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Pancreatic Neuroendocrine
with Superior Mesenteric Vein–Portal
26
Vein Thrombus
Jeffrey A. Norton, E. John Harris and Robert T. Jensen
Introduction
Recent studies suggest that pancreatic neuroendocrine tumors (PNET) account for
10% of all pancreatic tumors [1]. Nonfunctional tumors are the most common type
of PNET. They can present as an incidentally identified pancreatic mass on a CT
done for another reason, or as a large invasive tumor with or without distant
metastases. Approximately 25% will have liver metastases [2]. In large nonfunctional PNETs, tumor thrombi may exist when the primary tumor invades through
the wall of one or more adjacent venous structures [3]. Tumor venous thrombi are
more frequently seen in renal cell cancer and hepatocellular cancer, and the treatment of this condition is well described. The incidence of venous thrombi with
PNETS, the clinical impact of these thrombi, and the optimal surgical treatment of
them, is unclear [4]. In patients with PNET that extend into the portal vein from
either the superior mesenteric vein (SMV) or the splenic vein (SV), we have
resected tumor from within these structures during the concomitant pancreatic
resection. This chapter gives an in-depth review of the surgical procedures
J.A. Norton (&)
Department of Sugery, Stanford University Medical Center,
300 Pasteur Drive, Room H3591, 94305-5641 Stanford, CA, USA
e-mail: janorton@stanford.edu
E. John Harris
Division of Vascular Surgery, Stanford University Medical Center,
300 Pasteur Drive, H-3641, 94305 Stanford, CA, USA
e-mail: edjohn@stanford.edu
R.T. Jensen
Digestive Diseases Branch, National Institutes of Health, Bdg. 10,
Rm 9C103, 20892 Bethesda, MD, USA
e-mail: robertj@bdg10.niddk.nih.gov
© Springer International Publishing AG 2017
T.M. Pawlik et al. (eds.), Case-Based Lessons in the Management of Complex
Hepato-Pancreato-Biliary Surgery, DOI 10.1007/978-3-319-50868-9_26
339
340 J.A. Norton et al.
necessary to remove tumor thrombus from these structures, and the long-term
outcome of patients with these findings.
Case Studies
Case #1
A 54-year-old truck driver from Oregon presents with hematemesis. He has had two
episodes in which he was vomiting up large amounts of blood and he has had six
units of pRBCs during the intitial episode and three units during the second episode. CT shows large gastric varices secondary to splenic vein occlusion by a large
pNET that involves the body and tail of the pancreas, with extension into the portal
vein (Fig. 26.1). There is tum or thrombus in the portal vein, without any evidence
of distant metastases.
The splenic artery was embolized with coils on the night before surgery by
interventional radiology. PNET resection required subtotal pancreatectomy with
Fig. 26.1 Computed tomography (CT) of a pancreatic neuroendocrine tumor (T) in the body of
the pancreas that obstructs the splenic vein with extensive short gastric collaterals and extends into
the lumen of the portal vein
26 Pancreatic Neuroendocrine with Superior Mesenteric … 341
Fig. 26.2 Drawing of the tumor in Fig. 26.1 at surgery just prior to resection. One can see that
the pancreas is transected and oversewn to the right of the superior mesenteric vein (SMV)/portal
vein confluence. The coronary vein is ligated and divided. Vascular control of the portal vein and
SMV proximal and distal to where the tumor extends through the splenic vein into the portal vein
is obtained prior to resection of the tumor within the portal vein and splenic vein
splenectomy, obtaining proximal and distal control of the portal vein, and extraction
of tumor thrombi from portal vein (Fig. 26.2) with patch closure of portal vein
(Fig. 26.3).
Case #2
A 67-year-old man who presents with pain after eating, and weight loss. CT
demonstrates a 3 cm pancreatic mass in the uncinate portion of the head abutting
the SMV (Fig. 26.4), with subsequent evidence of invasion into the lumen
(Fig. 26.5). EUS was performed and FNA of the pancreatic head tumor shows
NET. At surgery he had a Whipple pancreaticoduodenectomy with obtaining
proximal and distal control of the SMV , portal vein and splenic vein; given heparin;
and removing the tumor thrombus from the portal vein and using a venous patch to
reconstruct the SMV at the venotomy (Fig. 26.6).
342 J.A. Norton et al.
Fig. 26.3 Drawing of closure of a portal vein venotomy with a bovine patch. Proximal and distal
control of the vein is obtained with vascular clamps. A venotomy is made and the tumor within the
portal vein is excised. Following the excision of tumor a pericardial patch is used to reconstruct the
vessel and not narrow the lumen
Fig. 26.4 Computed tomography (CT) of a neuroendocrine tumor (NET) in the uncinate portion
of the head of the pancreas
26 Pancreatic Neuroendocrine with Superior Mesenteric … 343
Fig. 26.5 The same PNET as seen in Fig. 26.4 extends through the wall of the superior
mesenteric vein into the lumen of the portal vein (T) on superior CT cuts
Fig. 26.6 Drawing of the PNET in Fig. 26.5 that extends into the SMV and is in the process of
being removed surgically. Note vascular control of the SMV, portal vein, and coronary vein is
obtained prior to excision
344 J.A. Norton et al.
Proximal and distal control of the portal v ein, splenic vein, inferior mesenteric
vein, and the superior mesenteric vein is done with vessel loops and vascular
clamps, as seen in Fig. 26.2. Any other smaller branches are ligated and divided.
