Cystic tumours of the pancreas

Eur. Radiol. 6, 844-850 (1996) © Springer-Verlag 1996 European Radiology Pictorial essay Cystic tumours of the pancreas Y. Itai 1, K. Ohtomo 2 1 Department of Radiology, Institute of Clinical Medicine, University of Tsukuba, 1-1-1 Tennodai, Tsukuba 305, Japan 2 University of Tokyo Hospital, Tokyo, Japan Received 15 January 1996; Accepted 10 February 1996 Introduction With the advent of non-invasive imaging modalities, cys- tic masses of the pancreas are not infrequently encoun- tered in daily clinical practice. Cystic tumours are not so common among cystic masses of the pancreas. How- ever, many of them are overtly or latently malignant and can still be surgically removed before extrapancre- atic invasion or penetration occurs. Typical cystic neo- plasms of the pancreas are correctly diagnosed by imag- ing modalities. However, they have such a wide spec- trum of appearances that one-third of resected cystic tu- mours are preoperatively diagnosed as pseudocysts, and serous cystadenomas (benign) are often mistaken for mucinous cystic neoplasms (malignant) [1]. On the other hand, some pseudocysts mimic cystic tumours of the pancreas. Classically, cystic tumours of the pancreas consist of serous cystadenoma and mucinous cystic neoplasm. Any pancreatic tumours liable to necrotic change look like cystic tumour of the pancreas and are included in the entity of cystic tumour in the broad sense. Moreover, it has been clarified that excessive mucin in the pancreatic duct (either main, branch or both) re- sults in the formation of a cystic pancreatic lesion (ac- tually dilatation of the main and/or branch duct) and is produced by adenocarcinoma, adenoma or even hy- perplasia histopathologically [2]. From the viewpoint of mucin production related to histopathology Nak- azawa et al. [3] have advocated the new concept of mu- cin-producing cystic tumour of the pancreas. This con- sists of three subtypes [3]: peripheral type (synonyms classical mucinous cystic neoplasm or mucinous cystad- enoma and cystadenocarcinoma), branch duct type (synonyms °ductectatic' mucinous cystadenoma and cystadenocarcinoma) and main duct type (synonyms mucin-producing tumour or mucin-hypersecreting tu- mour). In this pictorial essay we present the typical appear- ances of cystic pancreatic tumours, the wide spectrum of their features, and differential features among cystic pancreatic masses with an emphasis on CT. Serous cystadenoma Typical appearance Serous cystadenoma has the synonyms microcystic ade- noma and glycogen-rich adenoma [4]. Typical serous cystadenoma consists of innumerable tiny cysts from less than 1 mm to 20 mm in diameter, with a tendency for larger cysts to occur in the periphery (Fig. 1), and a central fibrous scar often associated with calcification loci (a dense scar is called a sunburst: Fig. 2). The num- ber of cysts within the tumour (more than six in micro- cystic adenoma and six or fewer in mucinous cystic neo- plasms) and the diameter of the majority of cysts within the tumour (_< 2 cm in serous cystadenomas and > 2 cm in mucinous cystic tumours) are the most helpful radiological findings in differentiating turnout types of classical cystic tumour of the pancreas [5]. The cysts are lined with a layer of cuboidal epithelium containing abundant glycogen. The subepithelial fibrous layer has a rich capillary network which shows hypervascularity and staining on angiography and dynamic CT/MRI. Thus, serous cystad- enoma appears as a hypoattenuating mass on non-con- trast-enhanced CT, shows marked enhancement or hypervascularity in the early phase of dynamic CT, and becomes a honeycomb or spongy mass on enhanced CT (Fig. 3 a-c). The central scar often shows delayed and prolonged enhancement (Fig. 3 d). On ultrasound, serous cystadenoma appears as an echogenic or hypo- echoic