CT imaging review of uncommon peritoneal-based neoplasms: beyond carcinomatosis

Pathologic involvement of the peritoneum can result from a wide variety of conditions, including both neoplastic and non-neoplastic entities. Neoplastic involvement of the peritoneal ligaments, mesenteries, and spaces from malignant spread of epithelial cancers, termed peritoneal carcinomatosis, is frequently encountered at CT evaluation. However, a host of other more unusual benign and malignant neoplasms can manifest with peritoneal disease, including both primary and secondary peritoneal processes, many of which can closely mimic peritoneal carcinomatosis at CT. In this review, we discuss a wide array of unusual peritoneal-based neoplasms that can resemble the more common peritoneal carcinomatosis. Beyond reviewing the salient features for each of these entities, particular emphasis is placed on any specific clinical and CT imaging clues that may allow the interpreting radiologist to appropriately narrow the differential diagnosis and, in some cases, make an imaging-specific diagnosis.

The peritoneum consists of a continuous serous membrane that lines the abdominal cavity (parietal portion), as well as the intraperitoneal organs, ligaments, and mesenteries (visceral portion). These parietal and visceral linings contain the peritoneal cavity, a potential space where pathologic conditions can collect. Deep to the mesothelial lining of the peritoneum, the subperitoneal space consists of a thin layer of connective tissue containing fat, vessels, lymphatics, and nerves. The subperitoneal space can give rise to many pathological entities, allows for spread of pathologic processes, and is a key concept for CT interpretation.1,2 Although other imaging modalities such as US, MR, and PET can provide complementary assessment, CT remains the workhorse for imaging peritoneal disease. CT provides a comprehensive evaluation for detection and characterization of peritoneal pathology, which can manifest with varying degrees of soft tissue infiltration, mass-forming lesions, calcification, and fluid (air as well, but pneumoperitoneum is not germane to this review). To optimize peritoneal evaluation at CT for tumor detection, both oral and intravenous contrast are generally indicated. Although some interpretive pitfalls and logistical challenges may exist with positive oral contrast material,3 we feel that it will generally improve overall peritoneal evaluation at CT. Furthermore, multi planar evaluation, especially inclusion of coronal reformats, can facilitate detection of more subtle peritoneal-based tumors and implants. Peritoneal carcinomatosis from malignant spread of nearly any epithelial malignancy, but most often from gastrointestinal or gynecological primaries, is encountered daily at CT in most radiology practices. However, peritoneal involvement can also result from a wide variety of other neoplastic and non-neoplastic conditions,1,2 many of which can closely mimic peritoneal carcinomatosis at CT. In this review, we discuss a wide array of unusual peritoneal-based neoplasms that can appear similar to peritoneal carcinomatosis at CT. These include a variety of primary peritoneal tumors, as well as some unusual secondary processes (Table 1). Beyond reviewing the salient background features for each of these entities, particular emphasis is placed on any specific clinical and CT imaging clues that may allow the interpreting radiologist to appropriately narrow the differential diagnosis and, in some cases, make an imaging-specific diagnosis (Table 2). Primary peritoneal and subperitoneal neoplasms When faced with non-specific CT findings of presumed “peritoneal carcinomatosis”, a search for an organ-based primary is warranted. Gastrointestinal and gynecological primary malignancies are of course most common, but correlation for any extra-abdominal cancer is also indicated. In the absence of an organ-based epithelial cancer, primary peritoneal neoplastic processes should also be considered, in addition to a wide variety on non-neoplastic conditions beyond the scope of this review, but recently covered elsewhere.4 Both primary peritoneal serous carcinoma (PPSC) and malignant mesothelioma closely mimic peritoneal carcinomatosis at CT imaging. Some primary peritoneal mesenchymal tumors can also resemble carcinomatosis, especially those that give rise to peritoneal sarcomatosis. Primary peritoneal serous carcinoma PPSC, previously referred to as papillary serous carcinoma of the peritoneum, is an aggressive and typically high-grade malignancy that almost exclusively