DOI: 10.1148/rg.241035178
(Radiographics. 2004;24:225-246.)
From the Archives of the AFIP
Radiologic Staging of Ovarian Carcinoma with Pathologic Correlation1
Paula J. Woodward, MD,
Keyanoosh Hosseinzadeh, MD and
Jeff S. Saenger, MAJ(P), MC, USAR
1 From the Departments of Radiologic Pathology (P.J.W.) and GYN and Breast Pathology (J.S.S.), Armed Forces Institute of Pathology, 14th St at Alaska Ave, Bldg 54, Rm M-121, Washington, DC 20306-6000; and the Department of Diagnostic Radiology, University of Maryland Medical System, Baltimore (K.H.). Received July 31, 2003; revision requested September 10 and received September 30; accepted October 1. All authors have no financial relationships to disclose. Address correspondence to P.J.W. (e-mail: woodwardp@afip.osd.mil).
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Abstract
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Ovarian cancer is the deadliest gynecologic malignancy, with approximately 70% of patients having peritoneal involvement at the time of diagnosis. It spreads predominantly by direct invasion and intraperitoneal dissemination. The staging system is surgically based, with stage I disease being limited to one or both ovaries. In stage II disease, there is extraovarian spread of tumor, but it does not extend beyond the pelvis. Stages III and IV disease are considered advanced, with stage III ovarian cancer including diffuse peritoneal disease involving the upper abdomen and stage IV disease having distant metastases including hepatic lesions. Common sites of intraperitoneal seeding include the omentum, paracolic gutters, liver capsule, and diaphragm. Thickening, nodularity, and enhancement are all signs of peritoneal involvement. Although computed tomography is the most common imaging modality used to stage ovarian cancer, magnetic resonance imaging has been shown to be equally accurate. Currently, however, no imaging modality allows microscopic spread of disease to be ruled out, and a full staging laparotomy is always required. Early ovarian cancer is treated with comprehensive staging laparotomy, whereas advanced but operable disease is treated with primary cytoreductive surgery (debulking) followed by adjuvant chemotherapy. Patients with unresectable disease may benefit from neoadjuvant (preoperative) chemotherapy before debulking.
Index Terms: Ovary, CT, 852.12112 • Ovary, MR, 852.121415 • Ovary, neoplasms, 852.323
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LEARNING OBJECTIVES FOR TEST 6
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After reading this article and taking the test, the reader will be able to:
- Describe the radiologic findings in stages I-IV ovarian carcinoma.
- Differentiate resectable from unresectable disease.
- Discuss the metastatic patterns and types of dissemination of ovarian carcinoma.
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Introduction
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Ovarian carcinoma is an insidious disease, and patients often present with an advanced (extrapelvic) stage of disease. Despite clinical advances and improved surgical techniques, it remains the deadliest form of gynecologic malignancy. Ovarian cancer is the fifth most common cause of death from cancer in women after lung, breast, colon, and pancreatic cancer. In the United States, an estimated 25,400 new cases and 14,300 deaths have been projected for 2003 (1).
Approximately 90% of ovarian cancers arise from the surface epithelium, with the most common histologic types being serous, mucinous, endometrioid, clear cell, and undifferentiated tumors (2). All these tumors carry the same overall poor prognosis when they are metastatic. There is, however, an important histologic subgroup of ovarian carcinomas: tumors of low malignant potential, formerly called borderline tumors. They are usually either mucinous or serous tumors and have a generally good prognosis (3,4). Granulosa cell tumors, dysgerminomas, immature teratomas, endodermal sinus tumors, and metastases constitute the majority of the remaining malignant ovarian tumors (2,5).
The pathogenesis of ovarian cancer is multifactorial. The most significant risk factor is a family history of the disease in which a genetic cause is often implicated. Hereditary causes account for 5%–10% of the total cases (6,7). Patients with hereditary ovarian tumors generally are younger, with most being premenopausal at presentation. Three different hereditary syndromes have been identified. The most common of these is the breast-ovarian cancer syndrome, which has been genetically linked to mutations in the BRCA1 and BRCA2 tumor suppressor genes (6,7). The lifetime risk of developing ovarian cancer for women with this syndrome ranges from 15% to 30%, although some reports have indicated that the risk is as high as 60% (7). Two other hereditary syndromes have also been identified: the site-specific ovarian cancer syndrome and the nonpolyposis colorectal cancer or Lynch syndrome II. The latter syndrome is characterized by early-onset colorectal carcinoma, endometrial cancer, upper gastrointestinal tract cancer, upper urothelial tract cancer, and ovarian cancer (8).
