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10.1245/s10434-006-9172-z
Annals of Surgical Oncology 13:1403-1411 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Bypass Surgery Versus Palliative Pancreaticoduodenectomy in Patients with Advanced Ductal Adenocarcinoma of the Pancreatic Head, with an Emphasis on Quality of Life Analyses

B. Schniewind, MD1, B. Bestmann1, R. Kurdow1, J. Tepel1, D. Henne-Bruns2, F. Faendrich1, B. Kremer1 and T. Kuechler1

1 Clinic for General and Thoracic Surgery, University Clinic of Schleswig-Holstein, Campus Kiel, Arnold-Heller-Str. 7, 24105, Kiel, Germany
2 Clinic for Visceral and Transplantation Surgery, University Clinic of Ulm, Steinhoevelstr. 9, 89075 Ulm, Germany

Correspondence: Address correspondence and reprint requests to: B. Schniewind, MD; E-mail: schniewind{at}surgery.uni-kiel.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: In some centers, palliative resection (PR; partial pancreaticoduodenectomy) is, in selected cases, promoted in preference to double loop bypass (DLB) surgery for advanced pancreatic cancer. This prospective study compares PR with DLB, placing particular focus on patients’ quality of life (QoL).

Methods: From 01/1993 to 09/2004, 167 patients were analyzed in a prospective single center study of palliative surgical treatment of advanced ductal adenocarcinoma of the pancreatic head. Thirty-eight underwent PR and 129 underwent palliative DLB. Patients undergoing DLB were divided into: (1) locally advanced disease (LAD-subgroup; n = 61; 47%) and (2) metastasized disease (MD-subgroup; n = 68; 53%). QoL was assessed using the EORTC QLQ-C30 questionnaire supplemented by a pancreatic cancer specific module. QoL data were collected pre-operatively and for up to 12 months after surgery.

Results: Median survival was 7.0 months (95% CI 4.09; 9.91) in PR patients and 6.0 months (95% CI 5.39; 6.61) in patients who received DLB. Mortality and morbidity were, respectively, 7.8 and 58% for PR, and 2.6 and 42% for DLB. QoL decreased more after PR than after DLB. The DLB-group recovered quicker, reaching pre-operative QoL levels after 3 months, and were less impaired when discharged. The LAD-subgroup and the MD-subgroup presented with equal levels of QoL.

Conclusions: QoL analysis revealed favorable QoL data after DLB. Additionally, the survival rates of the two groups did not differ significantly, but morbidity and mortality rates in the PR group were elevated. Therefore, the use of PR for advanced pancreatic cancer needs to be carefully evaluated.

Key Words: Pancreatic cancer • Quality of Life • Bypass surgery • Pancreaticoduodenectomy • PPPD • Whipple


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pancreatic cancer commonly presents at an advanced tumor stage, which is one of the many factors that contribute to its dismal prognosis. It is the fourth to sixth most common cause of cancer-related deaths in the USA and Europe,1 and the 5-year survival rate for all the tumor stages is barely 5%.2 As a consequence of its late diagnosis, resection rates with a curative intention rarely exceed 10%.3 Under these circumstances, the only option for the majority of patients is a palliative therapeutic regime focusing on extending their remaining lifetime and ensuring that they experience the best possible QoL. Surgery is important, to prevent and/or to treat obstruction of the biliary as well as the intestinal tract.4 Patients who receive biliary and gastric bypass surgery rarely require further operations or additional endoscopic treatment, which is usually associated with hospitalization prior to death.5

It has been suggested that palliative pancreaticoduodenectomy (leaving residual tumor behind) offers an adequate alternative to palliation through bypass surgery.6,7 Palliative resection (PR) is seen to combine the advantages of good palliation with prolonged patient survival, compared with the bypass procedure. This advantage is only achievable when the morbidity and mortality following a pancreaticoduodenectomy is low. Specialized referral centers have been shown to have mortality rates below 5% following this procedure.8 To date, very little valid data is available which compares PR with bypass surgery.9