Systemic heparin is given at a dose of 100 Units per Kg IV prior to clamping. We
incise the vein and use a spatula to mobilize the thrombus. It may require excision
and reconstruction of the vein wall. This can be done with a pericardial patch
venoplasty, shown in Fig. 26.3, a superficial femoral vein patch, or interposition
graft. After closure of the vein, the heparin is revered with protamine at a dose of
1 mg per 100 units of heparin infused. We start 81 mg per day of aspirin on
postoperative day 1. We do not use any other type of anticoagulation. Portal vein
thrombectomy is either done with concomitant Whipple pancreaticoduodenectomy
or subtotal pancreatectomy with splenectomy.
Clinical Pearls
• Proximal and distal control is necessary
• Ligate small posterior branches. Make sure that vein is free without any
branches
• Draw a line on interposition vein to maintain proper orientation
Results
We have published a series of 46 patients with major vascular abutment, involvement, or encasement who underwent surgery to remove all gross neuroendocrine
tumor [2]. Our series is contrasted to a more recent series from MD Anderson [1].
They reported on nine patients with PNETs who underwent portal venous tumor
thrombectomy. The mean age was 42 and 51, respectively. There were approximately 50% men in both studies. Our study had a much higher percentage of MEN-1
(i.e., 26% compared to 0%). The mean tumor size was similar, approximately 5 cm.
Most of their tumors were in the body and tail, while most of ours were in the head.
Although not all of the head tumors in our experience required a Whipple pancreaticoduodenectomy, the rate was 23%. Whipple was performed in one-third of
patients with pancreatic head tumors. The Ki67 rate was between 1 and 2% for all
our tumors because we selected them based on a low malignant potential, which is
defined as a positive SRS scan or a Ki67 < 2%, while theirs had a high rate in several
patients, and all except one was treated with preoperative chemotherapy. Each of
their patients had blood vessel involvement while only 34% of ours had it. Since our
patients had less blood vessel involvement; we performed fewer venotomies and
vascular reconstructions (Table 26.1 and 26.2).
26 Pancreatic Neuroendocrine with Superior Mesenteric … 345
% vessel
involvement
% head of
pancreas
NET Size
(cm)
%
MEN1
Table 26.1 Demographics of patients with PNETs and vascular involvement from two series
% functional
NET
Mean
age
(range)
%
Men
involvement
Study # patients with pNET + vascular
0 0 5.4 11 100
70 26 5.8 59 34
(24-76)
(38-67)
93351
46 46 42
Stanford
MD
NIH
Anderson
346 J.A. Norton et al.
Table 26.2 Extent of surgery, complications, disease status, and survival
Study % Up front
MD
Anderson
Stanford
NIH
chemotherapy
67 11 89 Not listed 33% 78% at
0 23 20 27 and no deaths 30% 60% at
% Whipple
procedures
% Vascular
resection and
reconstruction
% complications
(deaths)
%
Disease-free
Survival
3 years
10 years
However, the two illustrative cases presented here had tumor thrombus within
the vessel that can be excised with a spatula, except where it entered the vessel. We
used heparin for our venous procedures, and reversed it with protamine after the
procedure on the vessel was completed; however, it is controversial, and some do
not use it. We reconstructed the portal or superior mesenteric vein with a vein patch
from the femoral vein, or a bovine pericardial patch, while some others use the
internal jugular vein, but that is used more for complete replacement of these
vessels. We had no cases developing thrombosis of the portal vein, as we have
followed the flow through this vessel with Doppler ultrasound. These procedures
are done with acceptable morbidity and no operative mortality. The disease-free
survival was approximately 30% in both studies, and the long-term survival is
between 60 and 70%, suggesting that it is worthwhile to perform this more
aggressive surgery [1, 2].
Alternative Approaches
• Alternative systemic treatment
• Manage bleeding gastric varies with either sclerotherapy or embolization
of splenic artery
Discussion
Malignant pancreatic neuroendocrine tumors have a good prognosis [5–9].
Unfortunately, a significant proportion present late, with large tumors that encase or
invade adjacent blood vessels [3]. A number of studies have demonstrated that
vascular invasion with PNETs is associated with decreased survival [5, 10, 11]. The
surgical approach to this group of patients is controversial. Based on analogies to
pancreatic adenocarcinoma and limited experience with attempted surgical resection of patients with advanced PETs, for many, involvement of the superior
mesenteric vein (SMV), and portal vein (PV) is a contraindication to surgical