http://dx.doi.org/10.1016/j.hpb.2017.07.

007 HPB

ORIGINAL ARTICLE

The TRIANGLE operation – radical surgery after

neoadjuvant treatment for advanced pancreatic cancer: a
single arm observational study
Thilo Hackert, Oliver Strobel, Christoph W. Michalski, André L. Mihaljevic, Arianeb Mehrabi,
Beat Müller-Stich, Christoph Berchtold, Alexis Ulrich & Markus W. Büchler

Department of General, Visceral and Transplantation Surgery, University of Heidelberg, Heidelberg, Germany

Abstract
Background: Neoadjuvant therapy is an important strategy for locally advanced pancreatic cancer
(PDAC) as resection rates increase with modern chemotherapy regimens even in patients with arterial
tumor encasement. The aim of this study is the description of technique and initial outcomes of a new
type of radical and arterial-sparing resection after neoadjuvant treatment for locally advanced PDAC.
Methods: The surgical technique and perioperative results of a new type of operation are described,
comprising radical tumor removal by sharp dissection along the celiac axis and the superior mesenteric
artery with complete dissection of all soft tissue between both – arteries and superior mesenteric/portal
vein (TRIANGLE operation).
Results: 15 patients underwent artery-preserving tumor removal without mortality, 7/15 patients
showed postoperative complications and an R0 resection was achieved in 6/15 patients. Functional
outcome was good in 11/15 patients despite the extended approach of dissection.
Conclusion: After neoadjuvant therapy for locally advanced PDAC, surgical exploration should be
attempted in patients with stable disease or remission to clarify true vascular infiltration. In case of absent
viable tumor, the described technique allows to perform radical surgery without arterial resection in this
subgroup of patients.

Received 31 May 2017; accepted 29 July 2017

Correspondence
Markus W. Büchler, Department of General, Visceral and Transplantation Surgery, University of Heidel-
berg, Im Neuenheimer Feld 110, 69120 Heidelberg, Germany. E-mail: markus_buechler@med.uni-
heidelberg.de

Background margin along the SMA is the most frequent site of incomplete
tumor clearance.8 Especially with the neoadjuvant use of com-
Neoadjuvant therapy for borderline resectable (BR) and locally
bination chemotherapy regimens (i.e. FOLFIRINOX), resect-
advanced (LA) pancreatic cancer (PDAC) has become an
ability can be achieved in 40–60% of patients.2–4 The problem
important treatment option to increase the proportion of pa-
however is, that therapy response – especially in patients who
tients who can undergo resection leading to a better prognosis
receive FOLFIRINOX – is often hard to assess using conven-
and the chance of long-term survival in an otherwise palliative
tional cross-sectional imaging as it is not possible to differentiate
situation with very poor outcome.1–5 Regarding BR or LA
between viable tumor and fibrous tissue.3 For this reason it is
criteria, arterial involvement of the celiac axis (CA), the hepatic
current clinical practice that all patients with stable disease
artery (HA) or the superior mesenteric artery (SMA) is the
without a clearly visible regression of the tumor – are recom-
crucial point for surgical decision making,5 as resection of these
mended to undergo trial dissection even if an arterial vascular
arteries – although technically often possible – is associated
involvement may still be suspected from the radiologic
with a high perioperative morbidity and mortality and only
imaging.9
limited oncological benefit.6,7 Similarly the medial resection

HPB 2017, -, 1–7 © 2017 International Hepato-Pancreato-Biliary Association Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Hackert T, et al., The TRIANGLE operation – radical surgery after neoadjuvant treatment for advanced pancreatic cancer: a
single arm observational study, HPB (2017), http://dx.doi.org/10.1016/j.hpb.2017.07.007
2 HPB