The remaining 90% of ovarian cancer cases are sporadic and occur in a predominantly older, postmenopausal population. One theory set forth regarding a possible cause is "incessant ovulation" (9). The hypothesis suggests that ovulation causes repeated minor trauma and cellular repair of the surface epithelium, which predisposes it to neoplasia. This theory is supported by several epidemiologic observations. Nulliparity, early menarche, and late menopause are all identified as risk factors for ovarian cancer. Conversely, multiparity, late menarche, early menopause, and use of oral contraceptives (ie, fewer ovulation cycles) all are associated with reduced risk (10). This theory may also explain geographic differences in ovarian cancer rates. These rates are greater in more industrialized countries, where women tend to have fewer children, and lower in less modernized countries with higher birth rates (10).
Tumor stage is a major factor in patient prognosis (4). Although the overall 5-year survival rate improved from 37% in 1974 to 53% in 1998, there is large variability depending on the tumor stage at presentation (1). The 5-year survival rate is 80% for stage I disease, 50% for stage II, 30% for stage III, and a dismal 8% for stage IV (3). Multiple other factors that affect prognosis have also been identified, including histologic type, tumor grade, amount of residual disease after the initial cytoreductive surgery (debulking), and patient characteristics (age, performance status) (4).
The radiologist has an integral role in the evaluation of ovarian carcinoma, including detection, mass characterization, and staging. In this article, we focus on this latter role of staging. The importance of accurate staging cannot be overemphasized. Appropriate staging has not only prognostic implications, but it also directly affects management, with some patients benefiting from chemotherapy before surgical debulking. The role of the radiologist is to stage the disease with a high degree of accuracy by evaluating tumor location, volume, and extent. Specifically, factors are sought to guide subspecialty referral, plan treatment, and guide patient management. Herein, we discuss the staging system of ovarian cancer, including patterns of spread; histologic variability; the use of imaging in staging, with emphasis on computed tomography (CT) and magnetic resonance (MR) imaging; and treatment.
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Staging System
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Two staging systems exist: the TNM (tumor, node, metastasis) system and the more commonly used, surgically based system put forth by the International Federation of Obstetrics and Gynecology (FIGO) (11,12). The FIGO staging system is shown in Table 1. Accurate staging necessitates a complete, thorough staging laparotomy, which includes hysterectomy with bilateral salpingo-oophorectomy, pelvic and paraaortic lymph node biopsies, omentectomy, peritoneal biopsies, and washings (13,14).
Understaging is a common problem if a complete staging laparotomy is not performed. In over 30% of patients, ovarian cancer is understaged at initial laparotomy; in 77% of these cases, the tumor was thought to be confined to the pelvis but subsequently proved to be stage III disease when a full staging procedure was performed (15). Incorrect staging has obvious implications for the patient and results in erroneous counseling about treatment and prognosis. Sites of unsuspected disease most often included the pelvic peritoneum and tissues, ascitic fluid, paraaortic nodes, and diaphragm (15). In a review of surgical practices, it was found that 92% of gynecologic oncologists performed a complete staging procedure, in contrast to only 52% of obstetricians-gynecologists and 35% of general surgeons who performed an adequate evaluation (16).
Patterns of Spread
To understand the radiologic findings in each of the stages, it is important to have a thorough understanding of the mechanism of tumor spread. Ovarian carcinoma may spread through direct extension to surrounding pelvic tissues. The fallopian tubes, uterus, and contralateral adnexa are the most commonly involved tissues, but the rectum, bladder, and pelvic sidewall can also be directly invaded (14). Tumor may also metastasize beyond the pelvis through three mechanisms: intraperitoneal seeding, lymphatic invasion, and hematogenous dissemination.
