PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of ijsurgspringer.comThis journalToc AlertsSubmit OnlineOpen Choicespringer.comThis journal
 
Indian J Surg. Feb 2012; 74(1): 79–86.
Published online Nov 24, 2011. doi:  10.1007/s12262-011-0373-8
PMCID: PMC3259176
Surgery for Pancreatic Carcinoma: State of the Art
Shailesh V. Shrikhandecorresponding author1 and Savio George Barreto2
1Department of GI and HPB Surgical Oncology, Tata Memorial Centre, Ernest Borges Marg, Parel, Mumbai, 400012 India
2Department of Surgery, Modbury Hospital, Modbury, South Australia Australia
Shailesh V. Shrikhande, Phone: +91-22-24177173, Fax: +91-22-24148114, shailushrikhande/at/hotmail.com, shailesh.shrikhande/at/pancreaticcancerindia.org.
corresponding authorCorresponding author.
Received November 10, 2011; Accepted November 10, 2011.
Abstract
Carcinoma of the pancreas remains a malignancy with a generally dismal outcome owing to the delayed presentation of the disease. To date, surgery affords the best outcomes when a complete resection can be achieved. Improvements in imaging, surgical techniques and adjuvant therapies are perceived advancements in the management of this cancer. This article reviews the latest evidence in terms of the diagnosis and management of pancreatic cancer.
Keywords: Pancreatic cancer, Pancreatoduodenectomy, Complications, Anastomosis, Lymphadenectomy, Extended resections
Pancreatic cancer (PC) remains a deadly disease with a dismal prognosis in which the mortality rate nearly equals its incidence. In USA, the incidence rate of PC is 8–10/100,000 persons per year with 43,140 new cases estimated to occur in 2010 [1]. The incidence of PC has remained fairly stable over the years [2]. The approximate annual burden of PC in India is 14,230 and the incidence of 2.4/100,000 persons per year is low compared with western statistics [3]. The 5-year relative survival rate was 4.1% for PC in a population-based study from Mumbai [4].
Despite advances in modern chemoradiotherapy, the best and only chance of cure for patients with PC is an oncological surgical resection aimed at complete removal of all gross and microscopic disease. Early disease and curative-intent surgery are the best predictors of outcome [5].
Codivilla was the first person to perform an en bloc excision of the head of the pancreas and a major portion of the duodenum for a patient suffering from pancreatic carcinoma [6]. Unfortunately, his patient died after 24 days of the surgery as a result of disseminated malignancy (confirmed on autopsy). To this day, the pancreatoduodenectomy (PD) or the Whipple’s operation [7] continues to be the operation of choice for carcinomas involving the head, neck and/or uncinate process of the pancreas. In patients with carcinoma of the body and tail, distal or subtotal pancreatectomies constitute optimal surgical therapy.
This article provides a brief overview of the presentation and diagnosis of pancreatic carcinoma while focusing on the current evidence on the technical aspects of surgery for PC.
Symptoms and timing of presentation of patients with carcinoma of the pancreas vary depending on the location of the carcinoma. Ampullary carcinomas tend to present the earliest owing to the early obstruction of the biliary tree and resultant painless obstructive jaundice. The classic symptom reported with carcinomas in this location is the ‘waxing and waning’ of obstructive jaundice—a symptom noted in only 30% of individuals [8].
Carcinomas of the pancreatic head also tend to present as painless, progressive, obstructive jaundice. Tumours of the body and tail, in contrast, tend to present the latest, usually as a clinically discernible swelling [9]. By this time, generally, haematogenous and lymphatic spread may have already taken place.
Most common presenting symptoms of carcinomas of the pancreatic head, neck, body and tail are asthenia (>80%), anorexia (>80%), weight loss (>80%) and upper abdominal pain (70–80%) [10]. Features suggestive of gastric outlet obstruction may be encountered in advanced carcinomas of the pancreas.
Upper abdominal pain radiating to the back, though not always, is often a sign of an advanced tumour. New symptoms developing over an established case of chronic pancreatitis should arouse suspicion of PC [10].
Clinical signs in these patients may vary from jaundice in ampullary and pancreatic head cancers with a palpable gallbladder (Courvoisier’s law) to a hard, fixed palpable lump in the left hypochondrium in case of tumours of the body and tail.
Patients may have enlarged Virchow’s lymph nodes or even a Blumer’s shelf in advanced cases. Ascites is a sign of advanced disease.
Investigations
Biochemical Tests
The tumour marker, serum CA 19–9, is routinely measured in pancreatic carcinomas. Its overall sensitivity is approximately 80% with a specificity of 90% [11]. In terms of predicting unresectability, levels greater than 1,000 U/mL have been found to be linked to unresectable disease [11].
An obstructive pattern of liver function tests is encountered in pancreatic head and ampullary lesions obstructing the lower common bile duct.
Anaemia (sometimes associated with waxing and waning jaundice) may be encountered in patients with periampullary carcinomas where repeated sloughing off of the tumour tissue causes episodes of melaena.
Radiology
Multidetector computed tomography (MDCT) and angiography scans and magnetic resonance imaging (MRI) along with magnetic resonance cholangiopancreatography (MRCP) have been demonstrated to provide the highest accuracy in terms of non-invasive imaging modalities to diagnose, stage and determine the vascular involvement by pancreatic carcinomas of the head (>3 cm) [1215], body and tail [16].
Other imaging modalities, such as positron emission tomography-computed tomography, have been shown to provide a complimentary role to MDCT and MRCP in the detection of extra-abdominal metastases [17]. Thus, they may play a crucial role in the preoperative work-up of locally advanced cancers, since the treatment options would sharply vary based on the positron emission tomography scan findings.