mass with posterior echoenhancement. Angio- graphy shows hypervascularity and prominent staining with many, various-sized translucencies. Correspondence to: Y. Itai Y. Itai and K. Ohtomo: Cystic tumours of the pancreas 845 Fig.la, b. Serous cystadenoma, a T2-weighted image (2000/90); b proton-density image (2000/22). A huge, well-defined mass con- sists of many cysts (a), whose contents are different in some cysts due to bleeding (also hyperintense on the Tl-weighted image) Fig. 2. Serous cystadenoma. Plain CT reveals a multilobulated cys- tic mass with central dense calcified foci (sunburst) Fig.3a-d. Typical serous cystadenoma, a Plain CT; b arterial phase; c venous phase; d late phase. A hypodense mass is noted adjacent to the stomach on plain CT (a) that has enlarged arteries within the turnout at the arterial-dominant phase of dynamic CT (b: right lateral decubitus). At the venous phase the mass reveals a honeycomb appearance (e) and shows marked central, delayed and prolonged enhancement (d: supine position) Spectrum or features Serous cystadenoma can have a range of appearance from a unilocular cyst to quite a solid tumour at the cut surface of the gross specimen. Appearance of this tu- mour can be defined in terms of the size and number of cysts and the proportion of solid material [1]. Oligolocu- lar cysts are not infrequently encountered at imaging of serous cystadenoma (Fig. 4). However, there are many tiny cysts in some parts of the tumour which may in future be demonstrated with a high-frequency endoscopic ultrasound probe or MRI using a surface coil. Such oligolocular serous cystadeno- mas have a small proportion of solid material, and an- giography may fail to demonstrate any staining [6]. The other differential feature from mucinous cystic neo- plasm is the shape of the tumour contour: multilobulat- ed in serous cystadenoma (Fig. 4) and roundish in muci- nous cystic neoplasm. Marked enhancement in a small area of the periphery of a tumour, if present, favours the diagnosis of serous cystadenoma. In an extreme case, serous cystadenoma can histopathologically be a unilocular cyst [6]. In contrast, serous cystadenoma can appear as a so- lid, hypervascular tumour such as an islet cell tumour at both imaging and the gross specimen when the cysts are extremely small and the relative proportion of solid material increases [1]. A time-density curve may be of use, since serous cystadenoma is expected to show more prolonged enhancement due to large interstitial spaces in the fibrous tissue. Mucinous cystic neoplasm Mucinous cystadenoma and cystadenocarcinoma Mucinous cystadenoma and cystadenocarcinoma (muci- nous cystic neoplasm in the narrow sense) are unilocular or mutilocular cystic tumours with a smooth external surface (Fig.5). The cyst wall is thick (0.1-2 cm) and has mural projections and/or long septa internally. The internal septations are well-defined in contour and usu- ally curved, but sometimes straight (Fig. 6). Small calci- fication foci are occasionally noted in the cyst wall and septa. Some tumours have daughter cysts along the cyst wall. Overt malignant tumors have a relatively large so- lid component. The cyst walls are lined with mucin-producing colum- nar epithelium, but lack a rich capillary network. The cysts have varying content: mucin, haemorrhage and/or necrotic debris. These macroscopic findings are well 846 Y. Itai and K. Ohtomo: Cystic tumours of the pancreas Fig.4. Oligolocular serous cystadenoma. Enhanced CT depicts a multilobulated cystic mass with thin septa and a central dense area (calcification). Same case as Fig. 1. Note the small enhanced area. Fig.ga, b. Mucinous cystadenocarcinoma. A multilocular, round cystic mass has a thick wall with a slightly irregular inner surface. Mural projection and a daughter cyst are also noted (a). The den- sity of the small cyst is a little lower than that of the main locule (b) Fig.6a-d. Mucinous cystadenoma, a Enhanced CT; b ultrasound; c Tl-weighted image (400/20); d T2-weighted image (2000/80). An ovoid cystic mass has a thin wall and is associated with an internal septum most clearly demonstrated by ultrasound. Note the inter- mediate intensity of the cystic contents on the Tl-weighted image, which reflects the protein-rich content and/or mild old haemor- rhage (c) Fig.7a-c. 