The aim of this study was the description of technique and
report of perioperative short-term outcomes of a new surgical
technique called “TRIANGLE” operation for patients with LA
PDAC and stable disease following neoadjuvant therapy.
Methods
Patients
In a retrospective single-arm cohort study, patients with LA
PDAC or LA PDAC recurrence were recruited in the authors’
institution to evaluate the feasibility of resection after neoadju-
vant therapy. LA at the time of presentation was defined ac-
cording to the definition of the International Study Group for
Pancreatic Surgery (ISGPS5). In case of stable disease during re-
staging and good clinical performance status (ECOG 0-1), pa-
tients were scheduled for surgical exploration.
Surgical technique
After laparotomy and exploration of the abdominal cavity to rule
out peritoneal or hepatic metastases, the initial steps of the
operation were to determine if there was true arterial tumor
infiltration, along the CA, HA or SMA. To clarify this, an “artery-
first” maneuver was performed. As to date numerous variations
of artery-first maneuvers have been described,10 the strategy
depended on the results of preoperative imaging defining the site
of the most likely tumor infiltration. The SMA was approached
from a left-sided infracolic approach11 if tumors of the body or
tail of the pancreas were suspected to infiltrate the artery from
this direction or from a posterior approach12 in respective
situations.
Once the arterial level of suspected attachment/encasement
was reached, a frozen section was performed to confirm or
exclude viable tumor tissue at this site. In case of remaining
viable tumor, the decision to proceed is highly dependent on
individual considerations such as the technical possibility to
resect and reconstruct the respective artery as well as patient-
related factors. As the current evidence does not support
routine arterial resection in PDAC surgery, most patients will not
qualify for further surgical therapy at this point.5,7 In contrast, if
frozen section confirms fibrous tissue without viable tumor, this
offers the possibility to perform a radical but artery-sparing
procedure, the TRIANGLE operation. Fig. 1 shows a flow chart
of pre- and intraoperative decision making for the respective
patients.
Technically, the artery should be approached on the adven-
titial layer which opens longitudinally, once the adventitia has
been reached. The artery (SMA or HA/CA) can then be
followed in this layer until the site of fibrous adherence is freed
or continued to the origin of the aorta if there is tumor
extension along the neural or lymphatic plexi. All other surgical
steps are carried out as usual during partial pancreato-
duodenectomy (PD), distal (DP) or total pancreatectomy

Figure 1 Flow chart of pre- and intraoperative decision making

HPB 2017, -, 1–7 © 2017 International Hepato-Pancreato-Biliary Association Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Hackert T, et al., The TRIANGLE operation – radical surgery after neoadjuvant treatment for advanced pancreatic cancer: a
single arm observational study, HPB (2017), http://dx.doi.org/10.1016/j.hpb.2017.07.007
HPB 3

(TP) and superior mesenteric or portal vein resection and
reconstruction can be done when and as required. To achieve a
radical and oncologically complete resection, lymphadenectomy
of the respective area needs to be added. Lymphadenectomy
after neoadjuvant therapy is often more difficult due to fibrous
changes induced by neoadjuvant treatment and may therefore
result in a more extended lymph node dissection than usual to
achieve clearance of the entire soft tissue. The completed
dissection and resection reveals an anatomic triangle bordered
by the SMA, CA and portal vein confirming the complete
removal of all soft tissue usually contained within these borders.
The arterial structures (SMA and CA) should appear completely
skeletonized from the left (in case of DP) (Fig. 4) or the right
(in case if PD). If a total pancreatectomy has been performed,
both vessels will be skeletonized circumferentially. The coronary
vein is usually divided during the procedure when total
pancreatectomy is performed (Figs 2b,3b,5b) and a re-inser-
tion13 is not possible in most patients due to the extent of
resection. Therefore, stomach perfusion has to be critically
evaluated at the end of the operation and a distal or even
subtotal stomach resection may be required to avoid
congestion-related ischemia.
Patient data, surgical details and postoperative
outcome
Baseline parameters included age, sex, body mass index (BMI),
American Society of Anesthesiologist’s classification (ASA) and
Eastern Cooperative Oncology Group (ECOG) status. All pa-
tients underwent cross-sectional imaging (CT or MRI scan)
initially and after completion of neoadjuvant therapy and the
largest diameter of the pancreatic tumor was measured in the
axial imaging series in both examinations to determine therapy
response according to the RECIST criteria.14 Operative param-
eters included operation time, blood loss, the need for trans-
fusion and details of the surgical procedure. Postoperative
morbidity was classified according to the ISGPS definitions15,16
and the Clavien–Dindo classification.17 Histological workup of
the specimen was performed according to the Leeds protocol
defining an R0 resection as a minimum distance of 1 mm of
tumor cells to the resection margin.18
Results
15 patients underwent the “TRIANGLE” operation between 03/
2016 and 12/2016 following neoadjuvant therapy for LA-PDAC
(n = 14) or local PDAC recurrence (n = 1) with arterial infil-
tration at the time of diagnosis who were therefore considered
unresectable. Median age of the patients was 60 years (range
35–75 years), 8 were female, 7 male. Regarding co-morbidities,
10 patients were classified as ASA 2, the remaining 5 patients
as ASA 3. Preoperative BMI ranged from 19.8 to 28.7 (median
25) and ECOG performance status was 0 or 1 for all patients.
Median largest pre-therapeutic tumor diameter in cross-
sectional imaging was 34 mm (range 24–63 mm), whereas the
median diameter after completion of neoadjuvant therapy was
30 mm (range 21–60 mm). According to the RECIST response
evaluation, all patients showed stable disease, a reduction of
tumor diameter was observed in 11 patients, however this
decrease was <30% in largest diameter.
Median operation time was 320 min (range 180–488 min),
median blood loss was 1000 ml (range 300–1600 ml) and 5
patients required intraoperative transfusion of packed red blood
cells (1–6 units) or fresh frozen plasma (2–10 units).
Regarding histopathological workup, an R0 resection was
achieved in 6/15 patients, all R1 sites were located at peri-
pancreatic soft tissue margins, 9 patients showed a lymphovas-
cular and perineural tumor spread. Lymph node yield ranged
between 12 and 62 harvested lymph nodes and an N1 stage was
found in 10 patients (Table 1).
No postoperative mortality was observed, surgical morbidity
occurred in 7/15 patients, including fluid collection with
percutaneous drainage (n = 1), POPF grade B (n = 1), wound