affects females.5 Although considered rare, as most cases were previously lumped into “ovarian cancer”, more recent investigations have shown that the majority of high-grade serous carcinomas actually arise from the fallopian tubes. The relative frequency of tumors with non-tubal peritoneal primary origin is difficult to ascertain,6 but cases of PPSC have been reported after prophylactic bilateral salpingo-oophorectomy in females carrying BRCA1 and BRCA2 mutations.7 PPSC presumably arises from Mullerian-derived subperitoneal cell implants in females. As with most primary peritoneal tumors, the initial clinical presentation usually consists of non-specific abdominal distention and discomfort. Multimodality treatment typically combines debulking cytoreductive surgery (CRS) with combination chemotherapy, which may include hyperthermic intraperitoneal chemotherapy (HIPEC). At CT, calcified peritoneal-based soft tissue masses, especially involving the omentum, are highly suggestive of high-grade serous carcinoma in a post-menopausal female (Figure 1). The possibility of PPSC over the more common tubal origin “ovarian cancer” can be raised when adnexal or pelvic involvement is lacking or minimal. The presence of extensive tumoral calcification can be mistaken for positive oral contrast material. However, soft-copy cine review of the images, in addition to a wider CT window (Figure 1), should allow one to identify these dense extraluminal tumor deposits. In the absence of a calcific component, PPSC is generally indistinguishable from peritoneal carcinomatosis from organ-based primaries (Figure 1). Malignant mesothelioma Peritoneal mesothelioma is an uncommon but aggressive malignancy, with increasing worldwide incidence.8 Clinical presentation is non-specific and typically includes abdominal distension and pain. Although pleural-based mesothelioma still accounts for the majority of cases, primary peritoneal origin represents 10–30% of all cases. The link between asbestos exposure and peritoneal mesothelioma is present but less strong than with pleural mesothelioma, with up to 40% of cases arising spontaneously without history of prior asbestos exposure, especially in female patients.8 However, in one CT-based series of 33 cases, nearly one-quarter of patients with peritoneal mesothelioma also had pleural abnormalities.9 As with high-grade serous carcinoma, multimodality therapy combines debulking and combination chemotherapy. Inclusion of HIPEC is emerging as a new standard of care.8 The CT appearance of malignant peritoneal mesothelioma is somewhat variable and non-specific, closely resembling either carcinomatosis or peritoneal tuberculosis (TB). When more diffusely infiltrative and less bulky, the CT findings of peritoneal mesothelioma mimic either the “wet” or “dry” appearances of peritoneal TB, depending upon the amount of associated peritoneal fluid (Figure 2). In other cases, more bulky peritoneal based soft-tissue deposits can result in gross scalloping of solid abdominal organs (Figure 2). However, even without a bulky soft tissue component, fluorodeoxyglucose (FDG)-avidity at positron emission tomography (PET) can be striking (Figure 2). As with other peritoneal-based malignancies, early spread can be subtle at CT and may underestimate the extent of disease at laparoscopy (Figure 2). Unlike pleural mesothelioma, where associated calcified plaques are common, calcification in peritoneal mesothelioma is rare and should prompt consideration for other entities. Benign cystic mesothelioma Benign cystic mesothelioma is a rare primary peritoneal neoplasm occurring predominantly but not exclusively in females of reproductive age.10 As the name implies, this benign tumor derives from the peritoneal mesothelium. Tumor growth is characterized by multiple grapelike clusters of mesothelial-lined cysts separated by varying amounts of fibrous stroma. Most patients are managed by surgical resection with curative intent, but a relatively high incidence of cyst recurrence has been reported, despite the benign nature of this neoplasm. Adjuvant hormonal therapy to control cyst size and relieve local symptoms appears to have only marginal benefit. Incidence of benign cystic mesothelioma in males may be increasing (Figure 3), but the rarity of this disease precludes firm conclusions. The CT appearance of variable-sized clusters of thin-walled peritoneal-based cysts is characteristic (Figure 3). Involvement of the pelvic peritoneal cavity is most typical; significant mass effect is often lacking. In some cases, the thin cyst walls may be difficult