'Ductectatic~ mucinous cystic tumour, a Ultrasound; b enhanced CT; c endoscopic retrograde pancreatography (ERP). A multibolulated cystic mass is noted in the head of the pancreas (a, b) ERP reveals that the cystic mass consists of localized, promi- nent dilatations of the branch duct of the pancreatic head Y. Itai and K. Ohtomo: Cystic tumours of the pancreas 847 demonst ra ted at CT and MRI . In contrast to serous cys- tadenoma, the appearances before and after enhance- ment are essent ia l ly the same, and the densit ies/ intensi- ties of the cystic contents often vary in di f ferent locules [7, 8]. Muc inous cystic neop lasm is overt ly or latent ly mal ignant, and should be resected if surgery is possible. Fig. 8. 'Ductectatic" muci- nous cystic turnout. MR pan- creatography, depicts well the macroscopical characteriza- tion of this tumour (arrow) 'Ductectatic' mucinous cystadenoma and cystadenocarcinoma This ent i ty is character ized by local ized d i latat ion of a side branch of the main pancreat ic duct which is widely covered with ep i the l ium indist inguishable f rom that of mucinous cystic neop lasm [9] (Fig. 7). Endoscop ic retro- grade pancreatography (ERP) c lear ly demonst ra tes character ist ic findings: local ized prominent cystic di lata- t ion of a branch duct with a grape- l ike cluster or pear- Fig.9. 'Ductectatic' mucinous cystic tumour. Enhanced CTreveals a unilocular cystic mass with mural projection and an associated small cyst in the head of the pancreas as well as dilatation of the main pancreatic duct in the body and tail. ERP (not shown) dem- onstrated grape-like dilatation of the branch duct of the pancreatic head. Thin septa were equivocally demonstrated at enhanced CT Fig.lOa, b. Mucin-hypersecreting cancer. Enhanced CT shows a cystic mass associated with a large polypoid tumor in the head of the pancreas a. This area is actually a markedly dilated main pan- creatic duct, which has been induced by hypersecretion of mucin from the polypoid tumour located within the main pancreatic duct b. Note a similar lesion just anterior to the main lesion (arrow), which is a dilated branch duct also associated with a tumor therein (,) F ig. l la-c. Mucin-producing turnout, a MR pancreatography; b enhanced CT; c combined percutaneous cholangio-pancreatog- raphy. Localized marked dilatation of the main pancreatic duct is noted in the head (arrows) at MR cholangiopancreatography. Ar- rowheads point to a slightly dilated main pancreatic duct in the body and tail (a). Enhanced CT shows several round cystic areas which correspond to a dilated main pancreatic duct associated with mural tumour (arrow), a dilated common bile duct (arrow- head) and a dilated branch duct of the pancreas (b). Mucin is dem- onstrated by contrast pancreatography alone (e: courtesy of the Department of Surgery, University of Tsukuba) 848 "L Itai and K. Ohtomo: Cystic tumours of the pancreas 12a 12b Fig. 12 a, b. Classical mucinous cystic tumour associated with dilata- tion of the main pancreatic duct. Enhanced CT reveals cystic tu- mour in the tail a and moderate dilatation of the main pancreatic duct downstream of the tumour b. Fig.13a, b. 