Figure 2 a. CT scan (coronary reformatting) after neoadjuvant therapy. Tumor encasement (white circle) of CA and SMA. b. Intraoperative view
after total pancreatectomy and splenectomy with PV/SMV resection. The gray triangle, defined by PV/SMV, CA/HA and SMA, depicts the typical
view after completion of the resection

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Please cite this article in press as: Hackert T, et al., The TRIANGLE operation – radical surgery after neoadjuvant treatment for advanced pancreatic cancer: a
single arm observational study, HPB (2017), http://dx.doi.org/10.1016/j.hpb.2017.07.007
4 HPB

Figure 3 a. CT scan (coronary reformatting) after neoadjuvant therapy (patient 2). Circular tumor encasement (white circle) of the CA and SMA
(white arrows). No discrimination between viable tumor and residual fibrosis is possible in the CT scan. b. Intraoperative view after total
pancreatectomy, splenectomy, subtotal gastrectomy and portal vein resection (black arrow). CA and SMA are dissected without histological
evidence of tumor infiltration (white arrows). All soft tissue in the triangle between the arteries and SMV/PV is completely removed, no arterial
resection or reconstruction is required, histopathologically complete (R0) resection

Figure 4 a. CT scan (axial view) after neoadjuvant therapy. Tumor encasement of the CA extending to the HA (white circle). b. Intraoperative view
after distal pancreatectomy and splenectomy with SMV resection. CA and SMA are completely dissected (white arrows). SMV anastomosis
(black arrow), pancreatic cut margin (white circle). Histopathologically R1 (tumor cell proximity <1 mm) at the retroperitoneal margin

infections or abdominal fascia dehiscence (n = 3), chyle leak
(n = 1) and one re-operation due to colon perforation. Com-
plications were classified as Clavien–Dindo grade 3 (n = 5 pa-
tients) or grade 4 with the need for ICU care (n = 2 patients).
Median hospital stay was 13 days (range 7–41 days). There was
one readmission due to an infected fluid collection which was
successfully treated by percutaneous drainage but caused a
prolonged period of in-hospital stay.
Median follow-up of the included patients was 197 days (range
130–352 days). Three patients experienced tumor recurrence
(liver metastases n = 2, local recurrence n = 1) after 3, 7 and 11
months, respectively.
Regarding functional outcome, all patients after TP and two
patients after DP developed postoperative new-onset diabetes
mellitus with insulin therapy and all patients received long-term
oral pancreatic enzyme supplementation.
11 patients reported a good quality of life with stable weight
and no oral nutrition intake problems. Among the remaining
four patients, quality of life was compromised due to limited
mobilization (n = 2), the need for ongoing parenteral nutrition
(n = 1) and persisting diarrhea (n = 1).
Discussion
With the evolution of effective neoadjuvant therapy regimens,
the subgroup of patients with locally advanced PDAC who
qualify for a surgical exploration is increasing.2,3 Especially when
FOLFIRINOX is used in this setting, up to 60% of initially

HPB 2017, -, 1–7 © 2017 International Hepato-Pancreato-Biliary Association Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Hackert T, et al., The TRIANGLE operation – radical surgery after neoadjuvant treatment for advanced pancreatic cancer: a
single arm observational study, HPB (2017), http://dx.doi.org/10.1016/j.hpb.2017.07.007
HPB 5

