Pancreaticoduodenectomy with early superior mesenteric artery dissection

Yu-Fei Xu, Zuo-Jin Liu and Jian-Ping Gong

Chongqing, China

Pancreaticoduodenectomy with early superior mesenteric artery dissection

Yu-Fei Xu, Zuo-Jin Liu and Jian-Ping Gong

Chongqing, China

BACKGROUND:Pancreatic adenocarcinoma remains the fourth leading cause of cancer-related death and is one of the most aggressive human tumors. At present, surgical resection is the only potentially curative treatment. Early neck division is inadequate when invasion of the superior mesenteric artery (SMA) is suspected or in cases of replaced or accessory right hepatic artery. Malignant periampullary tumors often invade retroperitoneal peripancreatic tissues and a positive resection margin is associated with a poor long-term survival.

DATA SOURCES:English-language medical databases, PubMed, ELSEVIER and SPRINGERLINK, were searched for articles on "posterior approach pancreaticoduodenectomy", "superior mesenteric artery first approach", "retroperitoneal tissue", "hanging maneuver", and related topics.

RESULTS:The modification allowed the surgeon to early identify the nonresectability of a replaced right hepatic artery if present, enabling complete dissection of the right side of the SMA and portal vein as well as complete excision of the retroportal pancreatic lamina.

CONCLUSION:Pancreaticoduodenectomy with early retropancreatic dissection is a useful and safe technical variant, which is indicated for the improvement of the safety and curative effect of the procedure.

(Hepatobiliary Pancreat Dis Int 2010; 9: 579-583)

pancreaticoduodenectomy; superior mesenteric artery; retroperitoneal peripancreatic tissue; hanging maneuver

Introduction

Pancreaticoduodenectomy (PD) is considered a complex operative technique for the treatment of periampullary and pancreatic head tumors. Malignant periampullary tumors often invade retroperitoneal peripancreatic tissues, and a microscopic positive resection margin following PD is associated with a poor survival of patients.[1-3]Therefore, PD for a curative purpose should include complete clearance of peripancreatic retroperitoneal tissue, which is the most difficult and least codified step of PD with a high risk of intraoperative bleeding. We describe a new technique of PD.

PD with early retropancreatic dissection is one of the modifications of standard PD, and the procedure is focused on early dissection of the posterior pancreatic capsule and first dissection of the superior mesenteric artery (SMA).[4-8]The posterior part of the pancreatic head is dissected off the mesenteric vessels without dividing the pancreatic neck. The technique allows standardization and a complete resection of the retroperitoneal tissue, along with optimal control of bleeding.

Technique

The abdomen was explored through a bilateral subcostal incision. Upon opening the abdomen, a thorough and systematic exploration was performed to search for any evidence of tumor dissemination. A resection procedure is contraindicated in cases of liver metastases or peritoneal carcinomatosis. Routine biopsy of apparently normal regional lymph nodes is unnecessary, but suspicious lesions and enlarged lymph nodes outside the planned field of dissection should be biopsied and examined by frozen section and the resection is abandoned if positive for metastatic cancer. Positive lymph nodes within the planned field of resection are not considered a contraindication to PD.

The pancreas was exposed widely by incisingthe attachment of the transverse mesocolon to the right perinephric area. This mobilization was carried farther left by incising the omental attachment to the mesocolon along the avascular line. The transverse mesocolon was brought down completely to expose the superior mesenteric vessels where they lie anterior to the third part of the duodenum.