Nowadays, endoscopic retrograde cholangiopancreatography (ERCP) is hardly used as a diagnostic tool. It is now primarily used to aid histological/cytological confirmation of the presence of a periampullary cancer and head cancers, and its use is mainly therapeutic to enable preoperative biliary drainage.
In patients with ampullary or pancreatic head carcinomas with biliary obstruction, preoperative biliary stenting has been a practice [1820]. A recent meta-analysis [21] found that although the rate of wound infections were higher in patients who had undergone preoperative biliary drainage, there was no convincing evidence to indicate that biliary drainage prevented or promoted postoperative complications following PD. Preoperative biliary drainage is indicated in patients presenting acutely with cholangitis, obstructive jaundice with secondary renal impairment, or in whom delays in the performance of the PD due to co-morbidities or referral to specialist centres for surgery are anticipated.
If extended delays (>6 weeks) are anticipated between the stenting and PD, short-length self-expandable metal biliary stents [22, 23] should be considered.
Additionally, to better delineate the T stage of the tumour or the vascular involvement or to obtain tissue biopsies of the tumours of the head <3 cm or that of the body and tail, endoscopic ultrasonography (EUS) is the best modality available [24].
Diagnostic Laparoscopy and Laparoscopic Ultrasonography
The routine use of laparoscopy in the preoperative staging of periampullary cancer and PC is not recommended owing to the risk of complications associated with the procedure and the availability of state-of-the-art imaging in terms of MDCT and, MRI and MRCP [25]. However, in terms of the benefit in patients with locally advanced disease on imaging, the conclusion is unclear. A recent meta-analysis has concluded that it may be beneficial in downstaging patients deemed to be unresectable on imaging, rendering them as candidates for potentially curative resections [26].
Based on the staging of the pancreatic carcinoma by a combination of modalities, these tumours may be divided into the following groups in order of worsening prognosis [10, 27, 28]:
  • Resectable PC
  • Borderline resectable PC
  • Resectable locally advanced PC,
  • Non-resectable locally advanced PC,
  • Resectable but metastatic PC,
  • Non-resectable metastatic PC
Surgery offers the best outcome for tumours that are resectable, even those that are locally advanced so long as a complete resection (R0) can be achieved. Surgical resection for carcinoma of the head and/or neck of pancreas involves a PD, whereas a distal or subtotal pancreatectomy is performed for carcinomas of the body and tail and for some tumours at the junction of the neck and body.
Since the first PD performed by Codivilla [6], technical modifications have been undertaken in the procedure with an aim to improving outcomes for the patient. Only the most significant of these modifications will be discussed in this section. Despite the high morbidity and the risk of mortality associated with PD, centralization of major pancreatic resectional surgery to high-volume centres [2938] as well as a standardized technique [39, 40] have been linked to improved outcomes.
No difference in oncological outcomes has been noted between pylorus-preserving PD and the Classic Whipple [41]. As a result, in patients undergoing PD for periampullary and pancreatic head cancers, the performance of pylorus preservation or classic Whipple remains the prerogative of the surgeon. In contrast, the performance of the classic Whipple should be reserved exclusively for duodenal cancers (part of periampullary tumours) or large pancreatic head tumours invading the gastric antrum and/or the first part of duodenum.
As part of every oncological PD, a standard lymphadenectomy, i.e., removal of lymph nodes of the right side of the hepatoduodenal ligament (12b1, 12b1, 12c), posterior pancreaticoduodenal nodes (13a, 13b), nodes to the right side of the superior mesenteric artery (SMA) from the origin of the SMA at the aorta to the inferior pancreaticoduodenal artery (14a, 14b) and anterior pancreaticoduodenal nodes (17a, 17b), has been shown to be associated with improved outcomes with no additional benefit conferred by the performance of an extended lymphadenectomy [42, 43]. Additionally, the extended procedure was associated with an increased rate of intractable diarrhoea in the early postoperative phase.
Current literature [4448] does not favour the performance of a pancreaticojejunostomy over a pancreaticogastrostomy, as the outcomes of surgery appear to be the same irrespective of the technique employed.
Antecolic gastro-/duodenojejunostomy has been shown to be associated with a significantly reduced rate of delayed gastric emptying [4951], possibly due to the avoidance of torsion or angulation that may occur with a retrocolic anastomosis.
A review of the literature demonstrated that in order to improve outcomes of the anastomoses following PD, good vascularity, absence of tension, absence of main pancreatic ductal and distal obstruction, use of fine (4–0, 5–0, 6–0) sutures, main pancreatic duct to mucosa approximation and high volume (including high surgeon-volume) were important factors [52].
Distal/Subtotal Pancreatectomy
Brennan et al. [53] suggested an equally aggressive approach to PC when managing tumours of the body and tail of the pancreas. Current evidence supports the performance of a splenectomy along with a distal/subtotal pancreatectomy to attain a complete resection for carcinomas [54].
While the choice of closure of the pancreatic remnant has been a matter of debate, current evidence [55] concedes that although there is a trend towards the use of staplers [56], the available information cannot convincingly make a definite choice between sutures or staplers [57].
The term ‘extended resections’ encompasses numerous subclasses including, extended lymphadenectomy (discussed above), vascular resections, multivisceral resections and metastasectomies.
