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294 A. Mittal et al.
Conclusion
Anomalous RHA anatomy is relatively common, and should be identified prior to
pancreatoduodenectomy. Preoperative planning is important in deciding whether to
preserve, sacrifice, or reconstruct an anomalous artery. The relationship of the
tumor to the origin of the anomalous RHA is important to note. Pancreat oduodenecotmy with or without arterial resection can be safely performed in patients
with anomalous RHA, although the evidence is derived from small retrospective
case series. Artery-first approach may be adopted in patients with anomalous RHA
anatomy to allow earlier identification and safer dissection during PD.
References
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Oncol. 2016;17(3):e118–24.
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defined by the International Study Group for Pancreatic Surgery is associated with worse
survival but not with increased morbidity. Surgery. 2015;158(1):183–90.
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resectable pancreatic cancer: a consensus statement by the International Study Group of
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(5):833–46.
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cancer. Surgery. 2015;158(1):191–200.
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pancreatoduodenectomy. Br J Sur. 2012;99(8):1027–35.
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12. Murugiah M, Windsor JA, Redhead DN, O’Neill JS, Suc B, Garden OJ, et al. The role of
selective visceral angiography in the management of pancreatic and periampullary cancer.
World J Surg. 1993;17(6):796–800.
13. Chong M, Freeny PC, Schmiedl UP. Pancreatic arterial anatomy: depiction with dual-phase
helical CT. Radiology. 1998;208(2):537–42.
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14. Tanikake M, Shimizu T, Narabayashi I, Matsuki M, Masuda K, Yamamoto K, et al.
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Pancreatic Adenocarcinoma
in the Neck of the Pancreas Involving
23
the Celiac Trunk (Appleby Procedure)
Richard A. Burkhart and Matthew J. Weiss
Introduction
Pancreatic ductal adenocarcinoma (PDA) is a devastating disease. Despite progress
in other malignancies, the only chance for cure remains complete surgical extirpation of locally confined disease. PDA arising in the neck or body of the gland is
insidious, often only becoming apparent after local or distant disease progression.
Here we review our approach to patients who present with locally advanced PDA in
the pancreatic neck involving the celiac axis. Our preoperative workup with laboratory and imaging analysis is detailed. Key considerations before entertaining
surgical resection via a modified Appleby procedure are highlighted. Intra-operative
decision-making and technical challenges are reviewed in detail. Peri-operative and
postoperative care is reviewed in the context of a case recently encountered at our
institution. Throughout, clinical pearls are offered to assist advanced pancreatic
surgeons in the management of these complex patients.
R.A. Burkhart
Department of Surgery, The Johns Hopkins Hospital, 600 North Wolfe Street,
Blalock 611, Baltimore, MD 21287, USA
e-mail: rburkha6@jhmi.edu
M.J. Weiss (&)
Department of Surgery, The Johns Hopkins Hospital, 600 North Wolfe Street,
Halsted 608, Baltimore, MD 21287, USA
e-mail: mweiss5@jhmi.edu
© 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_23
297
298 R.A. Burkhart and M.J. Weiss
Case Presentation
A 48-year-old woman with mild hypertension presents to your surgical clinic with a
chief complaint of vague upper abdominal discomfort for 9 months. Her pain is
described as mild, 2 out of 10 in intensity, persistent, and located in the mid
epigastrum. Associated symptom s include intermittent nausea and postprandial
bloating. She cannot identify any aggravating or alleviating factors. Her primary
care physician suspected gastritis and prescribed proton pump inhibitor therapy.
This failed to improve her symptoms and an abdominal contrast-enhanced computed tomography (CT) scan was performed. This demonstrated a mass-like lesion
appearing to arise from the neck pancreas and involving the common hepatic artery.
This lesion was 5 cm in size and hypodense in relation to the surrounding pancreatic parenchyma. She arrives in your clinic with her husband and children to
discuss surgical management of this disease.