For patients in a palliative setting, it is particularly important to focus not only on prolonging survival, but also on how patients perceive their QoL during their remaining lifespan. This study sought to compare the outcome of patients with adenocarcinoma undergoing double loop bypass (DLB) surgery with those undergoing palliative pancreaticoduodenectomy, with particular emphasis on their QoL post-surgery.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From January 1993 to September 2004, 167 patients with "curative" irresectable adenocarcinoma of the pancreatic head and neck were studied. Clinical outcome and survival, as well as QoL, both prior to and following surgery, were investigated. Data were collected prospectively and survival analyses were based on regular follow-up consultations with the family practitioner or with the patient.

This study was restricted to adenocarcinoma of the pancreatic head and all other histological entities were excluded. Pre-operative staging included a CT-scan or MRI-scan, usually supplemented with an endoluminal ultrasound (EUS). All patients with irresectable adenocarcinoma of the pancreatic head received a "prophylactic" DLB (gastrojejunostomy and hepaticojejunostomy), irrespective of whether there was either solely biliary or intestinal obstruction evident at the time of operation. The intention was to prevent further interventions as a result of secondary obstructions during the course of the disease.

Based on the intra-operative findings, patients were sub-grouped into those with locally advanced disease (LAD, n = 61; 47%; stage III) and those with metastasized disease (MD, n = 68; 53%; stage IV) (Fig. 1Go).


Figure 1
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  		FIG. 1. Composition of patient groups. LAD, locally advanced disease; MD, metastasized disease.

 
Patients who underwent DLB were compared with those who initially underwent resection of the pancreatic head, with a curative intention, either by the classic Whipple procedure, or by pylorus-preserving pancreaticoduodenectomy (PPPD). Due to advanced local growth, it was necessary to leave either microscopic or macroscopic residual tumor in place. Therefore, the procedure was classified as PR.

In the palliative resected group (PR) n = 29 (76.3%) of 38 patients received adjuvant palliative chemotherapy. In the bypass group (DLB), n = 101 (78.3%) of 129 patients received palliative chemotherapy.

Study Design/Assessment of Health-Related Quality of Life
The QoL assessment was initiated prior to surgery and completed at the 2-year follow-up. Due to the limited long-term survival and resulting small numbers of long-term QoL results, however, only analyses up to 6 months after surgery were compared between the groups. Patients were given questionnaires pre-operatively (baseline), before discharge, and 3, 6, 12, and 24 months after surgery. Informed consent for treatment and clinical study was routinely obtained from all patients prior to surgery. Study design was a prospective evaluation of all patients with a diagnosis of suspected pancreatic cancer.

Of the group of patients who were palliatively resected (n = 38), 13 completed QoL questionnaires. In the bypass surgery group, 77 patients took part in the QoL analysis. During the time observed, the patients completed in average 2.5 questionnaires as displayed in Table 1Go. Within the bypass group, 37 patients made up the LAD sub-group and 40 patients the metastasized disease (MD) sub-group (Fig. 1Go).


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  		TABLE 1. Compliance rates concerning completed QoL questionnaires
 
The EORTC QLQ-C30 Core Questionnaire and a disease-specific module were used to assess Health-Related QoL (HRQoL). The EORTC QLQ-C30 is a cancer-specific 30-item questionnaire.10 It incorporates five functional scales (physical, role, cognitive, emotional, and social), three symptom scales (fatigue, pain, and nausea and vomiting), a global health/ general QoL scale, a number of single items assessing additional symptoms commonly reported by cancer patients (dyspnea, loss of appetite, insomnia, constipation, and diarrhea), and the perceived financial impact of the disease. All EORTC QLQ-C30 items have response categories with four levels (from "not at all" to "very much") except the two items for overall physical condition and for overall QoL, which use seven-point response categories, ranging from "very poor" to "excellent". High scale scores present high response levels, with high functional scale scores representing high/healthy levels of functioning, and high scores for symptom scales (or items) representing high levels of symptomatology/problems.11

