Cystic neoplasms of the pancreas 2007

Gastroenterol Clin N Am 36 (2007) 365–376

GASTROENTEROLOGY CLINICSOF NORTH AMERICA

Cystic Neoplasms of the Pancreas

Michael P. Federle, MDa,*, Kevin M. McGrath, MDb

aDepartment of Radiology, University of Pittsburgh Medical Center, 200 Lothrop Street,Suite 3950, Pittsburgh, PA 15213, USAbDivision of Gastroenterology, University of Pittsburgh Medical Center, 200 Lothrop Street,1255 Scaife Hall, Pittsburgh, PA 15213, USA

With the increased use of sophisticated imaging, particularly com-puted tomography (CT), cystic masses in the pancreas are beingrecognized with greater frequency. Several recent review articles

serve as an introduction to the clinical and imaging features of these masses[1–4]. Although imaging alone may not provide a specific diagnosis in manycases, a combination of imaging characteristics, clinical presentation, and judi-cious use of additional procedures, such as cyst aspiration, allows appropriatemanagement.

This article presents the approach to the most commonly encountered pan-creatic cystic masses that the authors employ at the University of PittsburghMedical Center. Variations on this approach are to be expected, based on sev-eral factors, including the availability of sophisticated imaging equipment andpersonnel.

ETIOLOGY OF CYSTIC PANCREATIC MASSESPancreatic cystic masses may be the result of congenital, inflammatory, or neo-plastic processes, as listed in Box 1 and Table 1 [5]. Some of these, such as an-aplastic carcinoma, cystic teratoma, and hydatid disease, will be considered toorare to warrant further discussion in this article. Intraductal papillary mucinousneoplasm is considered important enough to discuss in a separate article of thisissue.

Congenital‘‘True’’ cysts of the pancreas are those that are neither neoplastic nor the resultof prior inflammation. These are rare and cannot be distinguished from othercystic masses except for the presence of an epithelial lining [6]. Congenital cystsare usually single and small (1–2 cm), although larger symptomatic cysts havebeen reported in children.

Multiple pancreatic cysts may be encountered in several syndromes and mul-tisystem disorders, including autosomal dominant polycystic disease, cystic

*Corresponding author. E-mail address: [email protected] (M.P. Federle).

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366 FEDERLE & MCGRATH

fibrosis, and von Hippel-Lindau disease. The pancreatic cysts are of no clinicalconcern in these settings, and differential diagnosis is generally not a problem.In polycystic disease, family history and the presence of cysts in other organsare diagnostic. In cystic fibrosis, the pancreas contains not only cysts but alsofatty replacement of the pancreatic parenchyma. In patients who have von Hip-pel-Lindau disease, solid neoplasms develop in the brain, spinal cord, kidneys,and adrenals. These patients are also prone to developing pancreatic cysts andserous (microcystic) cystadenoma.

InflammatoryA pseudocyst is the result of acute or chronic pancreatitis, or pancreatic trauma(especially in children). A pseudocyst is usually regarded as the most commonetiology of a symptomatic pancreatic cystic mass. This ‘‘cyst’’ lacks an epithelial

Box 1: Cystic pancreatic masses

Congenital

True (epithelium-lined) cyst

Syndromes causing multiple cysts

Autosomal dominant polycystic disease

von Hippel-Lindau

Cystic fibrosis

Inflammatory

Pseudocyst

Pancreatic abscess

Hydatid cyst

Neoplastic

Benign

Serous (microcystic) cystadenoma

Cystic teratoma

Lymphoepithelial cyst

Malignant or potentially malignant

Mucinous cystic neoplasm

Solid and papillary epithelial neoplasm

Other (tumors that may have a cystic component)

Intraductal papillary mucinous neoplasm (IPMN)

Islet cell tumor

Anaplastic carcinoma

Metastases to pancreas (eg, ovarian cystadenocarcinoma)

367CYSTIC NEOPLASMS OF THE PANCREAS

lining, is walled off by fibrous and granulation tissue, and contains fluid thatcomprises pancreatic juice and variable amounts of necrotic debris and hemor-rhage. Pseudocysts should be distinguished from fluid collections in pre-exist-ing spaces, such as the lesser sac, that develop and resolve rapidly followingan attack of acute pancreatitis.

