- Email: [email protected]
Portal Veins Axis: An Alternative Procedure to Pancreaticoduodenectomy with Vein Resection
SURGEON AT WORK
Resection of Pancreatic Tumors Involving the Anterior Surface of the Superior Mesenteric/Portal Veins Axis: An Alternative Procedure to Pancreaticoduodenectomy with Vein Resection Yonghua Chen,
MD,
Chunlu Tan,
MD,
Gang Mai,
MD,
The technique of pancreaticoduodenectomy (PD) has evolved, particularly in relation to the techniques used to achieve negative resection margins. Early emphasis was placed on establishing a dissection plane between the anterior surface of the superior mesenteric/portal veins (SMPV) and the posterior surface of the neck of the pancreas.1 For a long time, diseases involving these veins were considered unresectable. Recently, however, extensive vascular resection has become a standard procedure at major pancreatic surgical centers2,3 and has been shown to improve the rates of R0 resection and survival4 without an increase in postoperative morbidity and mortality.5 Vein resections usually involve the right lateral portion of the SMPV or a cylinder of the superior mesenteric vein (SMV) below its confluence with the splenic vein (SV). Occasionally, the anterior surface of the SMPV axis and the posterior surface of the neck of the pancreas are both involved by the tumor or related inflammatory adhesions. This pattern of venous involvement is most likely to occur in tumors of the pancreatic neck or in the medial aspect of the head of the pancreas. The standard approach of developing a tunnel behind the neck of the pancreas, anterior to the SMPV axis, cannot be achieved with such involvement of the anterior surfaces of these veins at the pancreatic neck, and these tumors are frequently considered unresectable. The purpose of this “Surgeon at Work” report is to describe the technique we use for dealing with these difficult tumors, which we refer to as “Whipple at the inferior mesenteric vein”.
MD,
Xubao Liu,
MD
Preoperative imaging Preoperative evaluation included physical examination, chest roentgenography, and contrast-enhanced CT and/ or MRI, which predicts resectability with an accuracy of approximately 95%.6,7 Analysis of anatomic variants of mesenteric veins by 3-dimensional portography was performed using multidetector-row CT or MRI. To be considered for operation, the patients were required to fulfill the following objective CT criteria for tumor respectability8,9: no distant metastases and venous involvement of the SMPV without encasement of the nearby arteries. We consider vein involvement below the confluence of its ileal and jejunal tributaries, resulting in the lack of any available vein for anastomosis, a contraindication to resection. This problem was typically defined by preoperative imaging. In addition, when tumors involve the right lateral or posterior portion of the SMPV, we typically dissect the SMV and create a plane to the left of the PV on to the SV, as in the standard Whipple procedure. On the other hand, when a tumor involves a cylinder of the SMPV or when the anterior surfaces of the SMPV axis and posterior surface of the neck of the pancreas are both involved by the tumor or related inflammatory adhesions, the described technique is applicable. Anatomic considerations The typical plane of transection through the neck of the pancreas is shown in Figure 1 as “A”, which usually needs to create a tunnel between the anterior surface of the SMPV axis and the posterior surface of the neck of the pancreas. This plane of resection cannot be used because of adherence to the vessels due to tumor invasion or an inflammatory reaction and, if forced, would result in a positive margin or the potential for venous injury. So the plane of division must be moved to the left on the pancreas. The point at which the right portion of the inferior mesenteric vein (IMV) enters into the inferior border of the pancreas (plane B) was chosen as the site of transection to attain negative margins and identify and protect the SV. Note that the IMV, if drained into
METHODS Whipple at the inferior mesenteric vein is an alternative operative technique for resection of pancreatic tumors that involve the anterior axis of the SMPV. Disclosure Information: Nothing to disclose. Supported by the Research Special Fund For Public Welfare Industry of Health (201202007). Drs Chen and Tan contributed equally to this work. Received April 15, 2013; Revised June 24, 2013; Accepted July 9, 2013. From the Department of Hepatobiliopancreatic Surgery, West China Hospital, Sichuan University, Chengdu, China. Correspondence address: Xubao Liu, MD, Department of Hepatobiliopancreatic Surgery, West China Hospital, Sichuan University, Chengdu 610041, China. email: [email protected]
ª 2013 by the American College of Surgeons Published by Elsevier Inc.
Nengwen Ke,
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ISSN 1072-7515/13/$36.00 http://dx.doi.org/10.1016/j.jamcollsurg.2013.07.383
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Abbreviations and Acronyms
IMV PD SMA SMPV SV
¼ ¼ ¼ ¼ ¼
inferior mesenteric vein pancreaticoduodenectomy superior mesenteric artery superior mesenteric/portal veins splenic vein
the SV, contacts the inferior border of the pancreas approximately 2 cm to the left of the pancreatic neck and generally approaches the pancreas from an inferior and posterior direction.10 Pancreaticoduodenectomy technique A vertical midline incision was made, followed by abdominal exploration. Routine biopsy of apparently normal regional lymph nodes is unnecessary, but suspicious lesions and enlarged lymph nodes outside of the planned field of dissection should be biopsied and examined by frozen section, and the resection should be aborted if the enlarged lymph nodes are found to be positive for metastatic cancer. Positive lymph nodes within the planned field of resection are not considered a contraindication to PD. Mobilization of the head of the pancreas and isolation of the superior mesenteric vein The initial portions of the PD were conducted in a standard fashion for a patient who is expected to require a vein resection. Briefly, a modified Kocher maneuver (with partial resection of the pre-renal fascia) was begun at the right renal hilum, and all fibro-fatty and lymphatic tissue overlying the inferior vena cava was elevated with the pancreatic head and duodenum to the left lateral edge of the aorta. The infrapancreatic SMV was isolated in a more distal location, as initially described by Cameron.11 Sufficient vein must be available for segmental resection and anastomosis. The middle colic vein may need to be divided to expose the infrapancreatic SMV and prevent iatrogenic traction injury. We did not make any attempt to develop a plane of dissection between the anterior surface of the SMPV axis and the posterior surface of the neck of the pancreas because of the adherence of the pancreas to the vessels due to tumor invasion or inflammatory reaction. Adherence is especially relevant to cancers in the neck and body of the pancreas. Supraduodenal dissection and isolation of the splenic artery The supraduodenal portion of the dissection in the portal hepatis was performed, as usual, by cholecystectomy,
Figure 1. Pancreatic tumors involving the anterior of the superior mesenteric/portal veins axis (circles). Line A indicates the usual plane of transection of the neck of the pancreas in a Whipple procedure. Line B indicates the plane of transection in the inferior mesenteric vein proceduredjust to the right of the point of the entrance of the inferior mesenteric vein into the inferior border of the pancreas.
