontario, L85 3Z5, Canada
2 Department of Medicine, McMaster University, Hamilton, Canada
3 Department of Surgery, University of Western Ontario, University Hospital, London Health Sciences Centre, Room C8-114, 339 Windermere Road, London, Ontario, N6A 5A5, Canada
4 Basel Institute for Clinical Epidemiology, University Hospital Basel, Habelstasse 10, 3rd floor, Basel, Ch-4031, Switzerland
5 Department of Surgery, National Cheng Kung University Hospital, No. 138, Sheng-Li road, Tainan, 704, Taiwan
6 Department of Surgery, University Hospital Eppendorf, Martinistrasse 52, Hamburg, D-20246, Germany
7 Department of Surgery, Heinz Kalk-Hospital, Bad Kissingen, D-8730, Germany

Correspondence: Address correspondence and reprint requests to: Paul J. Karanicolas, MD; E-mail: pjkarani{at}uwo.ca


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Our objective was to determine the relative effects of pylorus-preserving pancreaticoduodenectomy (PPPD) and standard Whipple pancreaticoduodenectomy (SWPD) in patients with pancreatic or periampullary cancer.

Methods: We searched seven bibliographic databases, conference proceedings, and reference lists of articles and textbooks, and we contacted experts in the field of hepatobiliary surgery. We included published and unpublished randomized controlled trials. We evaluated the methodological quality of trials and, in duplicate, extracted data regarding operative, perioperative, and long-term outcomes. We contacted all authors and asked them to provide additional information regarding the trials. We pooled results from the studies by using a random-effects model, evaluated the degree of heterogeneity, and explored potential explanations for heterogeneity.

Results: Six trials that included a total of 574 patients met eligibility criteria. In the pooled analysis, PPPD was 72 minutes faster (P < .001, 95% confidence interval [95% CI], 53–92), with 284 mL less blood loss (P < .001, 95% CI, 176–391) and .66 fewer units of blood transfused (P = .002, 95% CI, .25–1.16). Other perioperative and long-term outcomes did not statistically differ, although the confidence intervals include important differences.

Conclusions: Moderate-quality evidence suggests PPPD is a faster procedure with less blood loss compared with SWPD. Large absolute differences in other key outcomes are unlikely; excluding relatively small differences will, however, require larger, methodologically stronger trials.

Key Words: Pancreatic cancer • Pancreaticoduodenectomy • Whipple procedure • Pylorus • Systematic review • Meta-analysis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pancreatic cancer is the fourth most common cause of cancer-related mortality in North America.1 Although surgical resection provides the only chance of cure, most patients present with advanced disease that precludes complete resection2 and contributes to the poor outcome. Patients with pancreatic cancer can anticipate a median survival of <6 months and a 5-year survival of <5%.3,4

Since its introduction by Kausch in 1912 and its later refinement by Whipple, the optimal extent of resection in pancreaticoduodenectomy (PD) has been a matter of debate.5,6 A standard Whipple pancreaticoduodenectomy (SWPD) involves resection of the distal stomach, pylorus, duodenum, common bile duct, gallbladder, and pancreatic head, with three anastomoses required for the reconstruction. In 1944, Watson described a modification of this procedure known as pylorus-preserving pancreaticoduodenectomy (PPPD); PPPD was reintroduced in the late 1970s for the treatment of chronic pancreatitis.7,8 Relative to the SWPD, the only modification of the PPPD is the proximal resection margin; the stomach and pylorus are left intact.

PPPD involves a less extensive dissection, which may result in decreased blood loss and operative time, as well as decreasing postoperative complications. Proponents of SWPD have raised concerns regarding the adequacy of surgical margins in patients with pancreatic or periampullary cancer, which may increase local recurrence and mortality. Furthermore, patients undergoing PPPD may experience an increased incidence of perioperative delayed gastric emptying. Our objective was to synthesize existing evidence from randomized controlled trials (RCTs) comparing the impact of PPPD and SWPD on perioperative and long-term outcomes in patients with pancreatic and periampullary cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Eligibility Criteria and Search Strategy
Table 1Go presents the review’s eligibility criteria. We searched Medline (OVID), Embase, the Cochrane Central Register of Controlled Trials, and the Web of Science from 1966 to January 25, 2006. We used the following MeSH terms and keywords without language restrictions: pancreatic neoplasms, pancreaticoduodenectomy, duodenopancreatectomy, whipple, pylorus. Two investigators (P.J.K. and D.M.P.) reviewed the titles and abstracts (when available) identified from the databases. We retrieved all articles that either reviewer thought had the potential to meet the eligibility criteria.