The duodenum was mobilized with an extensive Kocher maneuver which was accomplished by incising the posterior peritoneum superiorly from the inferior border of the Winslow foramen, and continuing downward along the posterior plane to the Treitz fascia in order to include all tissues covering the inferior vena cava and left renal vein. The Kocher maneuver was extended to the left border of the aorta, allowing a good exposure of the aorto-caval area. Lymphadenectomy of the inter-aorto-caval space was performed for frozen section examination. The presence of inter-aorto-caval lymph node metastases constitutes a contraindication to PD.[9-11]If any of these lymph nodes are positive, resection is abandoned.[12]

Dissection of SMA

The origin of the SMA was exposed at the point where the left renal vein crosses the aorta. The SMA was dissected along the plane of its adventitia to the junction of the third and fourth parts of the duodenum with a right-angled dissector. At a point 1-2 cm from the origin of the SMA, a replaced right hepatic artery can be identified. If present, this vessel was looped and safeguarded. If the tumor invaded the SMA, resection was abandoned at this stage and palliative measures were taken. A smooth right-angle dissector was passed along the SMA from its origin on the aorta to its emergence in the mesentery. A tape was grasped with the dissector and passed around the retroperitoneal peripancreatic tissue. At this time, the assistant lifted the tape upward, exposing the retro-portal lamina, and facilitating dissection of the retroperitoneal peripancreatic tissue from the SMA (Fig.). Bleeding was easily controlled by further lifting of the tape, leaving both of the surgeon's hands free for selective and definitive hemostasis with fine sutures.[4]

Dissection of hepatoduodenal ligament

After cholecystectomy, the bile duct was dissected along with the surrounding lymphatics and loose areolar tissue, and the bile duct was divided at the level of insertion of the cystic duct. This exposed the portal vein in the hepatoduodenal ligament. The portal vein was traced down to the level of the neck of the pancreas by ligating and dividing the areolar tissues surrounding it. This completely exposed the suprapancreatic portal vein. The hepatic artery lymph node was identified, and it was excised to identify the common hepatic artery in the suprapancreatic area. This vessel was traced distally along its course, and the gastroduodenal artery was identified at the point where the hepatic artery turns up toward the liver. The gastroduodenal artery was ligated in continuity and divided. The stump was suture ligated for additional protection. Now, further dissection of the posterolateral aspect of the portal vein in the region of the pancreas was carried out.

Dissection of the uncinate process and neck of the pancreas

The superior dissection of the portal vein up to the superior border of the pancreas was continued downward. At this stage, the posterior walls of the portal vein and superior mesenteric vein (SMV) were exposed and venous invasion was easily recognized. In this case, the neck of the pancreas was divided using a surgical blade leaving the specimen attached to the portal vein only. Venous resection was achieved with a short clamping time and reconstructed with an end-toend manner without any graft. In the absence of venous invasion, the posterolateral aspect of the portal vein was carefully dissected with a right-angled dissector. During this phase of dissection, the tributaries of theportal vein to the head of the pancreas were ligated and divided. Once these veins were divided and the loose areolar tissue around the portal vein was divided using electrocautery, the posterior aspect of the pancreas was exposed. This was easily separated from the portal vein as this plane is avascular and does not contain any important structures. This dissection was carried out a little more to the left until the splenoportal junction was exposed. Then, the posterior aspect of the pancreas was dissected free of the anterior surface of the portal vein bluntly as in classic PD.

Fig. Hanging maneuver [Adapted with permission from Pessaux et al, 2009]. RM: retroperitoneal margin.

After completely freeing the neck of the pancreas, the proximal jejunum and stomach were divided as in classic PD. Now, the only remaining attachment was the neck of the pancreas, which was divided with a surgical blade between hemostatic stay sutures to complete the resection. Reconstruction and restoration of gastrointestinal continuity were affected as in the classic procedure.

Evaluation

We describe a modified technique of PD with division of the retroperitoneal soft tissues around the SMA initially, but the division of the pancreatic neck is carried out as the final step. This technique is helpful during PD, particularly in cases of 1) suspected infiltration of the SMA; 2) a replaced right hepatic artery originating from the SMA; 3) infiltration of the SMV or portal vein; and 4) a periampullary neoplasm extending from the head to the body, or encasement of the portomesenteric junction by a head or neck tumor, thus needing pancreatic division on the body. Moreover, the technique of the “SMA first” approach follows oncologic principles.