In the case of carcinomas of the body and tail, it has been observed that at the time of surgery approximately 35% of the patients [58] with tumours of the body and tail have evidence of involvement of surrounding structures either by tumour infiltration or inflammatory adhesions. In such circumstances, it is advisable to even resort to en bloc resections to obtain negative surgical margins. Shoup et al. [59] found that patients undergoing extended resections for the carcinomas of the pancreatic body and tail have long-term survival rates similar to those for patients undergoing standard resection for less aggressive tumours, and markedly improved long-term survival compared with those who are not considered resectable because of locally advanced disease.
Multivisceral Resections
Multivisceral resections are technically feasible and, based on the limited data available, these resections are associated with improved survival (5-year survival rates of 16–22%) [59, 60] as compared with no resection, and comparable survival to standard resections for lesions that do not involve adjacent organs when performed in high -volume centres with the necessary expertise [61]. Given the high morbidity and even mortality associated with these procedures, they should be performed only when the possibility of achieving R0 seems distinctly feasible.
More recently, an entity termed borderline-resectable tumour (BRT) has been proposed and its definition continues to evolve [28, 6264]. The National Comprehensive Cancer Network describes borderline-resectable pancreatic head (and body) cancer as tumour abutment of the SMA, severe unilateral superior mesenteric vein (SMV) or portal vein (PV) impingement, gastroduodenal artery encasement up to its origin from the hepatic artery, or colon and mesocolon invasion [62]. The ideal treatment of patients with BRTs needs to be established. The choice of management of these patients varies between neoadjuvant chemoradiotherapy [28] versus surgery at the first instance [27, 65]. Till further data is available, to dictate the benefit of each treatment strategy over the other, the management of the BRT remains controversial.
A meta-analysis on venous resections at the time of PD [66] failed to demonstrate any benefit in overall survival. Following this manuscript, there were publications [67, 68] indicating that if an R0 could be achieved, this could translate into improved outcomes (5-year survival rates of 23%) [67].
However, it must be pointed out that certain factors play a role in these outcomes [61], viz. (1) Depth of venous invasion [69]–Involvement of tunica media and intima was associated with poor outcomes even in a complete resection; and (2) Length of invasion [67]–Length of involvement more than 3 cm was associated with poor outcomes.
There is no data to support the performance of arterial resections at the time of surgery for PC [61].
The Uncinate-First Approach
The uncinate-first approach was specifically described in 2007 [70] and is similar to the approach described by Hackert et al. [71]. This approach seems to be more suitable for infiltration of the SMV or portal vein. The SMA-first approach seems to be suitable for infiltration of the arterial axis.
The SMA-First Approach
The operative technique of the SMA-first approach comprises of early dissection of the SMA (after ‘kocherization’ of the duodenum) along with the posterior pancreatic capsule. The potential advantage of this approach [7274] is that technical difficulties that may be encountered either due to tumour infiltration of the SMV, main PV or tumour proximity to the right side of the SMA can be handled right at the initial stages of the resection. This may also help in reducing the chances of margin-positive pancreatic head resections. Other reported advantages are improved lymph node yield by dissection of more lymph nodes along the right border of the SMV/main PV and SMA [7274]. Both these approaches aid in vascular resections, large uncinate process tumours and also in multivisceral resections (Fig. 1)
Fig. 1
Fig. 1
Intraoperative photograph of SMA-first approach for a borderline-resectable pancreatic head cancer. Primary resection and anastomosis of the SMV–portal vein have been performed. The SMA is looped with red tape
Pancreatic Resection in Metastatic Disease
Although technically feasible [75], there is no clear evidence to demonstrate an overall survival benefit of the performance of metastasectomy in patients with resectable PC [61, 76].
Although technically feasible, [7780], at present there is no high-level evidence to suggest that laparoscopic PD is equal or superior to open surgery in terms of overall survival. In the case of a complex procedure like PD, the appreciation that the morbidity of PD (pancreatic leak, haemorrhage, delayed gastric emptying) is not related to the length of the abdominal incision, but to the extensive nature of the actual intra-abdominal surgery [81] deserves due consideration.
Laparoscopic distal pancreatectomy has also been demonstrated to be technically feasible with acceptable perioperative outcomes [82]. The perceived short-term benefits of accelerated recovery have recently been questioned in a well-conducted trial looking at readmission rates [83]. The perceived benefit of reduced hospital stay appears to be completely offset by the high readmission rates following laparoscopic distal pancreatectomy. There is no long-term data demonstrating an improvement in survival of laparoscopic surgery over open surgery for carcinomas of the pancreas.
Fast-Track Protocols/Enhanced Recovery
Fast-track surgery (or enhanced recovery after surgery), an interdisciplinary, multimodal concept designed to accelerate postoperative recovery by combining various techniques used in the care of patients undergoing elective surgery has been trialed in patients undergoing pancreatic surgery [84]. Although the feasibility of such protocols has been demonstrated [85], conflicting evidence on the physiological mechanisms that contribute to accelerated patient recovery as well as certain safety issues associated with postoperative morbidity (higher overall complication rates) [86] have been flagged.
Chemotherapy plays an important role in the adjuvant setting for patients with margin-positive disease following surgical resection and for lymph node metastases.
For non-resectable pancreatic carcinomas–locally advanced or metastatic, neoadjuvant therapies including chemotherapy or a combination of chemotherapy and radiotherapy are being extensively used with an aim to either downstage the tumour, thereby rendering them amenable to surgical resection, or keeping tumour growth under control with an aim to prolonging life.
Salient features on the role of chemotherapy and radiotherapy in pancreatic carcinoma include the following:
  • Gemcitabine and 5-fluorouracil constitute the two most important chemotherapeutic drugs available in the treatment of pancreatic carcinomas [10]. The European Study Group for Pancreatic Cancer (ESPAC-3) trial confirmed the lack of benefit of gemcitabine over the current standard treatment regimen–5-fluorouracil/folinic acid in terms of overall survival in patients with completely resected PC [87].
