ORIGINAL ARTICLE
Pancreatectomy for Pancreatic Cancer with Reference to
Combined Resection of the Vessels,
Twenty Nine Year Experience by a Single Surgeon
Yoshiaki Sugiura,1 Takuya Horio,2 Satoshi Aiko,2 Takamitu Ishizuka,2 Isao Kumano,2Yutaro Kato,1 Ayu Kato1 and Masaki Kitajima1

Department of Surgery and Gastroenterology,
International University of Health and Welfare Mita Hospital, Tokyo, Japan2
Department of Surgery II, National Defense Medical College, Saitama, Japan
1(Received for publication on March 25, 2008)(Revised for publication on December 25, 2008)(Accepted for publication on January 15, 2009)

Abstract
Between 1978 and 2007 one hundred and seven patients consecutively underwent resection
for primary pancreatic adenocarcinoma. There were 28 pN0 patients, 41 pN1 and 37 pN2 ormore (one unknown). Combined resection of the portal vein was performed in 62 out of 107
patients (58%). The hepatic artery in 10 patients, superior mesenteric artery in 8 patientsand celiac trunk in 7 patients were also resected additionally to the portal vein. The 5-year
survival rate and 10-year survival rate of all 107 cases were 12.1% and 2.8% respectively.
The 5-year survival rate of the pN0 group was 37%, significantly better than the 14% 5-year
survival rate in the pN1 group (p=0.043). Of 69 patients with pN0 or pN1, 38 patients underwent combined resection of the portal vein. There was not significant difference between
the 24% 5-year survival rate in the group without the portal vein resection and the 19%
5-year survival rate in the group with portal vein resection. The 20% 5-year survival rate of
the portal vein only group and the 5-year survival rate of both the portal vein and hepatic
artery group were the same. The groups of the further resection of the superior mesentericartery and of the celiac trunk showed no long-term survival. It is concluded that aggressive
combined resection of the portal vein or additional resection of the hepatic artery be feasible
for a survival benefit in pN0 and pN1 diseases. (Keio J Med 58 (2) : 103－ 109, June 2009)

Keywords: pancreatic cancer, pancreatectomy, portal vein, hepatic artery
Introduction
Nothing else than pancreatic cancer has been so muchoperated, by so many surgeons, to so few long-term survivors. When pancreatic cancer is detected, the lesion isalready grown enough to destroy desmoplastically thesurrounding soft tissue, vessels or organs. In Japan combined resection of the portal vein and wide resection of
the lymphnode around the aorta have prevailed as feasible in an advanced facility. Despite extended retroperitoneal lymphadenectomy or extended surgery the patient’s
survival rate was not yet improved.1 The outcome wasanalyzed by focusing on feasibility of combined resection of the major vessels.
Patients and Methods
Between 1978 and 2007 one hundred and seven patients consecutively underwent resection for primarypancreatic adenocarcinoma excluding mucin producing
carcinoma, cystadenocarcinoma, endocrine tumor aswell as solid pseudopapillary tumor (resectability 50%).
There were 69 males and 38 females. The ages ranged
from 23 to 79 years (mean 62±10). The procedures were

Reprint requests to: Yoshiaki Sugiura, M.D., IUHW Mita Hospital, 1-4-3 Mita Minato-ku, Tokyo 108-8329, Japan, E-mail: ysugiura@iuhw.ac.jp103Sugiura Y, et al: Pancreatectomy with Reference to Resection of the Vassels

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Table 1
PV resection and plus α
procedurenPV resection

HA

SMA

Ce

total pancreatectomy

28

23

3

4

7

PD or PpPD

64

35

6

4

0

distal pancreatectomy

15

4

1

0

1*

toal

107

62

10

8

8

(HA=hepatic artery, SMA=superior mesenteric artery, Ce=celiac trunk)(* independent resection)

decided by the location of the main lesion as 64 pancreatoduodenectomies or pylorus preserving pancreatoduodenectomies, 28 total pancreatectomies and 15 distal
pancreatectomies (Table 1). Four patients died in thehospital, of complication due to surgery (mortality rate3.7%). All patients underwent lymphadenectomy aroundthe pancreatic head, in the hepatoduodenal ligament,along the common hepatic duct and the right side of superior mesenteric artery. The paraaortic node was pickedjust behind the pancreatic head. The lymphnode status
was classified as pN0: no metastasis, pN1: metastasis
only in the local node which attaches to the pancreas parenchyma, pN2: metastasis in the regional node which isable to resect easily by a competent surgeon and pN3:
metastasis in the far node which cannot be resected without resection of the organs, due to the location of cancer
in the head, body and tail, respectively, modifying theGeneral Rules for Study of Pancreatic Cancer.2 There
were 28 pN0 patients, 41 pN1 and 37 pN2 or more.
Combined resection of the portal vein was performed in
62 out of 107 patients (58%). The portal vein and superior mesenteric vein were resected on grounds of preoperative CT findings and the intraoperative judgment, ligating the distal splenic vein. The superior mesenteric arteryand celiac trunk were indicated to resection also on
grounds of preoperative CT findings and the intraoperative judgment. Anastomosis of a vessel was done in theend to end fashion using a graft in cases. The hepatic artery was resected when the gastroduodenal artery was
impossible to sever from the common hepatic artery forinvasion of carcinoma, anastomosing the common hepatic artery and proper hepatic artery. The portal vein wasresected in 35 of 64 pancreatoduodenectomies or pylorus
preserving pancreatoduodenectomies (55%), 23 of 28 total pancreatectomies (82%) and 4 of 15 distal pancreatectomies (27%). The hepatic artery in 10 patients, superior mesenteric artery in 8 patients and celiac trunk in
7 patients were also resected additionally to the portal
vein.
The actuarial survival rate was calculated with the Ka-