Many patients with neoplasms arising from the periampullary region, especially pancreatic adenocarcinoma, present with advanced disease that is not curatively resectable. The most frequent features that preclude curative resection are liver metastases, local vascular invasion, peritoneal carcinomatosis, and lymph node metastases.[13]

One major factor that influences the resectability of tumors is vascular invasion by the tumor. The major periampullary vessels analyzed in the literature are the SMA and SMV, celiac trunk, portal vein, and hepatic artery. At present, the common tests used to predict resectability and stage of pancreatic or periampullary malignancy are contrast-enhanced spiral CT, multidetector row CT, and MR imaging. The multidetector row CT has an excellent positive predictive value of 100% for vascular invasion and a good negative predictive value of 87% for overall tumor resectability. The accuracy of resectability is 87% in patients with pancreatic adenocarcinoma, suggesting an improvement of previous results reported using single-detector CT.[14,15]Vascular involvement is graded from 0 to 4, with grade 0 representing no vascular involvement and grade 4 total encasement of either the SMV or artery. Resectability for grades 0 to 3 are 96%, 100%, 50%, and 9%. Patients with grade 4 lesions are considered unresectable.[16]The results reveal that it is doubtful to predict resectability by CT in patients with vascular encroachment (grade 2), which is usually determined by the extent of local disease rather than the presence of extra-pancreatic metastases. The prediction of artery invasion has a higher specificity (92%), but the sensitivity (68%) is not good enough. CT has a high specificity and positive predictive value, but gives a low negative predictive value and accuracy for vascular invasion: 67% and 75% for the artery and 58% and 64% for the vein, respectively.[17]It is necessary to explore peripancreatic vascular structures for R0 resection in patients with vascular encroachment (grade 2).

One advantage of this surgical technique is to identify invasion of the SMA early. Infiltration of the SMA is considered a contraindication for PD.[18]Invasion of this major vessel is usually identified only toward the end of the resection process during classic PD, when the neck of the pancreas has already been divided. At this embarrassing point, the surgeon has only to commit to resection with a positive margin. These patients with margin-positive resection have a poor prognosis that is often no better than that of patients with nonresection.[19]The method of dissecting the SMA and the posterior pancreatic capsule first enables the surgeon to identify the presence of early SMA involvement. The neck of the pancreas is divided as the final step of the operation, so this dilemma is avoided.

This procedural variant allows early identification and preservation of a replaced right hepatic artery arising from the SMA. The most common aberration in hepatic arterial anatomy is a replaced right hepatic artery arising from the SMA, which has been reported to occur in 9.8% to 21% of the normal population.[20]These vessels usually pass lateral to and behind the portal vein and enter the hepatoduodenal ligament posterolateral to the bile duct, and can be felt in this location when palpating the structures at the porta hepatis in the foramen of Winslow. It is possible to injure the artery inadvertently during the classic surgical procedure, particularly in cases of advanced tumors. This may lead to bilioenteric anastomoses that are ischemic and dehisced secondary to interruption ofhepatic arterial blood flow,[20-22]because the right hepatic artery is the chief source of blood supply to the bile duct.

This procedure should always be considered in case of suspected tumor infiltration of the portal/SMV to achieve a negative resection margin, in the absence of other contraindications for resection.[23,24]The infiltration of the SMV or portal vein is encountered in 71% of resected specimens in patients with pancreas head tumors because of the intimate relationship of the pancreatic head and uncinate process with these vessels. in this situation, en bloc resection and reconstruction of the vein can be performed to obtain negative margins without increased morbidity and mortality.[25-27]Early dissection from the SMA results in the tumor being attached only to the involved veins, so clamping of the porto-mesenteric confluence may be easier and shorter.

In some cases, when the tumor is located on the pancreatic body, en bloc resection needs a PD with pancreatic division located on the body. In these cases, final transection of the pancreas, instead of neck transection followed by additional body resection, can be performed at the desired level if sufficiently mobilized from the splenic vessels and prevents the tumor from opening, which might disseminate cancer into the abdomen. Furthermore, dissection along the splenic vessels can be extended up to the splenic hilum and allows splenic preservation if the whole pancreas must be resected.

