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436 3 HEPATOBILIARY AND PANCREAS CANCER
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22 Management of Cystic Neoplasms of
https://t.me/medicina_free
the Pancreas
Umar Hayat1, Mahnur Haider2, Brooke Glessing1 & Amitabh Chak
1
Division of Gastroenterology and Hepatology, University Hospitals Cleveland Medical Center, Cleveland, Ohio, USA
2
Department of Hepatology, Cleveland Clinic, Cleveland, Ohio, USA
Introduction
Pancreatic cystic neoplasms (PCN) encompass a large spectrum
of benign, premalignant, and malignant cysts. They are being
diagnosed with increasing frequency due to the widespread
use of cross-sectional imaging often during work-up for unrelated medical problems (Gardner etal. 2013). The overall risk
of a PCN being malignant is low, at less than 0.1% (Scheiman
etal. 2015). Despite the increased detection of PCNs, the incidence of pancreatic cancer has remained relatively stable yet
there has been a 189% increase in pancreatectomies over the
last two decades. Therefore, the tremendous clinical variability of pancreatic cysts presents a significant diagnostic and
therapeutic challenge to clinicians. A key component of clinical
management of these cysts is to accurately identify the small
percentage of cysts with early invasive cancer or high-grade
dysplasia and to predict which will develop cancer in the future
so as to avoid both missing detection of early cancer and referring for unnecessary surgical intervention (Klibansky et al.
2012; Yoon etal. 2021).
The estimated prevalence of asymptomatic pancreatic cystic
neoplasms (PCNs) in the general population is 2.5–15%. Studies
have reported high variability in the prevalence of PCNs depending on the imaging modality used, ranging from 2.4% to 44% on
magnetic resonance imaging (MRI), to 3% on computed tomography (de Jong etal. 2010; Falqueto etal. 2018; Girometti etal. 2011;
Laffan etal. 2008). In one of the largest, population-based studies
looking at 25,300 healthy individuals who had an abdominal CT
as a part of a health screening exam, the age and sex-adjusted prevalence of PCNs was 2.2% (Chang etal. 2016). In a meta-analysis
of 17 studies that included CT and MRI, the global pooled prevalence of PCNs was 8% with the highest prevalence reported in the
Americas and in older persons (Zerboni etal. 2019).
Age has been strongly associated with PCN prevalence and it is
estimated that 10% of people above 70 years have a pancreatic cyst
(Elta etal. 2018). A six-fold increase in the rate of detection has
Gastrointestinal Oncology: A Critical Multidisciplinary Team Approach,
Second Edition. Edited by Janusz A. Z. Jankowski.
© 2024 John Wiley & Sons Ltd. Published 2024 by John Wiley & Sons Ltd.
1
been observed in persons in their eighth decade of life compared
to those in their fourth decade of life (Gardner et al. 2013).
Moreover, the prevalence, number, and size of cysts have been
shown to increase with age. After five years of follow up of participants (mean age of 60.52 years) with PCNs, 30.8% had an
increase in size and number of cysts, 24.1% had no change and
1.3% had a reduction in cyst size and number (Kromrey et al.
2018). No difference in prevalence of PCNs by sex have been
observed (de Jong etal. 2010; Girometti etal. 2011; Kromrey etal.
2018; Laffan etal. 2008).
The cause of concern when a PCN is detected is the potential
for malignant transformation. While the overall risk of malignant transformation for all PCNs remains low (Elta etal. 2018),
the risk becomes clinically relevant in mucin producing cystic
neoplasms such as intraductal papillary mucinous neoplasm
(IPMNs) or mucinous cystic neoplasms (MCNs). In a population-based, cross-sectional analysis comparing the prevalence
of mucin-producing adenocarcinomas from the Surveillance
Epidemiology and End Results (SEER-18) data to the estimated prevalence of PCNs in the US, the calculated prevalence rate for malignant transformation was rare at 33.2 per
100,000 people (Gardner etal. 2013). However, retrospective
studies based on surgical series have estimated a much higher
rate of malignancy with a pooled estimate of 15% in resected
cysts from an analysis of 1296 patients (Scheiman etal. 2015).