plan Meier method. The difference of the two groups
was examined with Logrank test defining the P valueless than 0.05 as significant. All 107 cases including
deaths in the hospital and later deaths due to other causes
than cancer recurrence were used for these statistics.
Results
The 5-year survival rate and 10-year survival rate of
all 107 cases were 12.1% and 2.8% respectively. The
5-year survival rate of the pN0 group was 37%, significantly better than the 14% 5-year survival rate in the
pN1 group (p=0.043). In the patients with positive nodes
the pN1 group could live significantly longer than thegroup with pN2 or more (Fig. 1). Of 69 patients with
pN0 or pN1, 38 patients underwent combined resectionof the portal vein. There was not significant difference
between the 24% 5-year survival rate in the group without the portal vein resection and the 19% 5-year survival
rate in the group with portal vein resection (Fig. 2). Further resection of the hepatic artery was performed in 5
patients out of 69 patients with pN0 or pN1. The 20%
5-year survival rate of the portal vein only group and the
5-year survival rate of both the portal vein and hepatic
artery group were the same(p=0.88) (Fig. 3). A 65 y-omale with pancreatic head cancer lived more than five
years. The hepatic artery was combinedly resected as thegastroduodenal artery was difficult to sever from thecommon hepatic artery for invasion of carcinoma. There
was histologic invasion to the gastroduodenal artery but
not to the hepatic artery. The groups of the further resection of 6 cases of the superior mesenteric artery and of 5cases of the celiac trunk showed no long-term survival(Fig. 4, 5).
Last fifteen patients of this series have had adjuvant
chemotherapy. The results are not yet evaluated for the
short observation period. A noteworthy patient is a62-y-o female who underwent Pylorus preserving Pancreatoduodenectomy and combined resection of the portal vein for pancreatic head carcinoma. The pathology

Keio J Med 2009; 58 (2):103－ 109

105

Fig. 1 Survival curves due to pN. The 5-year survival rate of the pN0 group was 37%, significantly better than the 14% 5-year
survival rate in the pN1 group (p=0.043). In the patients with positive nodes the pN1 group could live significantly longer than thegroup with pN2 or more (p=0.015).

Fig. 2 Of 69 patients with pN0 or pN1, 38 patients underwent resection of the portal vein. There was not significant difference
between the 24% 5-year survival rate in the portal vein “No” group (solid line N) and the 19% 5-year survival rate in the portal vein “Yes”
group (broken line Y) (p =0.11).

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Sugiura Y, et al: Pancreatectomy with Reference to Resection of the Vassels

Fig. 3 Further resection of the hepatic artery was performed in 5 patients out of 69 patients with pN0 or pN1. The 5-year survival rateof the portal vein only group (solid line N: Hepatic artery “No”) was 20% while the 5-year survival rate of both the portal vein and hepatic
artery group (broken line Y: Hepatic artery “Yes” ) was same (p=0.88).

Fig. 4 Further resection of the superior mesenteric artery(SMA) was performed in 6 patients out of 69 patients with pN0 or pN1. Six
patients (broken line Y: SMA“Yes”) tended to live less longer than the group of the portal vein only (solid line N: SMA“No”) (p=0.07).

Keio J Med 2009; 58 (2):103－ 109

107

Fig. 5 Further resection of the celiac artery(CA) was performed in 5 patients out of 69 patients with pN0 or pN1. The survival curveof the 5 patients (broken line Y: CA“Yes”) showed no long-term survival as compared to the group of the portal vein only (solid line N:
CA“No”). There was no significance.