  • There is little evidence to support the use of intraoperative radiotherapy either alone or in combination [10].
  • A recent meta-analysis has demonstrated improved 12-month survival rates in protocols utilizing gemcitabine and radiotherapy for locally advanced pancreatic carcinomas [88]. However, drug toxicity was noted to be higher.
  • In patients with metastatic PC but with a good performance status, a recent randomized controlled trial has demonstrated improved survival in patients randomized to receive a combination chemotherapy regimen consisting of oxaliplatin, irinotecan, fluorouracil and leucovorin (FOLFIRINOX) as compared with gemcitabine [89].
Newer imaging modalities have facilitated improved preoperative staging of carcinomas of the pancreas. This has enabled better identification of patients likely to benefit from surgical exploration, and thus, possibly, even reducing the number of non-resectable explorations. Surgery remains the modality of choice in achieving longer survival in patients with PC as long as a R0 can be achieved. Refinements in surgical techniques have helped improve perioperative outcomes. The role of laparoscopy remains experimental in the management of pancreatic carcinoma. The development of newer adjuvant and neoadjuvant therapies alone and in combination has witnessed a modest improvement in survival on the balance of increased risk of toxicity.
Acknowledgments
Conflict of interest None
1. Lee TY, Kim MH, Park H, Seo DW, Lee SK, Kim JS, et al. Utility of 18F-FDG PET/CT for differentiation of autoimmune pancreatitis with atypical pancreatic imaging findings from pancreatic cancer. AJR Am J Roentgenol. 2009;193(2):343–348. doi: 10.2214/AJR.08.2297. [PubMed] [Cross Ref]
2. Shaib YH, Davila JA, El-Serag HB. The epidemiology of pancreatic cancer in the United States: changes below the surface. Aliment Pharmacol Ther. 2006;24(1):87–94. doi: 10.1111/j.1365-2036.2006.02961.x. [PubMed] [Cross Ref]
3. Dhir V, Mohandas KM. Epidemiology of digestive tract cancers in India IV. Gall bladder and pancreas. Indian J Gastroenterol. 1999;18(1):24–28. [PubMed]
4. Yeole B, Kumar A. Population-based survival from cancers having a poor prognosis in Mumbai (Bombay), India. Asian Pac J Cancer Prev. 2004;5(2):175–182. [PubMed]
5. Shaib Y, Davila J, Naumann C, El-Serag H. The impact of curative intent surgery on the survival of pancreatic cancer patients: a U.S. population-based study. Am J Gastroenterol. 2007;102(7):1377–1382. doi: 10.1111/j.1572-0241.2007.01202.x. [PubMed] [Cross Ref]
6. Shukla P, Barreto S, Shrikhande S (2011) The evolution of pancreatoduodenectomy. Hepatogastroenterology [In press]
7. Whipple AO, Parsons WB, Mullins CR. Treatment of carcinoma of the ampulla of vater. Ann Surg. 1935;102(4):763–779. doi: 10.1097/00000658-193510000-00023. [PubMed] [Cross Ref]
8. Barreto S, Shukla P, Shrikhande S. Periampullary carcinoma. In: Shrikhande S, Friess H, Buechler M, editors. Surgery of pancreatic tumors. New Delhi: BI publications; 2007. pp. 206–215.
9. Barreto S, Shukla P, Shrikhande S. Tumors of the pancreatic body and tail. World J Oncol. 2010;1(2):52–65.
10. Shrikhande S, Barreto S, Shrikhande V (2011) Pancreatic cancer. In: Haribhakti S (ed) Clinical GI surgery [In press]
11. Steinberg W. The clinical utility of the CA 19–9 tumor-associated antigen. Am J Gastroenterol. 1990;85(4):350–355. [PubMed]
12. Fusari M, Maurea S, Imbriaco M, Mollica C, Avitabile G, Soscia F, et al. Comparison between multislice CT and MR imaging in the diagnostic evaluation of patients with pancreatic masses. Radiol Med. 2010;115(3):453–466. doi: 10.1007/s11547-010-0490-7. [PubMed] [Cross Ref]
13. Shukla PJ, Barreto SG, Kulkarni A, Nagarajan G, Fingerhut A. Vascular anomalies encountered during pancreatoduodenectomy: do they influence outcomes? Ann Surg Oncol. 2010;17(1):186–193. doi: 10.1245/s10434-009-0757-1. [PubMed] [Cross Ref]
14. Tapper EB, Martin D, Adsay NV, Kooby D, Kalb B, Sarmiento JM. An MRI-driven practice: a new perspective on MRI for the evaluation of adenocarcinoma of the head of the pancreas. J Gastrointest Surg. 2010;14(8):1292–1297. doi: 10.1007/s11605-010-1221-z. [PubMed] [Cross Ref]
15. Zhao WY, Luo M, Sun YW, Xu Q, Chen W, Zhao G, et al. Computed tomography in diagnosing vascular invasion in pancreatic and periampullary cancers: a systematic review and meta-analysis. Hepatobiliary Pancreat Dis Int. 2009;8(5):457–464. [PubMed]