Intraperitoneal dissemination is the most common mode of tumor spread in ovarian cancer, with approximately 70% of patients having peritoneal metastases at staging laparotomy. The three most commonly involved sites found at laparotomy are the greater omentum, right subphrenic region, and pouch of Douglas (17). Peritoneal seeding occurs when malignant cells are shed from the tumor surface into the peritoneal cavity, where they follow normal routes of peritoneal fluid circulation. Shed tumor cells often first implant in the cul-de-sac and other dependent portions of the pelvis. Fluid then flows along the paracolic gutters to the diaphragm (18). There is preferential flow and subsequent tumor seeding along the right paracolic gutter, liver capsule, and diaphragm (19). Fluid then normally drains through the rich lymphatic capillary network of the diaphragm to the anterior mediastinal nodes (20). These diaphragmatic lymphatics may become occluded by tumor cells, thus blocking absorption of peritoneal fluid and contributing to the accumulation of malignant ascites.
Ovarian cancer may also metastasize through the lymphatic system. The ovaries have three pathways of lymphatic drainage. The main lymphatics follow the ovarian veins to the paraaortic and paracaval nodes at the level of the renal hilum. This area is the most common site for metastatic adenopathy. Lymph vessels also pass through the broad ligament to involve the pelvic lymph nodes, including the external iliac, hypogastric, and obturator chain and along the round ligament to the inguinal nodes (21,22).
Hematogenous dissemination is the least common mode of tumor spread in ovarian cancer. Hematogenous metastases are usually not present at the time of initial diagnosis but can be the site of recurrent disease and have been reported in up to 50% of patients at autopsy (22–24). The most common sites of involvement are the liver followed by the lung, but other locations including the brain, bone, adrenal gland, kidney, and spleen have all been reported (22–24).
Stage I
In stage I disease, the tumor is limited to either one (stage IA) or both (stage IB) ovaries (Figs 1, 2). The capsule is intact, and there has been no spread of tumor to the ovarian surface. In stage IC disease, malignant ascites may be present with histologic evidence of tumor on the ovarian surface or capsule rupture.
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Figure 2a. Stage IA ovarian carcinoma. (a) Transverse ultrasonographic (US) image of the left ovary (cursors) shows a complex left ovarian mass with both cystic and solid components. (b) Intraoperative photograph shows the enlarged left ovary (arrow) posterior to the uterus. The capsule was intact, and there was no intraperitoneal spread of disease.
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Figure 2b. Stage IA ovarian carcinoma. (a) Transverse ultrasonographic (US) image of the left ovary (cursors) shows a complex left ovarian mass with both cystic and solid components. (b) Intraoperative photograph shows the enlarged left ovary (arrow) posterior to the uterus. The capsule was intact, and there was no intraperitoneal spread of disease.
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Although ascites may represent stage I disease, when present it should be viewed with great caution. In a recent study by Coakley et al (25), the presence of ascites had a positive predictive value of 72%–80% as a sign of peritoneal metastases. Ascites is a common finding in ovarian cancer patients and results from either increased production with "weeping" of fluid from the tumor surface or decreased resorption. It is this latter mechanism, caused by invasion and blockage of the diaphragmatic lymphatics by tumor cells, that is thought to be the most important (2,20) (Fig 3). If ascites is present, there should always be concern that the diaphragmatic lymphatics are involved, which would be stage III disease. Biopsies along the diaphragm would be imperative at the time of staging laparotomy.
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Figure 3a. Ascites in a patient with ovarian cancer. (a) Axial CT scan shows marked ascites and serosal implants on the bowel (arrows). (b) Photograph of cut autopsy specimens of the diaphragm shows confluent, tan deposits of tumor along the inferior margin (arrows) that occluded lymphatic transport of fluid.
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Figure 3b. Ascites in a patient with ovarian cancer. (a) Axial CT scan shows marked ascites and serosal implants on the bowel (arrows). (b) Photograph of cut autopsy specimens of the diaphragm shows confluent, tan deposits of tumor along the inferior margin (arrows) that occluded lymphatic transport of fluid.
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Stage II
Stage II disease is characterized by local extension of tumor to involve surrounding organs. Spread of tumor is confined to the pelvis without upper abdominal involvement. In stage IIA disease, there is either direct extension or implants on the uterus or fallopian tubes. With stage IIB disease, there is further local extension to involve surrounding pelvic tissues including the rectum, bladder, and peritoneum (Fig 4). Findings that suggest local extension of tumor include distortion or irregularity between the tumor and the myometrium, obscuration of tissue planes with either the bladder or colon, less than 3 mm between the tumor and pelvic sidewall, and displacement or encasement of iliac vessels (26) (Figs 5–7). Direct invasion is often easier to identify with MR imaging than with either CT or US because of its superior soft-tissue contrast (26).
