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Journal of Digestive Diseases 2014; 15; 211–215
doi: 10.1111/1751-2980.12128
Case report
A case of solid-type serous cystadenoma mimicking neuroendocrine tumor of the pancreas Yoshihiro KISHIDA,* Hiroyuki MATSUBAYASHI,* Yukiyasu OKAMURA,† Katsuhiko UESAKA,† Keiko SASAKI,‡ Hiroaki SAWAI,* Kenichiro IMAI* & Hiroyuki ONO* Divisions of *Endoscopy, †Hepato-Pancreato-Biliary Surgery, and ‡Pathology, Shizuoka Cancer Center, Suntogun, Shizuoka, Japan
INTRODUCTION
CASE REPORT
Pancreatic cystic neoplasms, including serous cystic neoplasm (SCN) and mucinous cystic neoplasm, constitute approximately only 1–2% of all pancreatic tumors.1 Nevertheless, a great proportion of pancreatic cystic neoplasms are now being detected due to the recent improvements in imaging modalities. SCN is currently categorized into five subtypes: serous microcystic adenomas, serous oligocystic ill-demarcated adenomas, solid-type serous cystadenomas or solid serous adenoma (SSCA),2,3 von Hippel–Lindau disease-associated cystic neoplasms and serous cystadenocarcinomas.1,4 Among them, SSCA is by far the rarest subtype. SCN is a basically benign entity, so watchful observation is recommended unless the patients appear to have symptoms or the tumor turns to have malignant potential.1,5 However, an accurate preoperative diagnosis of SSCA is difficult because of its rarity and its resemblance in image findings to neuroendocrine tumor (NET) of the pancreas.6 Here we report a case of SSCA which was preoperatively diagnosed as NET of the pancreas, with a review of the published literatures.
A 58-year-old Japanese man was admitted to our hospital for a pancreatic mass that was found incidentally during a routine medical check. He had no specific symptoms or underlying diseases and his family history was not remarkable. Laboratory data were within the normal range, including serum markers of exocrine and endocrine pancreatic tumors (carcinoembryonic antigen [CEA], carbohydrate antigen 19-9 [CA19-9], insulin, gastrin and glucagon). Abdominal ultrasonography showed a well-demarcated, round low echoic tumor (28 mm in diameter) at the pancreatic body (Fig. 1a). Doppler ultrasonography demonstrated a rich blood flow at the tumor margin (Fig. 1b). Plane computed tomography (CT) revealed a solid mass with lower density (11.1 Hounsfield unit [HU]) than other parts of the pancreas (31.2 HU). Contrast injection showed increased enhancement (165.8 HU) of the marginal zone of the tumor until the late arterial phase. In the delayed phase, weak tumor enhancement remained (107.3 HU) compared with the adjacent normal pancreatic tissues (73.8 HU). The central part of the tumor was consistently poorly enhanced throughout the scan (Fig. 2). None of the well-known characteristics of SCN was apparent, such as honeycomb appearance, polycystic pattern, macrocystic or oligocystic pattern, central scarring or sunburst appearance (stellate calcification).1 Magnetic resonance imaging (MRI) revealed hypointensity of the tumor on T1-weighted image and high intensity on T2-weighted image (Fig. 3). A dynamic MRI showed a marked enhancement from the edge towards the center of the tumor. No central scar-like delayed enhancement was observed.7 Magnetic resonance cholangiopancreatography (MRCP) indicated elevated intensity in the
Correspondence to: Hiroyuki MATSUBAYASHI, Division of Endoscopy, Shizuoka Cancer Center, 1007, Nagaizumi, Suntogun, Shizuoka 411-8777, Japan. Email: [email protected] Conflict of interest: None. © 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
211
212
Y Kishida et al.
