A selective approach to the surgical management of periampullary cancer patients and its outcome

Omar J Shah, Irfan Robbani, Parveen Shah, Sadaf A Bangri, Irfan J Khan, Mohammad Y Bhat and Manmohan Singh

Kashmir, India

A selective approach to the surgical management of periampullary cancer patients and its outcome

Omar J Shah, Irfan Robbani, Parveen Shah, Sadaf A Bangri, Irfan J Khan, Mohammad Y Bhat and Manmohan Singh

Kashmir, India

BACKGROUND:Pancreaticoduodenectomy is a high risk, complex, technically challenging operation associated with significant perioperative morbidity and mortality. This study on the surgical management of periampullary cancer patients is based on our experience in a period of nearly 13 years.

METHODS:The study was conducted on two groups of patients: group A included 42 patients who were treated between January 2000 and September 2005 and group B included 134 patients who were treated between October 2005 to October 2012. Preoperative, intraoperative and postoperative details of all these patients were collected, tabulated and analyzed to assess the impact of the selective approach introduced in the department with effect from October 2005.

RESULTS:Intraoperative details revealed highly significant differences in the management of the two groups of patients in respect of operative time (250.4 vs 126.6 minutes;P＜0.001), operative blood loss (1070.2 vs 414.9 mL;P＜0.001) and intraoperative blood transfusion (1.4 vs 0.2 units;P＜0.001). Variations between the two groups in the frequency of complications were found to be statistically insignificant. However, the difference between the two groups in the overall morbidity of patients (47.6% vs 26.1%;P=0.009) and the length of their hospital stay (11.8 vs 7.8 days;P＜0.001) were significant.CONCLUSION:A selective approach applied to the surgical management of periampullary cancer patients is a step in the right direction.

(Hepatobiliary Pancreat Dis Int 2014;13:628-633)

pancreaticoduodenectomy;

superior approach technique;

Whipple's operation

Introduction

Pancreaticoduodenectomy (PD) is the only effective surgical option available for the management of pancreatic and periampullary malignancy although it is considered a high risk surgical procedure with considerable postoperative morbidity and mortality. Given the limited number of long-term survivors among PD patients, it is imperative that its postoperative morbidity and mortality was reduced to the extent possible. In this connection, the empirical relationship established by Luft and colleagues[1]and another study[2]between higher surgical volume and lower postoperative mortality holds promise.

With this end in view, it was in October 2005 that the Department of Surgical Gastroenterology was created within the surgical division of Sher-i-Kashmir Institute of Medical Sciences (SKIMS) in the Indian valley of Kashmir. And a team of skilled and experienced hepatopancreato-biliary surgeons was constituted out of the in-service manpower of the surgical division of SKIMS and entrusted with responsibility of establishing and organizing the Department of Surgical Gastroenterology on modern lines for extending tertiary care services to deserving patients and in the process growing into a high volume center registering a declining postoperative morbidity and mortality trend.

Methods

The patients of periampullary cancer who had undergone PD in SKIMS before and after the creation of the Department of Surgical Gastroenterologyconstituted the material for this study. To study the impact of selective approach introduced by the department after October 2005, all the patients that were treated between January 2000 and September 2005 were included in group A and the rest who were treated between October 2005 and October 2012 in group B. To facilitate objective assessment of the treatment modalities applied to the two groups of patients, all the necessary information was retrieved from the records section of the department. The information consisted of preoperative, intraoperative and postoperative details of patients. This information was analyzed and tabulated to facilitate a comparative assessment of the kind of treatment received by the two groups as also the outcome of the selective treatment extended to group B patients. Group A consisted of 42 patients and group B 134; 26 patients in group A were treated by classical Whipple's procedure and the remaining 16 patients were subjected to classical pylorus preserving pancreaticoduodenostomy (PPPD) procedure. In group A, pancreaticojejunostomy was performed by duct to mucosa (38 patients) or invagination (4 patients) method; end to side gastrojejunostomy was performed in a retrocolic or antecolic fashion. All the patients in group B were treated by a single team with a modified PPPD approach, developed by our group and here referred to as the superior approach technique.[3]This technique involves early ligation and division of gastroduodenal and the inferior pancreaticoduodenal arteries.

In group B, pancreaticojejunal anastomosis was carried out by invagination method in all patients. No pancreatic stent was used; after end to side hepaticojejunostomy, an antecolic duodenojejunostomy was carried out. Bedsides duodenojejunal anastomosis, pyloric dilatation was performed by metal sizers of 28-34 mm in diameter.

