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1 Department of Radiology, Brigham and Women's Hospital, Harvard Medical School,
75 Francis St., Boston, MA 02115.
2 Department of Pathology, Brigham and Women's Hospital, Harvard Medical School,
Boston, MA 02115.
Received July 26, 2002;
accepted after revision November 27, 2002.
Address correspondence to B. Khurana.
Abstract
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MATERIALS AND METHODS. Of seven cases fulfilling the pathology criteria for macrocystic serous adenoma over an 11-year period, five patients underwent preoperative CT and MR imaging at our institution. In addition to the clinical presentation and pathologic features of the tumor, the following CT and MR imaging features were reviewed: size and location; wall thickness; internal septations; and presence of mural nodules, papillary projections, or calcifications.
RESULTS. All patients but one were women (age range, 36–78 years; mean age, 48.6 years). The sizes of the tumors ranged from 1.5 to 5.0 cm (mean, 3.1 cm). Three (60%) of five tumors were located in the pancreatic head. The wall measured less than 2 mm in four lesions and 4 mm in one. No mural nodules, papillary projections, or calcifications were present. Lesions were unilocular (n = 3) or bilocular (n = 2). Excellent correlation of imaging features with gross pathology was observed.
CONCLUSION. On CT and MR imaging, the macrocystic variant of serous adenoma typically appears as a small (< 5 cm), uni- or bilocular cyst with a thin (< 2 mm) wall that lacks mural nodules or calcifications. The imaging appearance of macrocystic serous adenoma is distinctly different from that of microcystic serous cystadenoma, but the imaging appearance of macrocystic serous adenoma is indistinguishable from mucinous cystadenoma and cystadenocarcinoma of the pancreas.
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In this study, we describe the CT and MR imaging features in a series of five consecutive pathologically proven cases of macrocystic serous cystadenoma and review the literature. The aim of our retrospective analysis was to provide a more conclusive presentation of the various radiologic data and the predominant pathologic findings.
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CT and MR Imaging Analyses
Because this study is retrospective and includes CT and MR imaging studies
performed over a 12-year period, the scanning protocols for the examinations
varied. Four of five patients underwent both unenhanced and contrast-enhanced
CT studies with reconstruction intervals ranging from 3 to 10 mm. MR imaging
was performed after contrast-enhanced CT in one patient for further
evaluation. The images were evaluated by two experienced abdominal
radiologists in consensus to define the following morphologic features: the
diameter of the tumor (measured in centimeters), location of the tumor in the
pancreas, tumor margin (well-defined or ill-defined, smooth or irregular),
wall thickness (> 2 or ≤ 2 mm), septations (present or absent, unior
multilocular), mural nodules (present or absent), papillary projections
(present or absent), and calcifications (present or absent).
Pathologic Examination
All tumors were surgically resected. Preoperative fine-needle aspiration
was performed in one patient, and cytologic examination of the cysts' contents
was performed in three cases. After the tumors were resected, the tissue was
fixed in 10% formaldehyde, processed routinely, and embedded in paraffin.
Paraffin sections were stained with H and E, periodic acid—Schiff with
and without diastase digestion, and mucicarmine. The descriptions of the gross
tumors and the microscopic slides were reviewed in all cases by an experienced
pathologist, and the diagnosis of macrocystic serous adenoma was confirmed in
all cases.
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CT and MR Imaging Analyses
On CT and MR images, all tumors were cystic and ranged in size from 1.5 to
5.0 cm (mean, 3.1 cm). Three tumors (60%) were located in the pancreatic head,
one (20%) in the pancreatic neck, and one (20%) in the tail. All the tumors
were round or oval with well-defined margins. No invasion of surrounding
pancreatic parenchyma was seen. The wall was smooth in all cases and was less
than 2 mm thick in four (80%) of the five tumors. Only one case showed a
thicker wall, measuring up to 4 mm. At pathologic examination of the largest
lesion, this thickening was found to correlate with a focus of old intracystic
hemorrhage because hemosiderin was found in the wall. No mural nodules,
papillary projections, or calcifications were seen in any of the tumors (Figs.
1A,
1B,
1C,
1D,
1E).