Journal of Digestive Diseases 2014; 15; 211–215
a
b
Figure 1. Abdominal ultrasonography. (a) The tumor appears as a well-demarcated round low echoic lesion surrounded by a low echoic capsule (arrow). Fine high echoic foci are visible inside the tumor and echo enhancement appears at the posterior side of the tumor. (b) Doppler image shows rich blood flow at the tumor margin.
a
Figure 3. T2-weighted magnetic resonance imaging showing a higher intensity of the tumor than the usual neuroendocrine tumor.
a
b
c
d
b
c
Figure 2. Contrast enhanced computed tomography (CT). (a) Plane CT. A low density mass is seen at the body of the pancreas. (b) Early phase dynamic CT (40 s). The marginal zone of the tumor is increasingly enhanced, while its central part is poorly enhanced. (c) Delayed phase dynamic CT (120 s). Although weak, the tumor enhancement remains at the tumor periphery but is still poorly enhanced in the central area.
tumor. And endoscopic ultrasonography guided-fine needle aspiration (EUS-FNA) was avoided to prevent the seeding of the tumor. These image findings raised the suspicion of a nonfunctional NET with central necrosis; therefore, the patient underwent distal pancreatectomy. Histological examination revealed a solid, well-circumscribed tumor with heterogeneous density; dense at the marginal site and sparse towards the center, in the absence of necrosis or hemorrhage (Fig. 4). High magnification (HE stain, ×400). The tumor consisted of clustered microcysts organized as a single layer of
e
Figure 4. Resected specimen of the tumor. (a) Macroscopic view. The tumor is ashen in color, soft and solid with thin, whitish-yellow central tissues. (b) Whole view of the section (HE stain, ×20) showing a well-circumscribed tumor capsulized by thick fibrosis. (c) Low power view of the tumor (HE stain, ×40) showing that the histological structures, both cyst and stroma, are dense at the marginal site and tend to be sparse towards the center. (d) High magnification (HE stain, ×400). The edge of the tumor contains densely clustered microcysts organized as a single layer of cubic epithelial cells with bright cytoplasm. (e) CD31 immunostain (×200) shows rich microvessels in the marginal area of the tumor.
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 211–215
Solid-type serous cystadenoma
213
cubicepithelial cells with bright cytoplasm. Periodic acid-Schiff staining was positive in the cytoplasmic granules following digestion with diastase and was negative for Alcian blue, indicating the presence of glycogen. Immunostaining for CD31 indicated a higher density of microvessels at the tumor margin than that at its center. These findings led us to the pathological diagnosis that this tumor was a solid variant of SSCA. The patient’s postsurgical course was uneventful and no recurrence or residual lesion was evident after 2 years.
tumor grows and appears as a hypovascular area.17 Differentiation between a moisture-rich area occurring in SSCA and a necrotic area is extremely difficult using only imaging findings and this led to our misdiagnosis of the current tumor. However, in general, the necrosis occurs in the large-sized NET (8 cm on average) and is rare in the small NET (about 2–3 cm in size).17 The use of ultrasonography or EUS can rule out the presence of necrosis and could permit characteristic findings such as central scar or dense fibrous septa to be recognized in the tumor.
DISCUSSION
The published reports involving 11 cases of SSCA found strong enhancement in the early phase of dynamic CT.3,5,7,9–12,14,15 Interestingly, as in the current case, many of these patients showed a weak or poor enhancement during the early to the late phase in the central area of the tumor compared with the marginal area,5,7,12 although no necrosis was found in the resected samples. In our case, this phenomenon can be explained by the high density of microvessels at the tumor margin and the presence of a surrounding fibrous capsule. Alternatively, it may be explained by the rich vascularity and drainage speed of this tumor. Hayashi et al.5 compared sequential tumor enhancement by dynamic CT between SSCA and NET and reported a faster contrast washout rate in SSCA (SSCA 0.55 vs NET 0.29, P < 0.05). In our current case the washout rate was 0.55, which is quite compatible with that of SSCA, and this finding is supposedly helpful for diagnosis.