'Ductectatic' mucinous cystic tumour associated with dilatation of part of the main pancreatic duct. A lobulated unilocu- lar cyst is demonstrated in conjunction with dilatation of the main pancreatic duct in the body a. The cystic mass at the cephalad site has several thin internal septations b shaped pools of contrast agent associated with filling de- fects of various sizes due to the presence of mucin. The cystic lesions are usually located in the uncinated process but are also found in other parts of the head, body or even the tail of the pancreas. The lesions are mostly less than 3 cm in diameter, and lack definite mu- ral nodules or thick septa. Thus, 'ductectatic' mucinous cystic neoplasms appear as round or multilobulated cysts with thin walls and/or thin septa at CT and ultra- sound. MR pancreatography can clearly demonstrate the characteristic findings of multilobulated cyst and communication with the dilated main pancreatic duct [10] (Fig. 8). Most cases have been reported from Japan. However, small but increasing number of cases have re- cently been reported from Europe and the United States under the name of 'mucinous ductal ectasia' [11, 12]. Without knowledge of this entity, its cystic lesions are easily mistaken for pseudocysts or true cysts (Fig. 9). It is difficult to determine how to treat this entity since: (1) it occurs mostly in the old (male preponderance over female), (2) the tumour is slow growing, (3) the le- sion is indistinguishable from that produced by hyperpla- sia, (4) biopsy or cytology is of little value for establishing whether the lesion is malignant, benign or hyperplastic [13]. Surgical resection is positively recommended when: (1) the cystic lesion is over 3 cm in diameter, (2) the main pancreatic duct is 10 mm or more in width, (3) any solid component or thick septa are identified [14]. Mucin-producing tumour Mucin-producing tumor (synonym mucin-hypersecre- tion tumour) is characterized by: (1) diffuse dilatation of the main duct, (2) association with filling defects on ERP and (3) excretion of mucin through the patulous orifice of the enlarged papilla of Vater at endoscopy [2]. Excessive mucin is produced by adenocarcinomas and adenomas located in the main pancreatic duct and/ or large branch duct that are polypoid or sessile tumours with spread along the ductal surface (Fig. 10). Hyperpla- sia can also cause a similar appearance, as is the case with mucocoele of the appendix. Filling defects on ERP consist of well-defined tu- mour and amorphous mucin. Thin-slice CT using a large amount of contrast agent can depict the tumour as a polypoid or cystic mass with excrescent nodules and/or septa within the dilated pancreatic duct [15] (Figs. 10, 11]. Mucin can be detected by ultrasound but hardly at all by CT and MRI. Impacted mucin at the papilla of Vater or a large branch results in dilatation of the pancreatic duct and can also cause pancreatitis clinically. The prognosis of mucin-producing cancer is gener- ally good, until invasion of the pancreatic duct or pene- tration into other organs (duodenum or common bile duct) occurs. Combined type and new classification There have been sporadic case reports of mucinous cys- tadenoma and cystadenocarcinoma associated with a diffusely dilated main pancreatic duct (Fig. 12), or of ERP demonstrating communication with classical muci- nous cystic neoplasm [3]. Nakazawa et al. [3] reported that two-thirds of classi- cal mucinous cystic neoplasms had communication with a non-dilated or mildly dilated main pancreatic duct on ERP when injection of contrast agent was carefully per- Y. Itai and K. Ohtomo: Cystic tumours of the pancreas 849 Fig.14a, b. Solid and papillary epithelial neoplasm, a Enhanced CT; b Tl-weighted image (800/25). There is an oval-shaped cystic mass associated with an internal, ill-defined solid component and partly thickened wall (a). Most parts of the cystic content show a high intensity, while other parts have slight hypointensity (b) Fig.15a, b. Malignant islet cell tumour, a Plain CT; b