division of the common hepatic duct, division of the gastroduodenal artery, and dissection of all soft tissue and nodes off the portal vein and hepatic arteries from the level of the confluence of the common hepatic duct to the duodenum. The periarterial soft tissues of the common hepatic artery and proximal splenic artery were also mobilized and removed with the specimen. The proximal splenic artery was encircled with a vessel loop. Isolation of the inferior mesenteric vein and dissection of the tunnel behind the body of pancreas As shown in Figure 2, the transverse colon and its mesentery were elevated cephalically, followed by flipping the small bowel to the patient’s right side to facilitate exposure and dissociation of the IMV. The IMV can be traced up to the IMV-SV confluence for rapid identification by mobilization of the retroperitoneal attachments down to the level of the body of the pancreas. There are no direct anterior branches to the IMV-SV confluence. So, the anterior surface of the vein confluence was separated by blunt dissection from the pancreas, creating a tunnel behind the body of the pancreas, and the body of the pancreas was encircled with a vessel loop (Fig. 3). Transection of the stomach, jejunum, and pancreas The stomach and jejunum were divided using a linear stapling device in a standard Whipple procedure as shown in Figure 4. The pancreas may then be divided as usual. We normally divide the pancreas with stay sutures and a knife, controlling bleeding on the “pancreatic remnant
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Figure 3. (A) Schematic diagram and (B) intraoperative photograph: creating the tunnel between the anterior surface of the splenic vein and the posterior surface of pancreas, the body of pancreas was encircled with a vessel loop. IMV, inferior mesenteric vein.
Figure 2. (A) Exposing the inferior mesenteric vein after dividing the peritoneum to the left of the duodenojejunal flexure in the transverse mesocolon. (B) Intraoperative image demonstrating the area of incision of the peritoneum at the duodenojejunal flexure. The small bowel is displaced to the right of the patient, and the colon is displaced toward the head of the patient. IMV, inferior mesenteric vein.
side” with 3-0 absorbable sutures and on the “specimen side” with penetrating ligature and cautery. A vascular forceps was passed behind the body of the pancreas to elevate and protect the vein during division. On either side of the proposed line of transection, 3-0 silk stay
sutures were placed on the superior and inferior borders of the pancreas. The superior and inferior borders of the pancreas on the “specimen side” were exposed by dividing the overlying peritoneum, and the venous tributaries of the SV were ligated and divided. Isolation of the specimen and clearance of the superior mesenteric artery After ligating and dividing some of the easily accessible SMPV tributaries, the dissection plane could be continued in a cephalad direction along the anterior aspect of the superior mesenteric artery (SMA) toward its origin. Dissection of the SMA was maintained on the right hemicircumference until the posterior aspect of the SMA was reached (Fig. 5). Branches to the pancreatic head and uncinate coming off the right side or the
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Figure 5. Clearance of the superior mesenteric artery (SMA). IMV, inferior mesenteric vein; SMV, superior mesenteric vein.
Figure 4. (A) Schematic diagram and (B) intraoperative photograph: the pancreas is transected immediately to the right of the plane in which the inferior mesenteric vein (IMV) enters into the inferior border of the pancreas. SMV, superior mesenteric vein; SV, splenic vein.
right posterior edge of the artery were tied or clipped. The many variations of the SMA-first approach allow the pancreatic head to be completely freed from retroperitoneal surrounding tissues, as described by others.12,13 At this stage, the pancreatic head was held in place only by tumor adhering to the SMPV structures. The involved segment of vein can then be clamped proximally and distally at least 0.5 to 1 cm away from the tumor and resected en bloc with the specimen. Splenic vein ligation occasionally resulted in gastrointestinal hemorrhage because of sinistral portal hypertension. We therefore attempted to preserve a part of the SMPV-SV confluence when technically possible to facilitate the venous anastomosis. The SMPV-SV confluence was entirely resected only when deemed necessary to complete a negativemargin PD.
Reconstruction of veins Patients requiring segmental resection of the SMPV underwent reconstruction with a primary end-to-end anastomosis whenever possible using 5-0 synthetic, monofilament, nonabsorbable polypropylene suture (Ethicon Inc) in a running fashion and tied loosely (Fig. 6). It is possible to perform an end-to-end anastomosis even after excision of as much as 5 cm of the PV, SMV, or the confluence of these vessels.14 The tension at the venous anastomosis site is reduced by a number of factors, including mobilization of the mesentery of the small bowel along with the right colon and the
Figure 6. Completed procedure. The superior mesenteric vein (SMV) has been anastomosed to the portal vein (PV) without a graft. IMV, inferior mesenteric vein; SV, splenic vein.
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Table 1. Demographic Data, Operative Characteristics, Perioperative Complications, Pathologic Findings, and Method of Vascular Reconstruction Variable
n Age, y, median (range) Sex, n (%) Male Female Operative characteristics Operative blood loss, mL, median Intraoperative transfusion, n (%) Packed red blood cells, U Pathologic characteristic, n (%) Adenocarcinoma Pancreas Bile duct Neuroendocrine carcinoma Tumor size, cm, median Degree of differentiation Well to moderately differentiated, n Moderately to poorly differentiated, n Positive pancreatic margin, n Positive bile duct margin, n Microscopically positive retroperitoneal margin, n (%) Perineural invasion, n (%) Lymphatic invasion, n (%) Vascular invasion, n (%) Vessel resected, n (%) SMPV or SMPV-SV confluence, n Preservation of a part of SV confluence Resection of entire SV confluence Method of reconstruction Primary end-to-end anastomosis with ligation of the SV, n Primary end-to-end anastomosis with revascularization of the SV, n Perioperative complications, n (%) Postoperative pancreatic fistula Grade A Grade B Grade C Postoperative hemorrhage/ulcer bleeding Intra-abdominal collection Delayed gastric emptying Wound infection/Superficial wound infection Pulmonary infection Reoperation, n Perioperative deaths,* n Postoperative hospital stay, d, mean (range) *In-hospital or within 30 days of operation. SMPV, superior mesenteric-portal vein; SV, splenic vein.