SSCA of the pancreas is quite rare, accounting for only 3% of all SCA.1 Until the writing of the article, only 15 cases including ours have been published with a pathological confirmation since the first report by Perez-Ordonez et al.2 in 1996 (Table 1). Knowledge of this disease is important because on image its features resemble those of other solid tumors such as NET, metastasis of renal cell carcinoma and solid pseudopapillary tumor, but the clinical management of these diseases is quite different.8 Compared with the common types of SCA, this subtype tends to have tumors of smaller size (2.9 cm),1 with no obvious gender predilection (M : F = 7:8), although the age of the patients and the location of the tumors are similar to those of the common SCA types (Table 1). Characteristic SCA image findings,1 such as honeycomb appearance, polycystic pattern, lobularity, sunburst appearance (central calcification) and hemorrhage have not been reported for SSCA.2–5,7,9–15 A multicenter study by the Japan Pancreatic Society concluded that this subtype of SCA is difficult to distinguish from other pancreatic solid tumors using clinical images.1 Tissues obtained by EUS-FNA is also essentially non-diagnostic for SCA.16 However, hints for its accurate diagnosis may be hidden in the various image findings that may reflect its unique histological appearances.
MRI findings of SSCA reported by Gabata et al.7 and Yamamoto et al.15 pointed to a marked, high-intensity lesion on the T2-weighted image (higher than hemangioma and almost equal to cyst on MRCP), which was strongly enhanced in the early phase of dynamic MRI. Notably, MRI images of NET show a low-intensity signal on the T1-weighted image and high intensity on the T2-weighted image, although the latter is not as high as that of a cyst. These findings are also useful for differential diagnosis.
The available literatures report 10 cases of SSCA with written information of preoperative diagnosis, among which eight cases (including our patient) were diagnosed preoperatively as pancreatic NET2,3,10,11,13–15 and only two cases were diagnosed correctly7,9 (Table 1). NET is the most common solid hypervascular tumor of the pancreas and dynamic images of this tumor typically show a marked enhancement during the arterial and portal phases.6 However, another characteristic of NET, namely central necrosis, occurs when the
EUS-FNA does not provide adequate samples for diagnosing cases of SCA16 and SSCA,14 but it remains a powerful and highly sensitive tool for the diagnosis of solid pancreatic masses (accuracy >90% in tumor ≥2 cm).18 This is also true for pancreatic NET.19 SCA is a slow-growing tumor, mostly without malignant transformation, therefore, if NET or other malignant tissues is negative by FNA, a careful follow-up can be chosen in cases where the image findings are suggestive of SSCA.
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
M M F
50 60 59
58 66 62 74 59 72 74 57 58 56 58
Yamaguchi3 (2005) Reese et al.11 (2006) Stern et al.13 (2007) Sanaka et al.14 (2007) Casadei et al.9 (2008) Yasuda et al.10 (2009) Hayashi et al.5 (2012) Hayashi et al.5 (2012) Hayashi et al.5 (2012) Lee et al.12 (2013) Current case (2013) Pb Ph Ph Pb Pb Pt Ph Pb Ph Pb Pt Pb
Ph Ph Pb
Pt
2 4 4.2 1.6 4 1.7 4.2 2.1 3.2 2.5 2.8
2.5 2 2.0
4.0
Size Location (cm) –
MRI (T1/T2)
– Low/high Low/high and central low -/Well enhanced/– -/Well enhanced/– -/-/Enhanced heterogeneously – -/Enhanced/– Well-defined/well enhanced/– Low/well enhanced/prolonged -/high Low/well enhanced/low† – Low/well enhanced/low† – Low/well enhanced/low† – -/Enhanced/enhanced – Low/well enhanced/enhanced† Low/high
– Low/enhanced uniformly/Low/enhanced homogeneously/low†
–
CT (U/E/D)
–
NET
NET NET NET, others‡ NET SSCA NET – – –
NET SSCA
NET
Clinical diagnosis
FS, FS, FS, FS, FC FC FC FC
FC CS
– –
– FC FC FC FC
–
–
Pathology
†A tumor with central low-density area shown on the figure of the reports. ‡Others include pancreatic cancer, solid pseudopapillary tumor, metastatic carcinoma. CS, central scar; CT (U/E/D), computed tomography (unenhanced/early phase/delayed phase); F, female; FC, fibrous capsule; FS, fibrous septa within the tumor; M, male; MRI, magnetic resonance imaging; NET, neuroendocrine tumor; Pb, pancreas body; Ph, pancreas head; Pt, pancreas tail; SSCA, solid-type serous cystadenoma.