enhanced CT. Contrast enhancement reveals ill-defined, thick septa and an irregularly thick wall in a round cystic mass. Note the metastatic foci in the liver Fig.16. Cystic islet cell turnout mimicking a simple cyst. A round cyst is noted in the head of the pancreas. Although the surgical specimen was diagnosed as a cystic islet cell tumour, there was not sufficient solid component to identify with imaging. The density of the cystic content is not elevated (+10 HU) Fig.17a, b. Pseudocyst mimicking a cystic neoplasm, a Plain CT; b enhanced CT. A triangular mixed tumour (a) is revealed as a multilocular cyst with straight, internal septation after contrast en- hancement (b) Fig. 18. Mucinous cystadenoma mimicking a simple cyst. There is an elliptical cyst looking like an ordinary pseudocyst (same case as Fig. 6) fo rmed under excessive pressure [3], as was the case with a pancreat icogram in a surgical specimen. On the basis of morphological (macroscopic and histopatholog- ical) and functional analogies, these authors advocated the new entity of 'mucin-producing cystic tumour ' of the pancreas, to include classical mucinous cystic neo- p lasm (per ipheral type of the new entity), 'ductectat ic ' mucinous cystic neop lasm (branch duct type) and mu- cin-hypersecret ing tumour (main duct type). The major differences between classical mucinous cystic neoplasm and mucin-producing tumour are in the sexual p reponderance ( female preponderance in the former vs male in the latter), location (tail vs head) and degrees of mucin secretion and ductal di latation (mild vs prominent) . (Fig. 13) as well as in the symptoms (abdominal mass vs abdominal pain). Necrotic tumour Some solid tumours have a tendency to induce massive necrosis and mimic cystic tumour of the pancreas. The most famous ones are solid and papi l lary epithelial neo- p lasm (synonym solid and cystic tumor; Fig. 14) and cys- tic islet cell tumor (Figs. 15, 16). Both tumours are shar- 850 ply defined, round masses consisting of both cystic and solid portions, a l though the ratio of cystic to solid com- ponents varies [16]. Solid and cystic tumours are pre- dominant ly found in young females and have a higher density/intensity cystic content, since the cystic port ions are produced by repeated haemorrhagic necrosis [16, 17]. Well-defined internal septations are not seen but calcification is occasionally noted in the wall or solid components in both tumours. On CT the solid compo- nent of islet cell tumour shows marked contrast en- hancement in the arter ial -dominant phase while solid and cystic tumour demonstrates only mild enhance- ment. Ductal adenocarc inoma, anaplastic carcinoma and lymphoma may infrequently mimic cystic tumour of the pancreas due to massive necrosis. Cyst versus cystic tumour Pseudocysts are the most common cystic lesion in the pancreas and can be induced by pancreatitis, t rauma or surgery. Pseudocysts appear as a round cystic mass with a definite wall. However , they can mimic cystic tu- mours associated with internal septation and/or ne- crotic mass of various shapes (Fig. 17). Conversely, cys- tic tumours can appear as a simple cyst lacking any thickening of wall, septation or mural nodule (Fig. 18). Pancreat ic carc inoma not infrequently induces second- ary cysts upstream of the obstructed pancreatic duct [18]. The cysts are pseudocysts or retention cysts in na- ture. When cysts are formed in the pancreatic paren- chyma or adjacent to pancreatic carc inoma they may mimic cystic tumour. References 1. Itai Y, Ohhashi K, Furui S, Araki T, Murakami Y, Ohtomo K, Atomi Y (1988) Microcystic adenoma of the pancreas: spec- trum of computed tomographic findings. J Comput Assist Tomogr 12:797 2. Itai Y, Kokubo T, Atomi Y, Kuroda A, Haraguchi Y, Terano A (1987) Mucin-hypersecreting carcinom a of the pancreas. Radi- ology 