Five patients who had two staged PD were excluded from the study; no patient received prophylactic octreotide or neoadjuvant therapy. None of the patients underwent extended lymphadenectomy or portal vein resection. Postoperative complications were classified as per Clavien and Dindo criteria.[4,5]Accordingly a postoperative pancreatic fistula was defined as a drain output of a measurable volume of fluid appearing on or after the third postoperative day, with amylase content three times greater than the serum amylase level. Pancreatic fistulas were graded as A, B and C as per the International Study Group of Pancreatic Fistula (ISGPF).[6]Delayed gastric emptying was pronounced where there was a need for a nasogastric tube for 3 days or a need for its reinsertion after the third postoperative day or the patient was unable to tolerate solid food after the seventh postoperative day.[7]

Mortality and morbidity rates were computed on the basis of deaths and complications occurring within 30 days of surgery. Post discharge follow-up schedule of patients comprised three monthly clinic reviews in the first two years, half yearly reviews in the subsequent three years and yearly follow-up visits thereafter. All statistical tests were performed with statistical software (SPSS version 16) including the independent t test for continuous variables and the Chi-square test and Fisher's exact test for categorical variables. Univariate analysis was made with and without Yate's continuity correction. P value of ＜0.05 was considered statistically significant.

Results

The age and gender distribution of patients in both groups was similar. There were 25 male and 17 female patients in group A and 79 male and 55 female patients in group B. The age of patients ranged between 42 and 83 years in group A and between 40 and 83 years in group B. The mean age of patients was 62.3 years in group A and 60.7 years in group B. All these differences were statistically insignificant. The preoperative profile of patients is presented in Table 1. This table gives information on the distribution of various types of periampullary adenocarcinoma between the two groups, their American Society for Anesthesiologists (ASA)risk scores, and their co-existing medical conditions. Obviously, the two groups of patients are similar in all respects and well-matched; minor variations, if any, are statistically insignificant. It may be added here that the mean preoperative levels of hemoglobin and albumin were 9.7 mg/dL and 3.3 mg/dL in group A and 9.6 mg/dL and 3.4 mg/dL in group B, respectively. Biliary stenting was performed in 6 patients in group A and 15 patients in group B.

Intraoperative details of patients relating to operative time, operative blood loss, intraoperative blood transfusion and the diameter of the pancreatic duct are presented in Table 2. All these differences between the two groups were statistically highly significant (P＜0.001). The intergroup differences in the texture of the affected pancreatic tissue and the diameter of pancreatic ducts at their neck levels were statistically insignificant (Table 3).

The postoperative complications in the two groups of patients including delayed gastric emptying, infection at the surgical site and the appearance of pancreatic fistulas, bile leak, intra-abdominal bleeding, abdominal abscess, respiratory tract infection and cardiovascular disturbance are given in Table 4. The majority of types of complications in both groups were similar and the variations between the two groups were found to be statistically insignificant. However the overall morbidity in group B was found statistically significant when compared with group A (26.1% vs 47.6%;P=0.009). The length of hospital stay ranged between 9-23 days in group A and between 6-17 days in group B patients. The differences in the rate of overall morbidity and the length of hospital stay were statistically significant. Univariate analysis of factors associated with complications revealed that operative time, operative blood loss and requirement of blood transfusion were statistically significant (Table 5).

Table 2.Intraoperative profile

Table 3.Particulars of affected pancreas (n, %)

Table 4.Postoperative profile (n, %)

Table 5.Univariate analysis of factors associated with complications between the two groups

Discussion

Despite a history of more than 100 years, PD remains a formidable and lengthy procedure with substantial risks. Although the mortality rate related to this operation has dramatically reduced from more than 20% in the 1970s to less than 3% at present, the morbidity has remained relatively consistent at approximately 40%.[8-10]PD continues to remain associated with challenging postoperative complications. Among these, delayed gastric emptying known to occur in 15%-45% of patients after PPPD is a frustrating problem usually faced by surgeons.[11,12]The factors responsible for this complication are multiple and include postoperative sepsis, appearance of biliary or pancreatic fistulas, decreased plasma motilin concentration and the nature of surgical procedure applied to patients.[13]The denervation and devascularization of the pylorus during PD can lead to pylorospasm which can delay gastric emptying. However, if pyloric dilatation is performed during surgery, it can temporarily weaken the grip of pyloric muscle and allow smooth passage of food during the postoperative period.[14]Manes et al[15]reported a decrease in the incidence of delayed gastric emptying with pyloric dilatation. Antecolic duodenojejunostomy facilitates increased mobility of the stomach and provides an anatomical barrier against the pancreas.