None None Abdominal pain None Abdominal pain None – – – None None
– Epigastric distention Abdominal pain
Abdominal pain
Symptoms
Y Kishida et al.
F M M M F F F F F M M
F
70
Age (years) Gender
Literature review of the clinicopathological findings of patients with solid-type serous cystadenomas
Perez-Ordonez et al.2 (1996) Kosmahl et al.4 (2004) Yamamoto et al.15 (2004) Gabata et al.7 (2005)
Study
Table 1.
214
Journal of Digestive Diseases 2014; 15; 211–215
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 211–215 SSCA typically shows very rich vascularity (especially at the marginal side of the tumor), a faster contrast washout on CT and a signal of very high intensity on T2-weighted MRI or MRCP. In contrast, NET shows slower contrast washout on CT than SSCA and relatively high intensity on T2-weighted MRI or MRCP, but not as high as SSCA. A moisture-rich area of SSCA is shown on CT as a hypovascular area even if the tumor is small, but in NET such areas can be seen when the tumor is large. REFERENCES 1 Kimura W, Moriya T, Hirai I et al. Multicenter study of serous cystic neoplasm of the Japan pancreas society. Pancreas 2012; 41: 380–7. 2 Perez-Ordonez B, Naseem A, Lieberman PH, Klimstra DS. Solid serous adenoma of the pancreas. The solid variant of serous cystadenoma? Am J Surg Pathol 1996; 20: 1401–5. 3 Yamaguchi M. Solid serous adenoma of the pancreas: a solid variant of serous cystadenoma or a separate disease entity? J Gastroenterol 2006; 41: 178–9. 4 Kosmahl M, Wagner J, Peters K, Sipos B, Klöppel G. Serous cystic neoplasms of the pancreas: an immunohistochemical analysis revealing alpha-inhibin, neuron-specific enolase, and MUC6 as new markers. Am J Surg Pathol 2004; 28: 339–46. 5 Hayashi K, Fujimitsu R, Ida M et al. CT differentiation of solid serous cystadenoma vs endocrine tumor of the pancreas. Eur J Radiol 2012; 81: e203–8. 6 Rha SE, Jung SE, Lee KH, Ku YM, Byun JY, Lee JM. CT and MR imaging findings of endocrine tumor of the pancreas according to WHO classification. Eur J Radiol 2007; 62: 371–7. 7 Gabata T, Terayama N, Yamashiro M et al. Solid serous cystadenoma of the pancreas: MR imaging with pathologic correlation. Abdom Imaging 2005; 30: 605–9.
Solid-type serous cystadenoma
215
8 Kim HJ, Lee DH, Ko YT, Lim JW, Kim HC, Kim KW. CT of serous cystadenoma of the pancreas and mimicking masses. AJR Am J Roentgenol 2008; 190: 406–12. 9 Casadei R, D’Ambra M, Pezzilli R et al. Solid serous microcystic tumor of the pancreas. JOP 2008; 9: 538–40. 10 Yasuda A, Sawai H, Ochi N, Matsuo Y, Okada Y, Takeyama H. Solid variant of serous cystadenoma of the pancreas. Arch Med Sci 2011; 7: 353–5. 11 Reese SA, Traverso LW, Jacobs TW, Longnecker DS. Solid serous adenoma of the pancreas: a rare variant within the family of pancreatic serous cystic neoplasms. Pancreas 2006; 33: 96–9. 12 Lee SD, Han SS, Hong EK. Solid serous cystic neoplasm of the pancreas with invasive growth. J Hepatobiliary Pancreat Sci 2013; 20: 454–6. 