to discern at CT, and the process will appear more as loculated peritoneal fluid (Figure 3). These internal septations, however, are typically well seen at ultrasound and MR imaging (Figure 3). The main differential diagnostic consideration for this multicystic appearance is mesenteric lymphangioma (discussed below). The lack of mass effect, calcifications, and variable attenuation would argue against pseudomyxoma peritonei (also discussed below). The lack of liver involvement and cyst wall calcification would argue against secondary peritoneal echinococcosis.4 Desmoplastic small round cell tumor Desmoplastic small round cell tumor (DSRCT) is an aggressive malignancy associated with a poor prognosis that typically affects adolescent and young adult males. The peritoneum is clearly the most common site of origin, but DSRCT may also arise in pleural, paratesticular, retroperitoneal, and other locations. One of the “small blue round cell tumors”, DSRCT was originally believed to derive from the mesothelium, based on these typical sites of involvement. Although it is now classified as a soft tissue sarcoma, we have chosen to consider it separately given its somewhat unique features and peritoneal profile. At CT, the most typical appearance of DSRCT is multiple rounded peritoneal-based soft-tissue masses without an apparent organ of origin in a young male patient (Figure 4).11 These tumors are typically avid at FDG-PET imaging (Figure 4). An infiltrative pattern of peritoneal soft tissue involvement is less frequently observed. Generically, the imaging-based diagnosis is broad, including a wide variety of neoplastic and non-neoplastic conditions. In terms of a histopathological differential diagnosis, other small cell abdominal malignancies seen in young patients include rhabdomyosarcoma, non-Hodgkin lymphoma, Ewing sarcoma, primitive neuroectodermal tumor, Wilms tumor, and neuroblastoma.11 Primary peritoneal mesenchymal tumors The subperitoneal space consists of a variety of tissue types (e.g. fat, vessels, lymphatics, nerves, and fibrous stroma) that may give rise to primary mesenchymal neoplasms. These soft tissue tumors of mesenchymal origin can be categorized as benign, intermediate (locally aggressive or rarely metastasizing), and malignant (sarcomas). The wide breadth of mesenchymal tumors in this category precludes detailed discussion of each within this review. Rather, the salient clinical and CT features of certain select mesenchymal tumors will be briefly considered herein. Cystic lymphangiomas are benign lymphatic malformations that arise in the subperitoneal space.12 The most typical CT appearance is that of a multilocular low attenuation cystic peritoneal lesion, with thin walls and septations (Figure 5). Lymphangiomas usually lack significant mass effect upon abdominal organs but often appear infiltrative and can be mistaken for a more aggressive process. The main differential diagnostic consideration is benign cystic mesothelioma, but some cases may mimic mucinous processes such as early pseudomyxoma peritonei. Mesenteric lipomas are somewhat less common compared with other abdominal locations such as the body wall and retroperitoneum. As with other lipomas, a well-defined, homogeneous fat attenuation lesion with little or no soft tissue component can generally be left alone. However, some benign mesenteric lipomas may undergo resection if complicated by more than a minimal soft tissue component, which excludes the possibility of a well-differentiated lipoma (Figure 5). Liposarcoma is discussed below in the malignant mesenchymal section. Although previously considered by some to be a non-neoplastic entity, desmoid tumor (fibromatosis) is now generally best categorized as a benign neoplastic process. Aggressive fibromatosis is characterized by a rapid proliferation of well-differentiated fibroblasts, local infiltration, and a tendency to recur after surgical resection. Cases may be sporadic or related to familial adenomatous polyposis syndrome (FAPS, Gardner syndrome). At CT, mesenteric desmoid tumors can have either a well-defined or infiltrative appearance (Figure 5). More recently, the need for upfront surgical resection in all cases has been questioned as front-line therapy, as some sporadic cases may be safely observed.13 As such, management of desmoid tumors should likely undergo multidisciplinary expert review by an experienced team. Gastrointestinal stromal tumor (GIST) is a relatively common mesenchymal tumor that most often arises from the muscularis propria layer of the GI tract, specifically from the interstitial