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The lesions were unilocular (n = 3) or bilocular (n = 2). The latter two lesions each showed one septation (Figs. 2A, 2B). IV contrast material was administered in four patients, but when the lesion was compared with surrounding pancreatic parenchyma, no predominant enhancement of the wall or septa was seen (100%). MR imaging was performed in one patient, and the tumor appeared as a simple unilocular cyst, similar to its appearance on CT, homogenously hypointense on T1-weighted and hyperintense on T2-weighted images (Figs. 1A, 1B, 1C, 1D, 1E). In four of the five patients, the presumptive preoperative diagnosis was mucinous cystadenoma, and it was pseudocyst in one patient.
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Gross and Microscopic Features
CT and MR imaging depicted all features identified on gross pathologic
examination. All five tumors were well-circumscribed and did not infiltrate
the surrounding pancreatic parenchyma, as suggested by the radiologic
findings. All tumors contained one or two dominant cystic spaces, similar to
their radiologic appearances. However, two lesions that appeared bilocular on
CT contained additional (up to five) smaller cystic spaces adjacent to the
dominant spaces that were visible only on microscopic examination.
All macrocystic adenomas were lined by a single layer of cuboidal epithelium with uniform round nuclei and clear or eosinophilic cytoplasm (Figs. 3A, 3B, 3C). These cells showed positive cytoplasmic findings when periodic acid—Schiff stain that was sensitive to diastase digestion was used and negative findings when mucicarmine was used. The cyst walls were composed of hypocellular fibrous tissue. Gross examination confirmed the absence of mural nodules, papillary projections, or calcifications. However, in one case, two plaquelike white fibrous nodules (4 mm in diameter each) were noted microscopically.
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Preoperative biochemical analysis of the cystic fluid was performed in only one case. Carcinoembryonic antigen was found to be within normal limits (1.1 ng/mL). However, cancer antigen (CA) 19-9 was elevated (1351 U/mL).
Cytologic examination of pancreatic cystic fluid was performed in three cases after surgical resection. All three specimens were hypocellular with rare benign-appearing epithelial cells. In one case, mucicarmine staining was performed, and the results were negative, supporting the diagnosis of a serous tumor. In the other two, a distinction between a mucinous and a serous tumor could not be made.
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In contradistinction to serous microcystic adenoma, macrocystic serous adenoma is composed of fewer and larger cysts; however, in both types of tumors, the cyst walls are lined by epithelial cells and show evidence of ductal differentiation. Macrocystic serous adenomas are less common than serous microcystic adenomas, and, to date, the imaging findings of these tumors have been described only in case reports [3, 4]. Because the cystic spaces are larger, macrocystic serous adenoma may be confused on imaging with mucinous cystic neoplasm. This distinct pancreatic tumor is composed of mucin-producing epithelial cells, shows evidence of gastroenteropancreatic differentiation, has an "ovarian-type" stroma, and has significant malignant potential [1].
The optimal surgical management of cystic neoplasms of the pancreas depends on the specific type of cystic neoplasm present (serous cystic vs mucinous cystic vs intraductal papillary mucinous tumor). Most patients with serous cystadenoma do not require resection unless they are symptomatic (abdominal pain, jaundice, or recurrent pancreatitis) or the diagnosis is unclear on the basis of clinical or radiologic findings alone. In contrast, virtually all mucinous cystic neoplasms of the pancreas should be resected because of their potential for malignant degeneration [6]. Thus, the initial imaging-based differentiation of a serous cystic neoplasm from a mucinous cystic neoplasm becomes of primary importance.
The age of the patient at diagnosis of macrocystic serous adenoma has been described to range from 46 to 79 years (mean, 60 years), with tumor diameter at presentation ranging from 4 to 10 cm (mean, 6 cm) [5]. The patients in our series showed a slightly younger mean age (48.6 years) and a smaller tumor diameter at presentation (range, 1.5–5.0 cm; mean, 3.1 cm). The peak occurrence for ductal adenocarcinoma has been described to be in patients who are in the seventh or eighth decade of life, whereas mucinous macrocystic adenomas manifest with a wide age distribution, with the largest category of patients ranging in age from 40 to 60 years [7].
Similar to the series of Sperti et al. [5], our series also showed a female predominance (4:1), and three (60%) of five tumors were located in the pancreatic head. However, unlike previously reported cases, one (20%) of the five lesions was located in the pancreatic neck and one (20%) in the pancreatic tail.