16. Bipat S, Phoa SS, Delden OM, Bossuyt PM, Gouma DJ, Lameris JS, et al. Ultrasonography, computed tomography and magnetic resonance imaging for diagnosis and determining resectability of pancreatic adenocarcinoma: a meta-analysis. J Comput Assist Tomogr. 2005;29(4):438–445. doi: 10.1097/01.rct.0000164513.23407.b3. [PubMed] [Cross Ref]
17. Farma JM, Santillan AA, Melis M, Walters J, Belinc D, Chen DT, et al. PET/CT fusion scan enhances CT staging in patients with pancreatic neoplasms. Ann Surg Oncol. 2008;15(9):2465–2471. doi: 10.1245/s10434-008-9992-0. [PubMed] [Cross Ref]
18. Jagannath P, Dhir V, Shrikhande S, Shah RC, Mullerpatan P, Mohandas KM. Effect of preoperative biliary stenting on immediate outcome after pancreaticoduodenectomy. Br J Surg. 2005;92(3):356–361. doi: 10.1002/bjs.4864. [PubMed] [Cross Ref]
19. Sewnath ME, Birjmohun RS, Rauws EA, Huibregtse K, Obertop H, Gouma DJ. The effect of preoperative biliary drainage on postoperative complications after pancreaticoduodenectomy. J Am Coll Surg. 2001;192(6):726–734. doi: 10.1016/S1072-7515(01)00819-5. [PubMed] [Cross Ref]
20. Coates JM, Beal SH, Russo JE, Vanderveen KA, Chen SL, Bold RJ, et al. Negligible effect of selective preoperative biliary drainage on perioperative resuscitation, morbidity, and mortality in patients undergoing pancreaticoduodenectomy. Arch Surg. 2009;144(9):841–847. doi: 10.1001/archsurg.2009.152. [PubMed] [Cross Ref]
21. Velanovich V, Kheibek T, Khan M. Relationship of postoperative complications from preoperative biliary stents after pancreaticoduodenectomy. A new cohort analysis and meta-analysis of modern studies. JOP. 2009;10(1):24–29. [PubMed]
22. Mullen JT, Lee JH, Gomez HF, Ross WA, Fukami N, Wolff RA, et al. Pancreaticoduodenectomy after placement of endobiliary metal stents. J Gastrointest Surg. 2005;9(8):1094–1104. doi: 10.1016/j.gassur.2005.08.006. [PubMed] [Cross Ref]
23. Wasan SM, Ross WA, Staerkel GA, Lee JH. Use of expandable metallic biliary stents in resectable pancreatic cancer. Am J Gastroenterol. 2005;100(9):2056–2061. doi: 10.1111/j.1572-0241.2005.42031.x. [PubMed] [Cross Ref]
24. Soriano A, Castells A, Ayuso C, Ayuso JR, Caralt MT, Gines MA, et al. Preoperative staging and tumor resectability assessment of pancreatic cancer: prospective study comparing endoscopic ultrasonography, helical computed tomography, magnetic resonance imaging, and angiography. Am J Gastroenterol. 2004;99(3):492–501. doi: 10.1111/j.1572-0241.2004.04087.x. [PubMed] [Cross Ref]
25. Gaag N, Busch O, Bemelman W, Gouma D. Lapaproscopy in staging and assessment of hepatobiliary disease. In: Garden O, editor. A companion to specialist surgical practice: hepatobiliary and pancreatic surgery. Edinburgh: Elsevier; 2009. pp. 37–54.
26. Hariharan D, Constantinides VA, Froeling FE, Tekkis PP, Kocher HM. The role of laparoscopy and laparoscopic ultrasound in the preoperative staging of pancreatico-biliary cancers—a meta-analysis. Eur J Surg Oncol. 2010;36(10):941–948. doi: 10.1016/j.ejso.2010.05.015. [PubMed] [Cross Ref]
27. Shrikhande S, Arya S, Barreto S, Ingle S, D’souza M, Hawaldar R, et al. Borderline resectable pancreatic tumours: is there a need for further refinement of this stage? Hepatobiliary Pancreat Dis Int. 2011;10(3):319–324. [PubMed]
28. Varadhachary GR, Tamm EP, Abbruzzese JL, Xiong HQ, Crane CH, Wang H, et al. Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann Surg Oncol. 2006;13(8):1035–1046. doi: 10.1245/ASO.2006.08.011. [PubMed] [Cross Ref]
29. Balzano G, Zerbi A, Capretti G, Rocchetti S, Capitanio V, Carlo V. Effect of hospital volume on outcome of pancreaticoduodenectomy in Italy. Br J Surg. 2008;95(3):357–362. doi: 10.1002/bjs.5982. [PubMed] [Cross Ref]
30. Birkmeyer JD, Finlayson SR, Tosteson AN, Sharp SM, Warshaw AL, Fisher ES. Effect of hospital volume on in-hospital mortality with pancreaticoduodenectomy. Surgery. 1999;125(3):250256. doi: 10.1016/S0039-6060(99)70234-5. [PubMed] [Cross Ref]
31. Gordon TA, Bowman HM, Tielsch JM, Bass EB, Burleyson GP, Cameron JL. Statewide regionalization of pancreaticoduodenectomy and its effect on in-hospital mortality. Ann Surg. 1998;228(1):71–78. doi: 10.1097/00000658-199807000-00011. [PubMed] [Cross Ref]
32. Gouma DJ, Geenen RC, Gulik TM, Haan RJ, Wit LT, Busch OR, et al. Rates of complications and death after pancreaticoduodenectomy: risk factors and the impact of hospital volume. Ann Surg. 2000;232(6):786–795. doi: 10.1097/00000658-200012000-00007. [PubMed] [Cross Ref]