Workup
Despite the improvements in survival seen in many types of gastrointestinal
malignancies, pancreatic ductal adenocarcinoma (PDA) remains a highly lethal
disease. The disease burden in the United States is increasing, with an incidence of
nearly 50,000 cases annually [1]. With mortality rates approaching the incidence of
the disease, a diagnosis of PDA can be devastating. Only 7% of patients will be
alive at 5 years, with nearly all having disease surgically resected while still locally
confined [1]. Despite being only the 12th most frequent cancer encountered in the
U.S., it is currently the fourth leading cause of cancer-related death. Epidemiologic
estimates suggest that PDA will surpass breast and prostate cancer to become the
second-leading cause of cancer-related death in the U.S. by 2030 [2].
When considering a diagnosis of PDA, the initial clinic visit should include a
review of the patient’s medical history in detail and a thorough physical examination. Common presenting symptoms for patients with PDA can be vague, particularly when disease is located in the neck or body of the gland. Historical review
of these patients finds abdominal pain to be present in nearly 90% of patients, with
other symptoms including weight loss, nausea, vomiting, diarrhea, jaundice, and
constipation occurring at a far less frequent rate [3]. A review of personal, family,
and social history should focus on risk factors for pancreatic disease (including, at a
minimum, a personal history of pancreatitis, cancer, or endocrine neoplasia; a
family history of malignancy; or a social history of tobacco use). Physical examination should include an evaluation for jaundice, lymphadenopathy, abdominal
mass, liver fullness or mass, pain in the back or abdomen, and presence or absence
of ascites. An evaluation of blood work during this initial visit should also be
completed and should include complete blood count, chemistry profile (including
liver function testing), and pancreatic tumor markers (carbohydrate antigen 19-9
and carcinoembryonic antigen).
23 Pancreatic Adenocarcinoma in the Neck … 299
High-quality contrast-enhanced cross-sectional imaging is imperative when
evaluating solid pancreatic masses. In many cases, the initial study obtained will be
insufficient to provide an accurate characterization of the lesion. Clinicians entertaining a diagnosis of pancreatic malignancy should not hesitate to repeat
abdominal imaging in these scenarios. Both CT and magnetic resonance imaging
are good options, with a preference in our institution for CT due to physician
experience and prefer ence. Technical keys to CT performance are optimal timing of
contrast administration (in both the arterial and portal venous phases) and highly
selective use of oral contrast (in practice, oral contrast is rarely necessary and can
sometimes prove detrimental when evaluating pancreatic pathology).
Unfortunately, as is the case in our patient (Fig. 23.1), tumors that arise in the
body and tail of the pancreas are more often large (>2 cm) and less likely amenable
to immediate surgical resection than those patients who have tumors in the head of
the gland [4, 5]. When this is the case, further workup is required to obtain a tissue
diagnosis and guide therapy. The most commonly used modality is endoscopy with
ultrasound and needle biopsy. An experienced endoscopist should focus on the
mass’ location and tissue of origin, evaluate the locoregional lymphatic drainage
basins, and evaluate for evidence of vascular encasement or invasion. Biopsy can be
performed with either fine-needle aspiration or core needle sampling, based on the
practitioner and institutional experience. After cross-sectional imaging in our
patient, she underwent endoscopy with ultrasound and fine-needle aspirate biopsy
to conclude her workup.
Fig. 23.1 Diagnostic imaging with contrast-enhanced computed tomography (CT) scan. Our
diagnostic preference is to obtain a high-quality, intravenous contrast-enhanced CT scan. The scan
should be completed with dual phase images, once during arterial enhancement and once during
portal venous enhancement. Here we show our patient with a 5 cm mass in the neck/body of the
pancreas (white arrow) that completely encases the celiac axis and its proximal branches
300 R.A. Burkhart and M.J. Weiss
Diagnosis and Staging
A diagnosis of PDA can be made definitely based on hist opathologic analysis of
biopsy specimens . Typical findings include pleomorphic and hypercellular fragments of tissue with ductal features in a relative paucity of acinar epithelium. The
nuclei are characteristically enlarged with irregular contours. Multinucleated cells
and mitosis are often encountered. Cells are often found to be arranged haphazardly
and with a lack of discernible polarity, often described as a “drunken honeycomb”
arrangement [6]. Once the diagnosis has been confirmed, information gleaned from
the patient’s physical exam, imaging studies, endoscopy, and histology are combined to accurately stage the patient’s disease.