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Figure 5a. Local spread of ovarian carcinoma in a 77-year-old woman. (a) Transverse US image through the pelvis shows an enlarged, predominantly solid left ovary (arrow). (b) Axial CT image shows an irregular interface between the left ovary and the uterus (black arrow), a finding that suggests direct invasion. Irregular nodularity seen in the surrounding soft tissues (curved arrow) and a small amount of ascites (straight white arrow) are suggestive of stage IIC or higher disease. (c) Photograph of the uterus shows extensive implants involving the serosal surface (cf the normal uterine serosal surface in Fig 2). (d) Low-power photomicrograph (original magnification, x2; hematoxylin-eosin stain) of serous papillary carcinoma involving the paratubal and paraovarian soft tissues shows a prominent papillary growth pattern lined by cytologically malignant serous epithelium with destructive stromal invasion. The fallopian tube is seen in cross section (arrow).
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Figure 5b. Local spread of ovarian carcinoma in a 77-year-old woman. (a) Transverse US image through the pelvis shows an enlarged, predominantly solid left ovary (arrow). (b) Axial CT image shows an irregular interface between the left ovary and the uterus (black arrow), a finding that suggests direct invasion. Irregular nodularity seen in the surrounding soft tissues (curved arrow) and a small amount of ascites (straight white arrow) are suggestive of stage IIC or higher disease. (c) Photograph of the uterus shows extensive implants involving the serosal surface (cf the normal uterine serosal surface in Fig 2). (d) Low-power photomicrograph (original magnification, x2; hematoxylin-eosin stain) of serous papillary carcinoma involving the paratubal and paraovarian soft tissues shows a prominent papillary growth pattern lined by cytologically malignant serous epithelium with destructive stromal invasion. The fallopian tube is seen in cross section (arrow).
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Figure 5c. Local spread of ovarian carcinoma in a 77-year-old woman. (a) Transverse US image through the pelvis shows an enlarged, predominantly solid left ovary (arrow). (b) Axial CT image shows an irregular interface between the left ovary and the uterus (black arrow), a finding that suggests direct invasion. Irregular nodularity seen in the surrounding soft tissues (curved arrow) and a small amount of ascites (straight white arrow) are suggestive of stage IIC or higher disease. (c) Photograph of the uterus shows extensive implants involving the serosal surface (cf the normal uterine serosal surface in Fig 2). (d) Low-power photomicrograph (original magnification, x2; hematoxylin-eosin stain) of serous papillary carcinoma involving the paratubal and paraovarian soft tissues shows a prominent papillary growth pattern lined by cytologically malignant serous epithelium with destructive stromal invasion. The fallopian tube is seen in cross section (arrow).
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Figure 5d. Local spread of ovarian carcinoma in a 77-year-old woman. (a) Transverse US image through the pelvis shows an enlarged, predominantly solid left ovary (arrow). (b) Axial CT image shows an irregular interface between the left ovary and the uterus (black arrow), a finding that suggests direct invasion. Irregular nodularity seen in the surrounding soft tissues (curved arrow) and a small amount of ascites (straight white arrow) are suggestive of stage IIC or higher disease. (c) Photograph of the uterus shows extensive implants involving the serosal surface (cf the normal uterine serosal surface in Fig 2). (d) Low-power photomicrograph (original magnification, x2; hematoxylin-eosin stain) of serous papillary carcinoma involving the paratubal and paraovarian soft tissues shows a prominent papillary growth pattern lined by cytologically malignant serous epithelium with destructive stromal invasion. The fallopian tube is seen in cross section (arrow).
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Figure 6a. Direct uterine invasion. (a, b) Axial T2-weighted MR images show a complex, mixed cystic and solid mass of the ovary (a), which has invaded the myometrium (arrows) (b). (c) Photograph of the uterus shows irregular thickening of the myometrium in the area of invasion (arrow).