Data
8 53.5 (39e71) 6 (75) 2 (25) 475 1 (12.5) 2 7 6 1 1
(87.5) (75) (12.5) (12.5) 3.7 0 8 0 0
1 5 3 6
(12.5) (62.5) (37.5) (75)
8 6 (75) 2 (25)
0 8 3 (37.5) 1 (12.5) 0 1 (12.5) 0 1 (12.5) 1 (12.5) 2 (25) 2 (25) 1 (12.5) 0 0 13 (9e22)
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dissection the surrounding ligaments of liver.14,15 We attempted to preserve a part of the SMPV-SV confluence when technically possible to facilitate venous anastomosis. Whenever the entire confluence of the SMPV and SV is involved by the tumor, resection of these veins should be undertaken proximal to the confluence, and the SV is reimplanted into the SMV or PV in an end-to-side fashion. Reconstruction of the organs The remainder of the PD followed the standard protocol for a Whipple procedure. Pancreaticojejunostomy was performed using our standard protocol.16 The anastomotic area of pancreaticojejunostomy and biliary anastomosis were drained separately with open drains. Before closure of the abdomen, a visual inspection was performed to exclude narrowing of the SMPV system. The diameter of the anastomosis must be within 75% of the inflow vessel diameter. Pathologic analysis of the resected specimen Pathologic analysis followed a standardized system for the pathologic evaluation of PD specimens established previously.17 The operative specimen was oriented and dissected by the surgeon and pathologist in a pathology suite in the operating room complex. The retroperitoneal margin was defined as the soft tissue margin directly adjacent to the proximal 3 to 4 cm of the SMA. A 2- to 3-mm, full-face (en face) section of the margin was evaluated by frozen-section microscopic examination, and the margin was interpreted as positive if tumor was observed on the section. The presence or absence of tumor cell infiltration of the segment of the resected vein wall was defined as the presence of neoplastic cells within the tunica adventitia and/or tunica media of the vein wall. Tumor size was calculated after surgical resection by measuring the greatest transverse diameter of the tumor. Postoperative care All patients received intravenous somatostatin (Stilamin [Serum International], 3 mg/12 hours, for 5 days). No anticoagulant drug was used perioperatively or postoperatively. While a drain was in place in the patient, the volume and amylase concentrations in the fluid collected from the peripancreatic drain were measured every other day. The timing of removal of the intra-abdominal drains in our institution has recently been set at approximately postoperative day 5.
RESULTS To date, we have performed this procedure in 8 patients. Patient demographics, operative characteristics, perioperative
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complications, and pathologic findings are listed in Table 1. Most patients exhibited adenocarcinoma of pancreatic origin. We attempted to preserve a part of the SMPV-SV confluence when technically possible. The SMPV-SV confluence was entirely resected in only 2 patients. In these 2 patients, intraoperative attempts at mobilizing the proximal SV to the SMPV-SV confluence were unsuccessful; neoplastic cells and marked fibrosis extended into the wall of the proximal SV. No patient was found to have a grossly positive retroperitoneal margin of excision. A microscopically positive retroperitoneal margin was found in only 1 of 8 patients. Neoplastic cells were found to invade the vein wall in 6 (75%) of 8 specimens. All patients were successfully discharged from the hospital after a median hospital stay of 13 days. Three of 8 patients suffered perioperative complications, but no patient had a complication clearly related to the vascular resection and reconstruction. No postoperative mortality, which was defined as death within 30 postoperative days, occurred in this series. No narrowing in blood vessels or thrombosis were detected by ultrasound within 2 weeks or during the regular follow-up every 3 months after the operation. No other severe morbidity (obvious pancreatic or bile leakage) was observed in this group in the postoperative period and follow-up.
DISCUSSION Management of tumor adherence or invasion to the SMPV represents the most challenging technical aspect of PD. To achieve complete resection of a pancreatic tumor, resection of the SMPV needs to be performed if there is suspected invasion of the venous wall. To adhere to the principles of oncologic surgery, this resection should be performed without violating the integrity of the tumor. The standard approach of creating a tunnel behind the neck of the pancreas, anterior to the SMPV axis, cannot be achieved when these veins are infiltrated with tumor or related inflammatory adhesions. If such a procedure were undertaken, the surgery would result in positive margins or the potential for venous injury. So, these tumors are frequently considered unresectable. This pattern of venous invasion is most likely to occur in tumors of the neck or medial aspect of the head of the pancreas. Depending on the site of tumor invasion of the SMPV and therefore, the extent of venous resection required, different technical options for resection and reconstruction are available. When the lesion is adherent to a small part of the lateral or posterior wall of the PV and SMV, dissection of the SMV and creation of a plane to the left of the PV on to the SV as standard Whipple procedure are possible. On the other hand, when the tumor involves
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a cylinder of the SMPV or when the anterior surfaces of the SMPV axis and posterior surface of the neck of the pancreas are both involved by tumor or related inflammatory adhesions, the pancreas must be divided further to the left, abandoning the usual plane of the neck of the pancreas. Many have adopted a selective approach for pancreatic transaction, with some authors claiming that the body of the pancreas should be divided with preservation and control of the SV, as in the “central pancreatectomy” procedure,18,19 and others believe that it is safe to directly cut the pancreas at the body of the pancreas and the SV to the left of the PV without isolation and revascularization of the SV.15,20-22 However, routine procedures dividing the body of the pancreas and isolating the SV include complex and troublesome maneuvers. There are many tributaries behind the pancreas that enter the anterior aspect of the SV, and these can be easily damaged during dissection, which is especially difficult in patients with peripancreatic inflammation and adhesions around the body of the pancreas.13 Moreover, directly cutting the pancreas at the body plane without isolating the SV would result in the potential for venous injury and uncontrollable bleeding and could necessitate total pancreatectomy and splenectomy. Strasberg and colleagues21 recently described a procedure termed WATSA, in which the pancreas and SV are divided just to the right of the contact between the splenic artery and the superior border of the pancreas without SV revascularization. However, their routine SV ligation results in the potential development of left-sided portal hypertension and hypertensive gastropathy and/or gastric variceal hemorrhage.23,24 The SV is divided when tumor invasion at its junction with the PV is evident, when extra mobility for a direct end-to-end anastomosis between the PV and SMV is necessary, and, rarely, when it is necessary to provide better exposure for a thorough nodal clearance and soft tissue dissection at the proximal SMA. There is controversy in the surgical literature as to the safety of occluding the SV in a Whipple procedure, with some authors claiming that most patients would have no problem because the venous flow from the spleen and stomach could return to the systemic vein or the SMV through the short gastric vein and the esophageal vein,25 avoiding the development of symptomatic portal hypertension.20,22,23 Others describe complications related to this problem,3,26 including patterns of venous collateral development after SV occlusion. Using CT to evaluate the remnant SV patency after division close to its junction with the PV during PD 6 to 8 months after surgery, Strasberg and associates20 found that all 5 patients exhibited a patent