The most common staging system used for PDA (Table 23.1) is derived from a
consensus of experts in conjunction with the American Joint Committee on Cancer
with a goal of facilitati ng treatment decisions and prognosis [7]. Currently in its
seventh edition, the backbone relies on an evaluation of the primary tumor
(T-stage), regional lymph nodes (N-stage), and presence or absence of metastasis
(M-stage). Final anatomic or prognostic staging involves grouping of T, N, and M
categories as can be seen in Table 23.1. The T and M-stage categories reflect the
major determinant of survival in PDA: the capacity for complete surgical resection.
When the primary tumor extends beyond the pancreas to involve the celiac axis or
the superior mesenteric artery for greater than 180°, the term locally advanced PDA
is used. This is generally regarded as unresectable disease (T4). In the absence of
metastatic disease, a T4 tumor is considered stage III disease regardless of nodal
status. When associated with evidence of metastasis a T4 tumor is considered stage
IV.
It is worth a moment to discuss issues that arise in delivering a diagnosis of PDA
in the clinic to our patient. As one of the most commonly encountered malignancies
causing death, she may have preconceived notions regarding the meaning of the
diagnosis. Certainly, there is a fair amount of nihilism that is associated with PDA
in the general public. Practically, it can be helpful to deliver this news, when the
patient allows, in the presence of family and her loved ones, as this support system
may be an important part of the overall treatment plans. It can also be helpful to ask
what they may know of the disease and use this as a starting point for counsel and
guidance with medical decision-making (reinforcing accurate notions and correcting knowledge gaps). Ultimately, it is important to provide your patient with
accurate clinical knowledge so she and her family can formulate clear and consistent goals of care throughout her treatment course.
At the time of diagnosis, only 20% of PDA are amenable to complete surgical
resection [8, 9]. Of the remaining 80%, approximately one-third will have locally
advanced disease without evidence of metastasis (stage III). Due to a high incidence
of perioperative complications and a high rate of disease recurrence with poor
response to adjuvant therapies, patients with stage III disease have rarely been
offered attempts at surgical extirpation in the past. However, improvements in
peri-operative outcomes and responses to systemic chemotherapeutics have led to
more aggressive approaches in a highly selected group of patients. In the case
23 Pancreatic Adenocarcinoma in the Neck … 301
Table 23.1 Pancreatic
cancer staging
Primary tumor (T)
Tis Carcinoma in situ
T1 Tumor limited to the
pancreas, <2 cm
T2 Tumor limited to the
pancreas, >2 cm
T3 Tumor extends beyond the pancreas
but without involvement of CA or
SMA
T4 Tumor involves CA or SMA
Regional lymph nodes (N)
N0 No regional lymph node metastasis
N1 Regional lymph node metastasis
Distant metastasis (M)
M0 No distant metastasis
M1 Distant metastasis
Anatomic stage
Stage 0 Tis N0 M0
Stage IA T1 N0 M0
Stage IB T2 N0 M0
Stage IIA T3 N0 M0
Stage IIB T1 N1 M0
T2 N1 M0
T3 N1 M0
Stage III T4 Any N M0
Stage IV Any T Any N M1
Adapted from the 7th edition of the AJCC cancer staging manual
[7]
CA celiac axis; SMA superior mesenteric artery
presented here, we will discuss the management of a stage III PDA with tumor in
the pancreatic neck and body with involvement of the celiac trunk and common
hepatic artery.