In another analysis of 3980 patients with suspected IPMNs, the
risk of cancer was reported to be low at 2.8% (Scheiman etal.
2015) but other studies have shown contradictory results. In a
systematic review of 99 studies, 42% of the resected IPMNs had
either high-grade dysplasia or pancreatic cancer (Scheiman
et al. 2015). This significant variability in the reported risk
of malignant transformation of PCNs as detailed above is
likely due to a large selection bias in these surgical case series
and is overestimated which continues to make management
decisions challenging. Furthermore, no existing test can
identify the type of PCN pre-operatively with a high accuracy. Several guidelines (2015 American Gastroenterological
Association [AGA] (Vege etal. 2015), 2016 American Society
of Gastrointestinal Endoscopy [ASGE] (Committee, A.S.o.P.
438
22 MANAGEMENT OF CYSTIC NEOPLASMS OF THE PANCREAS 439
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et al. 2016), 2017 Fukuoka guidelines by International
Association of Pancreatology [IAP] (Tanaka etal. 2017), 2018
American College of Gastroenterology [ACG] (Elta et al.
2018), 2018 European Study Group, and American College of
Radiology (Elta etal. 2018)) have attempted to risk stratify the
PCNs by identifying features that are predictive of harboring
malignancy and thus minimizing diagnostic uncertainty that
can lead to clinically significant errors for our patients. These
features are discussed in detail later in the chapter (Elta etal.
2018; European Study Group on Cystic Tumours of the, P. 2018;
Scheiman etal. 2015; Tanaka etal. 2017).
PCNs can be broadly classified as neoplastic versus non-neoplastic and mucin producing versus non-mucin producing.
These can be differentiated by cross-sectional imaging and
endoscopic ultrasound (EUS) with or without cyst fluid and
cyst wall lining analysis though the accuracy of the currently
available diagnostic tools to identify the type of PCN remains
subpar with advancements in the fields of radiology and endosonography expected to continue to improve upon it (Elta etal.
2018). This chapter will highlight the various types of PCNs
(Table 1) and their management but will predominantly focus
on the diagnostic and therapeutic management of the mucin
producing cystic neoplasms (specifically IPMNs).
Neoplastic and Mucin Producing
Pancreatic Cystic Neoplasms
Intraductal Papillary Mucinous Neoplasms
An intraductal papillary mucinous neoplasm (IPMN) can be
diagnosed on imaging and is typically connected to the main
pancreatic duct; this differentiates IPMNs from mucinous cystic
neoplasms (Scheiman et al. 2015). They can be classified by
location: side-branch, main duct, or mixed (a combination of
side branch and main duct). A branch duct IPMN (BD-IPMN)
is the most common PCN and has the lowest risk of harboring
high-grade dysplasia and/or invasive cancer (Goh et al. 2014;
Nguyen etal. 2015; Sahora etal. 2013). Although some patients
with BD-IPMNs warrant consideration for surgical resection,
most are incidentally discovered in elderly patients where surveillance is a better option considering the risks associated with
surgery and a low annual rate of progression [1.4–6.9%]
(Lafemina etal. 2013; Malleo etal. 2015). Mixed and main duct
IPMNs are less common but have a higher risk for malignancy
with 38–68% of resected main duct IPMNs found to have
high-grade dysplasia and/or pancreatic cancer (Elta etal. 2018).
Therefore, surgical resection of all IPMNs with suspected main
duct involvement is recommended. One interesting endoscopic
feature of an MD-IPMN is a fish-eye papilla where a patulous,
mucin extruding pancreatic orifice which is visible during duodenoscopy in 20% to 55% of the cases and is more often noted in
malignant disease (Elta etal. 2018; Kitagawa etal. 2003; Maire
etal. 2003) (Figure 1).