165:51 3. Nakazawa S, Yamao K, Yamada M, Naito Y, Kimoto E, Inui K, Hayashi Y, Kano J, Mitake M, Kozuka S (1988) Study of the Y. Itai and K. Ohtomo: Cystic tumours of the pancreas classification of mucin-producing tumor of the pancreas [in Japanese with English abstract]. Jpn J Gastroenterol 85:924 4. Compagno J, Oertel JE (1978) Microcystic adenomas of the pancreas (glycogen rich cystadenomas): a clinicopathologic study of 34 cases. Am J Cliu Patho169:289 5. Johnson CD, Stephans DH, Charboneau JW, Carpenter HA, Welch TJ (1988) Cystic pancreatic tumors: CT and sonographic assessment. AJR 151:1133 6. Warshaw AI, Compton CC, Lewandrowski K, Cardenosa G, Mueller P (1990) Cystic tumors of the pancreas: new clinical, radiologic, and pathologic observations in 67 patients. Ann Surg 212:432 7. Itai Y, Moss AA, Ohtomo K (1982) Computed tomography of cystadenoma and cystadenocarcinoma of the pancreas. Radiol- ogy 145:419 8. Minami M, Itai Y, Ohtomo K, et al (1989) Cystic neoplasms of the pancreas: comparison of MR imaging with CT. Radiology 171:53 9. Itai Y, Ohhashi K, Nagai H, Murakami Y, Kokubo T, Makita K, Ohtomo K (1986) 'Ductectatic' mucinous cystadenoma and cystadenocarcinoma of the pancreas. Radiology 161:697 10. Takehara Y. Personal communication 11. Agostini S, Choux R, Payan MJ, Sastre B, Sahel J, Clement JP (1989) Mucinous pancreatic duct ectasia in the body of the pan- creas. Radiology 170:815 12. Tian F, Myles J, Howard JM (1992) Mucinous pancreatic ductal ectasia of latent malignancy: an emerging clinicopathologic en- tity. Surgery 111:109 13. Tanaka A, Ito K, Matsui T, Ito Y, Ohnishi H, Hayakawa T (1995) Clinicopathological evaluation of pancreatic mucin-pro- ducing tumors of the branch type [in Japanese with English ab- stract]. J Jpn Pancreas Soc 10:368 14. Obara T, Maguchi H, Saitoh Y, Arisato S, Itoh A, Nishono N, Yamano M, Taruishi M, Suzuki H, Watari J, Ura H, Namiki M (1994) Mucin-producing tumor of the pancreas: surgery or fol- low-up? [in Japanese with English abstract]. Jpn J Gastroen- terol 91:66 15. Itoh S, Ishiguchi T, Ishigaki T, Sakuma S, Maruyama K, Senda K (1992) Mucin-producing pancreatic tumor: CT findings and histopathologic correlation. Radiology 183:81 16. Choi Bi, Kim KW, Han MC, Kim YI, Kim CW (1988) Solid and papillary epithelial neoplasms of the pancreas: CT findings. Ra- diology 166:413 17. Ohtomo K, Furui S, Onoue M, Okada Y, Kusano S, Shiga J, Suda K (1992) Solid and papillary epithelial neoplasm of the pancreas: MR imaging and pathologic correlation: Radiology 184:567 18. Itai Y, Moss AA, HI Goldberg (1982) Pancreatic cysts caused by carcinoma of the pancreas: a pitfall in the diagnosis of pan- creatic carcinoma. J Comput Assist Tomogr 6:772 Obermann W.R.: Radiology of Carpal Instability. A Practical Ap- proach. Amsterdam, New York: Elsevier Science, 1994, 200 pages, $ 211.75,-, ISBN 0444820809 This unique book deals with a very delicate area of the orthopedic sector, the carpal joint and its instability. The author, an expert in musculoskeletal radiology, has succeeded in providing a full ana- tomical understanding and an overview on the physiology and pathophysiology of the carpal joints. Well illustrated and with con- vincing drawings, the major imaging modalities for radiological evaluation of the carpal joint are provided. Clinical chapters in- clude all essential evaluation studies with a special focus on US, CT, arthrography, and MRI. An excellent referencing helps the reader to get more detailed information, if desired. The author di- rects his book primarily to radiologists. In my opinion, however, it should also be of great interest to orthopedic surgeons and rheu- matologists involved in the diagnosis and treatment of joint dis- eases, as well as many other readers who want to learn more on the carpal joint and its pathology. T.J. Vogl, Berlin