The pancreatic cancer module was developed by Kuechler et al.12 and consists of 24 items addressing pancreatic-cancer specific issues such as reduced efficiency, change of eating habits, icterus, weight loss, or treatment strain.13

The calculated QoL results were compared with those from a healthy, age-matched, German reference population published by Schwarz et al.14

Statistical Analysis
Data were analyzed using SPSS for Windows (Version 12.0, Chicago, IL). The results are presented as total numbers, percentages or the mean ± standard deviation (SD). All distribution and frequencies of medical data were compared using the Chi-square test. The EORTC QLQ-C30 core questionnaire and the pancreatic module scales were scored according to the EORTC-QLQ-C30 Scoring Manual: raw scores were transformed linearly, ranging from 0 to 100. All scales were calculated when at least half of the items were completed by the patients.11 Since the QoL data were not normally distributed, non-parametric methods were used in the statistical analysis. The Mann–Whitney U test was used to compare the QoL of the two groups (i.e., patients who underwent PR vs. those who underwent bypass surgery). The compliance rates for each time point are displayed in Table 2Go.


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  		TABLE 2. Compliance rates concerning completed QoL questionnaires for each time point
 
No missing data imputation was applied, but all available data were analyzed.15 Survival curves were calculated for patients using the Kaplan–Meier method. Differences in survival between relevant subgroups were analyzed using the log rank test.

A global P value of less than 0.05 was considered to be statistically significant, whereas a mean difference ≥10 points on the QoL scales was considered to be clinically significant/relevant.16


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The results of this study are presented in the following order: (1) procedure-associated morbidity and mortality as well as survival analysis; (2) a comparison of the QoL of the group of patients who underwent PR for pancreatic carcinoma with that of the patients who received DLB surgery; (3) a subgroup analysis, with respect to survival and QoL between locally advanced and metastasized disease in bypass surgery patients.

Sample and Procedure Description
Patient characteristics, operative specifications, procedure-associated complications, and in-hospital mortality rates are shown in Table 3Go. The two groups studied were comparable in terms of age and gender. Operative times (6.5 vs. 4.1 h for PR and DLB, respectively), procedure-associated complications and procedure-associated mortality were higher in the palliative resected group. Length of hospital stay and operative time were the only parameters which differed significantly, while PR showed a trend towards a higher rate of postoperative complications. In particular, the rate of pancreatic fistula (11% vs. 3%) and pulmonary complications (10% vs. 1%) were elevated in the patients who underwent resection. In addition, the operation-related mortality rate was higher in the resection group (7.8% vs. 2.6%), although the difference between the two groups was not statistically significant.


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  		TABLE 3. Patient, surgical procedure and complication characteristics
 
Procedure Description and Resectability
In the PR group some patients (n = 24; 63%) received a classic Whipple resection while others (n = 14; 37%) received a PPPD. In the bypass group all (n = 129) patients received a DLB; this involved a hepaticojejunostomy and a retrocolic gastrojejunostomy, and reconstruction of the intestinal passage by Roux-en-Y anastomosis. For the majority of patients, the residual macroscopic or microscopic tumor was located in the mesenteric root. In 18% of patients, infiltration of the superior mesenteric artery was proven by biopsy. Of the patients who underwent PR, 21% demonstrated residual retroperitoneal tumor and 37% advanced mesenteric and/or portal vein infiltration (Table 4Go).


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  		TABLE 4. Procedure description and tumor infiltration sites in palliative resected patients
 
In the group of patients who underwent the palliative bypass procedure, surgical exploration revealed either LAD or proven distant metastasis (Table 5Go).