13 Stern JR, Frankel WL, Ellison EC, Bloomston M. Solid serous microcystic adenoma of the pancreas. World J Surg Oncol 2007; 5: 26. 14 Sanaka MR, Kowalski TE, Brotz C, Yeo CJ, McCue P, Palazzo J. Solid serous adenoma of the pancreas: a rare form of serous cystadenoma. Dig Dis Sci 2007; 52: 3154–6. 15 Yamamoto T, Takahashi N, Yamaguchi T, Imamura Y. A case of solid variant type of pancreatic serous cystadenoma mimicking islet cell tumor. Clin Imaging 2004; 28: 49–51. 16 Belsley NA, Pitman MB, Lauwers GY, Brugge WR, Deshpande V. Serous cystadenoma of the pancreas: limitations and pitfalls of endoscopic ultrasound-guided fine-needle aspiration biopsy. Cancer 2008; 114: 102–10. 17 Buetow PC, Parrino TV, Buck JL et al. Islet cell tumors of the pancreas: pathologic-imaging correlation among size, necrosis and cysts, calcification, malignant behavior, and functional status. AJR Am J Roentgenol 1995; 165: 1175–9. 18 Imai K, Matsubayashi H, Fukutomi A, Uesaka K, Sasaki K, Ono H. Endoscopic ultrasonography-guided fine needle aspiration biopsy using 22-gauge needle in diagnosis of autoimmune pancreatitis. Dig Liver Dis 2011; 43: 869–74. 19 Bernstein J, Ustun B, Alomari A et al. Performance of endoscopic ultrasound-guided fine needle aspiration in diagnosing pancreatic neuroendocrine tumors. Cytojournal 2013; 10: 10.
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 211–215
doi: 10.1111/1751-2980.12128
Case report
A case of solid-type serous cystadenoma mimicking neuroendocrine tumor of the pancreas Yoshihiro KISHIDA,* Hiroyuki MATSUBAYASHI,* Yukiyasu OKAMURA,† Katsuhiko UESAKA,† Keiko SASAKI,‡ Hiroaki SAWAI,* Kenichiro IMAI* & Hiroyuki ONO* Divisions of *Endoscopy, †Hepato-Pancreato-Biliary Surgery, and ‡Pathology, Shizuoka Cancer Center, Suntogun, Shizuoka, Japan
INTRODUCTION
CASE REPORT
Pancreatic cystic neoplasms, including serous cystic neoplasm (SCN) and mucinous cystic neoplasm, constitute approximately only 1–2% of all pancreatic tumors.1 Nevertheless, a great proportion of pancreatic cystic neoplasms are now being detected due to the recent improvements in imaging modalities. SCN is currently categorized into five subtypes: serous microcystic adenomas, serous oligocystic ill-demarcated adenomas, solid-type serous cystadenomas or solid serous adenoma (SSCA),2,3 von Hippel–Lindau disease-associated cystic neoplasms and serous cystadenocarcinomas.1,4 Among them, SSCA is by far the rarest subtype. SCN is a basically benign entity, so watchful observation is recommended unless the patients appear to have symptoms or the tumor turns to have malignant potential.1,5 However, an accurate preoperative diagnosis of SSCA is difficult because of its rarity and its resemblance in image findings to neuroendocrine tumor (NET) of the pancreas.6 Here we report a case of SSCA which was preoperatively diagnosed as NET of the pancreas, with a review of the published literatures.