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Figure 6b. Direct uterine invasion. (a, b) Axial T2-weighted MR images show a complex, mixed cystic and solid mass of the ovary (a), which has invaded the myometrium (arrows) (b). (c) Photograph of the uterus shows irregular thickening of the myometrium in the area of invasion (arrow).
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Figure 6c. Direct uterine invasion. (a, b) Axial T2-weighted MR images show a complex, mixed cystic and solid mass of the ovary (a), which has invaded the myometrium (arrows) (b). (c) Photograph of the uterus shows irregular thickening of the myometrium in the area of invasion (arrow).
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Figure 7. Bilateral serous cystadenocarcinomas with encasement of the right external iliac vessels. Axial CT image shows the irregular interface between the tumor and the vessels (white arrow) and the extension to the opposite side (black arrow), indicating encasement.
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Stage III
Stage III disease is defined by the spread of tumor outside the pelvis and requires the recognition of peritoneal, omental, and mesenteric implants (Fig 8). Peritoneal disease may be microscopic or small (stage IIIA or IIIB) and therefore undetectable with imaging (Fig 9). It is important to recognize that radiologically occult disease may be present, and a "limited" surgical procedure is never indicated when metastases are not detected on images.
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Figure 8. Drawing illustrates stage III ovarian carcinoma. Metastases may be on the liver capsule (peritoneal seeding) but not within the parenchyma (hematogenous metastases). (Adapted from reference 12.)
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Figure 9a. (a) Low-power photomicrograph (original magnification, x4; hematoxylin-eosin stain) of an omental biopsy specimen shows a noninvasive implant from a serous tumor of low malignant potential. Psammoma bodies (arrows) are present within the fibrous bands that track between adipose lobules. (b) Photograph of a surgical specimen shows small omental implants from clear cell carcinoma (arrows). These examples represent clinically important disease that would be difficult or impossible to detect with imaging.
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Figure 9b. (a) Low-power photomicrograph (original magnification, x4; hematoxylin-eosin stain) of an omental biopsy specimen shows a noninvasive implant from a serous tumor of low malignant potential. Psammoma bodies (arrows) are present within the fibrous bands that track between adipose lobules. (b) Photograph of a surgical specimen shows small omental implants from clear cell carcinoma (arrows). These examples represent clinically important disease that would be difficult or impossible to detect with imaging.
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Great care must be taken in searching for subtle thickening, nodularity, or enhancement along peritoneal surfaces that may indicate metastatic involvement (25). As previously mentioned, the presence of ascites is suggestive of peritoneal disease. When present, ascites aids in lesion conspicuity (27) (Fig 10). The omentum is the most common site of peritoneal spread of tumor (28). This involvement may be microscopic, however. In a pathologic review, 22% of omenta that appeared normal at gross inspection had histologically proved tumor (29). Because of the propensity for tumor spread in this area, the omentum should be scrutinized closely in imaging examinations. The radiologic appearance of omental involvement may begin as a subtle, fine reticulonodular pattern (Fig 11). Later in the disease course, there is often marked thickening (omental cake) (Fig 12). In addition to the omentum, other common sites of involvement should be carefully evaluated, including the subphrenic space, mesentery, and paracolic gutters (28).
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Figure 10a. Stage III endometrioid carcinoma. (a, b) Axial CT images through the upper abdomen (a at a higher level than b) show multiple implants along the diaphragm (curved arrow) and liver capsule (straight arrows). Note how visualization and tumor localization is aided by the presence of ascites. (c) Axial CT image through the pelvis shows more peritoneal involvement (arrows) and bilateral ovarian tumors.
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Figure 10b. Stage III endometrioid carcinoma. (a, b) Axial CT images through the upper abdomen (a at a higher level than b) show multiple implants along the diaphragm (curved arrow) and liver capsule (straight arrows). Note how visualization and tumor localization is aided by the presence of ascites. (c) Axial CT image through the pelvis shows more peritoneal involvement (arrows) and bilateral ovarian tumors.
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Figure 10c. Stage III endometrioid carcinoma. (a, b) Axial CT images through the upper abdomen (a at a higher level than b) show multiple implants along the diaphragm (curved arrow) and liver capsule (straight arrows). Note how visualization and tumor localization is aided by the presence of ascites. (c) Axial CT image through the pelvis shows more peritoneal involvement (arrows) and bilateral ovarian tumors.