Technical Pearls
• Diagnostic laparoscopy prior to laparotomy for planned curative resection
can be used liberally in this patient cohort, as patients with unresectable or
metastatic disease rarely require intestinal or biliary bypass.
• Prior to addressing the technically challenging hepatoduodenal ligament
and superior pancreatic dissection, assessment of the retroperitoneal vasculature can be completed by mobilizing the duodenum and right colon
with wide kocherization and a Cattell–Braasch maneuver.
302 R.A. Burkhart and M.J. Weiss
• Liver perfusion is dependent upon retrograde flow through the gastro-
duodenal artery (GDA) to the proper hepatic artery. Double-check adequacy of flow with both palpation and Doppler before common hepatic
artery transection. Protect the GDA by transecting the pancreas well away
from its course over the pancreatic head and neck.
Preoperative Management
In a simplified model, patients such as ours with locally advanced PDA arising in
the neck and body of the pancreas can be separated into two groups (Fig. 23.2). In
the first group, patients are thought to have “poor” disease biology, with rapid local
tumor growth and evidence of early disease metastasis. The second group is said to
have “favora ble” disease biology, with a long period of time during which the
Suspicion of PDA in
neck of gland
History and physical
Labs: CA 19-9, CEA
Imaging: Pancreas protocol CT
Obtain Ɵssue diagnosis: EGD + FNA Biopsy
Confirm Stage III disease
Test disease biology:
Neoadjuvant treatment
Poor biology:
Tumor growth/metastasis
Treatment opƟons include:
Standard chemotherapy
Chemoradiotherapy
Clinical trial enrollment
Disease palliaƟon
Fig. 23.2 Treatment diagram outlining the steps taken when pancreatic ductal adenocarcinoma is
suspected in the neck of the gland. PDA pancreatic ductal adenocarcinoma; CA 19-9 carbohydrate
antigen 19-9; CEA carcinoembryonic antigen; CT computed tomography; EGD esophagogastroduodenoscopy; FNA fine-needle aspiration; MDC multidisciplinary conference
Favorable biology:
Stable disease burden
Restage with CT:
Confirm technical resectability
Seek MDC consensus
OperaƟve exploraƟon with
aƩempted resecƟon
23 Pancreatic Adenocarcinoma in the Neck … 303
disease burden will remain relatively stable, without further local growth or evidence of metastasis. It is this second group that may benefit from more aggressive
surgical therapies for local disease control. The rationale here is twofold: first,
identification of a group of patients in whom disease is truly limited to the gland
and surrounding structures where resection would therefore achieve cure (i.e., resect
all disease prior to metastasis); and second, identification of a group of patients in
whom survival will be driven primarily by local, rather than systemic, disease (i.e.,
systemic disease appears to be well controlled by chemotherapeutics).
Despite a plethora of research on the topic, there remains no prospective way to
dichotomize patients into these two biologic groups based on the tissue sampling or
clinical laboratory analysis at the time of diagnosis. As a result, our preferred
method for patient selection based on disease biology is by treating first with
non-surgical therapies and restaging at an interval. Experience with neoadjuvant
approaches to stage III PDA is increasingly being reported in the literature [10–12].
Combination cytotoxic chemotherapeutics, particularly modified fluorouracil, leucovorin, irinotecan, and oxaliplatin (mFOLFIRINOX) with or without radiotherapy,
is beginning to repeatedly demonstrate a capacity to downstage patients into a
surgical paradigm of management. In data focused primarily on pancreatic head
lesions, R0 resection in locally advanced disease can be achieved at rates exceeding
85% [10, 13, 14]. Experience with these regimens appears safe, with variable levels
of toxicity based predominantly on the appearance of side effects from systemic
chemotherapeutics.