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  		TABLE 1. Study eligibility criteria
 
We hand-searched the bibliographies of two major textbooks in hepatobiliary surgery9,10 and the conference proceedings of four major hepatobiliary association meetings (International Hepatopancreaticobiliary Association, American Hepatopancreaticobiliary Association, European Hepatopancreaticobiliary Association, and Asian Society of Hepatobiliarypancreatic Surgery) and the American Society of Clinical Oncology annual meeting over the past year. Our search included two indices of conference proceedings (ProceedingsFirst, ArticlesFirst) and a search of the database of registered trials at http://www.clinicaltrials.gov/. Reference lists of all identified articles and overviews, and a Science Citation Index Search (SciSearch) of relevant articles provided additional sources of potentially eligible RCTs.

Ten experts in the field of pancreatic surgery (presidents of international societies and authors of review articles) reviewed a comprehensive list of relevant articles and suggested additional potentially eligible RCTs of which they were aware. We contacted the principal investigator of unpublished RCTs and requested a full report of the study.

Study Selection
Two English-language reviewers (H.P.K., S.E.S.) and two reviewers for non-English-language articles (M.B., R.K.) assessed each article on the basis of the eligibility criteria with a standardized form. The reviewers were blinded to the journal in which the article was published, the authors, the institution, and the results. The reviewers met and reached a consensus for any disagreements. We measured agreement between reviewers for each inclusion criterion by {kappa} with quadratic weighting.11,12

Validity Assessments
Two reviewers (H.P.K., S.E.S. or M.B., R.K.) assessed the methodological quality of the primary research by using standardized forms. We assessed primary studies for the presence of specific methodological components, rather than incorporating a summary score.13,14 We limited the number of methodological components to four: concealment of allocation, blinding of patients, blinding of outcome assessors, and proportion of patients lost to follow-up.

We resolved disagreements between reviewers by using the same method as for the assessments of relevance, and we measured agreement for the quality component assessments by using the weighted {kappa} measurement.

Data Extraction
Two investigators (D.M.P., P.J.K. or M.B., R.K.) abstracted relevant information regarding the population, intervention, and outcomes from each selected article by using standardized data extraction forms. We contacted the corresponding author of each trial and requested any relevant information that was not reported in the published article. The reviewers discussed any disagreements and came to a consensus. Wherever possible, the reviewers extracted data in a method that allowed comparison of the two groups by using the intention-to-treat principle. If this was not possible, we contacted the authors and requested original data in a form that would allow analysis consistent with the intention-to-treat principle.

Analysis
We used Reference Manager 4.2.8 (Cochrane Collaboration) to conduct all analyses. We converted continuous data that was reported as a median and range to the mean and standard deviation by using the method of Hozo.15 We analyzed survival data at annual intervals after surgery. For each outcome with data from five or more studies, we began the analysis by creating a funnel plot, comparing the magnitude of the relative risk on the horizontal axis against the standard error of the log relative risk on the vertical axis.16

We pooled data across studies and calculated the relative risks, absolute risk reductions, and associated 95% confidence intervals (95% CI) for dichotomous outcomes. For continuous outcomes, we pooled data by using the weighted mean difference (WMD). For both measures, we used a random-effects model.17

We tested for heterogeneity between included trials by using the Breslow-Day test.18 In addition, we calculated the I2 statistic, which estimates the proportion of total variance across studies that is apparently due to true between-study differences rather than chance.19 If the Breslow-Day test revealed statistically significant heterogeneity (P < .1) or if the I2 value was >20%, we undertook sensitivity and subgroup analyses by using hypotheses generated a priori (Table 2Go).20,21


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  		TABLE 2. Potential sources of heterogeneity explored in the analysis
 
We constructed tables by using the GRADE system to summarize the findings and rate the overall quality of evidence.22,23


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Trial Identification
We identified 371 citations from our initial search strategy, of which one or both of the reviewers considered 25 to be potentially eligible. We excluded 15 of the studies during the second phase of the inclusion process; 9 were nonrandomized comparisons, and 6 were studies that did not compare the interventions of interest (Fig. 1Go).


Figure 1
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  		FIG. 1. Overview of trial identification and selection process.