Imaging characteristics of a mature pseudocyst include near water-attenua-tion fluid contents and a thin wall (rarely with curvilinear calcification). Less-mature cysts have complex fluid and inflammatory infiltration of adjacentstructures such as the gastric wall and mesenteric fat (Fig. 1A). Septationsare uncommon, and enhancing mural nodules are absent. Pseudocysts usuallyshow a fairly rapid (days to weeks) evolution in size, unlike cystic neoplasms.CT and MR generally show ancillary findings that help to establish the diag-nosis of pseudocysts, such as signs of acute or chronic pancreatitis (inflamma-tory infiltrates, ductal dilation, calcifications, and so forth) (Fig. 1B, C).

Cyst contents are generally thin fluid (unless grossly infected) that may looklike a cola beverage. Analysis shows an elevated amylase level (often >10,000IU) that is diagnostic. However, mature noncommunicating pseudocysts maylose amylase activity with time.

Pseudocysts generally take 4 to 6 weeks to develop a fibrous wall. Even ma-ture pseudocysts may resolve spontaneously, often by erosion into the stomachor bowel, and do not require intervention except for complications such as in-fection, hemorrhage, or persistent obstruction of bowel or bile ducts. Interven-tion is also required for persistent symptomatic cysts causing abdominal painand/or early satiety.

For symptomatic pseudocysts, management options include percutaneousdrainage, endoscopic drainage (transpapillary or transmural), or surgical drain-age (cyst enterostomy). An experienced multidisciplinary team, taking into ac-count patient wishes, ductal anatomy, and surgical risk, best makesmanagement decisions.

Table 1General characteristics of pancreatic cystic lesions

Morphology Cytology CEAFluidcharacteristics

Serous Microcystic Small, cuboidalcells withoutmucin

Low or absent Thin, clear

Mucinous Macrocystic,usually septated

Mucinousepithelial cells

Moderatelyincreased

Clear, mucoid,viscous

Malignant Mural nodularity,septation

Malignantmucinousepithelial cells

Markedlyincreased

Clear, mucoid,viscous

Pseudocyst Thin walled, usuallynonseptated

Inflammatorycells

Low Thin, dark

Abbreviation: CEA, carcinoembryonic antigen.


A pancreatic abscess is generally the result of severe acute pancreatitis and isusually not a diagnostic problem. Infected pancreatic necrosis is a dreaded com-plication of necrotizing pancreatitis and would not be confused with a cysticneoplasm, based on the clinical presentation.

Benign NeoplasmsCystic teratomaCystic teratoma occurs rarely in the pancreas. Imaging evidence of liquid fatplus calcification and soft tissue may allow preoperative diagnosis.

Lymphoepithelial cystLymphoepithelial cyst is another rare pancreatic tumor with imaging character-istics (septated cystic mass in the body/tail segment) that often cannot be distin-guished from cystic neoplasm (see later discussion) [7].

Serous (microcystic) cystadenomaSerous (microcystic) cystadenoma is an uncommon tumor that typically occursin elderly women, with a female/male ratio of 1.5–4.5:1. The median age at

Fig. 1. Fifty-six-year-old man who has a pancreatic pseudocyst. (A) Endoscopic ultrasound im-age shows a spherical mass with a thin but measurable wall (between cursors) and a fluid-debris level (arrow) in its dependent portion. (B) A CT scan performed 2 months later showsdecrease in size of the pseudocyst (arrow), a thin wall, and near-water-attenuation contents.(C) The body-tail segment of the pancreas (arrow) is atrophic and the pancreatic duct is di-lated, indicating chronic pancreatitis.


diagnosis is approximately 70, and 80% of reported cases have been in patientsover the age of 60 [8–10].

Serous microcystic adenomas occur with increased frequency in patientswho have von Hippel-Lindau disease. Even in patients who do not have otherfeatures of von Hippel-Lindau disease, similar genetic mutations are found inmost patients who have serous cystadenomas.

The typical imaging appearance of a serous cystadenoma is that of a spongeor honeycomb, with innumerable tiny cystic spaces separated by thin septa(Fig. 2A). The septa may coalesce into a central scar that may calcify. The smallsize of the cysts and the numerous septa may cause the mass to appear solid onimaging. Thin-section, contrast-enhanced CT or MR allows confident diagno-sis in 20% to 30% of cases [10]. The septa and peripheral capsule of this well-circumscribed tumor show brisk contrast enhancement. MR shows thesefeatures as well as CT. In addition, the fluid content of the mass may be moreevident on MR as low signal (dark) on T1-weighted images, and high signal(bright) on T2-weighted images.