The technique of PD follows oncologic principles, including en bloc resection of lymph nodes along the right and anterior aspect of the SMA (between the SMA and SMV) and the hepatoduodenal ligament. The poor prognosis associated with pancreatic carcinoma has been attributed to early lymph node involvement as well as to distant metastases. Retroperitoneal lymph node metastases are present in 20%-77% of resected specimens from patients with carcinoma of the head of the pancreas.[21,22]Hence, adequate lymphadenectomy is definitely indicated during the performance of PD. Extended lymphadenectomy has been shown to increase postoperative morbidity with no significant increase in survival.[28]En bloc resection of the lymphatics lying along the right side of the SMA is minimal during this operation.

Funding:None.

Ethical approval:Not needed.

Contributors:GJP proposed the study. XYF wrote the first draft. LZJ and GJP examined and verified the results. All authors contributed to further drafts. GJP is the guarantor.

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.

1 Neoptolemos JP, Stocken DD, Dunn JA, Almond J, Beger HG, Pederzoli P, et al. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann Surg 2001;234:758-768.

2 Sommerville CA, Limongelli P, Pai M, Ahmad R, Stamp G, Habib NA, et al. Survival analysis after pancreatic resection for ampullary and pancreatic head carcinoma: an analysis of clinicopathological factors. J Surg Oncol 2009;100:651-656.

3 Westgaard A, Tafjord S, Farstad IN, Cvancarova M, Eide TJ, Mathisen O, et al. Resectable adenocarcinomas in the pancreatic head: the retroperitoneal resection margin is an independent prognostic factor. BMC Cancer 2008;8:5.

4 Pessaux P, Rosso E, Panaro F, Marzano E, Oussoultzoglou E, Bachellier P, et al. Preliminary experience with the hanging maneuver for pancreaticoduodenectomy. Eur J Surg Oncol 2009;35:1006-1010.

5 Varty PP, Yamamoto H, Farges O, Belghiti J, Sauvanet A. Early retropancreatic dissection during pancreaticoduodenectomy. Am J Surg 2005;189:488-491.

6 Pessaux P, Varma D, Arnaud JP. Pancreaticoduodenectomy: superior mesenteric artery first approach. J Gastrointest Surg 2006;10:607-611.

7 Partensky C. Pancreaticoduodenectomy by a superior mesenteric artery first approach. J Chir (Paris) 2008;145:598-600.

8 Weitz J, Rahbari N, Koch M, Büchler MW. The "artery first" approach for resection of pancreatic head cancer. J Am Coll Surg 2010;210:e1-4.

9 Shimada K, Sakamoto Y, Sano T, Kosuge T. The role of paraaortic lymph node involvement on early recurrence and survival after macroscopic curative resection with extended lymphadenectomy for pancreatic carcinoma. J Am Coll Surg 2006;203:345-352.

10 Yoshida T, Matsumoto T, Sasaki A, Shibata K, Aramaki M, Kitano S. Outcome of paraaortic node-positive pancreatic head and bile duct adenocarcinoma. Am J Surg 2004;187:736-740.

11 Doi R, Kami K, Ito D, Fujimoto K, Kawaguchi Y, Wada M, et al. Prognostic implication of para-aortic lymph node metastasis in resectable pancreatic cancer. World J Surg 2007;31:147-154.

12 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;14:118-127.

13 Valls C, Andía E, Sanchez A, Fabregat J, Pozuelo O, Quintero JC, et al. Dual-phase helical CT of pancreatic adenocarcinoma: assessment of resectability before surgery. AJR Am J Roentgenol 2002;178:821-826.

14 Park HS, Lee JM, Choi HK, Hong SH, Han JK, Choi BI. Preoperative evaluation of pancreatic cancer: comparison of gadolinium-enhanced dynamic MRI with MR cholangiopancreatography versus MDCT. J Magn Reson Imaging 2009; 30:586-595.