cells of Cajal. However, approximately 10% of GISTs have an extraintestinal abdominal site of origin, most frequently arising from the peritoneum.14 These extraintestinal tumors tend to be more aggressive, have a worse prognosis, and less often have the characteristic KIT mutation relative to conventional GISTs. However, given the typical exoenteric growth pattern of conventional GISTs, distinguishing primary GI vs peritoneal origin at CT is difficult, as large peritoneal tumors will contact bowel. Distinguishing benign from malignant GISTs at CT is also difficult but, in the absence of metastatic disease, lesion size is the most important imaging feature (Figure 6). Patients with neurofibromatosis type-1 (NF-1) are at high risk for GISTs, which are often multifocal and challenging to determine peritoneal origin vs metastatic (Figure 6). Associated CT findings of NF-1 increase the likelihood that a suspicious intra-abdominal tumor or tumors represents GIST (Figure 6). Other predominately benign peritoneal-based mesenchymal tumors include hemangioma, nerve sheath tumors, leiomyoma, inflammatory myofibroblastic tumor, solitary fibrous tumor (previously called “hemangiopericytoma”), and perivascular epithelioid cell tumor (PEComa) (Figure 5). At the other end of the spectrum, a wide variety of primary sarcomas account for the malignant mesenchymal tumors, not to be confused with peritoneal sarcomatosis from metastatic spread. Peritoneal liposarcoma is considerably less common than retroperitoneal primaries, but the same imaging concepts apply.15 The presence of demonstrable fat within a complex, expanding peritoneal-based mass should suggest the diagnosis. Well-differentiated tumors are most frequent and typically low-grade, composed of predominately fat attenuation at CT (Figure 7). Myxoid and pleomorphic variants are typically of progressively higher grades, respectively, and correspond to increased tumor heterogeneity with non-fatty components at CT (Figure 7). Dedifferentiated tumors reflect high-grade changes that also correspond to increasing tumor heterogeneity, as well as worse prognosis (Figure 7). Beyond liposarcoma, the other peritoneal sarcomas have a less specific CT appearance, but tend to be bulky and heterogeneous (Figure 7). Lymphadenopathy is uncommon and should suggest a different etiology.16 Specific entities include leiomyosarcoma, angiosarcoma, fibrosarcoma, and undifferentiated pleomorphic sarcoma, which was previously known as malignant fibrous histiocytoma (Figure 7). Some sarcomas, such as angiosarcoma, are prone to bleeding with findings of hemoperitoneum on CT (Figure 7). Unusual “secondary” neoplastic peritoneal conditions Beyond typical metastatic peritoneal carcinomatosis (or sarcomatosis), a number of more unusual secondary peritoneal conditions exist. Categorization of some of these entities in terms of primary vs secondary involvement is challenging, such as with lymphoproliferative processes and leiomyomatosis. For most of the conditions discussed, there are either clinical or imaging clues that can suggest the diagnosis. Pseudomyxoma peritonei Mucinous appendiceal neoplasms, which tend to form mucoceles, may give rise to a unique pattern of peritoneal spread referred to as pseudomyxoma peritonei. In general, peritoneal carcinomatosis from other GI or ovarian mucinous cancers does not result in pseudomyxoma. With mucocele rupture, the risk of pseudomyxoma depends upon the cellularity of the peritoneal mucin.17 With low-grade tumors, the lack of viable cells (acellular mucin) confers a low risk for developing pseudomyxoma peritonei (<5%), whereas 40% of patients will progress when cellularity is detected within mucinous deposits.18 High-grade and signet ring mucinous appendiceal neoplasms are at higher risk for peritoneal disease, although the CT patterns differ, as discussed below. For most cases of pseudomyxoma peritonei, the clinical course is much less aggressive and more prolonged compared with peritoneal carcinomatosis from other colorectal cancers. Extensive surgical CRS and HIPEC may be required for cases with inexorable progression. At CT, the most characteristic appearance of pseudomyxoma peritonei is multiple loculated cystic peritoneal deposits of varying attenuation, often with mass effect and scalloping on adjacent abdominal organs (Figure 8). Septal calcifications are occasionally seen. In patients who initially present with widespread peritoneal disease, detection of the inciting appendiceal primary allows for a specific diagnosis (Figure 8). In patients with signet ring histology, consisting