(Radiographics. 1999;19:S85-S102.)
© RSNA, 1999
CT of Epithelial Ovarian Tumors1
Satomi Kawamoto, MD,
Bruce A. Urban, MD and
Elliot K. Fishman, MD
1 From the Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins Medical Institutions, Baltimore, Md. Recipient of a Certificate of Merit award for a scientific exhibit at the 1998 RSNA scientific assembly. Received January 20, 1999; revision requested February 12 and received March 9; accepted March 16. Address reprint requests to E.K.F., Department of Radiology, Johns Hopkins Hospital, 601 N Caroline St, Baltimore, MD 21287.
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Abstract
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Ovarian cancer is the second most common gynecologic malignancy in the United States and causes more deaths than any other cancer of the female reproductive system. Approximately two-thirds of patients have tumors that have spread beyond the pelvis at the time of diagnosis. Ovarian tumors arise from the surface epithelium or mesothelium, germ cells, or the gonadal stroma. Epithelial ovarian tumors include serous, mucinous, endometrioid, clear cell, and undifferentiated tumors. In general, the likelihood of malignancy increases with increasing solid-tissue elements and thicker septa. Surgery is central to the management of ovarian cancer. At the initial exploratory laparotomy, surgicopathologic staging and debulking of the tumor are undertaken. Patients with advanced cancer frequently undergo second-look surgery after chemotherapy to detect any residual disease. CT can provide staging information for preoperative planning and determination of surgical resectability, demonstrate tumor response to therapy, and allow detection of persistent or recurrent disease. However, a major limitation of CT is the lack of sensitivity for detection of small tumor implants, especially on the small intestine or mesentery. Dedicated CT of the pelvis is best performed with spiral CT. Ovarian carcinoma can spread by means of intraperitoneal implantation, lymphatic invasion, and hematogenous dissemination.
Index Terms: Ovary, CT, 852.12115 • Ovary, neoplasms, 852.30
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INTRODUCTION
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Ovarian cancer is the second most common gynecologic malignancy in the United States and accounts for 4% of all cancers among women (1). It is the fifth leading cause of cancer deaths in women after lung, breast, colon, and pancreatic cancer. Ovarian cancer is the cause of more deaths than any other cancer of the female reproductive system. The 5-year survival rate is 46% (1). It has been estimated that, in the United States, one woman in 70 will develop ovarian cancer during her lifetime and one woman in 100 will die of this disease (2). Ovarian cancer is often "silent," showing no obvious signs or symptoms until late in its course. Approximately two-thirds of patients have tumors that have spread beyond the pelvis at the time of diagnosis (2). Primary prevention and early detection are crucial to increasing the chances for survival.
In cases of ovarian cancer, computed tomography (CT) can provide staging information for preoperative planning and determination of surgical resectability, demonstrate tumor response to therapy, and allow detection of persistent or recurrent disease. In this article, the epidemiology of ovarian cancer, classification of primary ovarian tumors, types of epithelial ovarian tumors, staging of ovarian cancer, and therapy options for ovarian cancer are described. The role of imaging in evaluation of ovarian cancer and the CT technique and diagnostic pitfalls are then discussed. Finally, the CT appearances of the primary tumor and local extension and the pathways of tumor spread are presented.
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EPIDEMIOLOGY OF OVARIAN CANCER
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In the development of ovarian cancer, hormonal, environmental, and genetic factors have been identified as important (3). The protective effects of multiparity, a history of breast-feeding, and use of oral contraceptives support the "ovulation hypothesis," according to which the risk of ovarian cancer is a direct function of the number of ovulatory cycles in a woman's life span (2). One percent to 5% of cases of ovarian cancer are hereditary; such cases are defined as those in which the patient has at least two first-degree relatives with ovarian cancer. These patients have a lifetime probability as high as 50% of developing ovarian cancer. Three distinct genotypes of hereditary ovarian cancer have been identified: (a) breast cancer–ovarian cancer syndrome, (b) ovarian cancer only syndrome, and (c) Lynch type II cancer family syndrome, which is characterized by inheritance of nonpolyposis colorectal cancer, endometrial cancer, and, to a lesser extent, ovarian cancer (2). Recently, mutations in two genes, BRCA1 and BRCA2, were identified in women from early-onset hereditary breast cancer families and breast-ovarian cancer families (4,5). Somatic BRCA1 mutations have also been found in 8%–10% of sporadic ovarian cancers (6,7). The discovery of these genes may affect the diagnosis and prevention of familial ovarian cancer (7).
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CLASSIFICATION OF PRIMARY OVARIAN TUMORS
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The classification of ovarian tumors is based on the presumed cell of origin. Tumors arise from one of the three major categories: (a) the surface epithelium or mesothelium, (b) germ cells, or (c) the specialized gonadal stroma (sex cord stromal tumors) (8). The majority (75%) of ovarian neoplasms are benign. Malignant tumors and tumors of borderline malignancy account for 21% and 4% of primary ovarian neoplasms, respectively (9). Among the malignant neoplasms, the epithelial type, malignant germ cell, and malignant stromal neoplasms represent approximately 85%, 7%, and 7% of cases, respectively (9). The proportion of malignant tumors increases with age: Before 20 years of age, malignant tumors represent 4% of all ovarian neoplasms; however, after 50 years of age, this proportion increases to 40% (8). The germ cell tumors represent two-thirds of ovarian malignancies in females less than 20 years of age (10). This article focuses on the evaluation of epithelial ovarian tumors.