Encouraging results have been achieved in this direction as reflected in several reports. In our study, the frequency of postoperative complications was not materially different between the two groups of patients except for postoperative morbidity rate and the length of hospital stay of patients; both of which were significantly less among group B patients. The steady improvement shown by our team in the management of patients with periampullary cancer is due to several factors, the most important being our switch over from the classical PPPD operation to a modified PPPD technique referred to as a superior approach technique. This technique was developed and standardized by our department after October 2005. Other factors contributing to improved performance are dedication and commitment of our surgical and supportive staff as also our adherence to a standardized patient management protocol. This is in tandem with the global phenomenon of growing subspecialty based surgical practice, regionalization of apical surgical care and establishment of high volume centers in response to increasing patient volumes. Birkmeyer and colleagues[16]demonstrated the relationship between hospital volume and surgical mortality for complex surgical procedures including PD which has been confirmed several times with reported mortality rates of less than 4% in high volume centers versus over 12% in low volume centers.[16-18]High volume centers offer high quality patient care through specially trained and technically competent surgeons using advanced technology in the preoperative, intraoperative and postoperative settings with commendable results. In high volume centers, increasing surgeon frequency is directly related to increasing hospital volume. More recent analyses of the volume-outcome relationship have shown that surgeon characteristics and system resources, not merely hospital volume, are the underlying factors that determine the outcome and are more likely to be present at a high volume center.[19,20]It seems that both hospital volume and surgeon volume interact synergistically towards an improved outcome.

Greater surgeon frequency or experience has been shown to be associated with shorter length of stay, lower patient morbidity and mortality and of course decreased hospital charges.[21,22]These factors are independent of hospital volume; experience of surgeons determines the quality of patient outcome. According to Schmidt et al,[23]surgeons with less experience (less than 50 PDs) perform with more complications, more operative blood loss and more operative time than those with more experience (more than 50 PDs). Kennedy et al[24]reported that surgeons with 10 or more PDs experience per year performed much better in terms of morbidity than surgeons with less experience.

A US study covering 39 hospitals has classified hospitals into 3 categories on the basis of their frequency of PD operations and their associated mortality. According to this classification a hospital conducting more than 20 PD cases per year with a mortality of 2.2% is a high volume center; a hospital conducting 6-20 PD cases per year with a mortality of 12% is a medium volume center; and a hospital conducting 1-5 cases of PD per year with a mortality of 19% is a low volume center.[25]As per to this classification, by performing 15 PD operations per year, our department falls in the category of medium volume centers; and by having a mortality rate of 1.1%, it excels even the performance of a high volume center.[26,27]

By introducing a modified technique of PD, our team has succeeded in reducing intraoperative blood loss in diminishing intraoperative blood transfusion requirement and in shortening the operative time undertaken. All these differences between the two groups were highly significant. Nevertheless, the experience and competence of operating surgeons and the role of non-technical skills in the management of patients cannot be underestimated. Lack of team work,[28]lack of decision making[29]and behavior failure[30]rather thandeficiency in technical experience are being reported as contributing positively to poor surgical outcome. These intangible non-technical factors are regarded as important, and sometimes even more important, in ensuring optimum surgical outcome. We feel that dedication and commitment of surgical team are equally desirable attributes that can contribute to better performance.

It is clear, therefore, that subspecialization of surgical services and regionalization of care reserving complex surgical procedures for distinct centers improve the outcome of PD and reduce the associated morbidity and mortality of patients. These centers should excel in the quality of team work, intensive care management and interventional radiology support. This will ensure selective surgical approach to the patients suffering from periampullary cancer.

Acknowledgement:We thank Rayees A Dar, Statistician SKIMS, who performed statistical analysis for this paper.

Contributors:SOJ proposed the study. SOJ, RI and KIJ performed research and wrote the first draft. SP, BSA, BMY and SM collected and analyzed the data. All authors contributed to the design and interpretation of the study and to further drafts. SOJ is the guarantor.

Funding:None.

Ethical approval:The study is approved by the Institutional Ethical Board.

Competing interest:No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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Received July 10, 2013

Accepted after revision March 31, 2014

Author Affiliations: Departments of Surgical Gastroenterology (Shah OJ, Bangri SA, Khan IJ, Bhat MY and Singh M), Radiodiagnosis & Imaging (Robbani I) and Pathology (Shah P), Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India

Omar J Shah, MD, Department of Surgical Gastroenterology, Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India (Tel: +91-0194-2463774; Fax: +91-0194-2471898; Email: omarjshah@yahoo.com)

? 2014, Hepatobiliary Pancreat Dis Int. All rights reserved.

10.1016/S1499-3872(14)60262-9

Published online May 29, 2014.