of intracellular mucin, a more infiltrative soft tissue pattern of peritoneal disease is typical. Leiomyomatosis Multifocal peritoneal-based leiomyomas can rarely occur in females as a primary process, which is referred to as leiomyomatosis peritonealis disseminata (LPD).19 The precise etiology of multiple subperitoneal smooth muscle tumors in these cases is unclear, but derivation from multipotential cells has been postulated. Others have suggested that detached subserosal uterine fibroids may develop a peritoneal-based blood supply and become “parasitic”. A hormonal stimulus to smooth muscle cell differentiation has also been suggested, and there may be a rare association with endometriosis. However, resection of uterine fibroids via History of treated is now a more common cause of peritoneal leiomyomatosis, and is why this entity is included herein as a secondary cause.20 This minimally invasive laparoscopic technique is associated with dissemination of cellular material throughout the peritoneum. The actual risk for peritoneal spread of “parasitic” leiomyomas, which effectively represents secondary LPD is low, around 1% or less, but considerably higher compared with open surgical hysterectomy or myomectomy.21 The consequences of peritoneal dissemination are particularly disturbing when unsuspected atypical pathology such as uterine leiomyosarcoma is later found.20,22 To reduce these risks, the U.S. Food and Drug Administration (FDA) now recommends that strict guidelines be followed for performing laparoscopic power morcellation, including the use of a “tissue containment system”. Whether related to a presumed primary process, or secondary to power morcellation, the CT appearance of peritoneal leiomyomatosis is similar. Multiple relatively homogenous soft tissue mases, often with a lobulated appearance, can be seen with varying extent of tumor bulk (Figure 9). Large-volume ascites or other associated findings are uncommon, and should instead suggest malignancy. The presence of multiple uterine fibroids may be a clue or simply a common incidental finding (red herring). More importantly, history of prior myomectomy, especially via laparoscopic morcellation, should strongly suggest this diagnosis. Lymphoproliferative disorders Whether considered a primary or secondary process, many subtypes of lymphoma and other lymphproliferative disorders may involve the peritoneum. Extranodal peritoneal involvement does not include mesenteric lymphadenopathy, which is a common component of typical nodal lymphoma. Relative to GI tract and solid organ involvement, peritoneal lymphomatosis is an uncommon manifestation of extranodal lymphoma.16 A detailed discussion of the histologic subtypes of lymphoma is beyond the scope of this review. However, most cases of peritoneal lymphomatosis are non-Hodgkin subtypes, with diffuse large B-cell lymphoma usually reported as most frequent (Figure 10).16 Burkitt lymphoma is a highly aggressive subtype that commonly involves the abdomen in its sporadic form, especially the ileocecal region, but may manifest with bulky peritoneal involvement (Figure 10).23 Extramedullary relapse from leukemia can result in peritoneal infiltration, as can be seen with myeloid sarcoma (Figure 10), which has been previously referred to as granulocytic sarcoma or chloroma. Multiple myeloma, another marrow-based process characterized by proliferation of malignant plasms cells, can rarely give rise to peritoneal-based extraosseous myelomatous masses (Figure 10).24 Hodgkin lymphoma rarely manifests with extranodal peritoneal involvement (Figure 10). In the setting of a solid organ transplant, extensive peritoneal soft tissue infiltration should suggest post-transplantation lymphoproliferative disorder (PTLD), which tends to be an extranodal process and is related to immunosuppression (Figure 10).25 Peritoneal lymphomatosis can often show dramatic improvement with chemotherapy and, unlike some cases of peritoneal carcinomatosis and sarcomatosis, surgical debulking is not indicated. CT findings of bulky, homogeneous peritoneal soft tissue and associated lymphadenopathy or splenomegaly helps distinguish lymphomatosis from sarcomatosis, but considerable overlap with peritoneal carcinomatosis still exists. Bowel obstruction is uncommon, even with bulky disease. Image-guided core biopsy is often pursued to establish the initial diagnosis, often targeting the omentum if involved. In patients with known lymphoma, FDG-PET/CT is frequently used for staging and surveillance.26 Growing teratoma syndrome & gliomatosis peritonei Patients