15 Vargas R, Nino-Murcia M, Trueblood W, Jeffrey RB Jr. MDCT in Pancreatic adenocarcinoma: prediction of vascular invasion and resectability using a multiphasic technique with curved planar reformations. AJR Am J Roentgenol 2004;182:419-425.

16 Saldinger PF, Reilly M, Reynolds K, Raptopoulos V, Chuttani R, Steer ML, et al. Is CT angiography sufficient for prediction of resectability of periampullary neoplasms? J Gastrointest Surg 2000;4:233-239.

17 Bao PQ, Johnson JC, Lindsey EH, Schwartz DA, Arildsen RC, Grzeszczak E, et al. Endoscopic ultrasound and computed tomography predictors of pancreatic cancer resectability. J Gastrointest Surg 2008;12:10-16.

18 Martin RC 2nd, Scoggins CR, Egnatashvili V, Staley CA, McMasters KM, Kooby DA. Arterial and venous resection for pancreatic adenocarcinoma: operative and long-term outcomes. Arch Surg 2009;144:154-159.

19 Raut CP, Tseng JF, Sun CC, Wang H, Wolff RA, Crane CH, et al. Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg 2007;246:52-60.

20 Shukla PJ, Barreto SG, Kulkarni A, Nagarajan G, Fingerhut A. Vascular anomalies encountered during pancreatoduodenectomy: do they influence outcomes? Ann Surg Oncol 2010;17:186-193.

21 Slidell MB, Chang DC, Cameron JL, Wolfgang C, Herman JM, Schulick RD, et al. Impact of total lymph node count and lymph node ratio on staging and survival after pancreatectomy for pancreatic adenocarcinoma: a large, population-based analysis. Ann Surg Oncol 2008;15:165-174.

22 Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, et al. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery 2007;141:610-618.

23 Yekebas EF, Bogoevski D, Cataldegirmen G, Kunze C, Marx A, Vashist YK, et al. En bloc vascular resection for locally advanced pancreatic malignancies infiltrating major blood vessels: perioperative outcome and long-term survival in 136 patients. Ann Surg 2008;247:300-309.

24 Ramacciato G, Mercantini P, Petrucciani N, Giaccaglia V, Nigri G, Ravaioli M, et al. Does portal-superior mesenteric vein invasion still indicate irresectability for pancreatic carcinoma? Ann Surg Oncol 2009;16:817-825.

25 Tseng JF, Raut CP, Lee JE, Pisters PW, Vauthey JN, Abdalla EK, et al. Pancreaticoduodenectomy with vascular resection: margin status and survival duration. J Gastrointest Surg 2004; 8:935-950.

26 Bachellier P, Nakano H, Oussoultzoglou PD, Weber JC, Boudjema K, Wolf PD, et al. Is pancreaticoduodenectomy with mesentericoportal venous resection safe and worthwhile? Am J Surg 2001;182:120-129.

27 Fujisaki S, Tomita R, Fukuzawa M. Utility of mobilization of the right colon and the root of the mesentery for avoiding vein grafting during reconstruction of the portal vein. J Am Coll Surg 2001;193:576-578.

28 Yeo CJ, Cameron JL, Lillemoe KD, Sohn TA, Campbell KA, Sauter PK, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Ann Surg 2002;236:355-368.

December 11, 2009

Accepted after revision April 8, 2010

Author Affiliations: Department of Hepatobiliary Surgery, Second Affiliated Hospital, Chongqing University of Medicine and Science, Chongqing 400010, China (Xu YF, Liu ZJ and Gong JP)

Jian-Ping Gong, MD, PhD, Department of Hepatobiliary Surgery, Second Affiliated Hospital, Chongqing University of Medicine and Science, Chongqing 400010, China (Tel: 86-23-63036701; Fax: 86-23-63711527; Email: gongjianping11@126.com)

? 2010, Hepatobiliary Pancreat Dis Int. All rights reserved.