A macrocystic variant of serous cystadenoma has been reported by severalgroups of investigators [11–13]. Rather than having innumerable tiny cysts,these are characterized by a single cystic mass with or without one or morethin septa. This variant may be difficult to distinguish from a mucinous cystictumor. The serous mass is favored by having a thin nonenhancing wall, a lob-ulated surface, and presence within the pancreatic head. Cyst aspiration is re-quired for further evaluation.

Endoscopic ultrasonography (EUS) is now frequently employed for furtherevaluation of cystic lesions discovered by cross-sectional imaging. EUS evalu-ation (typically at 5 MHz) provides high-resolution imaging that highlightsthe sponge-like or honeycomb appearance of the microcystic serous cystadeno-ma (Figs. 2B and 3A, B). The macrocystic variant may mimic a mucinous

Fig. 2. Eight-two-year-old woman who has a serous microcystic adenoma. (A) A contrast-enhanced CT scan shows a large spherical mass within the pancreatic head, having an ap-pearance of a sponge, with innumerable tiny cystic spaces separated by thin, enhancingsepta. (B) EUS confirms the innumerable tiny cystic spaces and septa. The patient had minimalsymptoms related to the mass, and no surgery was performed.


cystic neoplasm. Serous adenomas may also have few cystic spaces (‘‘oligocys-tic’’), and these may mimic side branch intraductal papillary mucinous neo-plasm. EUS-guided cyst aspiration can prove helpful in this situation. Thefluid content of macro- and microcystic serous tumors is thin and nonviscous.Glycogen-rich cuboidal epithelial cells, when seen in the cyst aspirate, are diag-nostic [14]. The carcinoembryonic antigen (CEA) level, which is the most ac-curate tumor marker to diagnose a mucinous cystic neoplasm [15], is low orundetectable. The authors currently only aspirate the macrocystic or oligocys-tic variants to differentiate them from mucinous lesions. They consider thesponge-like or honeycomb appearance of the microcystic variant pathogno-monic at EUS and, therefore, no longer perform fine needle aspiration(FNA) in this situation.

Serous cystadenomas are invariably benign and usually cause minimalsymptoms unless they attain sufficient size to compress upper abdominal con-tents. Notably absent are any signs of invasion of blood vessels or ducts.

Confident diagnosis of a serous cystadenoma may be challenging but is im-portant, because these are benign tumors that occur in elderly patients and of-ten are best managed without surgery unless the patient has substantialsymptoms, such as pain, early satiety, or jaundice.

Malignant or Premalignant NeoplasmsMucinous cystic neoplasm (mucinous cystadenoma and cystoadenocarcinoma)Mucinous cystic neoplasms are being diagnosed with considerable frequencythat, in the authors’ experience, exceeds the ‘‘1% of all pancreatic malignan-cies’’ figure that has been cited in prior studies and reviews. In the authors’practice, mucinous cystic neoplasms are encountered more frequently thanpseudocysts, further supporting other centers’ experiences that these are nowthe most common pancreatic cysts [4].

Fig. 3. Seventy-three-year-old man who has serous microcystic adenoma discovered on CTevaluation of an abdominal aortic aneurysm. (A) Contrast-enhanced CT shows a multicysticmass (arrow) in the pancreatic head. (B) EUS shows multiple small cystic spaces separatedby thin septa. A fine needle aspiration needle (arrow) was inserted and yielded thin fluidwith glycogen-rich cuboidal cells.


Mucinous cystic neoplasms tend to occur in a younger age group witha marked female predominance of approximately 80% [1,2,4,9]. Peak incidenceis in the 6th decade, but it is not rare to diagnose these in women as young as35 years old. Unlike serous tumors, approximately 70% to 95% of mucinouscystic tumors occur in the pancreatic body and tail segments.

Mucinous tumors are hypovascular, well-circumscribed masses with a wallof measurable thickness that is lined by tall, mucin-producing columnar cellsand ‘‘ovarian-type stroma,’’ which is now considered a required feature forconfident diagnosis of mucinous cystic neoplasms [16–18]. The mass is gener-ally unilocular or divided into fewer than six cystic spaces by septa (Fig. 4A, B).The septa and peripheral wall may calcify, said to occur in 10% to 25% of cases[16,18]. The mass may displace but usually does not obstruct the pancreaticduct.