treated with chemotherapy for malignant germ cell tumors rarely present later on with growth of mature teratomatous elements. Serum markers remain normal and the tumors are benign. Although originally described as predominately retroperitoneal tumors in males with a history of treated nonseminomatous germ cell tumors,27 this syndrome is now recognized following treatment of immature ovarian teratomas in younger females.28 This phenomenon is distinct from chemotherapeutic retroconversion of immature to mature teratomas. In females, the mature teratomatous elements are peritoneal in location. In some cases, the mature implants are composed entirely of mature glial tissue, which is then referred to as gliomatosis peritonei.29 In addition to representing a special subset of the growing teratoma syndrome, gliomatosis peritonei can also result from translocation of glial tissue from the cerebrospinal fluid into the peritoneal cavity via a ventriculoperitoneal (VP) shunt.30 For both the growing teratoma syndrome in general and VP shunt-related gliomatosis peritonei, the overall prognosis is good. At CT, the growing teratoma syndrome is characterized by well-defined, often bulky peritoneal-based masses containing varying amounts of fat, soft tissue, cysts, and calcification (Figure 11). Clinical history of prior treatment for an immature ovarian teratoma should strongly suggest the diagnosis. These benign tumors can remain stable without treatment for years (Figure 11). Biopsy is generally indicated to confirm the diagnosis and exclude tumor progression or malignant recurrence. In the special case of gliomatosis peritonei within the growing teratoma syndrome, homogeneous peritoneal soft tissue is seen, which more closely mimics malignancy. When related to VP shunt, a similar soft tissue appearance is seen, but the presence of the shunt itself is the key to suggesting the diagnosis (Figure 11).

A wide variety of unusual peritoneal-based neoplasms can simulate the appearance of peritoneal carcinomatosis at CT, including both primary and secondary peritoneal tumors. In many cases, there are certain clinical and CT imaging clues that may allow the interpreting radiologist to appropriately narrow the differential diagnosis and, in some cases, make an imaging-specific diagnosis. Table 1. | Primary peritoneal neoplasms | | Serous carcinoma | | Mesothelioma | | Malignant variant | | Benign cystic variant | | DSRCT | | Mesenchymal tumors | | Benign, intermediate, and malignant (sarcomas) | | Unusual secondary neoplastic conditions | | Pseudomyxoma peritonei | | Leiomyomatosisa | | Lymphoproliferative diseasea | | Growing teratoma syndrome | | Gliomatosis peritonei | DSRCT, desmoplastic small round cell tumor. These entities may also have a primary peritoneal counterpart. Table 2. | Peritoneal neoplasm | Clinical clues | Imaging clues | |---|---|---| | Primary serous carcinoma | Almost exclusively females | Calcified peritoneal masses (especially omental) | | Malignant mesothelioma | History of asbestos exposure (in 60%) | Lacks calcification; may be pleural involvement | | Benign cystic mesothelioma | Strong female predilection (child-bearing age) | Multicystic with thin septations; lacks calcification Tendency to recur | | Desmoplastic small round cell tumor | Adolescent and young adult males | Multifocal, rounded masses > infiltrative pattern | | Mesenchymal tumors | NF-1 (GIST); FAPS/Gardner syndrome (desmoid) | Fat attenuation (lipoma, liposarcoma) Associated lymphadenopathy uncommon | | Pseudomyxoma peritonei | History of mucinous appendiceal neoplasm | Malignant appendiceal mucocele still present Varying attenuation; septal calcification | | Leiomyomatosis | Prior laparoscopic myomectomy (w/ morcellator) | Homogenous soft tissue masses Presence of multiple (exophytic) uterine fibroids | | Lymphoproliferative disease | Solid organ transplantation (PTLD) | Associated lymphadenopathy Solid organ transplant (PTLD) | | Growing teratoma syndrome | History of treated malignant germ cell tumor | Teratomatous features (fat, calcium, cysts) | | Gliomatosis peritonel | History of VP shunt | VP shunt in place | FAPS, familial adenomatous polyposis syndrome; GIST, gastrointestinal stromal tumor; NF-1, neurofibromatosis type-1; PTLD, post-transplantation lymphoproliferative disorder; VP, ventriculoperitoneal. Contributor Information Perry J Pickhardt, Email: [email protected]. Alberto A Perez, Email: [email protected]. Mohab M Elmohr, Email: [email protected]. Khaled M Elsayes, Email: [email protected].

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