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TYPES OF EPITHELIAL OVARIAN TUMORS
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Epithelial ovarian tumors include serous, mucinous, endometrioid, clear cell, and undifferentiated tumors (11) (Table 1). All epithelial ovarian tumors can be classified as benign, borderline malignant, or malignant according to their histologic features and clinical behavior (Fig 1) (12). Tumors of borderline malignancy are characterized by early-stage diagnosis (nearly one-third are stage I at the time of diagnosis), infrequent and late recurrence, and long survival rates (8).
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Figure 1a. Malignant serous cystadenocarcinoma of the ovary. (a) Low-power photomicrograph (original magnification, x10; hematoxylin-eosin stain) shows papillary projections into a cyst (curved arrow). Note the normal ovary (straight arrow). (b) Higher-power photomicrograph (original magnification, x40; hematoxylin-eosin stain) shows a focus of invasive carcinoma (arrow). (Courtesy of Ralph Hruban, MD, Johns Hopkins Medical Institutions, Baltimore, Md.)
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Figure 1b. Malignant serous cystadenocarcinoma of the ovary. (a) Low-power photomicrograph (original magnification, x10; hematoxylin-eosin stain) shows papillary projections into a cyst (curved arrow). Note the normal ovary (straight arrow). (b) Higher-power photomicrograph (original magnification, x40; hematoxylin-eosin stain) shows a focus of invasive carcinoma (arrow). (Courtesy of Ralph Hruban, MD, Johns Hopkins Medical Institutions, Baltimore, Md.)
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Serous Carcinoma
Among epithelial neoplasms, serous tumors are the most common type within both the benign and malignant categories. Serous carcinomas account for 60%–80% of all epithelial malignancies of the ovary (8). Approximately 25% of serous tumors are malignant (13). The malignant lesions tend to have more solid tissue than the benign lesions (Fig 2), and areas of hemorrhage or necrosis are more common than in the benign tumors (13). Psammoma bodies (microscopic calcifications) are seen at histologic analysis in up to 30% of malignant serous tumors (8) and can be detected with CT in approximately 12% of tumors (14). However, psammoma bodies are a nonspecific finding, since they are also seen in benign serous tumors as well as other neoplasms, including mucinous adenocarcinoma of the colon and papillary thyroid cancer (8,13).
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Figure 2. Papillary serous adenocarcinoma (stage IIIb). CT scan shows bilateral complex solid and cystic adnexal tumors (open arrows). The right tumor is closely associated with the pelvic side wall (curved arrow). At surgery, the right ovarian tumor was adherent to the right pelvic side wall and the cul-de-sac. At pathologic analysis, there was extensive tumor involvement of the right and left ovaries, right fallopian tube, and left peritubal soft tissue. B = bladder.
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Mucinous Carcinoma
Ten percent of mucinous ovarian tumors are malignant (8,13). Mucinous carcinoma is less likely to be bilateral than serous carcinoma, with bilateral lesions occurring in 5%–10% of the stage I cases (8). Mucinous tumors are typically multilocular, with numerous smooth, thin-walled cysts (Fig 3). Mucoid material is found within the cysts, sometimes accompanied by hemorrhagic or cellular debris. The malignant lesions tend to have a proportionately greater solid-tissue component (13) (Fig 4). CT may demonstrate high attenuation in some loculi due to the high protein content of the mucoid material (13) (Fig 5). At histologic analysis, mucinous carcinomas of the ovary are difficult to differentiate from metastases to the ovary from an intestinal primary tumor (12).
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Figures 3-5. (3) Mucinous cystadenoma with a focus of low malignant potential (borderline malignancy) limited to the right ovary (stage Ia). CT scan shows a multiseptated tumor of low attenuation occupying the central portion of the pelvis. (4) Well-differentiated mucinous cystadenocarcinoma limited to the left ovary (stage Ia). CT scan shows a large, complex, cystic tumor with prominent solid-tissue elements (arrows). (5) Mucinous cystadenoma with a focus of low malignant potential (borderline malignancy) limited to the left ovary (stage Ia). CT scan shows a tumor with relatively high attenuation (20-30 HU), which reflects the high protein content of mucoid material.
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Figures 3-5. (3) Mucinous cystadenoma with a focus of low malignant potential (borderline malignancy) limited to the right ovary (stage Ia). CT scan shows a multiseptated tumor of low attenuation occupying the central portion of the pelvis. (4) Well-differentiated mucinous cystadenocarcinoma limited to the left ovary (stage Ia). CT scan shows a large, complex, cystic tumor with prominent solid-tissue elements (arrows). (5) Mucinous cystadenoma with a focus of low malignant potential (borderline malignancy) limited to the left ovary (stage Ia). CT scan shows a tumor with relatively high attenuation (20-30 HU), which reflects the high protein content of mucoid material.
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Figures 3-5. (3) Mucinous cystadenoma with a focus of low malignant potential (borderline malignancy) limited to the right ovary (stage Ia). CT scan shows a multiseptated tumor of low attenuation occupying the central portion of the pelvis. (4) Well-differentiated mucinous cystadenocarcinoma limited to the left ovary (stage Ia). CT scan shows a large, complex, cystic tumor with prominent solid-tissue elements (arrows). (5) Mucinous cystadenoma with a focus of low malignant potential (borderline malignancy) limited to the left ovary (stage Ia). CT scan shows a tumor with relatively high attenuation (20-30 HU), which reflects the high protein content of mucoid material.
