Pancreatoduodenectomy (PD) for pancreatic head cancer under a non-touch isolation technique has been difficult because of the complex peripancreatic vascular anatomy. In 1981, we developed an anti-thrombogenic bypass catheter for the portal vein (PV) to prevent portal congestion (Fig. 1).[1–5] This was accomplished by bypassing the portal blood through a branch of the superior mesenteric vein (SMV) either to the femoral vein (Fig. 1A) during PV resection and reconstruction or to the intrahepatic PV through the umbilical vein in the hepatic round ligament (Fig. 1B), preventing both portal congestion and hepatic ischemia during simultaneous resection and reconstruction of the PV and hepatic artery. This method removed time limitations on portal occlusion during surgery. We have since been aggressively resecting pancreatic cancer with portal invasion using catheter-bypass of the PV.[6–9]
The first step in PD is typically Kocher's maneuver. When we started performing PD combined with PV resection in the 1980s, Kocher's maneuver was routinely used as the first step. However, we sometimes encountered pancreatic cancer with PV obstruction and well developed collateral veins when resecting such cancer using Kocher's maneuver, and massive bleeding sometimes occurred even if we applied catheter-bypass of the PV. Therefore, we developed a mesenteric approach, and isolated PD was completed.[11–18]
In cancer surgery, “isolated” means en bloc resection using a non-touch isolation technique. In PD, all arteries that supply the pancreatic head region and all drainage veins in this region are ligated and divided before manipulation of the pancreatic head cancer. Our first step in performing PD is a mesenteric approach; we do not perform Kocher's maneuver. This approach involves clearance of the connective tissues around the SMV and superior mesenteric artery (SMA) in the mesenteric root, which includes systematic lymphadenectomy around the SMA. Resection starts from the non-cancerous side and cancer-free surgical margin, and resectability can be diagnosed at the beginning of the operation. The inferior pancreatoduodenal artery (IPDA) arising from the SMA is ligated and divided first in this approach; this, it is an artery-first operation. This approach makes it possible to perform total mesopancreas excision (i.e., total excision of the second portion of the pancreatic head nerve plexus [PLph II], which is the so-called SMA margin) (Fig. 2). This is the most important technique with which to obtain a cancer-free surgical margin in PD for pancreatic head cancer. The mesenteric approach also makes it easy to reconstruct the PV by end-to-end anastomosis after PV resection.
Surgical techniques of the Nakao mesenteric approach
The supramesocolic approach is usually indicated for cancer of the distal bile duct or duodenal papilla of Vater. After laparotomy by an upper midline skin incision, the gastrocolic ligament is divided and the lesser peritoneal cavity is opened. The middle colic artery (MCA) and middle colic vein (MCV) are visible on the anterior surface of the mesocolon. The SMV and SMA are exposed along the roots of the MCV and MCA. The SMV and SMA are taped. The connective tissues, including the lymph nodes along the SMA, are dissected. The first jejunal artery (JA1) and IPDA are exposed by this procedure. Pre-operative multidetector computed tomography is very important to detect the location of the IPDA. Total mesopancreas excision is usually unnecessary for cancer of the distal bile duct or papilla of Vater. The supramesocolic mesenteric approach makes it easy to perform systematic lymph node dissection around the SMA and early ligation of the IPDA.
The inframesocolic approach is usually indicated for ductal adenocarcinoma of the pancreatic head. This is the typical Nakao mesenteric approach.
Laparotomy is performed with an upper midline skin incision. The abdominal cavity is examined using washing cytology and ultrasound.
The first step of isolated PD is the mesenteric approach, and the first step of the mesenteric approach is incision of the mesentery from the ligament of Treitz to the lower border of the second portion of the duodenum using electric cautery (Fig. 3). The surface of the mesentery is incised until the anterior walls of the SMV and SMA are exposed. With this approach, Kocher's maneuver is not performed.