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SV. Venous drainage from the spleen was shown to be channeled via multiple collaterals, and none of the patients developed splenomegaly. Obviously, previous studies are too small and too short to establish the safety of SV occlusion during a Whipple procedure,19,20,22 and the indications for and long-term outcomes resulting from such extended venous resections will require further study and elucidation. Distal splenic-renal shunt has also been advocated by some authors.27 However, it is our opinion that a mandatory reconstruction is not a universally accepted practice. We attempted to preserve a part of SMPV-SV confluence when technically possible. When a segment of the PV must be sacrificed, primary endto-end anastomosis should be made with preservation of all venous branches, including the SV, whenever feasible.19 Several previous reports have analyzed the paths of the IMV on MRI or multidetector CT. The 3 most common variants (SV, SMV, and the SMV-SV confluence) of the drainage sites of the IMV differ among these reports. The IMV drains into the SV in 42.3% to 56% of Caucasian patients10,28 and in 45% to 68.5% of East Asian patients.29-31 In this type SV, the IMV runs along the left side of the SMA and apart from the root of the SMA in most patients31 and enters the SV at a mean distance (entering point in relation to the portal confluence) of 1.66 cm (range 0.27 to 3.48 cm),10 which is chosen as the site of transection of the pancreas to attain negative margin as well as identify, control, and protect the SV. Moreover, there are no direct anterior branches to the IMV-SV confluence, which is the ideal alternative plane to create a tunnel between the anterior surface of veins and the posterior surface of the pancreas by blunt dissection. The key component of the technique described here is identification of the IMV, if drained into the SV, which serves as a guide to securely create the tunnel between the anterior surface of SV and the posterior surface of pancreas for transection of the pancreas as a standard procedure. Our contribution is mainly to provide an alternative approach to the specific problem of the involvement of the anterior surface of the SMPV axis by tumor. This type of tumor involvement often results in the tumor exhibiting positive margins and being unresectable. Furthermore, this technique may be very helpful when there is severe inflammation around the veins and when it is difficult to distinguish the scar from the cancer intraoperatively. The SV remains intact, and venous outflow from the spleen is preserved, thereby avoiding the potential development of left-sided portal hypertension and hypertensive gastropathy and/or gastric variceal hemorrhage. In a standard Whipple procedure, venous injury, uncontrollable bleeding from within the tunnel
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behind the neck of the pancreas, and transection across the tumor are not rare events. This new approach can provide controlled rescue.
CONCLUSIONS In conclusion, an alternative method of resection of tumors that involve of the anterior surface of the SMPV axis has been described. Early results suggest that the procedure is effective in attaining negative margin resections and avoiding the potential for venous injury and uncontrollable bleeding. Author Contributions Study conception and design: Chen, Mai, Liu Acquisition of data: Chen, Tan, Mai, Ke Analysis and interpretation of data: Chen, Tan, Mai, Ke, Liu Drafting of manuscript: Chen, Tan, Mai, Ke, Liu Critical revision: Chen, Tan, Mai, Liu Acknowledgment: The authors thank Ruizhi Zhang (Sichuan Institute of Building Research; Landscape Architecture, School of Architecture, Southeast University) for her assistance with the preparation of the schematic diagrams. REFERENCES 1. Warshaw A, Thayer S. Pancreaticoduodenectomy. J Gastrointest Surg 2004;8:733. 2. Mueller SA, Hartel M, Mehrabi A, et al. Vascular resection in pancreatic cancer surgery: survival determinants. J Gastrointest Surg 2009;13:784e792. 3. Bold RJ, Charnsangavej C, Cleary KR, et al. Major vascular resection as part of pancreaticoduodenectomy for cancer: radiologic, intraoperative, and pathologic analysis. J Gastrointest Surg 1999;3:233e243. 4. Riall TS, Cameron JL, Lillemoe KD, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinomadd part 3: Update on 5-year survival. J Gastrointest Surg 2005;9: 1191e1206. 5. Glanemann M, Shi B, Liang F, et al. Surgical strategies for treatment of malignant pancreatic tumors: extended, standard or local surgery? World J Surg Oncol 2008;6. 6. Vargas R, Nino-Murcia M, Trueblood W, Jeffrey RB. MDCT in pancreatic adenocarcinoma: prediction of vascular invasion and resectability using a multiphasic technique with curved planar reformations. AJR Am J Roentgenol 2004;182: 419e425. 7. Lu D, Reber HA, Krasny RM, et al. Local staging of pancreatic cancer: criteria for unresectability of major vessels as revealed by pancreatic-phase, thin-section helical CT. AJR Am J Roentgenol 1997;168:1439e1443. 8. Fuhrman GM, Charnsangavej C, Abbruzzese JL, et al. Thinsection contrast-enhanced computed tomography accurately
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predicts the resectability of malignant pancreatic neoplasms. Am J Surg 1994;167:104e113. Callery M, Chang K, Fishman E, et al. Pretreatment assessment of resectable and borderline resectable pancreatic cancer: expert consensus statement. Ann Surg Oncol 2009;16:1727. Krumm P, Schraml C, Bretschneider C, et al. Depiction of variants of the portal confluence venous system using multidetector row CT: analysis of 916 cases. Rofo 2011;183:1123e1129. Cameron JL. Rapid exposure of the portal and superior mesenteric veins. Surg Gynecol Obstet 1993;176:395e398. Weitz J, Rahbari N, Koch M, Bu¨chler M. The “artery first” approach for resection of pancreatic head cancer. J Am Coll Surg 2010;210:e1. Sanjay P, Takaori K, Govil S, et al. ‘Artery-first’ approaches to pancreatoduodenectomy. Br J Surg 2012;99:1027e1035. Zhang J, Qian HG, Leng JH, et al. Long mesentericoportal vein resection and end-to-end anastomosis without graft in pancreaticoduodenectomy. J Gastrointest Surg 2009;13: 1524e1528. Wang F, Arianayagam R, Gill A, et al. Grafts for mesentericoportal vein resections can be avoided during pancreatoduodenectomy. J Am Coll Surg 2012;215:569e579. Chen Y, Tan C, Zhang H, et al. Novel entirely continuous running suture of two-layer pancreaticojejunostomy using only one polypropylene monofilament suture. J Am Coll Surg 2013;216:e17ee21. Staley C, Cleary K, Abbruzzese J, et al. The need for standardized pathologic staging of pancreaticoduodenectomy specimens. Pancreas 1996;12:373. Weitz J, Kienle P, Schmidt J, et al. Portal vein resection for advanced pancreatic head cancer. J Am Coll Surg 2007;204: 712e716. Lai EC. Vascular resection and reconstruction at pancreaticoduodenectomy: technical issues. Hepatobiliary Pancreat Dis Int 2012;11:234e242. Strasberg SM, Bhalla S, Sanchez LA, Linehan DC. Pattern of venous collateral development after splenic vein occlusion in an extended Whipple procedure comparison with collateral vein pattern in cases of sinistral portal hypertension. J Gastrointest Surg 2011;15:2070e2079. Strasberg SM, Sanchez LA, Hawkins WG, et al. Resection of tumors of the neck of the pancreas with venous invasion: the