 
There was good agreement regarding the application of study inclusion criteria (weighted {kappa} , .62–.96). Of the 10 studies remaining,24–33 4 were updates or extractions from other published trials. All duplicates were grouped together for review; thus, six unique trials ultimately proved eligible. We contacted an author from each trial; we received additional information from four studies.26,28,32,33

Characteristics of Included Studies
Two of the studies were published in English,24–27 three of the studies were published in German.28,32,33 and one study was published in both English and German.29–31 Sample size ranged from 40 to 214, with a total of 574 participants (Table 3Go). All of the studies had similar eligibility criteria, although two27,29–31 included patients with benign conditions but limited the survival analysis to patients with cancer. At the institutions of the authors that responded to our request, the total volume of pancreaticoduodenectomies performed during the study period ranged from 25 to 300 annually. The relative number of each procedure also varied; some institutions performed more SWPD, whereas others favored PPPD outside of the trial.


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  		TABLE 3. Characteristics of studies
 
All of the studies had methodological limitations (Table 4Go). One study reported the results by using the intention-to-treat principle;27 in two, all patients received the treatment to which they were randomized;28,33 and although two of the studies reported the results by using a per-protocol analysis, we used original data provided by the authors in our analysis following the intention-to-treat principle.26,32 In the final trial, the investigators excluded 11 patients who were randomized to receive PPPD because there was tumor infiltration of the proximal duodenum or positive peripyloric lymph nodes.29 We were unable to obtain data for these excluded patients; therefore, we conducted an additional sensitivity analysis excluding this study from all analyses. There was good agreement between reviewers for the validity assessments ({kappa} = .40–1.0).


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  		TABLE 4. Methodological components of included studies
 
Perioperative Outcomes
We extracted data for 11 perioperative outcomes from three to six studies. Five outcomes had data from enough trials to create funnel plots; all of these were symmetric except for delayed gastric emptying. For this outcome, the three smaller studies favored PPPD, whereas the two larger trials were neutral or slightly in favor of SWPD.

All trials reported the perioperative mortality with a total of 490 patients, for which outcomes were consistent across studies (heterogeneity P = .90, I2 = 0). There was a nonsignificant trend toward lower mortality in the PPPD group, with a relative risk of .40 (Fig. 2Go, P = .09, 95% CI, .14 to 1.13). This corresponds to an absolute risk reduction of .02 (95% CI, – .01 to .05).


Figure 2
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  		FIG. 2. Forest plot of perioperative mortality. PPPD, pylorus-preserving pancreaticoduodenectomy; SWPD, standard Whipple pancreaticoduodenectomy.

 
In all five studies that reported operative time, PPPD was faster than SWPD with a WMD of 72.3 minutes (Fig. 3Go, P < .001, 95% CI, 52.9 to 91.8). Similarly, there was less estimated blood loss (Fig. 4Go, WMD 283.7 mL, P < .001, 95% CI, 176.0 to 391.4) and blood transfusions (Fig. 5Go, WMD .66 U, P = .002, 95% CI, .25 to 1.16) in patients undergoing PPPD. No statistically significant heterogeneity was observed between studies for these outcomes, and all I2 values were <20%.


Figure 3
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  		FIG. 3. Forest plot of operative time. PPPD, pylorus-preserving pancreaticoduodenectomy; SWPD, standard Whipple pancreaticoduodenectomy.

 

Figure 4
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  		FIG. 4. Forest plot of operative blood loss. PPPD, pylorus-preserving pancreaticoduodenectomy; SWPD, standard Whipple pancreaticoduodenectomy.

 

Figure 5
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  		FIG. 5. Forest plot of blood transfusion. PPPD, pylorus-preserving pancreaticoduodenectomy; SWPD, standard Whipple pancreaticoduodenectomy.

 
The risks of postoperative bleeding, biliary leak, pancreatic leak, and gastroenteric leak did not differ significantly between groups, although the confidence intervals for each of these outcomes were wide in relative terms (Table 5Go). Because the event rates are low, the confidence intervals do not seem so wide in absolute terms. There was a trend toward a shorter length of hospital stay in patients that underwent PPPD (WMD – 1.5 days, P = .12, 95% CI, – 3.3 to .4).


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  		TABLE 5. GRADE system evidence table summarizing the outcomes measured
 
Results showed trends toward shorter duration of nasogastric intubation (P = .28, 2.36 days, 95% CI, – 1.96 to 6.67) and better gastric emptying (RR 1.52, P = .25, 95% CI, .74 to 3.14) with SWPD. There was substantial heterogeneity present in both of these outcomes (nasogastric intubation I2 = 88.2%, P < .001; delayed gastric emptying I2 = 72.6%, P = .006). We were unable to account for the heterogeneity with any of the a priori hypotheses. When we excluded the trial that used a per-protocol analysis from the analysis of delayed gastric emptying, the heterogeneity decreased (Fig. 6Go, I2 = 62.2%, P = .05), and the trend toward better emptying in the SWPD group increased (RR 2.08, P = .10, 95% CI, .87 to 4.95).