Mucinous cystic neoplasms should be considered malignant or premalig-nant. The World Health Organization has classified the pathologic spectrumof mucinous cystic neoplasms using three dysplastic grades: (1) adenoma (mu-cinous cystadenoma), (2) borderline (mucinous cystic tumor—borderline), and(3) carcinoma in situ (mucinous cystadenocarcinoma—noninvasive). An inva-sive mucinous cystadenocarcinoma category exists, representing truly invasivecystadenocarcinomas [5]. Any imaging evidence of mural nodularity, enhance-ment or calcification, or ductal obstruction should be interpreted as suggestiveof malignancy.

The mucinous content of these tumors is suggested by higher than water at-tenuation on CT and variable signal intensity (different than ‘‘simple’’ fluid) onMR, reflecting the proteinaceous nature of the fluid. This is confirmed withneedle aspiration of the cyst contents, generally as part of the evaluationwith EUS (Fig. 5A, B). EUS also allows high-resolution imaging of the cystwall and may depict clues, such as mural nodularity, more readily than CT

Fig. 4. Forty-seven-year-old woman who has a mucinous cystic neoplasm (cystadenoma)—-surgically proven. (A) Contrast-enhanced CT shows a spherical mass (arrow) arising fromthe tail of the pancreas. A thin septum is visible near the dependent wall of the cyst. (B) EUSdemonstrates the cystic mass. The septum (arrow) and debris or mural nodularity along the de-pendent wall are more evident than on CT.


or MR. True mass components or mural nodules involving the cystic tumorcan be accurately targeted by way of EUS-FNA for malignant cytologic confir-mation. In the absence of a solid component, EUS-guided cyst aspiration is per-formed for diagnostic purposes. Cyst fluid is slightly viscous to thick andmucoid. The authors have rarely encountered mucinous cystadenomas witha thin serous aspirate. As cyst aspirate cytology suffers from poor sensitivitydue to the paucicellular nature of the sample [2,4], cyst fluid tumor markersplay an important diagnostic role. Cyst fluid CEA level is the most accuratetumor marker for diagnosis of a mucinous cystic neoplasm, with a diagnosticaccuracy of 79% when levels are greater than 192 ng/mL [2].

Cyst fluid CEA level, unfortunately, cannot predict the presence or absenceof malignancy. As the cellular content of cyst fluid aspirates is frequently sub-optimal, it was hypothesized that cyst epithelial cells shed their DNA into thefluid during cell turnover. As pancreatic carcinogenesis is characterized by theaccumulation of genetic defects, these mutations should be detectable throughcyst fluid DNA analysis. Additionally, an evolving or frankly malignant cystshould have a higher DNA content due to a higher cell turnover rate, andmore mutations should be present. To test this hypothesis, molecular analysisof EUS-guided cyst fluid aspirates was performed by way of polymerase chainreaction amplification of individual microsatellite markers associated with pan-creatic carcinogenesis, along with direct sequencing of the k-ras-2 gene [15].The DNA amount within the fluid (reported as optical density), number of mu-tations, and temporal sequence of mutations were shown to accurately predictthe presence of malignancy. A first-hit k-ras mutation followed by an allelic losswas highly predictive of malignancy. Although based on this small preliminaryexperience, molecular analysis may serve as an adjunct test in the evaluation ofcystic pancreatic lesions and is currently being evaluated in a multicenter study.

Fig. 5. Sixty-one-year-old man who has a mucinous cystic neoplasm (cystoadenocarcinoma)—-surgically proven. (A) Contrast-enhanced CT shows a cystic mass (arrow) in the neck of the pan-creas, immediately adjacent to the splenic vein. The mass has a detectable wall but no obviousmural nodularity. (B) EUS shows a thick-walled cystic mass (arrow) just ventral to the splenicvein (block arrow). The FNA needle is seen and aspiration yielded thick mucinous fluid withan elevated CEA level.


Although mucinous cystic tumors are to be considered premalignant, thenatural history of these tumors and true malignant risk are largely unknown.Therefore, surgical resection is not necessarily required in all patients. Manage-ment decisions should be based on many factors including the characteristics ofthe tumor itself, the general age and condition of the patient, and the availabil-ity of surgical expertise. Factors that would favor a more conservative ap-proach would include advanced patient age or comorbidity; a pancreatic cystthat was small, thin-walled, and noninvasive; a low cyst-fluid CEA level; anda molecular analysis that revealed a low amount of poor-quality DNA withan absence of mutations. A more aggressive approach is often warranted inyounger patients who have fewer comorbid factors, a larger or symptomaticcyst, and the availability of a surgeon experienced and expert at partial pancre-atic resection. Frankly malignant cysts, when diagnosed, should be surgicallyresected if the patient is an acceptable operative candidate.