33. Lieberman MD, Kilburn H, Lindsey M, Brennan MF. Relation of perioperative deaths to hospital volume among patients undergoing pancreatic resection for malignancy. Ann Surg. 1995;222(5):638–645. doi: 10.1097/00000658-199511000-00006. [PubMed] [Cross Ref]
34. Nordback L, Parviainen M, Raty S, Kuivanen H, Sand J. Resection of the head of the pancreas in Finland: effects of hospital and surgeon on short-term and long-term results. Scand J Gastroenterol. 2002;37(12):1454–1460. doi: 10.1080/003655202762671350. [PubMed] [Cross Ref]
35. Shukla PJ, Barreto SG, Bedi M, Bheerappa N, Chaudhary A, Gandhi M, et al. Peri-operative outcomes for pancreatoduodenectomy in India: a multi-centric study. HPB (Oxford) 2009;11(8):638–644. doi: 10.1111/j.1477-2574.2009.00105.x. [PubMed] [Cross Ref]
36. Topal B, Sande S, Fieuws S, Penninckx F. Effect of centralization of pancreaticoduodenectomy on nationwide hospital mortality and length of stay. Br J Surg. 2007;94(11):1377–1381. doi: 10.1002/bjs.5861. [PubMed] [Cross Ref]
37. Heek NT, Kuhlmann KF, Scholten RJ, Castro SM, Busch OR, Gulik TM, et al. Hospital volume and mortality after pancreatic resection: a systematic review and an evaluation of intervention in the Netherlands. Ann Surg. 2005;242(6):781–788. doi: 10.1097/01.sla.0000188462.00249.36. [PubMed] [Cross Ref]
38. Shrikhande SV, D'Souza MA, Wente MN. Pancreaticoduodenectomy in India: how far are we from centralization? Pancreas. 2009;38(4):473–475. doi: 10.1097/MPA.0b013e31818d8e00. [PubMed] [Cross Ref]
39. Shrikhande SV, Barreto G, Shukla PJ. Pancreatic fistula after pancreaticoduodenectomy: the impact of a standardized technique of pancreaticojejunostomy. Langenbecks Arch Surg. 2008;393(1):87–91. doi: 10.1007/s00423-007-0221-2. [PubMed] [Cross Ref]
40. Barreto G, D'Souza MA, Shukla PJ, Shrikhande SV. The gray zone between postpancreaticoduodenectomy collections and pancreatic fistula. Pancreas. 2008;37(4):422–425. doi: 10.1097/MPA.0b013e318175ddd0. [PubMed] [Cross Ref]
41. Diener MK, Fitzmaurice C, Schwarzer G, Seiler CM, Antes G, Knaebel HP, et al. Pylorus-preserving pancreaticoduodenectomy (pp Whipple) versus pancreaticoduodenectomy (classic Whipple) for surgical treatment of periampullary and pancreatic carcinoma. Cochrane Database Syst Rev.5:CD006053. [PubMed]
42. Iqbal N, Lovegrove RE, Tilney HS, Abraham AT, Bhattacharya S, Tekkis PP, et al. A comparison of pancreaticoduodenectomy with extended pancreaticoduodenectomy: a meta-analysis of 1909 patients. Eur J Surg Oncol. 2009;35(1):79–86. doi: 10.1016/j.ejso.2008.01.002. [PubMed] [Cross Ref]
43. Michalski CW, Kleeff J, Wente MN, Diener MK, Buchler MW, Friess H. Systematic review and meta-analysis of standard and extended lymphadenectomy in pancreaticoduodenectomy for pancreatic cancer. Br J Surg. 2007;94(3):265–273. doi: 10.1002/bjs.5716. [PubMed] [Cross Ref]
44. McKay A, Mackenzie S, Sutherland FR, Bathe OF, Doig C, Dort J, et al. Meta-analysis of pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after pancreaticoduodenectomy. Br J Surg. 2006;93(8):929–936. doi: 10.1002/bjs.5407. [PubMed] [Cross Ref]
45. Wente MN, Shrikhande SV, Muller MW, Diener MK, Seiler CM, Friess H, et al. Pancreaticojejunostomy versus pancreaticogastrostomy: systematic review and meta-analysis. Am J Surg. 2007;193(2):171–183. doi: 10.1016/j.amjsurg.2006.10.010. [PubMed] [Cross Ref]
46. Bassi C, Falconi M, Molinari E, Salvia R, Butturini G, Sartori N, et al. Reconstruction by pancreaticojejunostomy versus pancreaticogastrostomy following pancreatectomy: results of a comparative study. Ann Surg. 2005;242(6):767–771. doi: 10.1097/01.sla.0000189124.47589.6d. [PubMed] [Cross Ref]
47. Duffas JP, Suc B, Msika S, Fourtanier G, Muscari F, Hay JM, et al. A controlled randomized multicenter trial of pancreatogastrostomy or pancreatojejunostomy after pancreatoduodenectomy. Am J Surg. 2005;189(6):720–729. doi: 10.1016/j.amjsurg.2005.03.015. [PubMed] [Cross Ref]
48. Yeo CJ, Cameron JL, Maher MM, Sauter PK, Zahurak ML, Talamini MA, et al. A prospective randomized trial of pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy. Ann Surg. 1995;222(4):580–588. [PubMed]
49. Chijiiwa K, Imamura N, Ohuchida J, Hiyoshi M, Nagano M, Otani K, 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(1):49–55. doi: 10.1007/s00534-008-0004-3. [PubMed] [Cross Ref]
50. Hartel M, Wente MN, Hinz U, Kleeff J, Wagner M, Muller MW, et al. Effect of antecolic reconstruction on delayed gastric emptying after the pylorus-preserving Whipple procedure. Arch Surg. 2005;140(11):1094–1099. doi: 10.1001/archsurg.140.11.1094. [PubMed] [Cross Ref]