Connective tissue clearance around the SMV and SMA
All of the connective tissues, including the lymph nodes around the SMV and SMA (no. 14d lymph nodes), are dissected to the lower border of the pancreatic head (Fig. 4). If no cancer invasion of the PLph II is observed, the nerve plexus around the SMA (PLsma) is completely preserved to avoid severe postoperative diarrhea. If cancer invasion into the PLph II or the PLsma is detected, the PLsma is resected to obtain a cancer-free surgical margin together with the PLph II. If it is difficult or impossible to obtain cancer-free surgical margins, the radical resection is stopped. Radical resection is also stopped when reconstruction of the SMV is determined to be impossible because of severe cancer invasion into the peripheral branches of the SMV.
Anti-thrombogenic catheter-bypass of the PV
When we determine that resection and reconstruction of the PV and SMV are possible even if the PV and SMV are severely stenosed or obstructed due to cancer invasion, the anti-thrombogenic catheter-bypass procedure of the PV will be applied to reduce PV congestion and operative bleeding (Fig. 5).
Division of the MCA and MCV
The MCA and MCV are exposed on the anterior side of the SMA and SMV. They are generally ligated and divided at the root. This makes it easier to perform connective tissue clearance around the root of the SMA (no. 14 lymph nodes) than preservation of the MCA and MCV.
Division of the gastrocolic ligament and incision of the mesocolon
The gastrocolic ligament is incised near the transverse colon, and the lesser abdominal cavity is opened. The mesocolon can therefore be examined from both the anterior and posterior sides, and the anterior surface of the pancreas can be visualized.
The root of the mesocolon is horizontally incised and resected, preserving the arcade of the MCA. Generally, no ischemic changes occur in the transverse colon by preservation of the arcade of the MCA. This makes it easier and safer to perform connective tissue clearance around the root of the SMA through the large opening in the mesocolon.
Connective tissue clearance around the root of the SMA and exposure of the mesopancreas (PLph II)
Connective tissue clearance around the SMV and SMA proceeds to the root of the SMV and SMA. All connective tissues of the mesenteric root are dissected, including the lymph nodes (no. 14d, p lymph nodes). The PLsma is preserved if cancer invasion to the PLph II or PLsma is not observed. The mesopancreas is exposed between the uncinate process of the pancreatic head and the SMA (Fig. 6). The term “mesopancreas” has been in use since 2007 by Gockel et al. However, there is no precise anatomical definition of the mesopancreas. In the Japanese classification of pancreatic cancer,[21,22] the anatomy of the extrapancreatic nerve plexuses are precisely described (Fig. 2), and I propose that “mesopancreas” refers to the PLph II (Fig. 2). During radical PD for pancreatic head cancer, the PLph I and PLph II are completely excised by the mesenteric approach.
Exposure of the jejunal arteries and IPDA and performance of total mesopancreas excision
The second and first branches of the jejunal artery generally lie behind the region of the SMA. The IPDA is usually a branch of the JA1 and lies within the region of the PLph II. There are many variations of the IPDA anatomy. Ligation and division of the IPDA (Fig. 6) and total excision of the PLph II (Fig. 7) from the attachment of the SMA complete the mesenteric approach (Fig. 7); that is, total mesopancreas excision is accomplished. Early ligation of the dorsal pancreatic artery from the SMA also reduces intraoperative bleeding. In patients with more locally advanced cancer, excision of the JA1 and second branches of the jejunal artery and total excision of PLsma may be necessary. If it is difficult to expose the IPDA or JA1 via the mesenteric approach, these vessels can be exposed by dividing the pancreas along the line of the SMA because the root of the SMA can be visualized easily. The mesenteric approach is completed by these procedures (Fig. 7).
Typical procedures after mesenteric approach to perform PD
After completion of the mesenteric approach, the operative field moves to the hepatic hilum. The gallbladder is resected along with the common hepatic duct. Clearance of the hepatoduodenal ligament including the lymph nodes (no. 12a, b, p) is performed, and the gastroduodenal artery is ligated and divided. The stomach is divided at the prepylorus, and lymph node dissection around the common hepatic artery (CHA) (no. 8a, p) and celiac artery (no. 9) is performed. The dorsal pancreatic artery from the CHA, celiac artery, or splenic artery will be ligated and divided by these lymph node dissection procedures. The PLph I is also dissected (Fig. 8). If cancer invasion into the PV or SMV is observed, the PV or SMV can be resected and reconstructed. End-to-end anastomosis of the portal reconstruction is easily performed by the mesenteric approach without tension. In the resection of the SMV–PV confluence, splenic vein reconstruction is generally unnecessary and left gastric vein preservation is very important to reduce left-sided portal hypertension[24,25] (Fig. 9). Simultaneous resection of the PV and CHA can be performed safely using catheter-bypass of the PV (Fig. 10). When we use anti-thrombogenic catheter-bypass of the PV, the catheter is extracted after vascular reconstruction. These procedures complete the isolated PD by the mesenteric approach.