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“Whipple at the Splenic Artery (WATSA)” procedure. J Gastrointest Surg 2012;16:1048e1054. Ferreira N, Oussoultzoglou E, Fuchshuber P, et al. Splenic vein-inferior mesenteric vein anastomosis to lessen left-sided portal hypertension after pancreaticoduodenectomy with concomitant vascular resection. Arch Surg 2011;146: 1375e1381. Arnaoutakis D, Eckhauser F. Safety and effectiveness of splenic vein to inferior mesenteric vein anastomosis during pancreaticoduodenectomy: comment on “Splenic vein-inferior mesenteric vein anastomosis to lessen left-sided portal hypertension after pancreaticoduodenectomy with concomitant vascular resection”. Arch Surg 2011;146:1381e1382. Fuhrman GM, Leach SD, Staley CA, et al. Rationale for en bloc vein resection in the treatment of pancreatic adenocarcinoma adherent to the superior mesenteric portal vein confluence. Ann Surg 1996;223:154e162. Misuta K, Shimada H, Miura Y, et al. The role of splenomesenteric vein anastomosis after division of the splenic vein in pancreatoduodenectomy. J Gastrointest Surg 2005;9: 245e253. Leach SD, Lee JE, Charnsangavej C, et al. Survival following pancreaticoduodenectomy with resection of the superior mesenteric-portal vein confluence for adenocarcinoma of the pancreatic head. Br J Surg 1998;85:611e617. Maillard JN, Le Baleur A, Hay JM, et al. [Resections of the portal vein. Anatomical basis, clinical results]. Chirurgie 1975;101:871e876. Graf O, Boland G, Kaufman J, et al. Anatomic variants of mesenteric veins: depiction with helical CT venography. AJR Am J Roentgenol 1997;168:1209. Zhang XM, Zhong TL, Zhai ZH, Zeng NL. MR venography of the inferior mesentery vein. Eur J Radiol 2007;64: 147e151. Kim H, Ko Y, Lim J, Lee D. Radiologic anatomy of the superior mesenteric vein and branching patterns of the first jejunal trunk: evaluation using multi-detector row CT venography. Surg Radiol Anat 2007;29:67. Sakaguchi T, Suzuki S, Morita Y, et al. Analysis of anatomic variants of mesenteric veins by 3-dimensional portography using multidetector-row computed tomography. Am J Surg 2010;200:15e22.
Resection of Pancreatic Tumors Involving the Anterior Surface of the Superior Mesenteric/Portal Veins Axis: An Alternative Procedure to Pancreaticoduodenectomy with Vein Resection Yonghua Chen,
MD,
Chunlu Tan,
MD,
Gang Mai,
MD,
The technique of pancreaticoduodenectomy (PD) has evolved, particularly in relation to the techniques used to achieve negative resection margins. Early emphasis was placed on establishing a dissection plane between the anterior surface of the superior mesenteric/portal veins (SMPV) and the posterior surface of the neck of the pancreas.1 For a long time, diseases involving these veins were considered unresectable. Recently, however, extensive vascular resection has become a standard procedure at major pancreatic surgical centers2,3 and has been shown to improve the rates of R0 resection and survival4 without an increase in postoperative morbidity and mortality.5 Vein resections usually involve the right lateral portion of the SMPV or a cylinder of the superior mesenteric vein (SMV) below its confluence with the splenic vein (SV). Occasionally, the anterior surface of the SMPV axis and the posterior surface of the neck of the pancreas are both involved by the tumor or related inflammatory adhesions. This pattern of venous involvement is most likely to occur in tumors of the pancreatic neck or in the medial aspect of the head of the pancreas. The standard approach of developing a tunnel behind the neck of the pancreas, anterior to the SMPV axis, cannot be achieved with such involvement of the anterior surfaces of these veins at the pancreatic neck, and these tumors are frequently considered unresectable. The purpose of this “Surgeon at Work” report is to describe the technique we use for dealing with these difficult tumors, which we refer to as “Whipple at the inferior mesenteric vein”.
MD,
Xubao Liu,
MD
Preoperative imaging Preoperative evaluation included physical examination, chest roentgenography, and contrast-enhanced CT and/ or MRI, which predicts resectability with an accuracy of approximately 95%.6,7 Analysis of anatomic variants of mesenteric veins by 3-dimensional portography was performed using multidetector-row CT or MRI. To be considered for operation, the patients were required to fulfill the following objective CT criteria for tumor respectability8,9: no distant metastases and venous involvement of the SMPV without encasement of the nearby arteries. We consider vein involvement below the confluence of its ileal and jejunal tributaries, resulting in the lack of any available vein for anastomosis, a contraindication to resection. This problem was typically defined by preoperative imaging. In addition, when tumors involve the right lateral or posterior portion of the SMPV, we typically dissect the SMV and create a plane to the left of the PV on to the SV, as in the standard Whipple procedure. On the other hand, when a tumor involves a cylinder of the SMPV or when the anterior surfaces of the SMPV axis and posterior surface of the neck of the pancreas are both involved by the tumor or related inflammatory adhesions, the described technique is applicable. Anatomic considerations The typical plane of transection through the neck of the pancreas is shown in Figure 1 as “A”, which usually needs to create a tunnel between the anterior surface of the SMPV axis and the posterior surface of the neck of the pancreas. This plane of resection cannot be used because of adherence to the vessels due to tumor invasion or an inflammatory reaction and, if forced, would result in a positive margin or the potential for venous injury. So the plane of division must be moved to the left on the pancreas. The point at which the right portion of the inferior mesenteric vein (IMV) enters into the inferior border of the pancreas (plane B) was chosen as the site of transection to attain negative margins and identify and protect the SV. Note that the IMV, if drained into
METHODS Whipple at the inferior mesenteric vein is an alternative operative technique for resection of pancreatic tumors that involve the anterior axis of the SMPV. Disclosure Information: Nothing to disclose. Supported by the Research Special Fund For Public Welfare Industry of Health (201202007). Drs Chen and Tan contributed equally to this work. Received April 15, 2013; Revised June 24, 2013; Accepted July 9, 2013. From the Department of Hepatobiliopancreatic Surgery, West China Hospital, Sichuan University, Chengdu, China. Correspondence address: Xubao Liu, MD, Department of Hepatobiliopancreatic Surgery, West China Hospital, Sichuan University, Chengdu 610041, China. email: [email protected]
ª 2013 by the American College of Surgeons Published by Elsevier Inc.