was invasive duct carcinoma invading the adventitia of
the superior mesenteric vein. One lymphnode behind thepancreatic head was involved. As two years later Carcinoembrionic Antigen was elevated, Gemcitabine of ten
courses was administered for 14 months and the tumor
marker was decreased. However, five years later the patient complained of back pain. A PET scan revealed amass on the abdominal aorta. After the S1 and Gemcitabine combination therapy for six months, the mass
was diminished on a PET scan.
Discussion
Why does a surgeon majoring in pancreatic cancer
continue to resect pancreatic cancer despite the miserable
postoperative outcome? One answer is that an advanced
cancer of the pancreas has never been reported to be
cured with chemotherapy only so far, thus we have paid
an effort to resect 37 cases of pN2 or more diseases and62 cases of portal vein infiltration. Since ten years ago
gemcitabine has been used for unresectable pancreaticcancer with a safety.3 The clinical response was recognized as relieving consistent painful complaints, however, long-term survivors have hardly been reported.4 A patient could live for a few years at the longest.5 Various

combinations of chemotherapy were developed. In Japancombination therapy using T-S1 and Gemcitabine isnoteworthy to have a high response rate at the present
time.6, 7 Antecedent T-S1 given everyday for seven days
and gemcitabine infused at the eighth day prolonged thepatient’s survival rate to 47.7% at one year and 20.7% at
two years. Although a surgeon may be relieved to knowthat among the various choices of treatment, such as palliative surgery, radical surgery, chemotherapy or radiotherapy, results following resection with adjuvant
chemoradiation therapy were the best,8 adjuvant chemoradiation was not widely adopted in Japan.
The extent of lymphadenectomy in this series might beappropriate. It was never so wide as performed by Nagakawa.9 Additional paraaortic lymphnode dissection was
also limited just behind the pancreatic head. Patients’ recovery is delayed by lymphorrhea due to wide dissection
along the aorta none the less patients’ survival benefit
was not proven.1 0 Surgical strategy of the combined resection of the perilesional vessels was based on the results of our previous analysis1 1 released midway of thisseries that patients with small tumors invading either tothe portal vein or to the hepatic artery but neither to thesuperior mesenteric artery nor to the celiac artery could
have good prognosis if the tumor were completely re-

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Sugiura Y, et al: Pancreatectomy with Reference to Resection of the Vassels

moved. It does not change at the present time. Imaizumi
taught us that combined resection of the vessels gained
more radicality in patients of M0 and no metastasis in
the further lymphnodes.1 2
The 5-year survival rate of 26 patients of pN2 was 4%. There, what is worse than pN2 patients, were no
5-year survivors in pN3 disease. The stage of pancreaticcancer is dominantly defined by lymphnode metastasis.
The most of stage 4 patients are pN3 disease. There areclinically still detectable N3 nodes and more undetectable N3 even with the newest CT. It cannot be clarified
for small nodes until a surgeon extirpates them whether
they are positive or negative. Another answer to resection of pancreatic cancer despite the miserable postoperative outcome is that the boundary between the stage 4aand 4b among N3 diseases becomes apparent on the histologic examination. Concerning the clinical staging other than using CT and US, Fujioka1 3 reported that the
combined preoperative CEA and CA 19-9 levels predicted curability and they would be useful for selection of
the patients. Patients whose levels of CEA and CA 19-9
over 5.5ng/ml and 78U/ml respectively would have lesscurative surgery.
Of the 107 patients finally 13 patients could live over
5 years (12.1%), however, only 3 patients could live over
10 years (2.8%). The behavior of pancreatic cancer
seems different from other periampulary carcinomas.
Yeo1 4 noted that particularly for patients with pancreatic
adenocarcinoma, 5-year survival was not equated with
cure, because many patients died of recurrent disease
over 5 years after resection. Effective adjuvant therapy iseager to be established.
The study analyzing the one year survival rate and the
median survival time by Tani1 5 clarified that postoperative chemotherapy using 5-fluorouracil via the common
hepatic artery or/and gemcitabine systemically was essential for the improvement of survival in patients withlocally invasive pancreatic cancer. On the other side arandomized trial for eight years by Kosuge 1 6 demonstrated no clear survival benefit for the long-term observation period although there were more survivors in thesurgery and chemotherapy group after five and six yearsof surgery. Current adjuvant chemotherapy is to use anagent with less toxicity such as gemcitabine as Oettle1 7
showed in the randomized controlled trial. Gemcitabinesignificantly delayed the development of recurrent disease after complete resection of pancreatic cancer compared with observation alone. A surgeon should not forget adjuvant chemotherapy. Last fifteen patients of thisseries have had adjuvant chemotherapy not yet analyzed
for the short observation period.
How to select an object for adjuvant chemotherapy?
Histologic findings, the preoperative levels of tumor
markers or the postoperative tumor markers levels
checked at intervals at an out-patient clinic are clinicallyused. Another method is to utilize some factors correlating to prognostication. One of our colleagues1 8 proved
the marked correlation between cytoplasmic overexpression of the epidermal growth factor receptor and tumor
aggressiveness in patients with pancreatic carcinoma.
Another colleague 1 9 suggested that examination of
S-phase kinase-associated protein 2 expression might beclinically useful prognostication in patients with pancreatic carcinoma.
An experienced fighter pilot who has been long timehandling a control stick of pancreatic cancer would almost shout may-day, may-day midst of the whirling
cloud. However, it is clarified that aggressive combined
resection of the portal vein or additional resection of thehepatic artery be feasible for a survival benefit in pN0
and pN1 diseases.
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