Kocher's maneuver is the first step in PD. Based on extensive experience with vascular resection using anti-thrombogenic catheter-bypass for the PV in PD,[1–5] we have developed a mesenteric approach.[11,12] In our opinion, isolated PD using this mesenteric approach and anti-thrombogenic catheter-bypass for the PV if necessary is the ideal surgery for treatment of pancreatic head cancer from both a surgical and oncological viewpoint. No randomized controlled trials have compared the surgical and oncological merits between the Nakao mesenteric approach and Kocher's conventional approach in PD. However, in patients with resectable pancreatic head cancer, isolated PD using the Nakao mesenteric approach is suspected to result in higher survival than conventional PD using Kocher's maneuver. In this procedure, the mean operative time, intraoperative blood loss, harvested lymph nodes, and curative resection rate in resectable pancreatic head cancer are 417 min, 313 mL, 23, and 100%, respectively. The postoperative complications over grade IIIa according to the Dindo-Clavien classification was 17.9% with no mortality. The postoperative diarrhea after this procedure is commonly not observed by the preservation of nerve plexus around SMA. Therefore, a randomized controlled trial has been started in Japan to compare the surgical and oncological benefits of these 2 procedures. These problems are thus expected to be clarified in the near future. The mesenteric approach allows dissection from the non-cancer-infiltrated side and initial determination of cancer-free margins and resectability, followed by systematic lymphadenectomy around the SMA. This approach also enables early ligation of the IPDA, which reduces venous congestion of the pancreatic head region along with ligation of the gastroduodenal artery and total mesopancreas excision. This means that it is an artery-first operation. The term “mesopancreas” has no precise anatomical definition. We propose that it can be defined as the second portion of the pancreatic head nerve plexus according to the classification of pancreatic carcinoma described by the Japan Pancreas Society.[21,22] In addition, it is better to use the PLph I or PLph II instead of the mesopancreas. The Nakao mesenteric approach has been gradually adapted throughout Japan. By mastering this mesenteric approach, surgeons can successfully perform pancreatic cancer surgery.
We have herein described the precise surgical procedures of the Nakao mesenteric approach in PD for treatment of pancreatic head cancer.
We thank Angela Morben, DVM, ELS, from Edanz Group (www.edanzediting.com/ac), for editing a draft of this manuscript.
Conflicts of interest
The author declares no conflicts of interest.
. Nakao A, Horisawa M, Suenaga M, et al. Temporal portosystemic bypass with the use of the heparinized hydrophilic catheter. Jpn J Artif Organs 1982;11:962–965. (In Japanese with English abstract).
. Nakao A, Hirosawa M, Kondo T, et al. Total pancreatectomy accompanied by portal vein resection using catheter-bypass of the portal vein. Shujutsu 1983;37:1–6. (In Japanese).
. Nakao A, Kondo T. New technique of radical pancreatectomy with the use of the heparinized hydrophilic bypass catheter of the portal vein. Jpn J Artif Organs 1983;12:697–700. (In Japanese with English abstract).
. Nakao A, Kano T, Nonami T, et al. Application of an antithrombogenic Anthron bypass tube to experimental orthotopic liver transplantation. Studies on blood coagulation and fibrinolysis. ASAIO Trans 1986;32:503–507.
. Nakao A, Nonami T, Harada A, et al. Portal vein resection with a new antithrombogenic catheter. Surgery 1990;108:913–918.
. Nakao A, Harada A, Nonami T, et al. Clinical experience of 107 cases with portal vein resection using catheter bypass of the portal vein. Artif Organs Today 1993;3:107–112.