Nengwen Ke,
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ISSN 1072-7515/13/$36.00 http://dx.doi.org/10.1016/j.jamcollsurg.2013.07.383
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Abbreviations and Acronyms
IMV PD SMA SMPV SV
¼ ¼ ¼ ¼ ¼
inferior mesenteric vein pancreaticoduodenectomy superior mesenteric artery superior mesenteric/portal veins splenic vein
the SV, contacts the inferior border of the pancreas approximately 2 cm to the left of the pancreatic neck and generally approaches the pancreas from an inferior and posterior direction.10 Pancreaticoduodenectomy technique A vertical midline incision was made, followed by abdominal exploration. Routine biopsy of apparently normal regional lymph nodes is unnecessary, but suspicious lesions and enlarged lymph nodes outside of the planned field of dissection should be biopsied and examined by frozen section, and the resection should be aborted if the enlarged lymph nodes are found to be positive for metastatic cancer. Positive lymph nodes within the planned field of resection are not considered a contraindication to PD. Mobilization of the head of the pancreas and isolation of the superior mesenteric vein The initial portions of the PD were conducted in a standard fashion for a patient who is expected to require a vein resection. Briefly, a modified Kocher maneuver (with partial resection of the pre-renal fascia) was begun at the right renal hilum, and all fibro-fatty and lymphatic tissue overlying the inferior vena cava was elevated with the pancreatic head and duodenum to the left lateral edge of the aorta. The infrapancreatic SMV was isolated in a more distal location, as initially described by Cameron.11 Sufficient vein must be available for segmental resection and anastomosis. The middle colic vein may need to be divided to expose the infrapancreatic SMV and prevent iatrogenic traction injury. We did not make any attempt to develop a plane of dissection between the anterior surface of the SMPV axis and the posterior surface of the neck of the pancreas because of the adherence of the pancreas to the vessels due to tumor invasion or inflammatory reaction. Adherence is especially relevant to cancers in the neck and body of the pancreas. Supraduodenal dissection and isolation of the splenic artery The supraduodenal portion of the dissection in the portal hepatis was performed, as usual, by cholecystectomy,
Figure 1. Pancreatic tumors involving the anterior of the superior mesenteric/portal veins axis (circles). Line A indicates the usual plane of transection of the neck of the pancreas in a Whipple procedure. Line B indicates the plane of transection in the inferior mesenteric vein proceduredjust to the right of the point of the entrance of the inferior mesenteric vein into the inferior border of the pancreas.
division of the common hepatic duct, division of the gastroduodenal artery, and dissection of all soft tissue and nodes off the portal vein and hepatic arteries from the level of the confluence of the common hepatic duct to the duodenum. The periarterial soft tissues of the common hepatic artery and proximal splenic artery were also mobilized and removed with the specimen. The proximal splenic artery was encircled with a vessel loop. Isolation of the inferior mesenteric vein and dissection of the tunnel behind the body of pancreas As shown in Figure 2, the transverse colon and its mesentery were elevated cephalically, followed by flipping the small bowel to the patient’s right side to facilitate exposure and dissociation of the IMV. The IMV can be traced up to the IMV-SV confluence for rapid identification by mobilization of the retroperitoneal attachments down to the level of the body of the pancreas. There are no direct anterior branches to the IMV-SV confluence. So, the anterior surface of the vein confluence was separated by blunt dissection from the pancreas, creating a tunnel behind the body of the pancreas, and the body of the pancreas was encircled with a vessel loop (Fig. 3). Transection of the stomach, jejunum, and pancreas The stomach and jejunum were divided using a linear stapling device in a standard Whipple procedure as shown in Figure 4. The pancreas may then be divided as usual. We normally divide the pancreas with stay sutures and a knife, controlling bleeding on the “pancreatic remnant
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Figure 3. (A) Schematic diagram and (B) intraoperative photograph: creating the tunnel between the anterior surface of the splenic vein and the posterior surface of pancreas, the body of pancreas was encircled with a vessel loop. IMV, inferior mesenteric vein.
Figure 2. (A) Exposing the inferior mesenteric vein after dividing the peritoneum to the left of the duodenojejunal flexure in the transverse mesocolon. (B) Intraoperative image demonstrating the area of incision of the peritoneum at the duodenojejunal flexure. The small bowel is displaced to the right of the patient, and the colon is displaced toward the head of the patient. IMV, inferior mesenteric vein.
side” with 3-0 absorbable sutures and on the “specimen side” with penetrating ligature and cautery. A vascular forceps was passed behind the body of the pancreas to elevate and protect the vein during division. On either side of the proposed line of transection, 3-0 silk stay
sutures were placed on the superior and inferior borders of the pancreas. The superior and inferior borders of the pancreas on the “specimen side” were exposed by dividing the overlying peritoneum, and the venous tributaries of the SV were ligated and divided. Isolation of the specimen and clearance of the superior mesenteric artery After ligating and dividing some of the easily accessible SMPV tributaries, the dissection plane could be continued in a cephalad direction along the anterior aspect of the superior mesenteric artery (SMA) toward its origin. Dissection of the SMA was maintained on the right hemicircumference until the posterior aspect of the SMA was reached (Fig. 5). Branches to the pancreatic head and uncinate coming off the right side or the
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Figure 5. Clearance of the superior mesenteric artery (SMA). IMV, inferior mesenteric vein; SMV, superior mesenteric vein.
Figure 4. (A) Schematic diagram and (B) intraoperative photograph: the pancreas is transected immediately to the right of the plane in which the inferior mesenteric vein (IMV) enters into the inferior border of the pancreas. SMV, superior mesenteric vein; SV, splenic vein.
right posterior edge of the artery were tied or clipped. The many variations of the SMA-first approach allow the pancreatic head to be completely freed from retroperitoneal surrounding tissues, as described by others.12,13 At this stage, the pancreatic head was held in place only by tumor adhering to the SMPV structures. The involved segment of vein can then be clamped proximally and distally at least 0.5 to 1 cm away from the tumor and resected en bloc with the specimen. Splenic vein ligation occasionally resulted in gastrointestinal hemorrhage because of sinistral portal hypertension. We therefore attempted to preserve a part of the SMPV-SV confluence when technically possible to facilitate the venous anastomosis. The SMPV-SV confluence was entirely resected only when deemed necessary to complete a negativemargin PD.
Reconstruction of veins Patients requiring segmental resection of the SMPV underwent reconstruction with a primary end-to-end anastomosis whenever possible using 5-0 synthetic, monofilament, nonabsorbable polypropylene suture (Ethicon Inc) in a running fashion and tied loosely (Fig. 6). It is possible to perform an end-to-end anastomosis even after excision of as much as 5 cm of the PV, SMV, or the confluence of these vessels.14 The tension at the venous anastomosis site is reduced by a number of factors, including mobilization of the mesentery of the small bowel along with the right colon and the
Figure 6. Completed procedure. The superior mesenteric vein (SMV) has been anastomosed to the portal vein (PV) without a graft. IMV, inferior mesenteric vein; SV, splenic vein.