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  		TABLE 5. Tumor infiltration site in patients with bypass surgery based on intra-operative findings
 
Survival
The number of months that patients who underwent palliative pancreaticoduodenectomy survived (median 7.0 months; CI 95% 4.09, 9.91) was slightly greater than that of the group who underwent bypass surgery (median 6.0 months; CI 95% 5.39, 6.61) (Fig. 2Go), although this difference was not statistically significant (Log rank: P = 0.192). Survival analyses between the bypass sub-groups are displayed in Fig. 3Go. The LAD- (median 7.0 months; CI 95% 4.67, 9.33) and MD-groups (median 5.0 months; CI 95% 4.30, 5.70), were both similar with respect to survival, although the MD-group showed a trend towards decreased survival compared with the LAD-group (Log rank: P = 0.094). One-year survival was 25% in the palliative resected group, as compared with 20% in the LAD-group and 15% in the MD group.


Figure 2
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  		FIG. 2. Actuarial Kaplan–Meier survival analysis of patients who underwent palliative pancreaticoduodenectomy (PD; n = 38) compared with patients who received double loop bypass surgery (DLB; n = 129). P = 0.192 (Log rank test).

 

Figure 3
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  		FIG. 3. Actuarial Kaplan–Meier survival analysis of patients who underwent DLB surgery, and were grouped into locally advanced disease (LAD; n = 61) and metastasized disease (MD; n = 68). P = 0.094 (Log rank test).

 
Quality of Life after Palliative Resection versus Bypass Surgery
Prior to surgery, there were only minor differences in QoL between the groups investigated. However, as seen in Fig. 4Go, the levels of QoL in the depicted scales were significantly worse than those of the age-matched reference population.14


Figure 4
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  		FIG. 4. Comparison of quality of life (QoL) after palliative resection (PR) compared with DLB surgery. The mean values of the corresponding items are displayed as columns and standard deviations are indicated as error bars. Statistical significant differences are indicated: *P = 0.045. QoL results of an age-matched reference group are indicated as a dotted line (only available for EORTC QLQ-C30 scales).

 
At discharge, the bypass group demonstrated better scores on the emotional and cognitive function scales relative to the palliative resected group (data not shown). However, patients in both groups estimated their global health status as fairly equal.

With respect to the symptom scales, diarrhea in particular was rated as more stressful in the palliative resected group (Fig. 4Go). Three months after surgery the differences in diarrhea symptoms increased between the groups and became statistically significant. Six months after surgery the differences in the symptom scales between the two groups leveled out, except in the case of diarrhea.

When the bypass group was divided into LAD-and MD-sub-groups, both groups performed equally until 3 months after surgery. Six months after surgery, pain (Fig. 5Go) and weight loss (data not shown) prevailed in the MD-subgroup (Fig. 5Go).


Figure 5
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  		FIG. 5. Comparison of QoL after DLB surgery for patients with LAD and metastasized disease (MD). The mean values of the corresponding items are displayed as columns and standard deviations are indicated as error bars. QoL results of an age-matched reference group are indicated as a dotted line (only available for EORTC QLQ-C30 scales).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Analysis of QoL in incurable patients is of major interest due to the fact that a major goal of palliative treatment is to ensure that these patients are as free as possible from complaints and subject to minimal levels of disease-related restrictions. Despite curative intention unresectable pancreatic cancer is a prime example for this incident.

In the late stage of this disease only a minority of patients are suitable for resection, and the potential of palliative radiochemotherapy to extend life expectancy is very limited.17 The biliary and intestinal obstruction experienced during the course of the disease can be successfully managed with endoscopy and surgery, although surgery seems to have a better long-term effect.18,19

Besides surgical bypass or endoscopic stenting procedures, some authors7 advocate palliative pancreaticoduodenectomy for the following reasons: (1) survival times are prolonged in comparison with those associated with bypass surgery; (2) it may improve the effects of additional palliative radiochemotherapy; (3) it may improve palliation by preventing either intestinal or biliary obstruction, and by improving pain control.6,7

This study found no statistically significant survival benefit in patients with locally advanced tumor undergoing PR. Although the median survival of the PR group was slightly superior to that of the bypass group, the difference was minimal when the subgroup of patients in the bypass group with LAD was compared with the palliative resected patients. Furthermore, one needs to take into account that all the patients who underwent PR were initially intended as "curative"/complete resection patients; only during the resection procedure did it become clear that they were unresectable and that residual tumor would have to be left in place. Therefore, in all likelihood, this group represents an earlier tumor stage than that represented by the bypass surgery group, a possibility which should be considered when interpreting the survival results.