51. Tani M, Terasawa H, Kawai M, Ina S, Hirono S, Uchiyama K, et al. Improvement of delayed gastric emptying in pylorus-preserving pancreaticoduodenectomy: results of a prospective, randomized, controlled trial. Ann Surg. 2006;243(3):316–320. doi: 10.1097/01.sla.0000201479.84934.ca. [PubMed] [Cross Ref]
52. Shrikhande SV, Qureshi SS, Rajneesh N, Shukla PJ. Pancreatic anastomoses after pancreaticoduodenectomy: do we need further studies? World J Surg. 2005;29(12):1642–1649. doi: 10.1007/s00268-005-0137-3. [PubMed] [Cross Ref]
53. Brennan MF, Moccia RD, Klimstra D. Management of adenocarcinoma of the body and tail of the pancreas. Ann Surg. 1996;223(5):506–511. doi: 10.1097/00000658-199605000-00006. [PubMed] [Cross Ref]
54. Shoup M, Brennan MF, McWhite K, Leung DH, Klimstra D, Conlon KC. The value of splenic preservation with distal pancreatectomy. Arch Surg. 2002;137(2):164–168. doi: 10.1001/archsurg.137.2.164. [PubMed] [Cross Ref]
55. Knaebel HP, Diener MK, Wente MN, Buchler MW, Seiler CM. Systematic review and meta-analysis of technique for closure of the pancreatic remnant after distal pancreatectomy. Br J Surg. 2005;92(5):539546. doi: 10.1002/bjs.5000. [PubMed] [Cross Ref]
56. D'Souza MA, Singh K, Hawaldar RV, Shukla PJ, Shrikhande SV. The vascular stapler in uncinate process division during pancreaticoduodenectomy: technical considerations and results. Dig Surg. 2010;27(3):175–181. doi: 10.1159/000264674. [PubMed] [Cross Ref]
57. Diener MK, Seiler CM, Rossion I, Kleeff J, Glanemann M, Butturini G, et al. Efficacy of stapler versus hand-sewn closure after distal pancreatectomy (DISPACT): a randomised, controlled multicentre trial. Lancet. 2011;377(9776):1514–1522. doi: 10.1016/S0140-6736(11)60237-7. [PubMed] [Cross Ref]
58. Christein JD, Kendrick ML, Iqbal CW, Nagorney DM, Farnell MB. Distal pancreatectomy for resectable adenocarcinoma of the body and tail of the pancreas. J Gastrointest Surg. 2005;9(7):922–927. doi: 10.1016/j.gassur.2005.04.008. [PubMed] [Cross Ref]
59. Shoup M, Conlon KC, Klimstra D, Brennan MF. Is extended resection for adenocarcinoma of the body or tail of the pancreas justified? J Gastrointest Surg. 2003;7(8):946–952. doi: 10.1016/j.gassur.2003.08.004. [PubMed] [Cross Ref]
60. Sasson AR, Hoffman JP, Ross EA, Kagan SA, Pingpank JF, Eisenberg BL. En bloc resection for locally advanced cancer of the pancreas: is it worthwhile? J Gastrointest Surg. 2002;6(2):147–157. doi: 10.1016/S1091-255X(01)00063-4. [PubMed] [Cross Ref]
61. Shrikhande SV, Barreto SG. Extended pancreatic resections and lymphadenectomy: an appraisal of the current evidence. World J Gastrointest Surg. 2010;2(2):39–46. doi: 10.4240/wjgs.v2.i2.39. [PMC free article] [PubMed] [Cross Ref]
62. National Comprehensive Cancer Network (NCCN) Practice guidelines for pancreatic cancer. . [cited]; Available from: http://www.nccn.org.2004.
63. Katz MH, Pisters PW, Evans DB, Sun CC, Lee JE, Fleming JB, et al. Borderline resectable pancreatic cancer: the importance of this emerging stage of disease. J Am Coll Surg. 2008;206(5):833–846. doi: 10.1016/j.jamcollsurg.2007.12.020. [PubMed] [Cross Ref]
64. Springett GM, Hoffe SE. Borderline resectable pancreatic cancer: on the edge of survival. Canc Contr. 2008;15(4):295–307. [PubMed]
65. Tucker ON, Rela M. Controversies in the management of borderline resectable proximal pancreatic adenocarcinoma with vascular involvement. HPB Surg. 2008;2008:839503. doi: 10.1155/2008/839503. [PMC free article] [PubMed] [Cross Ref]
66. Siriwardana HP, Siriwardena AK. Systematic review of outcome of synchronous portal-superior mesenteric vein resection during pancreatectomy for cancer. Br J Surg. 2006;93(6):662–673. doi: 10.1002/bjs.5368. [PubMed] [Cross Ref]
67. Kaneoka Y, Yamaguchi A, Isogai M. Portal or superior mesenteric vein resection for pancreatic head adenocarcinoma: prognostic value of the length of venous resection. Surgery. 2009;145(4):417–425. doi: 10.1016/j.surg.2008.12.009. [PubMed] [Cross Ref]
68. Toomey P, Hernandez J, Morton C, Duce L, Farrior T, Villadolid D, et al. Resection of portovenous structures to obtain microscopically negative margins during pancreaticoduodenectomy for pancreatic adenocarcinoma is worthwhile. Am Surg. 2009;75(9):804–809. [PubMed]