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Endometrioid Carcinoma
Endometrioid carcinoma of the ovary accounts for approximately 8%–15% of ovarian malignancies (2,8). The vast majority of endometrioid tumors are malignant and invasive (13). Approximately 15% of stage I endometrioid cancers are bilateral (8). The typical gross appearance of these tumors is similar to that of other epithelial lesions, with variable cystic and solid components (Fig 6); occasionally, they are completely solid (13). Endometrioid carcinomas are associated with hyperplasia or carcinoma of the uterine endometrium in 20%–33% of cases. The endometrial abnormality is thought to represent an independent, primary lesion rather than metastatic disease (13).
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Figure 6. Endometrioid carcinoma arising from the left ovary (stage IIc). CT scan shows a complex cystic and solid tumor with enhancement of the solid-tissue elements (arrow) and a thick, irregular wall.
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The ovary is capable of reproducing all the histologic subtypes of malignancy that arise from the endometrial glands or stroma of the uterus (8). Malignant mixed mesodermal tumors (carcinosarcoma) are grouped with endometrioid carcinoma, and the gross and microscopic features of these tumors are similar to those of the corresponding lesions of the uterus (13).
Clear Cell Carcinoma
Clear cell carcinomas of the ovary, also called mesonephroid carcinomas, are identical to clear cell carcinomas of the endometrium, cervix, or vagina (12). Most clear cell neoplasms are malignant (13). They represent 2%–5% of epithelial ovarian malignancies (8). The majority of clear cell carcinomas (75%) are stage I disease, and the prognosis is better than for other ovarian cancers (50% of patients survive 5 years after diagnosis) (12). Although the gross appearance is variable, clear cell tumors are frequently unilocular cysts with one or more solid tumor nodules protruding into the cavity (8) (Fig 7).
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Figure 7. Clear cell carcinoma arising from the left ovary (stage IV due to parenchymal liver metastases). CT scan shows a complex cystic and solid tumor with an irregular interface between the tumor and the myometrium (arrow). At pathologic analysis, the tumor involved the left ovary, left fallopian tube, and right peritubal soft tissue and extensively infiltrated the myometrium of the fundus and lower uterine segment.
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Undifferentiated Carcinoma
Approximately 4% of all ovarian carcinomas are undifferentiated carcinomas (12). In these tumors, the cellular differentiation is not sufficient for the tumor to be categorized into one of the previously described groups. Pure undifferentiated carcinomas are rare; most of these tumors are mixed, with areas of serous, glandular, or transitional cell differentiation. All undifferentiated carcinomas are malignant (13). Most of these tumors (91%) are stage III or IV (11) and have a poor outcome.
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STAGING OF OVARIAN CANCER
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The staging system most commonly used for ovarian carcinoma is that of the International Federation of Gynecology and Obstetrics (Table 2). The stage is defined as the extent of disease at the time of diagnosis and is based on findings at exploratory laparotomy and thorough evaluation of all areas at risk (2). In general terms, stages I and II are considered early disease, with the tumor limited to the ovaries (stage I) or pelvis (stage II). Stages III and IV are advanced disease, with the tumor limited to the abdomen (stage III) or extending beyond the abdomen or with parenchymal liver metastases (stage IV). The stage is important because it is one of the major factors affecting the prognosis. In addition, postoperative therapy is based on the initial stage of disease (2). The 5-year survival rate is 80% for stage I disease, 50% for stage II, 30% for stage III, and 8% for stage IV (13).
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THERAPY OPTIONS FOR OVARIAN CANCER
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Surgery is central to the management of ovarian cancer. At the initial exploratory laparotomy, surgicopathologic staging and debulking of the tumor are undertaken (2). Standard surgery for early ovarian cancer involves total abdominal hysterectomy, bilateral salpingo-oophorectomy, and omentectomy, as well as aspiration of ascites or peritoneal lavage for cytologic examination, random peritoneal biopsies including paracolic gutters and undersurfaces of hemidiaphragms, and sampling of pelvic and paraaortic lymph nodes (2). For patients with advanced ovarian cancer, surgical cytoreduction (debulking) is undertaken, followed by chemotherapy. Chemotherapy usually consists of a regimen involving platinum agents. More recently, chemotherapy also includes paclitaxel (Taxol; Bristol-Myers Oncology, Princeton, NJ), a new class of agent with cytotoxic effect on microtubules (2,15). Aggressive cytoreduction of tumor bulk is undertaken on the assumption that it enhances the response of the remaining tumor to chemotherapy, as the volume of residual disease after cytoreduction surgery has been directly correlated with survival (2,16).
Patients with advanced cancer frequently undergo abdominal exploration ("second-look" surgery) after induction chemotherapy to detect any residual disease. Undertaken routinely during the past 2 decades, second-look surgery is now considered controversial because it is a highly invasive diagnostic procedure without proved benefit (2,15). However, it is generally accepted that if the patient has no detectable disease at imaging, evaluation of serum CA-125 level, or physical examination, second-look laparotomy remains the standard of care for tissue confirmation of persistent small-volume tumor or to confirm complete disease remission after first-line chemotherapy (15).