As previous authors have noted,7 both the amount of time spent in hospital and the duration of the operation are greater for patients undergoing resection; this is likely to result in higher treatment costs and is probably synonymous with higher levels of discomfort during the prolonged hospital stay. This study confirms these observations, as the resection group experienced significantly longer hospital stays and operation times than the bypass group.

It is generally accepted that mortality rates following the Whipple procedure can be reduced below 5% and this has been demonstrated in many referral centers around the world,8,20,21 including our own.22 However, in this study, a mortality rate of 7.8% and a morbidity rate of 58% were observed in the palliative resected patients. Although the differences between the PR and DLB groups were not statistically significant, our results may indicate that PR is associated with an elevated peri-operative risk, and this needs to be taken into consideration. In contrast, the Johns Hopkins group, who are highly specialized in this field, reported a 1.6% in-hospital mortality rate in palliative resected patients.23 Whether this outcome can be generalized to other less specialized centers is an issue that needs to be discussed.

To date very few well-executed (e.g., using an adequate QoL questionnaire, prospective design, etc.) analyses of QoL after palliative pancreatic surgery have been reported.9,24 Previous studies, which include predominantly cross-sectional studies, have focused on pancreaticoduodenectomy with a curative intention.20,25,26 However, these studies contain no information on patients with PR. Whereas, especially in a palliative setting QoL is of major interest. Comparing the QoL of incurable patients with that of an age-matched healthy reference population demonstrates just how substantial a loss of QoL they suffer.15

Van Dijkum et al.9 compared patients who had undergone curative pancreaticoduodenectomy with those who had undergone palliative bypass surgery. Unsurprisingly, that author found that the palliatively treated patients performed worse with regard to QoL, as the two groups were in a different tumor stage and the treatment intention was different. A second study, by Van Heek et al., compared patients with peri-ampullary and pancreatic carcinoma after they had undergone either single or DLB surgery. Although the former group developed gastric outlet obstruction more often, both groups performed equally with respect to QoL. The QoL scores presented by that bypass group are comparable to the results obtained in the study presented here, since the same instrument was used to analyze QoL (i.e., the EORTC QLQ-C30).

In both the aforementioned studies, median survival times in the bypass surgery groups were longer (7.2–9.6 months) than those observed in this study (6.0 months). One possible explanation is that our study was restricted to patients with ductal adenocarcinoma of the pancreas and no other peri-ampullary entities. Such entities, known to be associated with better overall survival times, were included in the previously reported studies.

Quality of life in all the patients studied was shown to decrease following surgery. The bypass group was observed to recover to pre-operative levels of QoL within 3 months after surgery; however, this recovery was slightly delayed, in some cases by up to 6 months, in the palliative resected groups. This observation is comparable with the observations made in other longitudinal studies on QoL.27–29 The fact that in all groups QoL recovered to the preoperative level, despite the progression of the disease, may be explained by a so-called "response shift", where the patients are seen to adapt their standards and perceptions relative to their expectations.30

In summary, QoL in both the palliative resected group and the bypass group dropped for up to 3 months following surgery. Subsequently both groups recovered to preoperative levels, although in the short term, the speed of recovery of the palliative resected group was slightly lower than that of the bypass group. Furthermore, the palliative treated patients demonstrated a trend towards a higher rate of in-hospital mortality as well as an elevated rate of morbidity, whereas their survival rate was only slightly prolonged. Taking these data into consideration, the indication for intentional PR of pancreatic carcinoma of the pancreatic head should be considered carefully and needs to be justified for each individual case. The necessary assessment of perioperative risks also needs to encompass the individual surgeon’s experience in order to choose a therapeutic strategy which serves the patient’s best interests.

Received for publication June 5, 2006. Accepted for publication July 7, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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