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Figure 11a. Stage III ovarian carcinoma. (a) Axial CT image shows a fine reticulonodular pattern of the omentum (curved arrow) and an abnormally thickened, nodular loop of bowel (straight arrow). (b) Photograph of serial sections taken through the omentum shows multiple firm, tan, metastatic nodules. (c) Photograph of the resected small bowel loop, which was described as "stiff and leathery," demonstrates the irregular, "shaggy" appearance of the serosal surface, secondary to studding with tumor implants (arrows).
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Figure 11b. Stage III ovarian carcinoma. (a) Axial CT image shows a fine reticulonodular pattern of the omentum (curved arrow) and an abnormally thickened, nodular loop of bowel (straight arrow). (b) Photograph of serial sections taken through the omentum shows multiple firm, tan, metastatic nodules. (c) Photograph of the resected small bowel loop, which was described as "stiff and leathery," demonstrates the irregular, "shaggy" appearance of the serosal surface, secondary to studding with tumor implants (arrows).
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Figure 11c. Stage III ovarian carcinoma. (a) Axial CT image shows a fine reticulonodular pattern of the omentum (curved arrow) and an abnormally thickened, nodular loop of bowel (straight arrow). (b) Photograph of serial sections taken through the omentum shows multiple firm, tan, metastatic nodules. (c) Photograph of the resected small bowel loop, which was described as "stiff and leathery," demonstrates the irregular, "shaggy" appearance of the serosal surface, secondary to studding with tumor implants (arrows).
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Figure 12. Axial CT image shows marked thickening of the omentum referred to as "omental cake" (white arrow). Also note thickening along the peritoneum and mesentery (black arrows).
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Gastrointestinal involvement, particularly of the small bowel, is common. There may be serosal implants or frank wall invasion. Bowel obstruction is an important cause of morbidity in ovarian cancer patients and has been noted in approximately 50% of cases at autopsy (23). Although bowel obstruction may be from serosal metastases or associated adhesions, it is most commonly seen when the intestinal wall is invaded (23). Radiologic findings suggesting bowel involvement include thickening and distortion (25) (Fig 11).
Stage IV
In stage IV disease, there is distant spread of tumor, which includes any tumor outside the pelvis except for peritoneal spread (ie, hematogenous metastases to solid organs including the liver) (Fig 13). It is important to distinguish implants on the liver capsule (stage III) from true parenchymal metastases (stage IV) because they have very different implications with regard to prognosis and treatment. Capsular implants are still considered resectable, whereas parenchymal metastases generally are not. Capsular masses are usually smooth, are well defined, and have an elliptic or biconvex appearance. They may extend along the falciform ligament and potentially be mistaken for parenchymal metastases. True parenchymal metastases are much less well defined and are surrounded by liver parenchyma (Fig 14).
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Figure 14a. Hepatic metastases from stage III versus stage IV ovarian carcinoma. (a) Axial CT image of stage III disease shows multiple, biconvex low-attenuation masses along the capsule of the liver. Some extend along the expected course of the falciform ligament (arrow), a finding that could be confused with intraparenchymal metastases. There is also a small implant on the spleen (arrowhead). (b) Axial CT image shows obvious intraparenchymal liver metastases, representing stage IV disease.
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Figure 14b. Hepatic metastases from stage III versus stage IV ovarian carcinoma. (a) Axial CT image of stage III disease shows multiple, biconvex low-attenuation masses along the capsule of the liver. Some extend along the expected course of the falciform ligament (arrow), a finding that could be confused with intraparenchymal metastases. There is also a small implant on the spleen (arrowhead). (b) Axial CT image shows obvious intraparenchymal liver metastases, representing stage IV disease.
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The most common finding of stage IV disease is a malignant pleural effusion (30). However, an effusion alone is not sufficient for the designation of stage IV disease and cytologic evaluation is required. If pleural masses, nodularity, or thickening is identified, the likelihood of stage IV disease is extremely high (Fig 15).
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Figure 15a. Stage IV ovarian cancer. (a) Longitudinal US image through the midline of the pelvis shows a large, complex, cystic ovarian mass. Curved arrow = uterus. (b) Longitudinal US image of the right paracolic gutter demonstrates several peritoneal implants (arrows). (c) Axial US image at the level of the right hemidiaphragm shows multiple solid pleural masses (arrow) and an effusion.