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ROLE OF IMAGING IN EVALUATION OF OVARIAN CANCER
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The use of cross-sectional imaging in pretreatment evaluation of ovarian cancer is controversial because both staging and tumor debulking are undertaken at the time of exploratory laparotomy. However, cross-sectional imaging can provide staging information that may help in preoperative planning (17). In addition, neoadjuvant chemotherapy prior to debulking surgery has been used recently in patients with unresectable or stage IV disease (3), and cross-sectional imaging can help identify those patients who may benefit from preoperative neoadjuvant chemotherapy (17). The use of CT for staging of ovarian cancer has been extensively studied. The reported preoperative staging accuracy of CT is 70%–90% (18–21). CT is more sensitive than ultrasonography (US) for detection of abnormalities in the paraaortic lymph nodes, omentum, mesentery, and subdiaphragmatic regions (22). CT is a fast and widely available study, and it remains the most useful technique for preoperative staging of ovarian cancer (18).
CT is also frequently used to detect persistent or recurrent ovarian cancer and demonstrate tumor response to subsequent therapy (23). The reported sensitivity and specificity of CT performed before second-look surgery are 59%–83% and 83%–88%, respectively (23–26). Magnetic resonance (MR) imaging has similar sensitivity and specificity (26–28). A major limitation of both CT and MR imaging is relatively poor sensitivity for detection of small tumor implants, especially on the small intestine or mesentery (26,28). This limitation is related to the natural history of metastatic ovarian cancer. Disease that is grossly limited to the ovary is often associated with widespread peritoneal microscopic disease, which cannot be seen at radiologic or direct visual inspection and is detectable only with histologic examination (2). Several studies have shown that 1–3-cm-diameter lesions in the mesentery and omentum can be missed (18,23), although these studies were done before the advent of spiral CT. CT is often performed before the planned second-look surgery. If CT shows evidence of residual or recurrent tumor, unnecessary second-look laparotomy can be avoided in over 20% of patients subjected to second-look surgery with current restaging methods (2,13,15,22).
The continuous improvement of imaging techniques, including spiral CT, has improved the detection of small peritoneal implants. Recent studies have found that CT allows detection of 50% of peritoneal implants as small as 5 mm in diameter located in the subphrenic regions or profiled by ascites (29) and 28% of implants smaller than 5 mm in diameter (30). The use of intraperitoneally administered contrast material has also increased detection of peritoneal tumor implants as small as 5 mm in diameter (31,32). However, this technique is invasive and has not become widely used. The value of spiral CT in characterization and staging of ovarian tumors and detection of residual or recurrent disease remains to be fully evaluated but appears promising (7). Continuous volumetric data acquisition and acquisition of three-dimensional images may improve lesion detection and definition of tumor extent (17). Positron emission tomography and immunoscintigraphy with monoclonal antibodies directed at the tumor-associated glycoprotein may also improve detection of clinically occult residual or recurrent disease (33,34). The long-term objective of diagnostic imaging suggested at the Strategic Planning Conference on New Directions in Ovarian Cancer Research, held in December 1997, is to improve treatment planning for patients with ovarian cancer by the judicious use of noninvasive imaging tests (7). Specific objectives include assessment of the effects of screening the general and at-risk populations; assessment of the accuracy of imaging studies in evaluation of tumor volume; assessment of the usefulness of tumor location and resectability in guiding management; exploration of novel imaging methods; and refining analysis of existing imaging methods for early detection, characterization, staging, and monitoring (7).
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CT TECHNIQUE AND DIAGNOSTIC PITFALLS
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Dedicated CT of the pelvis is best performed with spiral CT (35,36). Spiral scanning begins after the administration of nonionic iodinated contrast material, typically at a rate of 1.5–2.0 mL/sec. Scanning is initiated 90–120 seconds after the onset of contrast material injection. This scanning delay—longer than the typical delay for spiral scanning in the upper abdomen—is necessary to optimize venous enhancement and is critical for differentiating iliac blood vessels from lymph nodes. Bolus administration of contrast material also demonstrates the pelvic anatomy and can help differentiate tumor from the normal enhancing uterus. When arterial anatomy is of major interest, scanning should begin earlier (50–70 sec) after contrast material injection performed at a faster rate (2.0–3.0 mL/sec). Typical scanning parameters are 5–8-mm collimation, 5–8-mm/sec table speed, and 5-mm reconstruction increments. Thinner collimation (3–5 mm) is helpful in the evaluation of known masses or tumors, for which accurate staging and characterization are important.
In most patients, images of the upper abdomen are obtained immediately before dedicated pelvic scanning to optimize contrast material dynamics in the liver, pancreas, and kidneys. This point is especially important in the evaluation of ovarian cancers, in which the detection of metastatic implants in the mid- and upper abdomen is crucial for accurate staging.
Potential diagnostic pitfalls can result from a poor CT technique. A common error is mistaking unenhanced small bowel loops for a cystic ovarian mass. For this reason, a delay of at least 1 hour after oral contrast material administration is recommended for all patients. Another pitfall involves misinterpreting the normal unenhanced bladder as a cystic ovarian mass or fluid collection. This is an increasingly common problem with the advent of spiral CT, in which images are routinely obtained before the bladder is enhanced. If uncertainty exists, delayed images after bladder enhancement should be obtained (35,36).
Care must be taken not to mistake every cystic ovarian lesion seen at CT for a tumor. A multitude of benign cysts can mimic the CT appearance of ovarian cancer, including follicular cysts, corpus luteum cysts, polycystic ovaries, and endometriosis (37). In addition, ovarian metastases can mimic the appearance of a primary ovarian tumor. For these reasons, correlation with the patient's clinical history, age, and menstrual status is mandatory whenever a cystic ovarian lesion is detected at CT. Less commonly, patients demonstrate CT findings from conditions that mimic metastatic ovarian cancer, including tuberculous peritonitis, primary mesothelioma of the peritoneum, and metastatic uterine carcinoma. Many times, the clinical presentation and CT findings are identical to those of metastatic ovarian cancer, and the diagnosis is made only at laparotomy.