Of note, patients with IPMNs are suspected to have a “field
defect” where all ductal epithelial cells in the pancreas are suspected to be at risk for dysplastic change and malignancy. This
may be why up to 40% of the patients present with multifocal
BD-IPMNs (Rodriguez etal. 2007; Waters etal. 2008) though
the cumulative risk of high-grade dysplasia or invasive cancer
does not seem to be higher (Tanaka et al. 2017). This is also
why it has been noted that patients with BD-IPMNs have an
increased risk (around 2–4%) of developing “concomitant”
pancreatic adenocarcinoma (PDAC) in an anatomically different area in the pancreatic parenchyma independent to the risk
of malignant transformation within the IPMN itself (Maguchi
et al. 2011; Tanno etal. 2010). This not only underlines the
importance of evaluating the entire pancreas at the time of cyst
evaluation but also the need to continue surveillance in the
pancreatic remnant after surgical resection of a BD-IPMN or a
main duct IPMN. Diagnostic techniques and management of
BD-IPMNs is discussed later in the chapter.
Mucinous Cystic Neoplasms
Mucinous cystic neoplasms (MCNs) are primarily found in
middle aged women in the body or tail of the pancreas.
Radiographically, MCNs are round, can be unilocular or multilocular and usually have thick cyst walls. They usually do not
communicate with the pancreatic duct and occasionally can
have peripheral “eggshell” calcification which is considered a
pathognomic feature for MCNs. Histologically, they are distinct from other types of PCNs as they have columnar epithelium surrounded by ovarian stroma. They do have a risk of
malignant transformation and in an analysis of resected MCNs
high-grade dysplasia or pancreatic cancer, it was demonstrated
to be around 10% (Park etal. 2014) though the risk is negligible
in MCNs that are smaller than 3 cm in size and have no other
concerning radiological characteristics (Goh etal. 2006).
Neoplastic and Non-Mucin Producing
Pancreatic Cystic Neoplasms
Serous Cystadenoma
Serous cystadenomas (SCAs) commonly occur in women in
their 50s and 60s. They can have three characteristic morphologic appearances on imaging including polycystic, microcystic, or honey combing and oligo-cystic. BD-IPMNs can be
differentiated from SCAs based on imaging if the SCA is polycystic or microcystic but this can be challenging if the SCA is
oligo-cystic. Another imaging characteristic associated with
SCAs is a central calcified scar that can be seen in less than
half of these PCNs (Figure 2). The reason why it can be important to differentiate these from mucin producing PCNs is that
the risk of malignancy is very low (0.1%) in SCAs and thus
surveillance is not generally required. Even though most of
these are asymptomatic, occasionally they can cause
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ductal adenocarcinoma
Jaundice is a clinical feature associated with
testing is recommended in
patients presenting with
obstructive jaundice worrisome
Surgical resection without further
considered a
Not discussed Presence of jaundice is
features
high-risk feature
and EUS±FNA and/
or a multidisciplinary
evaluation is
recommended
associated with pseudocysts and IPMNs
History of pancreatitis a clinical feature
evaluation and consider surgery
Recommend EUS for further
to cyst is considered
evaluation
MPD dilation warrants EUS/FNA
for symptom relief
a “worrisome feature”.≥10mm
dilation is considered a
“high-risk stigma” and surgical
Dilation of 5–9mm is considered
high-risk
considered a
>5mm dilation is
feature
Considered a high-risk
resection is recommended
high-risk feature
and EUS±FNA and/
or a multidisciplinary
evaluation is
recommended
evaluation
Presence of a mural nodule warrants EUS/FNA
and an evaluation with EUS is
recommended
Considered a “worrisome feature”
considered a
high-risk feature
and EUS±FNA and/
or a multidisciplinary
evaluation is
Not discussed Mural nodule
FNA
≥3 cm cyst size warrant EUS/
symptoms follow up is