Solid and papillary epithelial neoplasmThis is a rare tumor of low malignant potential that has been reported undervarious names including solid and pseudopapillary neoplasm, and solid andcystic tumor. Solid and papillary epithelial neoplasm has a predilection foryoung women, with over 90% of cases being reported in women under theage of 35, usually in non-Caucasians (Asian or African-American) [19]. The tu-mor is slow growing and may cause little or no discomfort until large.

Because of its indolent nature, solid and papillary epithelial neoplasm is oftendiagnosed when it has attained considerable size (on average, >10 cm). It isa hypovascular well-circumscribed mass, most often located in the pancreaticbody/tail segments (Fig. 6A–C). Depending on the extent of necrosis and hem-orrhage within the tumor, a solid and papillary epithelial neoplasm may appearalmost completely cystic or solid, though a poorly enhancing mass with centraland scattered necrosis is the most characteristic finding.

EUS-FNA can generally provide an accurate preoperative diagnosis, whichcan then direct the surgical approach (open or laparoscopic resection) [20].

Lymph node and liver metastases occur rarely and late in the disease. Com-plete surgical excision is generally possible and curative.

Cystic islet cell tumorPancreatic neuroendocrine (islet cell) tumors are usually hypervascular solidmasses and may be benign or malignant. Those that produce excessiveamounts of active polypeptide hormones, such as insulin or glucagon, are gen-erally diagnosed while the tumors are small (1–3 cm). Tumors that are ‘‘non-functional’’ are more likely to be diagnosed after they have attained large size;although in the authors’ experience, smaller incidental nonfunctioning tumorsare being detected, given increased use of abdominal imaging modalities[21–23].

Rarely, an islet cell tumor may be largely cystic (Fig. 7A, B). By imaging,these cannot be distinguished from other pancreatic cystic masses, especiallyif the mass is less than 2 cm in diameter. The diagnosis may be suggested


by evidence of hypervascular liver metastases or clinical signs or symptomssuch as palpitations, tremor, and headache (hypoglycemia due to an‘‘insulinoma’’).

EUS imaging typically reveals a thick-walled unilocular cyst, and EUS-FNAcan provide a definitive diagnosis on the basis of cytologic immunostaining pat-terns. Surgical resection is the treatment of choice.

SUMMARYPancreatic cystic lesions represent an increasingly common diagnostic and ther-apeutic challenge. Many cystic masses are pancreatic pseudocysts, and this di-agnosis is usually made readily by clinical history and imaging findings ofa unilocular pancreatic or peripancreatic mass with associated findings of acuteor chronic pancreatitis. CT and MR allow accurate depiction of the morphol-ogy of cystic pancreatic masses, and when in doubt, EUS-FNA can provide di-agnostic information based on fluid viscosity, CEA and/or amylase level, andmolecular analysis. In patients who have large, symptomatic, or complex cysticneoplasms and are suitable candidates for major surgery, preoperative

Fig. 6. Twenty-two-year-old woman who has a solid and papillary epithelial neoplasm. (A)Contrast-enhanced CT shows a mass (arrow) arising from the pancreatic tail. Peripheral calci-fication and enhancing nodules are seen along with cystic or necrotic areas. (B) EUS showsa complex cystic mass with peripheral calcifications (arrow). (C) Photograph of resectedmass shows an encapsulated tumor with foci of cystic necrosis and solid tumor.


evaluation by other imaging tests or cyst aspiration may be unnecessary. Forlesions that are small, asymptomatic, or occur in patients who have high surgi-cal risk, further evaluation with endoscopic ultrasonography is often useful.

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Fig. 7. Sixty-six-year-old man who has a cystic islet cell tumor. (A) Contrast-enhanced CTshows a small mass (arrow) in the pancreatic body that is mostly cystic, with a briskly enhanc-ing wall. (B) EUS confirms the small mass (arrow) with a central cystic space and a thicker wallthan was evident on CT.


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Cystic neoplasms of the pancreas 2007

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