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CT APPEARANCES OF PRIMARY TUMOR AND LOCAL EXTENSION
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Primary Tumor
The position of ovarian masses in the pelvis may vary due to mobility of the ovary. The ovary typically lies in the adnexa lateral to the uterus and posterior to the round ligament. Less common locations for ovarian masses are in the midline cul-de-sac or anterosuperior to the uterus and bladder in the midline (38). At presentation, most ovarian carcinomas are greater than 4–5 cm in diameter (17,22). CT features suggestive of malignancy include (a) lesion diameter greater than 4 cm; (b) papillary projections, which are often seen on contrast material–enhanced images; (c) walls and septa more than 3 mm thick; (d) a partially cystic, partially solid mass; (e) a lobulated solid mass; and (f) the presence of tumor vessels on contrast-enhanced images (39). None of these features are specific enough to indicate the diagnosis preoperatively. In general, however, the likelihood of malignancy increases with increasing solid-tissue elements and thicker septa (13).
Local Extension
Early in the disease, ovarian cancer is confined to the ovary. With time, capsular invasion takes place, and direct involvement of adjacent structures can occur. The anterior and posterior cul-de-sac, sigmoid colon, omentum, small intestine, pelvic wall peritoneum, uterus, fallopian tubes, and broad ligament are the most common sites of direct involvement (8). CT signs of tumor extension in the pelvic organs include (a) localized distortion of the uterine contour, (b) an irregular interface between the tumor and the myometrium (Fig 7), (c) loss of a tissue plane between the solid component of the tumor and the wall of the sigmoid colon or the bladder, (d) encasement of the sigmoid colon by the tumor or direct tumor extension to the sigmoid colon, (e) distance between the tumor and the pelvic side wall of less than 3 mm (Fig 2), and (f) iliac vessels surrounded or displaced by the tumor (40).
There is poor correlation between the gross pathologic appearance and the histologic type or aggressiveness of the tumor (22,23). However, secondary findings suggestive of malignancy such as pelvic organ and pelvic side wall invasion; peritoneal, omental, or mesenteric involvement; ascites; and lymphadenopathy increase the confidence in a diagnosis of malignancy (10). When these secondary criteria are used in addition to the primary criteria, the reported accuracy of CT in characterization of ovarian tumors as benign versus malignant is 92%–94% (39,41). In part, the excellent accuracy of CT reflects the advanced stage at presentation of many ovarian tumors.
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PATHWAYS OF TUMOR SPREAD
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Ovarian carcinoma can spread by means of (a) intraperitoneal implantation, (b) lymphatic invasion, and (c) hematogenous dissemination (8). Intraperitoneal implantation is the primary mode of spread of ovarian cancer (2).
Peritoneal Spread
After cancer penetrates the ovarian capsule, malignant cells seed the peritoneal cavity (2). The entire peritoneal surface is at risk; however, preferred sites of peritoneal implants include the posterior cul-de-sac, the infundibulopelvic ligaments, the omentum, the right paracolic gutter, and the undersurface of the right hemidiaphragm. These sites reflect the patterns of circulation of peritoneal fluid (2,8). Other common sites of involvement include the Morison pouch, liver surface, porta hepatis, intrahepatic fissure, and bowel mesenteries (17).
Ascites.—Ascites is helpful in detection of small peritoneal tumor implants (42,43) (Fig 8). The presence of ascites itself is not specific but usually indicates the presence of peritoneal metastases in patients with ovarian cancer (8). Patients with peritoneal carcinomatosis often have peritoneal fluid in both the greater sac and lesser sac (Fig 9), in contrast to patients with benign ascites, who tend to have large fluid collections in the greater sac with little fluid in the lesser sac (42). Loculated ascites is also seen secondary to adhesions and may appear as a well-defined area of fluid attenuation (42).
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Figure 8. Poorly differentiated carcinoma of the ovary. CT scan shows a small, plaquelike implant projecting from the parietal peritoneal surface along the undersurface of the right hemidiaphragm (curved arrow). Ascites can help in the detection of small peritoneal implants by outlining them with fluid. Thickening of the falciform ligament (straight arrow) and omentum (arrowheads) also suggests implants.
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Figures 9-11. (9) Serous cystadenocarcinoma of the ovary. (a) CT scan shows ascites in the lesser sac (LS), which displaces the stomach (S) anteriorly. There are diffuse implants (arrows) along the omentum; the parietal peritoneum (right hemidiaphragm); subcapsular regions of the liver; and the gastrosplenic, splenorenal, and hepatogastric and hepatoduodenal ligaments. The surgical clip is from a prior omentectomy. (b) CT scan shows ascites in the greater sac. Nodular masses along the mesentery near the ileocecal junction represent implants (arrows). Also note the subtle implants surrounded by ascites along the parietal peritoneum of the anterior abdominal wall (arrowheads). (10) Serous cystadenocarcinoma of the ovary with psammoma bodies. CT scan shows diffuse, calcified implants along the peritoneum and pleura (arrows). There is a small right pleural effusion. (11) Serous cystadenocarcinoma of the ovary. CT scan shows extensive metastatic involvement of the peritoneum and omentum, which extends through the abdominal wall to the subcutaneous fat (arrow). The tumor also involves the bowel wall, causing encasement and stricture of the small and large intestine, which were confirmed at pathologic analysis. There is a markedly dilated bowel loop (B) in the right abdomen proximal to the obstruction. The fat plane between the anterior abdominal wall and the intestinal wall is obscured.