A 58-year-old Japanese man was admitted to our hospital for a pancreatic mass that was found incidentally during a routine medical check. He had no specific symptoms or underlying diseases and his family history was not remarkable. Laboratory data were within the normal range, including serum markers of exocrine and endocrine pancreatic tumors (carcinoembryonic antigen [CEA], carbohydrate antigen 19-9 [CA19-9], insulin, gastrin and glucagon). Abdominal ultrasonography showed a well-demarcated, round low echoic tumor (28 mm in diameter) at the pancreatic body (Fig. 1a). Doppler ultrasonography demonstrated a rich blood flow at the tumor margin (Fig. 1b). Plane computed tomography (CT) revealed a solid mass with lower density (11.1 Hounsfield unit [HU]) than other parts of the pancreas (31.2 HU). Contrast injection showed increased enhancement (165.8 HU) of the marginal zone of the tumor until the late arterial phase. In the delayed phase, weak tumor enhancement remained (107.3 HU) compared with the adjacent normal pancreatic tissues (73.8 HU). The central part of the tumor was consistently poorly enhanced throughout the scan (Fig. 2). None of the well-known characteristics of SCN was apparent, such as honeycomb appearance, polycystic pattern, macrocystic or oligocystic pattern, central scarring or sunburst appearance (stellate calcification).1 Magnetic resonance imaging (MRI) revealed hypointensity of the tumor on T1-weighted image and high intensity on T2-weighted image (Fig. 3). A dynamic MRI showed a marked enhancement from the edge towards the center of the tumor. No central scar-like delayed enhancement was observed.7 Magnetic resonance cholangiopancreatography (MRCP) indicated elevated intensity in the
Correspondence to: Hiroyuki MATSUBAYASHI, Division of Endoscopy, Shizuoka Cancer Center, 1007, Nagaizumi, Suntogun, Shizuoka 411-8777, Japan. Email: [email protected] Conflict of interest: None. © 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
211
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Y Kishida et al.
Journal of Digestive Diseases 2014; 15; 211–215
a
b
Figure 1. Abdominal ultrasonography. (a) The tumor appears as a well-demarcated round low echoic lesion surrounded by a low echoic capsule (arrow). Fine high echoic foci are visible inside the tumor and echo enhancement appears at the posterior side of the tumor. (b) Doppler image shows rich blood flow at the tumor margin.
a
Figure 3. T2-weighted magnetic resonance imaging showing a higher intensity of the tumor than the usual neuroendocrine tumor.
a
b
c
d
b
c
Figure 2. Contrast enhanced computed tomography (CT). (a) Plane CT. A low density mass is seen at the body of the pancreas. (b) Early phase dynamic CT (40 s). The marginal zone of the tumor is increasingly enhanced, while its central part is poorly enhanced. (c) Delayed phase dynamic CT (120 s). Although weak, the tumor enhancement remains at the tumor periphery but is still poorly enhanced in the central area.
tumor. And endoscopic ultrasonography guided-fine needle aspiration (EUS-FNA) was avoided to prevent the seeding of the tumor. These image findings raised the suspicion of a nonfunctional NET with central necrosis; therefore, the patient underwent distal pancreatectomy. Histological examination revealed a solid, well-circumscribed tumor with heterogeneous density; dense at the marginal site and sparse towards the center, in the absence of necrosis or hemorrhage (Fig. 4). High magnification (HE stain, ×400). The tumor consisted of clustered microcysts organized as a single layer of
e
Figure 4. Resected specimen of the tumor. (a) Macroscopic view. The tumor is ashen in color, soft and solid with thin, whitish-yellow central tissues. (b) Whole view of the section (HE stain, ×20) showing a well-circumscribed tumor capsulized by thick fibrosis. (c) Low power view of the tumor (HE stain, ×40) showing that the histological structures, both cyst and stroma, are dense at the marginal site and tend to be sparse towards the center. (d) High magnification (HE stain, ×400). The edge of the tumor contains densely clustered microcysts organized as a single layer of cubic epithelial cells with bright cytoplasm. (e) CD31 immunostain (×200) shows rich microvessels in the marginal area of the tumor.
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 211–215
Solid-type serous cystadenoma
213
cubicepithelial cells with bright cytoplasm. Periodic acid-Schiff staining was positive in the cytoplasmic granules following digestion with diastase and was negative for Alcian blue, indicating the presence of glycogen. Immunostaining for CD31 indicated a higher density of microvessels at the tumor margin than that at its center. These findings led us to the pathological diagnosis that this tumor was a solid variant of SSCA. The patient’s postsurgical course was uneventful and no recurrence or residual lesion was evident after 2 years.
tumor grows and appears as a hypovascular area.17 Differentiation between a moisture-rich area occurring in SSCA and a necrotic area is extremely difficult using only imaging findings and this led to our misdiagnosis of the current tumor. However, in general, the necrosis occurs in the large-sized NET (8 cm on average) and is rare in the small NET (about 2–3 cm in size).17 The use of ultrasonography or EUS can rule out the presence of necrosis and could permit characteristic findings such as central scar or dense fibrous septa to be recognized in the tumor.