Figure 5 a. CT scan (axial view) after neoadjuvant therapy showing a large residual soft tissue mass encasing the PV confluens and the CA
(white circle) and a metal bile duct stent inserted pre-therapeutically (white arrow). b. Intraoperative view after total pancreatectomy and
splenectomy with SMV resection showing the completely dissected triangle: CA-SMA-SMV/PV

unresectable patients may finally undergo successful resection.2
A majority of these patients, however, requires extended ap-
proaches, including venous and multivisceral resections. The
main unsolved problem after neoadjuvant therapy is the fact that
cross sectional imaging does not adequately reflect the extent of
therapy response and viable tumor tissue cannot be precisely
differentiated from residual fibrotic tissue.3,9 This is especially
important when arterial tumor encasement of the CA or the
SMA is present as a planned resection and reconstruction of
these arterial structures is not generally recommended, which
results in conversion to a palliative approach for these patients.5
Due to the failure of discrimination of viable tumor and fibrotic
tissue, however, many centers subject patients who show stable
disease after completion of neoadjuvant therapy without clear
tumor response to a surgical exploration to clarify this situation,
even if an arterial tumor encasement is still suspected from the
imaging preoperatively. To date, there are no valid recommen-
dations to further select these patients for surgery after neoad-
juvant therapy.19 A marked decrease of CA 19-9 or the utilization
of PET imaging may be helpful but clear cutoff values for CA 19-
9 or glucose uptake are not commonly accepted as standards. A
diagnostic laparoscopy may be performed as the initial step of the
surgical exploration to rule out peritoneal spread or liver me-
tastases and conversion to laparotomy can be restricted to pa-
tients with a localized tumor finding.
The surgical technique described above is a suitable approach
for such patients to achieve a complete and radical removal of the
tumor and associated lymphatic or perineural extension along
the arterial structures without requiring morbidity-prone arterial
resection and reconstruction. It should be considered once
intraoperative frozen section has ruled out a true and persisting
arterial infiltration by viable tumor. The specific feature of the
approach is the performance of the dissection in a tissue layer
directly on the arterial adventitia. In PD, a dissection technique
on the adventitial layer has been described for patients under-
going upfront surgery in case of tumors located in the caudal
head or uncinate process by Inoue and colleagues.20 This
approach has been defined as a “level 3” dissection to achieve
maximum radicality. However, it has not been widely adopted yet
and a similar technique in the neoadjuvant setting with the
specific feature of separating former tumor tissue converted to
fibrosis from the arterial wall in this dissection plane has not
been reported so far. The purposeful search for this layer and the
performance of the dissection along this plane facilitates the
resection after neoadjuvant therapy as a resection outside this
layer is much more difficult due to the fibrotic changes and
associated with the risk of unintended arterial injuries or a non-
radical tumor removal. Depending on the location of the tumor,
this approach can be performed in PD, DP or total pancreatec-
tomy which results in an exposure of the “triangle” from the
right, the left or circumferentially. For upfront PD without
neoadjuvant therapy, the concept of total mesopancreas excision
has been described in the past and standardized approaches have
been published, i.e. by Adham et al.,21 who described the aim of
achieving the triangle-shaped view after completed resection. As
during the described procedure, all structures of the autonomous
nerve system as well as all lymphatic tissue are removed, post-
operative diarrhea or chyle leaks may occur.22,23 In PD or DP,
respectively, the problem of autonomous denervation may
clinically not be relevant as the nerve structures along the
opposite circumference along the artery are still preserved. In
contrast, during TP clinical symptoms of long-lasting diarrhea
may be more pronounced and potentially difficult to treat.
However, these side effects have to be weighed against the benefit
of a radical tumor removal in an initially unresectable situation.
Postoperative chyle leaks are a well-known complication of
PDAC surgery and can mainly be treated conservatively with a
resolution of the chylous ascites within the first two or three
weeks postoperatively. The present collective of 15 patients
showed a good perioperative outcome without mortality and
with a morbidity rate that is within the expected range for
pancreatic surgery. However, it should be recognized that surgery
was performed in a high volume unit and such outcomes may
not be generalizable at a population level. The R0 resection in 6/