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Figures 9-11. (9) Serous cystadenocarcinoma of the ovary. (a) CT scan shows ascites in the lesser sac (LS), which displaces the stomach (S) anteriorly. There are diffuse implants (arrows) along the omentum; the parietal peritoneum (right hemidiaphragm); subcapsular regions of the liver; and the gastrosplenic, splenorenal, and hepatogastric and hepatoduodenal ligaments. The surgical clip is from a prior omentectomy. (b) CT scan shows ascites in the greater sac. Nodular masses along the mesentery near the ileocecal junction represent implants (arrows). Also note the subtle implants surrounded by ascites along the parietal peritoneum of the anterior abdominal wall (arrowheads). (10) Serous cystadenocarcinoma of the ovary with psammoma bodies. CT scan shows diffuse, calcified implants along the peritoneum and pleura (arrows). There is a small right pleural effusion. (11) Serous cystadenocarcinoma of the ovary. CT scan shows extensive metastatic involvement of the peritoneum and omentum, which extends through the abdominal wall to the subcutaneous fat (arrow). The tumor also involves the bowel wall, causing encasement and stricture of the small and large intestine, which were confirmed at pathologic analysis. There is a markedly dilated bowel loop (B) in the right abdomen proximal to the obstruction. The fat plane between the anterior abdominal wall and the intestinal wall is obscured.
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Peritoneal Implants.—Spread within the peritoneum can be along the surface of the peritoneum or within the ligaments (44). If the peritoneal implants are larger than approximately 10 mm in diameter, they appear as discrete nodular or plaquelike lesions adjacent to or projecting from the peritoneal surfaces. Diffuse tumor may coat the peritoneum over the bowel loops, the abdominal wall and retroperitoneum, and the undersurfaces of the hemidiaphragms, resulting in uneven thickening (Fig 9). These implants may enhance after intravenous injection of contrast material (22). Serous or mucinous lesions may demonstrate soft-tissue or fluid attenuation. The metastatic sites of the ovarian tumor can be completely fluid in appearance (44). Serous cystadenocarcinoma contains calcification in 30% of cases, and CT may demonstrate calcified peritoneal metastases or calcified metastatic lymph nodes in such cases (14) (Fig 10).
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Figures 9-11. (9) Serous cystadenocarcinoma of the ovary. (a) CT scan shows ascites in the lesser sac (LS), which displaces the stomach (S) anteriorly. There are diffuse implants (arrows) along the omentum; the parietal peritoneum (right hemidiaphragm); subcapsular regions of the liver; and the gastrosplenic, splenorenal, and hepatogastric and hepatoduodenal ligaments. The surgical clip is from a prior omentectomy. (b) CT scan shows ascites in the greater sac. Nodular masses along the mesentery near the ileocecal junction represent implants (arrows). Also note the subtle implants surrounded by ascites along the parietal peritoneum of the anterior abdominal wall (arrowheads). (10) Serous cystadenocarcinoma of the ovary with psammoma bodies. CT scan shows diffuse, calcified implants along the peritoneum and pleura (arrows). There is a small right pleural effusion. (11) Serous cystadenocarcinoma of the ovary. CT scan shows extensive metastatic involvement of the peritoneum and omentum, which extends through the abdominal wall to the subcutaneous fat (arrow). The tumor also involves the bowel wall, causing encasement and stricture of the small and large intestine, which were confirmed at pathologic analysis. There is a markedly dilated bowel loop (B) in the right abdomen proximal to the obstruction. The fat plane between the anterior abdominal wall and the intestinal wall is obscured.
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Tumor infiltration can also be seen along the falciform ligament (Fig 8); the gastrosplenic, hepatogastric, and hepatoduodenal ligaments (Fig 9); and the gastrocolic ligament. Intraperitoneal spread of ovarian cancer may also involve the umbilical region of the abdominal wall, producing periumbilical masses (42) (Fig 11).
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Figures 9-11. (9) Serous cystadenocarcinoma of the ovary. (a) CT scan shows ascites in the lesser sac (LS), which displaces the stomach (S) anteriorly. There are diffuse implants (arrows) along the omentum; the parietal peritoneum (right hemidiaphragm); subcapsular regions of the liver; and the gastrosplenic, splenorenal, and hepatogastric and hepatoduodenal ligaments. The surgical clip is from a prior omentectomy. (b) CT scan shows ascites in the greater sac. Nodular masses along the mesentery near the ileocecal junction represent implants (arrows). Also note the subtle implants surrounded by ascites along the parietal peritoneum of the anterior abdominal wall (arrowheads). (10) Serous cystadenocarcinoma of the ovary with psammoma bodies. CT scan shows diffuse, calcified implants along the peritoneum and pleura (arrows). There is a small right pleural effusion. (11) Serous cystadenocarcinoma of the ovary. CT scan shows extensive metastatic involvement of the peritoneum and omentum, which extends through the abdominal wall to the subcutaneous fat (arrow). The tumor also involves the bowel wall, causing encasement and stricture of the small and large intestine, which were confirmed at pathologic analysis. There is a markedly dilated bowel loop (B) in the right abdomen proximal to the obstruction. The fat plane between the anterior abdominal wall and the intestinal wall is obscured.