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Figure 15b. Stage IV ovarian cancer. (a) Longitudinal US image through the midline of the pelvis shows a large, complex, cystic ovarian mass. Curved arrow = uterus. (b) Longitudinal US image of the right paracolic gutter demonstrates several peritoneal implants (arrows). (c) Axial US image at the level of the right hemidiaphragm shows multiple solid pleural masses (arrow) and an effusion.
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Figure 15c. Stage IV ovarian cancer. (a) Longitudinal US image through the midline of the pelvis shows a large, complex, cystic ovarian mass. Curved arrow = uterus. (b) Longitudinal US image of the right paracolic gutter demonstrates several peritoneal implants (arrows). (c) Axial US image at the level of the right hemidiaphragm shows multiple solid pleural masses (arrow) and an effusion.
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Histologic Variability
Although the appearance of metastatic ovarian carcinoma is generally as described, there are a few variations according to histologic type that are important to know when interpreting the examination. Serous cystadenocarcinoma is the most common histologic type of ovarian cancer. As a primary tumor, it may be either unilocular or septated and is filled with thin serous fluid (3,21,31). These tumors often contain microcalcifications known as psammoma bodies, which may be visible on CT scans. Peritoneal calcification has been reported in 33% of cases of metastatic serous tumors (32) (Fig 16). Careful evaluation for calcification along peritoneal surfaces should be performed in every case.
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Figure 16a. Stage III serous cystadenocarcinoma. (a-c) Axial CT images (obtained at successively lower levels) show diffuse calcifications of peritoneal metastases, including those in a prominent omental cake (arrow in b). (d) Medium-power photomicrograph (original magnification, x10; hematoxylin-eosin stain) shows a noninvasive omental implant with prominent dark purple-staining psammoma bodies (cf Fig 9a).
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Figure 16b. Stage III serous cystadenocarcinoma. (a-c) Axial CT images (obtained at successively lower levels) show diffuse calcifications of peritoneal metastases, including those in a prominent omental cake (arrow in b). (d) Medium-power photomicrograph (original magnification, x10; hematoxylin-eosin stain) shows a noninvasive omental implant with prominent dark purple-staining psammoma bodies (cf Fig 9a).
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Figure 16c. Stage III serous cystadenocarcinoma. (a-c) Axial CT images (obtained at successively lower levels) show diffuse calcifications of peritoneal metastases, including those in a prominent omental cake (arrow in b). (d) Medium-power photomicrograph (original magnification, x10; hematoxylin-eosin stain) shows a noninvasive omental implant with prominent dark purple-staining psammoma bodies (cf Fig 9a).
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Figure 16d. Stage III serous cystadenocarcinoma. (a-c) Axial CT images (obtained at successively lower levels) show diffuse calcifications of peritoneal metastases, including those in a prominent omental cake (arrow in b). (d) Medium-power photomicrograph (original magnification, x10; hematoxylin-eosin stain) shows a noninvasive omental implant with prominent dark purple-staining psammoma bodies (cf Fig 9a).
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Mucinous tumors are more often multilocular, and the mucoid material within some of these loculi may appear as low-level echoes on US images, high attenuation on CT scans, and increased signal intensity on T1-weighted MR images (Fig 17) (3,31). Mucinous peritoneal implants generally have low attenuation on CT scans and do not calcify. Pseudomyxoma peritonei is another potential form of peritoneal spread described for mucinous ovarian tumors. It is characterized by amorphous, mucoid material that insinuates itself around and in between the mesenteric reflections, bowel, and solid organs (3). The low attenuation and diffuse nature of this process may be confused with ascites. Unlike simple ascites, however, pseudomyxoma peritonei has mass effect and causes scalloping along the liver capsule and abdominal organs. Bowel loops are matted posteriorly, rather than free floating, and subtle septations may be noted (Fig 18). The gelatinous, insinuating nature of this material makes complete resection difficult, and multiple laparotomies are often required. It is important to be aware that current thinking about the origin of pseudomyxoma peritonei has changed. It is now recognized that in the vast majority of cases the primary tumor is actually from the appendix with metastases to the ovary, rather than being a primary ovarian tumor (33,34). In every case of pseudomyxoma peritonei, the appendix should be thoroughly examined and special tissue testing done to differentiate pseudomyxoma peritonei of gastrointestinal origin from ovarian origin.