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Table 1. Demographic Data, Operative Characteristics, Perioperative Complications, Pathologic Findings, and Method of Vascular Reconstruction Variable
n Age, y, median (range) Sex, n (%) Male Female Operative characteristics Operative blood loss, mL, median Intraoperative transfusion, n (%) Packed red blood cells, U Pathologic characteristic, n (%) Adenocarcinoma Pancreas Bile duct Neuroendocrine carcinoma Tumor size, cm, median Degree of differentiation Well to moderately differentiated, n Moderately to poorly differentiated, n Positive pancreatic margin, n Positive bile duct margin, n Microscopically positive retroperitoneal margin, n (%) Perineural invasion, n (%) Lymphatic invasion, n (%) Vascular invasion, n (%) Vessel resected, n (%) SMPV or SMPV-SV confluence, n Preservation of a part of SV confluence Resection of entire SV confluence Method of reconstruction Primary end-to-end anastomosis with ligation of the SV, n Primary end-to-end anastomosis with revascularization of the SV, n Perioperative complications, n (%) Postoperative pancreatic fistula Grade A Grade B Grade C Postoperative hemorrhage/ulcer bleeding Intra-abdominal collection Delayed gastric emptying Wound infection/Superficial wound infection Pulmonary infection Reoperation, n Perioperative deaths,* n Postoperative hospital stay, d, mean (range) *In-hospital or within 30 days of operation. SMPV, superior mesenteric-portal vein; SV, splenic vein.
Data
8 53.5 (39e71) 6 (75) 2 (25) 475 1 (12.5) 2 7 6 1 1
(87.5) (75) (12.5) (12.5) 3.7 0 8 0 0
1 5 3 6
(12.5) (62.5) (37.5) (75)
8 6 (75) 2 (25)
0 8 3 (37.5) 1 (12.5) 0 1 (12.5) 0 1 (12.5) 1 (12.5) 2 (25) 2 (25) 1 (12.5) 0 0 13 (9e22)
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dissection the surrounding ligaments of liver.14,15 We attempted to preserve a part of the SMPV-SV confluence when technically possible to facilitate venous anastomosis. Whenever the entire confluence of the SMPV and SV is involved by the tumor, resection of these veins should be undertaken proximal to the confluence, and the SV is reimplanted into the SMV or PV in an end-to-side fashion. Reconstruction of the organs The remainder of the PD followed the standard protocol for a Whipple procedure. Pancreaticojejunostomy was performed using our standard protocol.16 The anastomotic area of pancreaticojejunostomy and biliary anastomosis were drained separately with open drains. Before closure of the abdomen, a visual inspection was performed to exclude narrowing of the SMPV system. The diameter of the anastomosis must be within 75% of the inflow vessel diameter. Pathologic analysis of the resected specimen Pathologic analysis followed a standardized system for the pathologic evaluation of PD specimens established previously.17 The operative specimen was oriented and dissected by the surgeon and pathologist in a pathology suite in the operating room complex. The retroperitoneal margin was defined as the soft tissue margin directly adjacent to the proximal 3 to 4 cm of the SMA. A 2- to 3-mm, full-face (en face) section of the margin was evaluated by frozen-section microscopic examination, and the margin was interpreted as positive if tumor was observed on the section. The presence or absence of tumor cell infiltration of the segment of the resected vein wall was defined as the presence of neoplastic cells within the tunica adventitia and/or tunica media of the vein wall. Tumor size was calculated after surgical resection by measuring the greatest transverse diameter of the tumor. Postoperative care All patients received intravenous somatostatin (Stilamin [Serum International], 3 mg/12 hours, for 5 days). No anticoagulant drug was used perioperatively or postoperatively. While a drain was in place in the patient, the volume and amylase concentrations in the fluid collected from the peripancreatic drain were measured every other day. The timing of removal of the intra-abdominal drains in our institution has recently been set at approximately postoperative day 5.
RESULTS To date, we have performed this procedure in 8 patients. Patient demographics, operative characteristics, perioperative
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complications, and pathologic findings are listed in Table 1. Most patients exhibited adenocarcinoma of pancreatic origin. We attempted to preserve a part of the SMPV-SV confluence when technically possible. The SMPV-SV confluence was entirely resected in only 2 patients. In these 2 patients, intraoperative attempts at mobilizing the proximal SV to the SMPV-SV confluence were unsuccessful; neoplastic cells and marked fibrosis extended into the wall of the proximal SV. No patient was found to have a grossly positive retroperitoneal margin of excision. A microscopically positive retroperitoneal margin was found in only 1 of 8 patients. Neoplastic cells were found to invade the vein wall in 6 (75%) of 8 specimens. All patients were successfully discharged from the hospital after a median hospital stay of 13 days. Three of 8 patients suffered perioperative complications, but no patient had a complication clearly related to the vascular resection and reconstruction. No postoperative mortality, which was defined as death within 30 postoperative days, occurred in this series. No narrowing in blood vessels or thrombosis were detected by ultrasound within 2 weeks or during the regular follow-up every 3 months after the operation. No other severe morbidity (obvious pancreatic or bile leakage) was observed in this group in the postoperative period and follow-up.