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Omental and Mesenteric Deposits.—The CT appearance of omental and mesenteric involvement by tumor ranges from small nodules (Fig 12) or strands of soft tissue that increase the attenuation of the fat anterior to the colon or small intestine (Fig 13) to marked omental thickening or a mass with poorly defined edges ("omental cake") (Fig 14). The fat plane between the anterior abdominal wall and the intestinal wall may be obscured (42,44) (Fig 11).
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Figures 12-14. (12) Poorly differentiated carcinoma of the ovary. CT scan shows implants as enhancing nodules along the surface of the colon (straight arrows). The thickened, radiating pattern of the mesenteric leaves (curved arrow) also suggests mesenteric tumor implants. There is extensive ascites. (13) Poorly differentiated carcinoma of the ovary. CT scan shows diffuse reticulonodular stranding and enhancement in the omental fat, which represent diffuse omental implants. There is also ascites with enhancement and minimal thickening of the peritoneal surface (arrows), findings indicative of implants. (14) Adenocarcinoma of the ovary. CT scan shows diffuse soft-tissue nodules (arrows) between the anterior abdominal wall and small bowel loops; these nodules represent extensive omental implants.
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Figures 12-14. (12) Poorly differentiated carcinoma of the ovary. CT scan shows implants as enhancing nodules along the surface of the colon (straight arrows). The thickened, radiating pattern of the mesenteric leaves (curved arrow) also suggests mesenteric tumor implants. There is extensive ascites. (13) Poorly differentiated carcinoma of the ovary. CT scan shows diffuse reticulonodular stranding and enhancement in the omental fat, which represent diffuse omental implants. There is also ascites with enhancement and minimal thickening of the peritoneal surface (arrows), findings indicative of implants. (14) Adenocarcinoma of the ovary. CT scan shows diffuse soft-tissue nodules (arrows) between the anterior abdominal wall and small bowel loops; these nodules represent extensive omental implants.
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Figures 12-14. (12) Poorly differentiated carcinoma of the ovary. CT scan shows implants as enhancing nodules along the surface of the colon (straight arrows). The thickened, radiating pattern of the mesenteric leaves (curved arrow) also suggests mesenteric tumor implants. There is extensive ascites. (13) Poorly differentiated carcinoma of the ovary. CT scan shows diffuse reticulonodular stranding and enhancement in the omental fat, which represent diffuse omental implants. There is also ascites with enhancement and minimal thickening of the peritoneal surface (arrows), findings indicative of implants. (14) Adenocarcinoma of the ovary. CT scan shows diffuse soft-tissue nodules (arrows) between the anterior abdominal wall and small bowel loops; these nodules represent extensive omental implants.
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Involvement of small bowel mesentery by disseminated ovarian tumor may be seen at CT as rounded masses (Fig 9); irregular, ill-defined masses; cystic masses; or stellate lesions, which consist of a thickened, radiating pattern of the mesenteric leaves due to infiltration of the perivascular bundles by tumor (42). When mesenteric involvement occurs with ascites, small bowel loops can appear tethered and will not float freely within the abdomen.
Perihepatic Involvement.—The liver surface, porta hepatis, and intrahepatic fissure are common sites of peritoneal deposits (10) (Fig 15). Nodular tumor implants on the parietal peritoneum of the right hemidiaphragm can indent the liver surface and may simulate capsular or parenchymal liver metastases (43,45). Ascites may help differentiate lesions on the liver surface from implants on the parietal peritoneum by separating the parietal and visceral peritoneum (43).
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Figure 15. Poorly differentiated adenocarcinoma of the ovary. CT scan shows a hypoattenuating mass in the posterior subcapsular region of the right hepatic lobe (straight arrow); the mass is growing into the liver parenchyma. A smaller mass (curved arrow) is seen near the portal vein.
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Splenic and Perisplenic Involvement.—Peritoneal implants on the surface of the spleen are frequently encountered (Fig 16). Intrasplenic metastases are less common and appear as hypoattenuating lesions of various sizes within the spleen (46).
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Figure 16. Serous cystadenocarcinoma of the ovary. CT scan shows multiple subcapsular splenic implants with scalloped margins (straight arrows). Subcapsular liver implants are also seen (curved arrows).
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Gastric Involvement.—The stomach may also be involved by ovarian cancer (Fig 17). In an autopsy study, gastric serosal metastases were found in 31% of cases, with wall invasion in 12% of cases (47). Ascites and metastatic implants in the lesser sac may displace the fundus and posterior wall of the stomach anteriorly and the gastrosplenic ligament laterally (Fig 9).
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Figure 17. Poorly differentiated adenocarcinoma of the ovary. The patient developed intractable nausea and vomiting during follow-up. CT scan shows a large cystic mass (m) arising from the posterior wall of the gastric fundus that markedly narrows the lumen. Endoscopic drainage of this mass revealed metastatic ovarian carcinoma.
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Bowel Involvement.—Involvement of the gastrointestinal tract by ovarian cancer is common in advanced disease. Bowel obstruction is a common complication of advanced ovarian cancer and is particularly common when invasion of the bowel wall (including the muscularis propria, submucosa, or mucosa) is present (47). Bowel obstruction was found to be the most common form of ovarian cancer–associated morbidity in an autopsy study (48). Bowel involvement manifests as nodular or plaquelike lesions along or projecting from the peritoneal surfaces (40) or wall thickening or distortion with or without obstruction (43) (Fig 18). Omental implants may also extend to the serosa of the transverse colon (49) (Fig 13). In patients with a history of prior surgery, small bowel obstruction can also occur as a complication of adhesions and does not necessarily indicate tumor recurrence.