Patients with macrocystic serous adenoma usually present with abdominal pain [2, 4–6], but the tumor is often fortuitously discovered. In our series, four patients presented with abdominal symptoms. However, none of them showed symptoms that were clearly associated with the tumor.
Our series showed an excellent correlation between radiologic and pathologic features. The tumors were uni- or bilocular cystic lesions containing no mural nodules, papillary projections, or calcifications. The gross examination of these tumors corresponded to the radiologic examinations, and, as described by Lewandrowski et al. [2] in three of the five tumors in their study, additional satellite microcysts were seen adjacent to the dominant cyst in two tumors in our series.
Calcification is considered to be more frequently present in serous cystic tumors than in mucinous cystadenomas. However, similar to the cases described in literature, ours did not show calcifications. We found these tumors to be thin-walled, with a wall thickness usually less than 2 mm. These findings may be slightly altered by intracystic hemorrhage, as seen on imaging in one case of our series and on sonography in a case reported by Gouhiri et al. [6].
Our study is limited in describing the sonographic features of these tumors because none of our patients underwent sonography. Sonography can be useful in revealing and characterizing the internal septations of these tumors. Similarly, because all our patients underwent CT on a single-detector CT scanner, we expect that multidetector CT using a standard pancreatic protocol would be more sensitive in depicting these internal septations and tiny focal calcifications.
Biochemical analysis of cystic fluid and determination of tumor markers (carcinoembryonic antigen, CA 15-3, CA 72-4, and 3-methylcholanthrene) have been reported as potentially useful preoperative tests to identify malignant or potentially malignant mucinous adenoma among the pancreatic cystic lesions. In our series, cystic fluid analysis was performed in only one case before surgery, which showed an elevated level of CA 19-9 and a normal level of carcinoembryonic antigen. On the basis of biochemical analysis of pancreatic cystic fluid, Sperti et al. [5] reported that none of the cysts in their series expressed CA 72-4, CA 15-3, or 3-methylcholanthrene (markers associated with mucinous tumors). The absence of these three tumor markers strongly suggests a nonmucinous tumor or a cystic lesion with low malignant potential. Unilocular lesions other than cystadenomas with low levels of tumor markers include benign congenital solitary cyst or the cysts diagnosed in patients with von Hippel's disease.
Although the presence of isolated or clustered cuboidal cells with uniform round nuclei and fine chromatin and granular cytoplasm is considered diagnostic of serous cystadenoma, the samples obtained at fine-needle aspiration of serous cystadenoma are often acellular or hemorrhagic [5]. This occurred in two of our three cases in which the cytologic examination of the cystic fluid after surgical resection was inconclusive.
Our series confirms that macrocystic serous cystadenoma is a rare pancreatic serous cystic tumor with a biologic behavior similar to that of microcystic serous cystadenoma but a distinctly different radiologic appearance. The superficial resemblance of macrocystic serous cystadenoma to mucinous cystadenoma and cystadenocarcinoma of the pancreas makes its diagnosis challenging for both the radiologist and the pathologist. The features seen in our series are similar to the radiologic findings, which predict benignity in a mucinous cystic tumor. In a series of 52 mucinous cystic tumors, lesions characterized by a multilocular macrocystic architecture with thick walls and calcifications in the wall or septa had the highest risk of malignancy [8]. Moreover, in lesions with unilocular architecture with thin walls and no calcifications, the incidence of malignancy was low. Thus, a preoperative presumptive diagnosis of a benign cystic pancreatic neoplasm can be suggested on the basis of these findings, although the distinction between serous and mucinous tumors cannot be made on the basis of radiologic findings only. Similarly, if the lesion shows multiple septations, significant enhancement, mural nodules, or papillary projections, the diagnosis of macrocystic serous cystadenoma should be downplayed.
A fine-needle aspiration and biochemical analysis of the cystic fluid showing low levels of mucinous tumor-related markers (e.g., CA 72-4, carcinoembryonic antigen, and 3-methylcholanthrene) could be useful to avoid performing surgery for benign pancreatic lesions. However, because of a lack of sufficient data with respect to the cytologic analyses of these tumors at present, the only way to obtain a correct diagnosis is to perform a careful pathologic examination after surgical removal of the tumor.
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