69. Fukuda S, Oussoultzoglou E, Bachellier P, Rosso E, Nakano H, Audet M, et al. Significance of the depth of portal vein wall invasion after curative resection for pancreatic adenocarcinoma. Arch Surg. 2007;142(2):172–179. doi: 10.1001/archsurg.142.2.172. [PubMed] [Cross Ref]
70. Shukla PJ, Barreto G, Pandey D, Kanitkar G, Nadkarni MS, Neve R, et al. Modification in the technique of pancreaticoduodenectomy: supracolic division of jejunum to facilitate uncinate process dissection. Hepatogastroenterology. 2007;54(78):1728–1730. [PubMed]
71. Hackert T, Werner J, Weitz J, Schmidt J, Buchler MW. Uncinate process first—a novel approach for pancreatic head resection. Langenbecks Arch Surg. 2010;395(8):1161–1164. doi: 10.1007/s00423-010-0663-9. [PubMed] [Cross Ref]
72. Pessaux P, Regenet N, Arnaud JP. Resection of the retroportal pancreatic lamina during a cephalic pancreaticoduodenectomy: first dissection of the superior mesenteric artery. Ann Chir. 2003;128(9):633–636. doi: 10.1016/j.anchir.2003.10.010. [PubMed] [Cross Ref]
73. Pessaux P, Varma D, Arnaud JP. Pancreaticoduodenectomy: superior mesenteric artery first approach. J Gastrointest Surg. 2006;10(4):607–611. doi: 10.1016/j.gassur.2005.05.001. [PubMed] [Cross Ref]
74. Popescu I, David L, Dumitra AM, Dorobantu B. The posterior approach in pancreaticoduodenectomy: preliminary results. Hepatogastroenterology. 2007;54(75):921–926. [PubMed]
75. Shrikhande SV, Kleeff J, Reiser C, Weitz J, Hinz U, Esposito I, et al. Pancreatic resection for M1 pancreatic ductal adenocarcinoma. Ann Surg Oncol. 2007;14(1):118–127. doi: 10.1245/s10434-006-9131-8. [PubMed] [Cross Ref]
76. Michalski CW, Erkan M, Huser N, Muller MW, Hartel M, Friess H, et al. Resection of primary pancreatic cancer and liver metastasis: a systematic review. Dig Surg. 2008;25(6):473–480. doi: 10.1159/000184739. [PubMed] [Cross Ref]
77. Kendrick ML, Cusati D. Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch Surg. 2010;145(1):19–23. doi: 10.1001/archsurg.2009.243. [PubMed] [Cross Ref]
78. Palanivelu C, Rajan PS, Rangarajan M, Vaithiswaran V, Senthilnathan P, Parthasarathi R, et al. Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary Pancreat Surg. 2009;16(6):731–740. doi: 10.1007/s00534-009-0157-8. [PubMed] [Cross Ref]
79. Ammori BJ. Laparoscopic hand-assisted pancreaticoduodenectomy: initial UK experience. Surg Endosc. 2004;18(4):717–718. doi: 10.1007/s00464-003-4268-z. [PubMed] [Cross Ref]
80. Staudacher C, Orsenigo E, Baccari P, Palo S, Crippa S. Laparoscopic assisted duodenopancreatectomy. Surg Endosc. 2005;19(3):352–356. doi: 10.1007/s00464-004-9055-y. [PubMed] [Cross Ref]
81. Shrikhande SV, Barreto SG, Shukla PJ. Laparoscopy in pancreatic tumors. J Minim Access Surg. 2007;3(2):47–51. doi: 10.4103/0972-9941.33272. [PMC free article] [PubMed] [Cross Ref]
82. Kooby DA, Chu CK. Laparoscopic management of pancreatic malignancies. Surg Clin North Am. 2010;90(2):427–446. doi: 10.1016/j.suc.2009.12.011. [PubMed] [Cross Ref]
83. Baker MS, Bentrem DJ, Ujiki MB, Stocker S, Talamonti MS. Adding days spent in readmission to the initial postoperative length of stay limits the perceived benefit of laparoscopic distal pancreatectomy when compared with open distal pancreatectomy. Am J Surg. 2011;201(3):295–299. doi: 10.1016/j.amjsurg.2010.09.014. [PubMed] [Cross Ref]
84. Wilmore DW, Kehlet H. Management of patients in fast track surgery. BMJ. 2001;322(7284):473–476. doi: 10.1136/bmj.322.7284.473. [PMC free article] [PubMed] [Cross Ref]
85. Berberat PO, Ingold H, Gulbinas A, Kleeff J, Muller MW, Gutt C, et al. Fast track–different implications in pancreatic surgery. J Gastrointest Surg. 2007;11(7):880–887. doi: 10.1007/s11605-007-0167-2. [PubMed] [Cross Ref]
86. Ypsilantis E, Praseedom RK. Current status of fast-track recovery pathways in pancreatic surgery. JOP. 2009;10(6):646–650. [PubMed]
87. Neoptolemos JP, Stocken DD, Bassi C, Ghaneh P, Cunningham D, Goldstein D, et al. Adjuvant chemotherapy with fluorouracil plus folinic acid vs. gemcitabine following pancreatic cancer resection: a randomized controlled trial. JAMA. 2010;304(10):1073–1081. doi: 10.1001/jama.2010.1275. [PubMed] [Cross Ref]
88. Zhu CP, Shi J, Chen YX, Xie WF, Lin Y. Gemcitabine in the chemoradiotherapy for locally advanced pancreatic cancer: a meta-analysis. Radiother Oncol. 2011;99(2):108–113. doi: 10.1016/j.radonc.2011.04.001. [PubMed] [Cross Ref]
89. Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364(19):1817–1825. doi: 10.1056/NEJMoa1011923. [PubMed] [Cross Ref]
Articles from The Indian Journal of Surgery are provided here courtesy of
Springer