DISCUSSION
The published reports involving 11 cases of SSCA found strong enhancement in the early phase of dynamic CT.3,5,7,9–12,14,15 Interestingly, as in the current case, many of these patients showed a weak or poor enhancement during the early to the late phase in the central area of the tumor compared with the marginal area,5,7,12 although no necrosis was found in the resected samples. In our case, this phenomenon can be explained by the high density of microvessels at the tumor margin and the presence of a surrounding fibrous capsule. Alternatively, it may be explained by the rich vascularity and drainage speed of this tumor. Hayashi et al.5 compared sequential tumor enhancement by dynamic CT between SSCA and NET and reported a faster contrast washout rate in SSCA (SSCA 0.55 vs NET 0.29, P < 0.05). In our current case the washout rate was 0.55, which is quite compatible with that of SSCA, and this finding is supposedly helpful for diagnosis.
SSCA of the pancreas is quite rare, accounting for only 3% of all SCA.1 Until the writing of the article, only 15 cases including ours have been published with a pathological confirmation since the first report by Perez-Ordonez et al.2 in 1996 (Table 1). Knowledge of this disease is important because on image its features resemble those of other solid tumors such as NET, metastasis of renal cell carcinoma and solid pseudopapillary tumor, but the clinical management of these diseases is quite different.8 Compared with the common types of SCA, this subtype tends to have tumors of smaller size (2.9 cm),1 with no obvious gender predilection (M : F = 7:8), although the age of the patients and the location of the tumors are similar to those of the common SCA types (Table 1). Characteristic SCA image findings,1 such as honeycomb appearance, polycystic pattern, lobularity, sunburst appearance (central calcification) and hemorrhage have not been reported for SSCA.2–5,7,9–15 A multicenter study by the Japan Pancreatic Society concluded that this subtype of SCA is difficult to distinguish from other pancreatic solid tumors using clinical images.1 Tissues obtained by EUS-FNA is also essentially non-diagnostic for SCA.16 However, hints for its accurate diagnosis may be hidden in the various image findings that may reflect its unique histological appearances.
MRI findings of SSCA reported by Gabata et al.7 and Yamamoto et al.15 pointed to a marked, high-intensity lesion on the T2-weighted image (higher than hemangioma and almost equal to cyst on MRCP), which was strongly enhanced in the early phase of dynamic MRI. Notably, MRI images of NET show a low-intensity signal on the T1-weighted image and high intensity on the T2-weighted image, although the latter is not as high as that of a cyst. These findings are also useful for differential diagnosis.
The available literatures report 10 cases of SSCA with written information of preoperative diagnosis, among which eight cases (including our patient) were diagnosed preoperatively as pancreatic NET2,3,10,11,13–15 and only two cases were diagnosed correctly7,9 (Table 1). NET is the most common solid hypervascular tumor of the pancreas and dynamic images of this tumor typically show a marked enhancement during the arterial and portal phases.6 However, another characteristic of NET, namely central necrosis, occurs when the
EUS-FNA does not provide adequate samples for diagnosing cases of SCA16 and SSCA,14 but it remains a powerful and highly sensitive tool for the diagnosis of solid pancreatic masses (accuracy >90% in tumor ≥2 cm).18 This is also true for pancreatic NET.19 SCA is a slow-growing tumor, mostly without malignant transformation, therefore, if NET or other malignant tissues is negative by FNA, a careful follow-up can be chosen in cases where the image findings are suggestive of SSCA.