recommended. For cysts >
5mm dedicated imaging is
For cysts < 5mm and no
recommended
considered a
≥3 cm cyst size
considered a high-risk
≥3 cm cyst size
recommended for
high-risk feature
and EUS±FNA and/
or a multidisciplinary
feature
Not discussed
“worrisome feature” and EUS is
Pancreatic atrophy is considered a
considered a
recommended
high-risk feature and
EUS±FNA and/or a
characterization of cyst
evaluation is
recommended
multidisciplinary
evaluation is
recommended
is considered
predictive of
malignancy and
should be
evaluated
Jaundice Presence of jaundice
European AGA ACG IAP ASGE
Pancreatitis Not discussed Not discussed Pancreatitis secondary
PD dilation ≥10mm dilation is
M
Imaging
predictive of
malignancy
characteristics
malignancy
Mural Nodule ≥5mm predictive of
≥40mm associated
with cancer
Cyst size cyst diameter
Not discussed Not discussed Upstream atrophy
Pancreatic
atrophy
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every 2 years if no
change
in 6 months, then
for 1 year, then
yearly for 2 years
CT / MRI for 6 months
Not discussed
and then every 2
years if stable
EUS in 3-6 months,
followed by
alternating MRI with
EUS every year. Can
consider surgery in
young patients
alternating with
3-6 months. Should
consider surgery in
young patients
Not discussed
and EUS is recommended
Considered a “worrisome feature”
elevated CA19-9 are
not found, then a
Not discussed If benign causes of
2-3 cm MRI or EUS every 6–12 2-3
cm
multidisciplinary group MRI with EUS every
>3cm Referral to >3cm Close surveillance
examination
with EUS-FNA
Recommend
months for 3 years
>3
cm
and MRI alternating with
EUS every 6 months for 3 years
cm
Not discussed Not discussed
concerning symptom
and EUS or MRI
multidisciplinary
evaluation should be
pursued
Not discussed Considered a
should be considered
< 1cm MRI every 2 years for 4years < 1cm CT / MRI
surveillance in 1
MRI for
cm
< 3
every 2 years for
a total of 5 years
if there is no
change in size or
characteristics
when there is
concern for
malignancy
European AGA ACG IAP ASGE
Serum Based CA 19-9 Can be considered
surgery
Relative indication for
Diabetes
New-onset
CA19-9, MRI and/
Clinical evaluation,
diagnosis
Surveillance First year of
or EUS every 6
months
year and then
1-2 cm MRI every year for 3 years 1-2
CA19-9, MRI and/
or EUS every year
Clinical evaluation,
year of
diagnosis
After the first
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Table 1 Characteristic and epidemiology of different pancreatic cystic neoplasms.
Characteristic MCN BD-IPMN SCA SPN
Sex (% Female) >95% ~ 55% ~70% Females> males
Age (decade) 4th, 5th (“Mother”) 6th, 7th 6th, 7th (“Grandmother”) 2nd, 3rd
Asymptomatic ~ 50% Mostly when small ~ 50% ~ 50%
Location (% body/tail) 95% 30% 50% Predominantly
Common capsule Yes No Ye s Yes
Calcification Rare, curvilinear in the cyst
wall
Gross appearance Orange Grape-like Spongy/honeycomb like Round, soft, encapsulated
Multifocality No Yes No Solid and cystic
Internal structure Cysts in cyst Cyst by cyst Microcystic and/or
Main PD communication Infrequent Ye s No No
Overall risk of malignancy/
HGD
Aspirate characteristic Viscous Viscous, or thin Thin, often bloody Bloody
Cytology Findings Columnar cells with
CEA levels > 200 ng/ml in ~75% < 5 – 20 ng/ml > 200 ng/ml in ~75% Insufficient data
~10% ~7% in 10 yrs (low risk),
variable atypia, Stain
mucin < 50%
No 30–40%, central Occasional
hemorrhagic mass
components
Unilocular
macrocystic
0.10% ~ 10%
~24% in 10 yrs (high risk)
Cuboidal cells +ve for
glycogen (< 50%)
Columnar cells with
variable atypia, Stain
mucin < 50%
Branching papillae with
myxoid stroma (high
yield from solid
component)
Figure 1 Main duct IPMN with a gaping papilla which is extruding mucus.
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symptoms such as pancreatitis or obstructive jaundice when
they enlarge, especially if located in the head of the pancreas,
in which case surgical resection can be considered (Elta etal.
2018; Jais etal. 2016).