Following neoadjuvant therapy, restaging of the patient should be performed as
a surrogate indicator of disease biology. “Favorable” biology, as evident by disease
stability or regression in combination with an absence of metastatic spread over
time, should be a trigger to critically evaluate the patient’s imaging for technical
barriers to surgical extirpation. In those patients with elevated CA19-9 levels upon
presentation, a decrease in that labor atory value may also be an indicator of
favorable disease biology. The importance of surgical resection for the group of
patients with favorable tumor biology and technically resectable disease should not
be trivialized. Surgical resection, even in a locally advanced cohort of patients,
remains the only chance for cure. Direct tumor invasion into adjacent locoregional
structures does not always preclude an operation. Shoup et al., for example,
demonstrated that patients requiring multivisceral resections for PDA of the body or
tail have improved survival over locally advanced patients who do not undergo
resection. Further, the long-term survival after multiv isceral resection is similar to
that following standard pancreatic resection [15].
PDA involving the celiac (CA) and common hepatic (CHA) arteries represents a
unique surgical challenge. En-bloc resection of these arterial structures has been
avoided in the past due to increased perioperative morbidity and questionable
benefit. As the relative oncologic benefit improves (better chemotherapies, favorable tumor biology), the perioperative morbidity may become acceptable for select
patients. Increased morbidity, as compared to standard distal pancreatectomy, is
largely due to the potential for ischemia from devascularization of the liver,
stomach, and spleen. In practice, ligation of the splenic artery is required for
304 R.A. Burkhart and M.J. Weiss
splenectomy, and carries little to no added morbidity. Similarly, ligation of the left
gastric artery should have little effect on a stomach with intact collateralization. In
stark contrast, however, devascularization of the liver remains a concern, as collateralization through the GDA is required to maintain adequate perfusion.
Resection of the distal pancreas and spleen, en-bloc with the CA, was first
described by Appleby in 1953 as a surgical therapy for locally advanced gastric
cancer [16]. Modification of this original operation, leaving the stomach intact, for
use in resection of locally advanced PDA was first proposed in Japan and has been
subsequently reported with increasing frequency in the literature [11, 12, 17–19].
With expanded experience, many high-volume pancreas centers have now
demonstrated the safety of the modified Appleby procedure for PDA. Multidisciplinary management is a key to appropriate patient selection in this cohort. For
example, if concern exists regarding the adequacy of collateral flow to the liver,
preoperative angiography with coil embolization can be considered and, if needed,
safely utilized [11, 14].
In ou r case, our female patient was seen in our multidisciplinary pancreas clinic
by surgeons, oncologists, radiation oncologists, pathologists, and radiologists,
where consensus supported initial combination cytotoxic chemotherapy (mFOLFIRINOX) followed by chemoradiotherapy (stereotactic body radiation therapy:
33 Gy). Her total course of therapy lasted 9 months, at which time she was restaged
with cross-sectional imaging. She had disease, which remained confined to the
pancreatic body and surrounding tissues without growth or metastasis, suggesting
favorable disease biology. Her imaging continued to show circumferential
involvement of the celiac trunk and common hepatic artery, while the portal vein
and superior mesenteric artery remained free from involvement. The distal common
hepatic artery at the GDA takeoff, as well as the entire length of the GDA, remained
free from tumor involvement. She therefore was determined to have biologically
favorable locally advanced (stage III) PDA of the pancreatic neck and body that
was amenable to extended surgical resection (i.e., distal pancreatectomy and
splenectomy with en-bloc celiac resection, a modified Appleby procedure).
Operative Management
Patients undergoing an Appleby procedure are evaluated in an anesthesia preoperative clinic at least 1 week prior to the planned operation. Additional consultation
with cardiology or pulmonology staff is obtained based on patient comorbidities
and risk factors for complications. On the day of operation, oral intake is prohibited
after midnight. Preoperative placement of large-bore peripheral intravenous access
and a radial arterial line is done after anesthetic induction and orotracheal intubation. Intravenous antibiotics and a prophylactic dose of subcutaneous heparin are
administered within 1-hour prior to incision. A nasogas tric tube is placed for gastric
decompression. Placement of an epidural catheter and a central venous catheter is at
the discretion of the operating team.