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
M M F
50 60 59
58 66 62 74 59 72 74 57 58 56 58
Yamaguchi3 (2005) Reese et al.11 (2006) Stern et al.13 (2007) Sanaka et al.14 (2007) Casadei et al.9 (2008) Yasuda et al.10 (2009) Hayashi et al.5 (2012) Hayashi et al.5 (2012) Hayashi et al.5 (2012) Lee et al.12 (2013) Current case (2013) Pb Ph Ph Pb Pb Pt Ph Pb Ph Pb Pt Pb
Ph Ph Pb
Pt
2 4 4.2 1.6 4 1.7 4.2 2.1 3.2 2.5 2.8
2.5 2 2.0
4.0
Size Location (cm) –
MRI (T1/T2)
– Low/high Low/high and central low -/Well enhanced/– -/Well enhanced/– -/-/Enhanced heterogeneously – -/Enhanced/– Well-defined/well enhanced/– Low/well enhanced/prolonged -/high Low/well enhanced/low† – Low/well enhanced/low† – Low/well enhanced/low† – -/Enhanced/enhanced – Low/well enhanced/enhanced† Low/high
– Low/enhanced uniformly/Low/enhanced homogeneously/low†
–
CT (U/E/D)
–
NET
NET NET NET, others‡ NET SSCA NET – – –
NET SSCA
NET
Clinical diagnosis
FS, FS, FS, FS, FC FC FC FC
FC CS
– –
– FC FC FC FC
–
–
Pathology
†A tumor with central low-density area shown on the figure of the reports. ‡Others include pancreatic cancer, solid pseudopapillary tumor, metastatic carcinoma. CS, central scar; CT (U/E/D), computed tomography (unenhanced/early phase/delayed phase); F, female; FC, fibrous capsule; FS, fibrous septa within the tumor; M, male; MRI, magnetic resonance imaging; NET, neuroendocrine tumor; Pb, pancreas body; Ph, pancreas head; Pt, pancreas tail; SSCA, solid-type serous cystadenoma.
None None Abdominal pain None Abdominal pain None – – – None None
– Epigastric distention Abdominal pain
Abdominal pain
Symptoms
Y Kishida et al.
F M M M F F F F F M M
F
70
Age (years) Gender
Literature review of the clinicopathological findings of patients with solid-type serous cystadenomas
Perez-Ordonez et al.2 (1996) Kosmahl et al.4 (2004) Yamamoto et al.15 (2004) Gabata et al.7 (2005)
Study
Table 1.
214
Journal of Digestive Diseases 2014; 15; 211–215
© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 211–215 SSCA typically shows very rich vascularity (especially at the marginal side of the tumor), a faster contrast washout on CT and a signal of very high intensity on T2-weighted MRI or MRCP. In contrast, NET shows slower contrast washout on CT than SSCA and relatively high intensity on T2-weighted MRI or MRCP, but not as high as SSCA. A moisture-rich area of SSCA is shown on CT as a hypovascular area even if the tumor is small, but in NET such areas can be seen when the tumor is large. REFERENCES 1 Kimura W, Moriya T, Hirai I et al. Multicenter study of serous cystic neoplasm of the Japan pancreas society. Pancreas 2012; 41: 380–7. 2 Perez-Ordonez B, Naseem A, Lieberman PH, Klimstra DS. Solid serous adenoma of the pancreas. The solid variant of serous cystadenoma? Am J Surg Pathol 1996; 20: 1401–5. 3 Yamaguchi M. Solid serous adenoma of the pancreas: a solid variant of serous cystadenoma or a separate disease entity? J Gastroenterol 2006; 41: 178–9. 4 Kosmahl M, Wagner J, Peters K, Sipos B, Klöppel G. Serous cystic neoplasms of the pancreas: an immunohistochemical analysis revealing alpha-inhibin, neuron-specific enolase, and MUC6 as new markers. Am J Surg Pathol 2004; 28: 339–46. 5 Hayashi K, Fujimitsu R, Ida M et al. CT differentiation of solid serous cystadenoma vs endocrine tumor of the pancreas. Eur J Radiol 2012; 81: e203–8. 6 Rha SE, Jung SE, Lee KH, Ku YM, Byun JY, Lee JM. CT and MR imaging findings of endocrine tumor of the pancreas according to WHO classification. Eur J Radiol 2007; 62: 371–7. 7 Gabata T, Terayama N, Yamashiro M et al. Solid serous cystadenoma of the pancreas: MR imaging with pathologic correlation. Abdom Imaging 2005; 30: 605–9.
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© 2014 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