. Nakao A, Harada A, Nonami T, et al. Clinical significance of portal invasion by pancreatic head carcinoma. Surgery 1995;117:50–55.
. Nakao A, Harada A, Nonami T, et al. Regional vascular resection using catheter bypass procedure for pancreatic cancer. Hepatogastroenterology 1995;42:734–739.
. Nakao A, Kanzaki A, Fujii T, et al. Correlation between radiographic classification and pathological grade of portal vein wall invasion in pancreatic head cancer. Ann Surg 2012;255:103–108.
. Kocher T. Mobilisierung des duodenum und gastroduodenostomie. Zentralblatt für Chirurgie 1903;2:33–40. (In German).
. Nakao A, Takagi H. Pancreatoduodenectomy, non-touch isolation technique using catheter-bypass of the portal vein and Imanaga method. Shujutsu 1992;46:1457–1463. (In Japanese).
. Nakao A, Takagi H. Isolated pancreatectomy for pancreatic head carcinoma using catheter bypass of the portal vein. Hepatogastroenterology 1993;40:426–429.
. Nakao A, Takeda S, Inoue S, et al. Indications and techniques of extended resection for pancreatic cancer. World J Surg 2006;30:976–982.
. Nakao A. Selection and outcome of portal vein resection in pancreatic cancer. Cancers 2010;2010:1990–2000.
. Nakao A. Nakao A. Isolated pancreatoduodenectomy combined with portal vein resection. Isolated Pancreatoduodenectomy Nagoya: Takeda Printing Co., Ltd; 2014;3–11.
. Nakao A, Beger HG, Nakao A, et al. Extended resection for pancreatic cancer: risks and benefits. Pancreatic cancer, cystic neoplasms and endocrine tumors: diagnosis and management. Oxford: Wiley-Blackwell; 2015. 47–53.
. Nakao A. The mesenteric approach in pancreatoduodenectomy. Dig Surg 2016;33:308–313.
. Nakao A. Kim SW, Yamaue H. Concepts in isolated pancreatectomy for pancreatic cancer using Nakao mesenteric approach and catheter bypass of the portal vein. Pancreatic Cancer: With Special Focus on Topical Issue and Surgical Techniques 2017;Springer-Verlag Berlin Heidelberg, 225–230.
. Nakao A, Harada A, Nonami T, et al. Lymph node metastases in carcinoma of the head of the pancreas region. Br J Surg 1995;82:399–402.
. Gockel I, Domeyer M, Wolloscheck T, et al. Resection of the mesopancreas (RMP): a new surgical classification of a known anatomical space. World J Surg Oncol 2007;5:44.
. Japan Pancreas SocietyClassification of Pancreatic Carcinoma. 3rd English ed.Tokyo: Kanehara; 2011.
. Yoshioka H, Wakabayashi T. Therapeutic neurotomy on head of pancreas for relief of pain due to chronic pancreatitis: a new technical procedure and its results. Arch Surg 1958;76:546–554.
. Iede K, Nakao A, Oshima K, et al. Early ligation of the dorsal pancreatic artery with a mesenteric approach reduces intraoperative blood loss during pancreatoduodenectomy. J Hepatobiliary Pancreatic Sci 2018;25:329–334.
. Tanaka H, Nakao A, Oshima K, et al. Splenic vein reconstruction is unnecessary in pancreatoduodenectomy combined with resection of the superior mesenteric vein-portal vein confluence according to short-term outcomes. HPB 2017;9:785–792.
. Nakao A, Yamada S, Fujii T, et al. Gastric venous congestion and bleeding in association with total pancreatectomy. J Hepatobiliary Pancreatic Sci 2018;5:150–154.
. Hirono S, Kawai M, Okada K, et al. Mesenteric approach during pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. Ann Gastroenterol Surg 2017;1:208–218.
. MAPLE–PD trial: mesenteric approach vs. conventional approach for pancreatic cancer during pancreaticoduodenectomy. ClinicalTrials.gov, NCT03317886, UMIN000029615 Registered on 15 January 2018.