Solid Pseudopapillary Neoplasms
Solid pseudopapillary neoplasms (SPNs) are rare and are more
commonly found in young women in their 20s. Radiographically,
SPNs have solid growth with cystic degeneration with both solid
and cystic areas noted on imaging. The age at detection is highly
variable ranging from childhood to adulthood and can be found
in any part of the pancreas. Even though about 10% of SPNs can
be aggressive tumors they have a better prognosis than pancreatic
adenocarcinoma with a 5-year disease-specific survival of 98%
(Elta etal. 2018). A referral to a high-volume pancreatic center for
surgical resection is recommended for all patients with SPNs.
Cystic Pancreatic Neuroendocrine Tumors
Pancreatic neuroendocrine tumors (pNETs) are rare tumors
that usually presents in the 60s. They are non-secreting tumors
and morphologically can be solid, cystic, or mixed (Elta etal.
2018). The management of these lesions is not discussed and is
out of the scope of this chapter.
Non-Neoplastic and Non-Mucin
Producing Pancreatic Cysts
Pseudocysts
Pseudocysts are usually found in patients with a history of pancreatitis. They are less common than PCNs but it is important to
differentiate between them because pseudocysts do not have a
malignant potential and thus do not require surveillance or intervention if asymptomatic. Additionally, if symptomatic, pseudocysts can be treated with endoscopic drainage alone whereas
PCNs may require surgery and are not treated with endoscopic
drainage. Cystic lesions in the pancreas are suspected to be a
pseudocyst in patients with a prior history of pancreatitis whose
cystic lesion develops on imaging after the episode of pancreatitis.
In individuals with idiopathic pancreatitis over the age of 40, an
underlying PCN as a cause of pancreatitis if the cystic lesion is
seen on initial imaging should be strongly considered prior to
labeling the cystic lesion as a pseudocyst (Elta etal. 2018).
Epidemiology of PCNs
The evolving fields of radiology and endosonography have
improved the diagnostic ability to differentiate different types of
PCNs but this should not overshadow the importance of several
epidemiological factors that can provide useful hints toward the
diagnosis. Factors such as gender, age of diagnosis, and location
of the cystic lesion in the pancreas can all be used in solving the
diagnostic dilemma of PCNs as detailed in Table 1.
Clinical Presentation of PCNs
Majority of PCNs are discovered incidentally in asymptomatic
individuals in clinical practice but retrospective surgical case
series have reported symptoms in as high as 80% of individuals
with PCNs (Parra-Herran etal. 2010; Walsh etal. 2002). This
high percentage is likely a result of selection and referral bias
since other observational studies show the prevalence of symptoms to be much lower around ~20% (Crippa et al. 2017;
Mukewar etal. 2017). Of note, symptomatic IPMNs have been
noted to have an association with malignancy (OR 1.6 CI 1.0-
2.6) (Anand etal. 2013). A myriad of gastrointestinal symptoms has been reported to have an association with PCNs in
surgical case series [abdominal pain (69%), weight loss (38%),
back pain (18%), palpable mass (5%), and postprandial fullness
(4%)] but it is extremely difficult to attribute these to the PCNs
due to the non-specific nature of these symptoms. On the contrary, pancreatitis (36%) and obstructive jaundice (18%) can
more directly be attributable to PCNs. It is especially important
to consider a PCN as the cause of pancreatitis and not misdiagnose it as a pseudocyst in patients presenting with pancreatitis
above the age of 40. Furthermore, PCN related acute pancreatitis and obstructive jaundice can both be an indicator of
advanced neoplasia within the PCN (or indicator that the PCN
is harboring advanced neoplasia) (Del Chiaro et al. 2013;
Rivera etal. 1997; Shin etal. 2010; Vege etal. 2015). Therefore,
lesion related obstructive jaundice is considered an absolute
criterion for surgery and lesion related acute pancreatitis is
considered a “worrisome feature” and a relative indication for
surgery (Tanaka etal. 2017, 2012). New-onset diabetes is also a
concern in patients with IPMNs above the age of 50 since these
patients are noted to have an increased risk of high-grade dysplasia or pancreatic cancer and thus a thorough evaluation is
warranted with an MRI /MRCP and/or EUS (Leal et al. 2015;
Mimura etal. 2010).