DISCUSSION Management of tumor adherence or invasion to the SMPV represents the most challenging technical aspect of PD. To achieve complete resection of a pancreatic tumor, resection of the SMPV needs to be performed if there is suspected invasion of the venous wall. To adhere to the principles of oncologic surgery, this resection should be performed without violating the integrity of the tumor. The standard approach of creating a tunnel behind the neck of the pancreas, anterior to the SMPV axis, cannot be achieved when these veins are infiltrated with tumor or related inflammatory adhesions. If such a procedure were undertaken, the surgery would result in positive margins or the potential for venous injury. So, these tumors are frequently considered unresectable. This pattern of venous invasion is most likely to occur in tumors of the neck or medial aspect of the head of the pancreas. Depending on the site of tumor invasion of the SMPV and therefore, the extent of venous resection required, different technical options for resection and reconstruction are available. When the lesion is adherent to a small part of the lateral or posterior wall of the PV and SMV, dissection of the SMV and creation of a plane to the left of the PV on to the SV as standard Whipple procedure are possible. On the other hand, when the tumor involves
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a cylinder of the SMPV or when the anterior surfaces of the SMPV axis and posterior surface of the neck of the pancreas are both involved by tumor or related inflammatory adhesions, the pancreas must be divided further to the left, abandoning the usual plane of the neck of the pancreas. Many have adopted a selective approach for pancreatic transaction, with some authors claiming that the body of the pancreas should be divided with preservation and control of the SV, as in the “central pancreatectomy” procedure,18,19 and others believe that it is safe to directly cut the pancreas at the body of the pancreas and the SV to the left of the PV without isolation and revascularization of the SV.15,20-22 However, routine procedures dividing the body of the pancreas and isolating the SV include complex and troublesome maneuvers. There are many tributaries behind the pancreas that enter the anterior aspect of the SV, and these can be easily damaged during dissection, which is especially difficult in patients with peripancreatic inflammation and adhesions around the body of the pancreas.13 Moreover, directly cutting the pancreas at the body plane without isolating the SV would result in the potential for venous injury and uncontrollable bleeding and could necessitate total pancreatectomy and splenectomy. Strasberg and colleagues21 recently described a procedure termed WATSA, in which the pancreas and SV are divided just to the right of the contact between the splenic artery and the superior border of the pancreas without SV revascularization. However, their routine SV ligation results in the potential development of left-sided portal hypertension and hypertensive gastropathy and/or gastric variceal hemorrhage.23,24 The SV is divided when tumor invasion at its junction with the PV is evident, when extra mobility for a direct end-to-end anastomosis between the PV and SMV is necessary, and, rarely, when it is necessary to provide better exposure for a thorough nodal clearance and soft tissue dissection at the proximal SMA. There is controversy in the surgical literature as to the safety of occluding the SV in a Whipple procedure, with some authors claiming that most patients would have no problem because the venous flow from the spleen and stomach could return to the systemic vein or the SMV through the short gastric vein and the esophageal vein,25 avoiding the development of symptomatic portal hypertension.20,22,23 Others describe complications related to this problem,3,26 including patterns of venous collateral development after SV occlusion. Using CT to evaluate the remnant SV patency after division close to its junction with the PV during PD 6 to 8 months after surgery, Strasberg and associates20 found that all 5 patients exhibited a patent
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SV. Venous drainage from the spleen was shown to be channeled via multiple collaterals, and none of the patients developed splenomegaly. Obviously, previous studies are too small and too short to establish the safety of SV occlusion during a Whipple procedure,19,20,22 and the indications for and long-term outcomes resulting from such extended venous resections will require further study and elucidation. Distal splenic-renal shunt has also been advocated by some authors.27 However, it is our opinion that a mandatory reconstruction is not a universally accepted practice. We attempted to preserve a part of SMPV-SV confluence when technically possible. When a segment of the PV must be sacrificed, primary endto-end anastomosis should be made with preservation of all venous branches, including the SV, whenever feasible.19 Several previous reports have analyzed the paths of the IMV on MRI or multidetector CT. The 3 most common variants (SV, SMV, and the SMV-SV confluence) of the drainage sites of the IMV differ among these reports. The IMV drains into the SV in 42.3% to 56% of Caucasian patients10,28 and in 45% to 68.5% of East Asian patients.29-31 In this type SV, the IMV runs along the left side of the SMA and apart from the root of the SMA in most patients31 and enters the SV at a mean distance (entering point in relation to the portal confluence) of 1.66 cm (range 0.27 to 3.48 cm),10 which is chosen as the site of transection of the pancreas to attain negative margin as well as identify, control, and protect the SV. Moreover, there are no direct anterior branches to the IMV-SV confluence, which is the ideal alternative plane to create a tunnel between the anterior surface of veins and the posterior surface of the pancreas by blunt dissection. The key component of the technique described here is identification of the IMV, if drained into the SV, which serves as a guide to securely create the tunnel between the anterior surface of SV and the posterior surface of pancreas for transection of the pancreas as a standard procedure. Our contribution is mainly to provide an alternative approach to the specific problem of the involvement of the anterior surface of the SMPV axis by tumor. This type of tumor involvement often results in the tumor exhibiting positive margins and being unresectable. Furthermore, this technique may be very helpful when there is severe inflammation around the veins and when it is difficult to distinguish the scar from the cancer intraoperatively. The SV remains intact, and venous outflow from the spleen is preserved, thereby avoiding the potential development of left-sided portal hypertension and hypertensive gastropathy and/or gastric variceal hemorrhage. In a standard Whipple procedure, venous injury, uncontrollable bleeding from within the tunnel
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behind the neck of the pancreas, and transection across the tumor are not rare events. This new approach can provide controlled rescue.
CONCLUSIONS In conclusion, an alternative method of resection of tumors that involve of the anterior surface of the SMPV axis has been described. Early results suggest that the procedure is effective in attaining negative margin resections and avoiding the potential for venous injury and uncontrollable bleeding. Author Contributions Study conception and design: Chen, Mai, Liu Acquisition of data: Chen, Tan, Mai, Ke Analysis and interpretation of data: Chen, Tan, Mai, Ke, Liu Drafting of manuscript: Chen, Tan, Mai, Ke, Liu Critical revision: Chen, Tan, Mai, Liu Acknowledgment: The authors thank Ruizhi Zhang (Sichuan Institute of Building Research; Landscape Architecture, School of Architecture, Southeast University) for her assistance with the preparation of the schematic diagrams. REFERENCES 1. Warshaw A, Thayer S. Pancreaticoduodenectomy. J Gastrointest Surg 2004;8:733. 2. Mueller SA, Hartel M, Mehrabi A, et al. Vascular resection in pancreatic cancer surgery: survival determinants. J Gastrointest Surg 2009;13:784e792. 3. Bold RJ, Charnsangavej C, Cleary KR, et al. Major vascular resection as part of pancreaticoduodenectomy for cancer: radiologic, intraoperative, and pathologic analysis. J Gastrointest Surg 1999;3:233e243. 4. Riall TS, Cameron JL, Lillemoe KD, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinomadd part 3: Update on 5-year survival. J Gastrointest Surg 2005;9: 1191e1206. 5. Glanemann M, Shi B, Liang F, et al. Surgical strategies for treatment of malignant pancreatic tumors: extended, standard or local surgery? World J Surg Oncol 2008;6. 6. Vargas R, Nino-Murcia M, Trueblood W, Jeffrey RB. MDCT in pancreatic adenocarcinoma: prediction of vascular invasion and resectability using a multiphasic technique with curved planar reformations. AJR Am J Roentgenol 2004;182: 419e425. 7. Lu D, Reber HA, Krasny RM, et al. Local staging of pancreatic cancer: criteria for unresectability of major vessels as revealed by pancreatic-phase, thin-section helical CT. AJR Am J Roentgenol 1997;168:1439e1443. 8. Fuhrman GM, Charnsangavej C, Abbruzzese JL, et al. Thinsection contrast-enhanced computed tomography accurately
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