Figure 6
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  		FIG. 6. Forest plot of delayed gastric emptying. PPPD, pylorus-preserving pancreaticoduodenectomy; SWPD, standard Whipple pancreaticoduodenectomy.

 
Long-Term Mortality
One trial reported survival up to 3 years following surgery, and three trials reported survival up to 5 years (Table 5Go). Heterogeneity P values were consistently > .10 and I2 < 20%. Results consistently favored PPPD, although the trends were weak and the confidence intervals relatively wide.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our systematic review identified six RCTs that addressed the relative impact of PPPD and SWPD. In general, the trials had important methodological limitations, including questionable concealment of randomization, suboptimal blinding, and substantial loss to follow-up. Sample sizes were inadequate to completely assess the crucial outcome of long-term mortality, and the important outcome of delayed gastric emptying. We can say with confidence, however, that PPPD reduces operative time by approximately 1 hour, and blood loss and the transfusion requirements by almost 1 U of blood.

The outcome of delayed gastric emptying deserves special attention because of its clinical importance and because of the results observed. The Forest plot suggested that heterogeneity was present among included studies, and it was reduced when the trial that analyzed patients by using a per-protocol analysis was excluded. Marked heterogeneity remained after excluding this study, which could not be explained by any of the a priori hypotheses. One difficulty with measuring gastric emptying is the potential for bias on the part of the outcome assessors, particularly because only one of the studies involved assessments that were blinded to treatment group. All of the trials used definitions of delayed gastric emptying that included length of nasogastric intubation, which was at the discretion of the unblinded caregivers. Furthermore, there was a trend toward decreased length of hospital stay in favor of PPPD. Theoretically, the length of hospital stay should reflect the length of nasogastric intubation. This seemingly counterintuitive finding further weakens inferences regarding delayed gastric emptying.

Proponents of SWPD have expressed concerns that the resection margins of PPPD may predispose patients to cancer recurrence, and an increased mortality.34,35 The confidence intervals from the pooled mortality analysis are relatively wide (from .87 to 1.11 after 5 years), but do make relative differences of >13% in favor of PPPD very unlikely.

Strengths of the review include the rigorous, comprehensive search for published and unpublished studies, inclusion of non-English-language studies, the participation of the authors of the original articles in the review (and thus the availability of data not in the published reports), and the duplicate assessment of eligibility and validity. The most crucial additional information allowed us to follow the intention-to-treat principle in all but one study. Although this approach is always ideal, it is critical in this case. There is a clear biological reason to believe that patients with the most advanced cancer, and hence the worst prognosis, would be selectively excluded from one group (PPPD) and not excluded from the other group (SWPD), biasing results in favor of PPPD. Finally, we analyzed the data by using commonly accepted methods that were specified a priori.

Methodological limitations of the primary studies constitute the major weakness of the review. Possible problems with concealment, lack of blinding, and loss to follow-up could have introduced bias. The relatively small sample size—a total of 574 patients—results in wide confidence intervals for some outcomes and leaves the relevant impact of the procedures on major outcomes of mortality and gastric emptying unresolved. The unexplained heterogeneity in gastric emptying results constitutes another limitation.

The GRADE system provides a structure for rating the overall quality of the evidence and making treatment recommendations.22,23 In this system, RCTs provide high-quality evidence unless limited by methodological weaknesses, imprecision, inconsistency, indirectness, or high risk of publication bias. Our assessment is that for the outcomes of operative time, bleeding, and long-term mortality, studies are limited only by weaknesses related to study design and implementation, and provide moderate-quality evidence. For postoperative complications and hospital length of stay, the estimates of treatment effect are also limited by imprecision and provide only low-quality evidence. The additional limitation of the heterogeneity in gastric emptying leads us to classify the evidence as very low quality for that outcome.

In conclusion, the results provide moderate-quality evidence that PPPD requires less operative time, results in less bleeding, and achieves similar long-term survival to SWPD. The evidence does not permit any conclusions about the incidence of perioperative complications or delayed gastric emptying, although these occur infrequently enough that absolute differences are likely to be small. Determining the impact of the two procedures on these major outcomes will require one or more large, well-designed, appropriately powered RCTs. Given the difficulty blinding the personnel involved and the extensive experience many surgeons have with the procedures, an expertise-based design would be the ideal method of exploring this question.36


   ACKNOWLEDGMENTS
 
P.K. holds a Canada Graduate Scholarship from the Canadian Institutes of Health Research. M.B. is a scholar of the Swiss National Science Foundation.

Received for publication August 24, 2006. Accepted for publication October 18, 2006.


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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