Diagnostic Tools for PCNs
Radiology
Cross-sectional imaging serves a dual purpose in the diagnostic
evaluation of a PCN. It helps characterize the type of PCN and
assesses for presence of high-grade dysplasia and/or pancreatic
cancer. Different retrospective studies have shown variable
rates of diagnostic accuracy of the contrast enhanced computed
tomography (CECT) scans and Magnetic Resonance Imaging
(MRI)/Magnetic Resonance Cholangiopancreatography (MRCP)
in identifying the type of PCN as well as differentiating between
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benign and malignant cystic lesions. In a systematic review of 19
studies, CT can accurately pick up benign from malignant PCNs
in 70–80% of the cases with a sensitivity of 80% for IPMNs. MRI/
MRCP had a similar accuracy for differentiating a benign from a
malignant PCN ranging from 55–76% though had a much higher
sensitivity of around 96% for diagnosing IPMN (Jang etal. 2015;
Jones etal. 2013; Lee etal. 2011).
MRI/MRCP is preferred over CT due to its lack of radiation
and a higher sensitivity for identification of cyst communication with the pancreatic duct (that likely explains its higher
accuracy for diagnosing a BD-IPMN), for detecting presence
of a solid component within the cystic lesion and for
identification of multifocal PCNs (Sahani etal. 2013; Waters
et al. 2008). Despite its many advantages, MRI/MRCPs do
have some cons including lower spatial resolution, decreased
sensitivity for detecting calcification within the cystic lesion,
longer imaging duration, and increased susceptibility to
motion artifact. Secretin enhanced MRCP can improve the
visualization of the pancreatic duct and detect communication between the pancreatic duct and the PCN when it would
not be obvious otherwise though the small incremental
benefit in the diagnostic yield is a questionable justification at
this time for the higher cost associated with secretin use. The
use of a combined approach with MRI or CT with EUS as
discussed below or even Positron Emission Tomography with
CT has also been suggested to increment the low diagnostic
yield of single imaging modalities for differentiating benign
from malignant PCNs. A small study has shown that PET
combined with CT had a diagnostic yield of around 94% in
this scenario as compared to 77% for CT and 86% for MRI
with MRCP (Kauhanen etal. 2015).
Endoscopic retrograde cholangiopancreatography (ERCP)
may have a limited role in evaluation of a MD-IPMN. The use
of ERCP in routine evaluation of PCNs remains limited though
due to its invasive nature and high risk of complications and
cross-sectional imaging along with EUS remain the mainstay
for diagnostic management of PCNs.
Endoscopic Ultrasound
Endoscopic Ultrasound (EUS) is an extremely useful tool that
aids in the diagnosis of PCNs not only as a stand along imaging
technique but also via sampling of the cyst fluid and its analysis.
Cyst fluid analysis increases the diagnostic yield and can especially help in the differentiation between mucin producing and
non-mucin producing PCNs. EUS imaging alone (without cyst
fluid analysis) is accurate in 65–96% of the cases when differentiating benign from a malignant PCN. This is similar to the
accuracy of the MRI and the CT noted above and though EUS
alone adds only a limited incremental value over cross-sectional
imaging, it does have a higher resolution and has been demonstrated to have a higher sensitivity for identification of a mural
nodule (MN) within a PCN. The mural nodule has irregular
borders on EUS and usually has a hyperechoic center as opposed
to a mucin ball which has a smoother wall with a hyperechoic
rim and hypoechoic center (Tirkes etal. 2014). Additionally, an
EUS without features of concern in a PCN has a high negative
predictive value for ruling out malignancy (Scheiman et al.
2015). Despite several advantages, EUS should be used judiciously in the diagnostic management of PCNs due to its invasive nature when CT/MRI are not sufficiently diagnostic or
there are cystic features of concern on cross-sectional imaging
warranting further evaluation (European Study Group on Cystic
Tumours of the, P. 2018; Harima etal. 2015; Tanaka etal. 2017).