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Figure 18. Mucinous adenocarcinoma of the ovary. CT scan shows small bowel obstruction due to an ill-defined soft-tissue mass in the right pelvis that involves the distal small intestine (arrows). At pathologic analysis, metastatic adenocarcinoma was found to involve the serosa and smooth muscle of the small intestine.
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Pseudomyxoma Peritonei.—A complication of mucinous tumors, pseudomyxoma peritonei is characterized by gelatinous material filling the peritoneal cavity, typically due to a ruptured mucinous cystadenocarcinoma or cystadenoma of the ovary or appendix. The gelatinous material cannot be drained percutaneously and often requires repeated laparotomy (8). The CT appearance of pseudomyxoma peritonei is distinctive: diffuse intraperitoneal hypoattenuating material that may contain septa and cause scalloping of the liver or splenic margin (42) (Fig 19). Less commonly, pseudomyxoma peritonei appears as discrete hypoattenuating masses. Enhancement of the septa or the margins of each tumor nodule may be seen on contrast-enhanced images (43). The walls of the septa may contain calcifications (42).
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Figure 19. Pseudomyxoma peritonei due to mucinous cystadenocarcinoma of the ovary. CT scan shows diffuse intraperitoneal hypoattenuating material in the lesser sac and greater sac with associated scalloping of the liver margin.
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Lymphatic Spread
Because the principal lymphatic drainage of the ovaries parallels the gonadal veins in the infundibulopelvic ligament to terminate in the paraaortic and pericaval lymph nodes at the level of the renal vessels, metastases are most frequently detected in these regions (22,50) (Fig 20). Lymph node channels also pass laterally through the broad ligament and parametrial channels to terminate in the lymphatic vessels of the pelvic side wall, which include the external iliac, obturator, and hypogastric chains (2). A short-axis diameter of more than 1 cm is often used as the CT criterion for malignant lymph nodes in the abdomen and pelvis, with a reported accuracy of 88% in ovarian cancer (40).
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Figure 20. Mesodermal mixed tumor (carcinosarcoma) of the ovary. CT scan shows retroperitoneal adenopathy (arrows) at the level of the renal hilum. The affected nodes have low attenuation due to chemotherapy. A right nephrostomy tube is also evident and was placed to treat ureteral obstruction due to tumor implants in the pelvis.
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Hydronephrosis is occasionally seen at CT in patients with advanced disease and may be associated with retroperitoneal adenopathy or tumor implants. In an autopsy study, Dvoretsky et al (48) found that hydronephrosis due to ureteral obstruction, which is often related to neoplastic invasion of the ureteral wall, was the second most common form of tumor-related morbidity after bowel obstruction (Fig 20).
In addition to abdominal and pelvic adenopathy, thoracic adenopathy may also be encountered at CT. Holloway et al (51) found that 28% of patients with stage II, stage III, or recurrent epithelial ovarian cancer had enlarged paracardiac lymph nodes (>5 mm in diameter). This factor indicates a poor prognosis in terms of survival. Mediastinal adenopathy may also be seen (Fig 21), and metastases in mediastinal lymph nodes have been found in 29% of cases of ovarian cancer at autopsy (47).
Hematogenous Spread
Hematogenous spread was once considered uncommon. However, imaging studies with US or CT, clinical review of large numbers of patients, and autopsy studies have proved that the prevalence of metastases in advanced disease is higher than previously believed (21,22,47,50,52). The reported prevalence of metastases at autopsy is 45%–48% in the liver (Fig 22), 34%–39% in the lung, 15%–21% in the adrenal gland, 11%–21% in the pancreas (Figs 23, 24), 15%–20% in the spleen, 11% in bone and bone marrow (Fig 25), 7%–10% in the kidney, 5% in the skin (Fig 26), and 3%–6% in the brain (Fig 27) (47,50). Rarely, distant metastases are encountered in other locations (Fig 28).
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Figures 22-26. (22) Malignant carcinoid tumor of the ovary. CT scan shows a mass with peripheral enhancement in the right lobe of the liver (arrow), a finding consistent with a liver metastasis. The liver has diffusely decreased attenuation due to fatty infiltration. (23) Endometrioid carcinoma of the ovary. CT scan shows a large metastatic mass (m) in the region of the pancreas that extends to the lesser sac and compresses the stomach (s). The mass also invades the anterior aspect of the left kidney (straight solid arrow). The splenic vein is occluded. There are tumor implants along the undersurface of the right hemidiaphragm (curved arrow), the posterior liver surface, and the fissure for the ligamentum teres (open arrows). Minimal ascites is noted around the liver. (24) Adenocarcinoma of the ovary with psammoma bodies. CT scan shows a large, calcified metastasis that involves the pancreas and displaces the posterior wall of the stomach anteriorly. The splenic vein is occluded. (25) Malignant granulosa cell tumor. The patient developed multiple lytic metastases involving the lumbar spine and pelvis. CT scan shows a lesion in the lumbar spine (arrow) that extends posteriorly through the cortex and effaces the thecal sac. (26) Adenocarcinoma of the ovary. CT scan shows multiple soft-tissue nodules in the subcutaneous tissue and skin of the right gluteal region (open arrows), with an i | |
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Abstract
INTRODUCTION