HPB 2017, -, 1–7 © 2017 International Hepato-Pancreato-Biliary Association Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Hackert T, et al., The TRIANGLE operation – radical surgery after neoadjuvant treatment for advanced pancreatic cancer: a
single arm observational study, HPB (2017), http://dx.doi.org/10.1016/j.hpb.2017.07.007
6 HPB

Table 1 Patient data of fifteen patients undergoing the described procedure

No. Patient age & gender Neoadjuvant therapy Operation Histopathology

1 55, m Gem/Abraxane pr Whipple ypT3N0 R0
2 67, f FOLFIRINOX Total PE, PV resection, splenectomy, subtotal gastrectomy ypT3N0 R0
3 49, f FOLFIRINOX Total PE, PV resection, splenectomy yp3N1 R1
4 59, m FOLFIRINOX DP, splenectomy, SMV res yp3N1 R1
5 70, f FOLFIRINOX DP, splenectomy, PV resection, gastrectomy, nephrectomy ypT3N1 R1
6 71, f FOLFIRINOX DP, PV resection ypT3N1 R1
7 67, m FOLFIRINOX Total PE, PV resection, splenectomy ypT3N1 R1
8 35, m FOLFIRINOX Total PE, PV resection, splenectomy ypT3N1 R1
9 68, m FOLFIRINOX Total PE, PV resection, splenectomy, subtotal gastrectomy ypT3N1 R1
10 53, f FOLFIRINOX Total PE, PV resection ypT2N0 R0
11 60, m FOLFIRINOX Remnant pancreatectomy, liver segment 2/3 R0
resection, gastrectomy for PDAC recurrence after PD
12 54, f FOLFIRINOX Total PE, PV resection, splenectomy ypT3N1 R1
13 57, f FOLFIRINOX Total PE, PV resection, splenectomy ypT3N1 R0
14 75, m FOLFIRINOX Total PE, PV resection, splenectomy ypT3N1 R1
15 73, f FOLFIRINOX Total PE, PV resection, splenectomy, subtotal gastrectomy ypT3N0 R0

Gem, gemcitabine; pr, pylorus-resecting; PE, pancreatectomy; PV, portal vein; DP, distal pancreatectomy; SMV, superior mesenteric vein; PDAC,
pancreatic ductal adenocarcinoma.

15 patients is comparable with the rate of patients undergoing
upfront resection for PDAC as when the pathological workup
was performed according to the protocol by Verbeke et al.18
Contrary to patients without neoadjuvant therapy,24 the clin-
ical impact of this strict definition after neoadjuvant therapy has
not been evaluated yet, mainly due to inconsistent pathology
reporting in many studies.25 A localization of an R1 position
towards the arterial resection margin would require an arterial
resection and reconstruction to achieve a more radical result.
Due to the high morbidity and mortality associated with this
type of operation, it does not seem reasonable to routinely
perform intended arterial resections during PDAC surgery.6,7
Instead, the opportunity to remove the tumor without arterial
resection seems to be safer and even an R1 situation in combi-
nation with adjuvant chemotherapy may provide better onco-
logical results than a merely palliative treatment approach which
would be the only option to avoid both – arterial resection as
well as the possibility to finally result in an R1 situation. Other
locally ablative treatment possibilities, i.e. irreversible electro-
poration (IRE), may be considered, however, large data on their
substitution therapy schemes but may have an additional impact
on postoperative quality of life.26
These potential debilitating postoperative consequences need
to have been fully discussed with patients who are being
considered for such surgery particularly in the light of the lack of
knowledge regarding the effect on oncological outcome.
In conclusion, the described technique offers the possibility
to achieve a radical tumor removal after neoadjuvant therapy
in locally advanced PDAC encasing the CA or SMA without the
need for an arterial resection and reconstruction. Conse-
quently, radical tumor removal can be achieved and the
considerable surgical morbidity and mortality of arterial re-
sections may be avoided. Whether such an approach ultimately
improves the long-term outcome for such patients is still to be
determined.
Conflict of interest
None declared.
References

efficacy after neoadjuvant treatment are not available to date.
Although follow-up data are limited in the reported collective,
functional outcome data seem to justify the radical surgical
approach. 11/15 patients had a good quality of life and only 2/15
patients showed clinically relevant diarrhea or inability to sup-
plement nutritional needs by oral intake alone. Due to the
advanced tumors a high proportion (10/15) patients received a
total pancreatectomy compulsorily leading to type 3c diabetes.
This situation can certainly be managed by modern insulin
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single arm observational study, HPB (2017), http://dx.doi.org/10.1016/j.hpb.2017.07.007
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