Adverse events are reports in 2.7% to 5% of the cases undergoing EUS-FNA (Wang KX Assessment 2011). Most common
adverse events include abdominal pain, pancreatitis and intracystic hemorrhage (Al-Haddad et al. 2008; Lee et al. 2005;
Tarantino etal. 2014; Varadarajulu and Eloubeidi 2004). Cyst
infection rates of as high as 14% have also been quoted in older
studies (Wiersema etal. 1997) though more recent data has
shown much lower rates of less than 1% (Guarner-Argente
etal. 2011). The current ASGE guidelines suggest consideration
of prophylactic antibiotics when performing EUS-FNA in
PCNs, but this practice remains variable in the real world
(Committee, A.S.o.P. etal. 2016).
Radiomics
Radiomics is the analysis of mathematically derived textural features from cross-sectional imaging that are not perceptible to
human eyes. Multiple studies in radiomics have employed variable extraction of radiometric data from CECTs via machine
learning algorithms with some combining radiomics, cyst morphology and clinical features to differentiate types of PCNs
(Dmitriev etal. 2017; Xie etal. 2020; Yang etal. 2019) and more
recently, risk stratify IPMNs (Attiyeh etal. 2019; Hanania etal.
2016; Hoffman etal. 2017). While radiomics is an exciting tool
in the arsenal for classification and risk stratification of PCNs,
its use has largely been limited to clinical trials at large academic
centers and is several years away from prime-time utilization.
Cytology, Biomarkers, and Molecular Analysis
EUS-guided fine-needle aspiration (FNA) of the pancreatic
cystic fluid is considered when additional diagnostic information
is warranted such as in patients being considered for surgery or
in patients where a diagnosis of a serous cyst would help avoid
surveillance. The cyst fluid obtained via FNA can be sent for
biochemical, cytological, and molecular analysis. This can be
very useful in trying to distinguish mucin producing from nonmucin producing PCNs and avoid unnecessary surveillance.
Even though cytology of the cyst fluid is highly specific
(83–100%), it has been shown to lack sensitivity for diagnosing PCNs (27–48%) and thus has a low diagnostic accuracy
(8–59%) (Stelow etal. 2003; Thosani etal. 2010; Wang etal.
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2015). The lack of sensitivity is likely a result of a low number
of intact exfoliated cells that are usually detected in the sample.
The analysis for fluid CEA and amylase levels is also useful
when distinguishing mucinous from non-mucinous PCNs but
these will not differentiate MCNs and IPMNs. A cutoff value of
≥192–200 ng/mL has previously been noted to have 79% accuracy in diagnosis of mucinous cysts (Brugge etal. 2004) but
more recent studies have shown a lower sensitivity and specificity (63% and 88% respectively) that can lead to a misdiagnosis of around ~40% of mucinous cysts (Thornton etal. 2013).
Additionally, higher CEA levels have not shown to correlate
with risk of high-grade dysplasia and/or invasive cancer in
PCNs (Brugge etal. 2004; Park etal. 2011). Cyst fluid amylase
levels are mostly helpful in excluding pseudocysts when they
are low but high amylase levels have limited diagnostic utility as
they can be elevated in IPMNs, pseudocysts and in rare
instances, MCNs as well (Ngamruengphong and Lennon 2016;
Thornton etal. 2013).
Intra-cystic glucose levels have recently gained traction as a
low-cost diagnostic test with many studies now showing that
intra-cystic glucose levels are superior to CEA levels in differentiating mucinous from non-mucinous PCNs. Mucinous
PCNs are expected to have low glucose levels partly due to the
metabolism from the active neoplastic cells. Intra-cystic
glucose concentration < 50 mg/dL has significantly better sensitivity than a CEA level > 192 ng/mL for diagnosing mucinous
cysts (93.6% vs 54.8%) (Ribaldone etal. 2020). A meta-analysis
of 8 studies with included 609 PCNs showed pooled sensitivities for glucose vs CEA of 91% vs 56% and pooled specificities
for glucose vs CEA of 96% vs 86% (McCarty etal. 2021a).
Next-generation sequencing (NGS) allows evaluation of
gene panels and whole exome in intact cell and cell-free nucleic
acid present in the cyst fluid and can look for DNA mutations
that are commonly associated with development of pancreatic
adenocarcinoma (RAS, CDKN2A, SMAD4, PTEN, PIK3CA,
and TP53). These can help with classification of mucinous
versus non-mucinous PCNs as well as risk stratification of
IPMNs. Presence of dual KRAS and GNAS mutations can diagnose mucinous PCNs with an accuracy of 97% (McCarty etal.
2021b). Moreover, presence of TP53, PIK3CA, and/or PTEN
mutation has 88% sensitivity and 95% specificity, respectively
for diagnosing IPMNs with advanced neoplasia (Singhi et al.
2018). Even though cyst fluid molecular analysis by NGS has a
high accuracy in identification of the type of PCN and risk
stratification for advanced neoplasia, limited availability and
high cost remain big deterrents for routine use. The clinical
utility of these biomarkers remains to be demonstrated.
Advanced EUS Based Techniques for Evaluation
of PCNs
EUS with and without cyst analysis remains a subpar test in
guiding management decisions due to low cellularity and a
suboptimal diagnostic accuracy of the biomarkers. Therefore,
several techniques have been developed for evaluation of cyst
wall including tissue acquisition from the lining of the cyst wall
for histology. Use of needle based confocal light endomicroscopy (nCLE) and through-the-needle intracystic biopsy (Moray
micro forceps; US Endoscopy, Mentor, Ohio) are the techniques that have shown the most promise in increasing the
diagnostic yield of EUS with an acceptable risk profile.
The microforceps biopsy (MFB) can be advanced through a
19G needle while performing EUS–FNA and allows for tissue
sampling of the cyst wall. The technical success of the device in
limited series is reported to be approximately 99% with a tissue
acquisition yield of 88% and a diagnostic accuracy of 69%
(Balaban etal. 2021). Adverse events are reported in around 9% of
the cases and include intracystic hemorrhage, mild acute pancreatitis, abdominal pain, and post-procedural infection (Balaban
etal. 2021). While EUS–FNA with MFB allows for a high diagnostic accuracy in management of PCNs, the higher risk of
adverse events as compared to EUS–FNA alone is likely a deterrent for incorporation of this technique in routine clinical
practice.
EUS guided nCLE is another advanced technique that allows
real-time in vivo endo-microscopic imaging of the intracystic epithelium of the cyst wall. Confocal images are obtained
when a low-power laser illuminates the tissue after intravenous
administration of fluorescent contrast agent (such as fluorescein [CellVizio; Mauna KeaTechnologies, Paris, France]) and
the reflected light is focused through a pinhole onto a detection
system that transforms it to a detailed bitmap gray scale image
on the computer (Neumann et al. 2010; Polglase et al. 2005).
Studies have established the characteristic features of IPMNs
(presence of villous structures), MCNs (a thick gray line), SCAs
(a superficial vascular network pattern corresponding to a dense
and subepithelial capillary vascularization only seen in SCAs),
cystic neuroendocrine tumors (black neoplastic cell clusters
with white fibrous areas) and pseudocysts (field of bright particles) (Napoleon et al. 2015, 2016). nCLE can differentiate
mucinous PCNs and non-mucinous PCNs with a diagnostic
accuracy of around 89–99%. The pooled risk of post-procedure
pancreatitis is around 1% (Facciorusso etal. 2020). In addition,
several imaging variables in nCLE have been identified that
determine the presence of advanced neoplasia in IPMNs with
papillary epithelial thickness (width ≥ 50 μm) and papillary epithelial darkness (cut-off ≤ 90 pixel intensity) having the highest
interobserver agreement for detection of advanced neoplasia
(Krishna etal. 2020). Similarly, a nCLE pattern of dark aggregates of neoplastic cells correlated with the morphologic features of irregular branching and budding and was diagnostic of
malignancy. The cost and unproven clinical utility have limited
the widespread adoption of nCLE in clinical practice.
Contrast-enhanced EUS (CE-EUS) has been proposed to be
useful in the presence of MNs or solid components to assess the
presence of vascularization. Even though earlier studies did not
report any improvement over traditional EUS at differentiating
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