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Figure 17a. Mucinous tumor of low malignant potential. (a) Longitudinal US image of the abdomen demonstrates a large cystic mass with multiple loculi of varying echogenicities. (b) Axial CT scan shows a massive tumor filling the abdomen with loculi of varying attenuation.
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Figure 17b. Mucinous tumor of low malignant potential. (a) Longitudinal US image of the abdomen demonstrates a large cystic mass with multiple loculi of varying echogenicities. (b) Axial CT scan shows a massive tumor filling the abdomen with loculi of varying attenuation.
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Figure 18a. Pseudomyxoma peritonei. (a, b) Axial CT images show low-attenuation material throughout the abdomen, with mass effect and distortion and scalloping of the liver margin, particularly involving the left lobe (arrows in a). The bowel is matted posteriorly, and there are subtle septations (arrows in b). (c) Intraoperative photograph shows thick, gelatinous material exuding from the incision site. (d) Medium-power photomicrograph (original magnification, x40; hematoxylin-eosin stain) shows pools of acellular mucin dissecting through bands of fibrous tissue, an appearance compatible with the clinical diagnosis of pseudomyxoma peritonei.
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Figure 18b. Pseudomyxoma peritonei. (a, b) Axial CT images show low-attenuation material throughout the abdomen, with mass effect and distortion and scalloping of the liver margin, particularly involving the left lobe (arrows in a). The bowel is matted posteriorly, and there are subtle septations (arrows in b). (c) Intraoperative photograph shows thick, gelatinous material exuding from the incision site. (d) Medium-power photomicrograph (original magnification, x40; hematoxylin-eosin stain) shows pools of acellular mucin dissecting through bands of fibrous tissue, an appearance compatible with the clinical diagnosis of pseudomyxoma peritonei.
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Figure 18c. Pseudomyxoma peritonei. (a, b) Axial CT images show low-attenuation material throughout the abdomen, with mass effect and distortion and scalloping of the liver margin, particularly involving the left lobe (arrows in a). The bowel is matted posteriorly, and there are subtle septations (arrows in b). (c) Intraoperative photograph shows thick, gelatinous material exuding from the incision site. (d) Medium-power photomicrograph (original magnification, x40; hematoxylin-eosin stain) shows pools of acellular mucin dissecting through bands of fibrous tissue, an appearance compatible with the clinical diagnosis of pseudomyxoma peritonei.
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Figure 18d. Pseudomyxoma peritonei. (a, b) Axial CT images show low-attenuation material throughout the abdomen, with mass effect and distortion and scalloping of the liver margin, particularly involving the left lobe (arrows in a). The bowel is matted posteriorly, and there are subtle septations (arrows in b). (c) Intraoperative photograph shows thick, gelatinous material exuding from the incision site. (d) Medium-power photomicrograph (original magnification, x40; hematoxylin-eosin stain) shows pools of acellular mucin dissecting through bands of fibrous tissue, an appearance compatible with the clinical diagnosis of pseudomyxoma peritonei.
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Although retroperitoneal adenopathy has been reported in 27%–44% of patients with stage III disease (28,35,36), peritoneal metastases usually predominate. Occasionally, this pattern can be reversed. A disproportionate amount of nodal disease, in comparison with peritoneal involvement, has been described in cases of poorly differentiated adenocarcinoma and dysgerminoma (Fig 19) (5).
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Figure 19a. Poorly differentiated adenocarcinoma. (a) Axial CT scan through the pelvis shows bilateral ovarian masses. (b) Axial CT image through the level of the kidneys shows significant retroperitoneal adenopathy (arrow) but no obvious intraperitoneal disease.
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Figure 19b. Poorly differentiated adenocarcinoma. (a) Axial CT scan through the pelvis shows bilateral ovarian masses. (b) Axial CT image through the level of the kidneys shows significant retroperitoneal adenopathy (arrow) but no obvious intraperitoneal disease.
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Other primary tumors may manifest with peritoneal carcinomatosis and potentially may be confused with metastatic ovarian carcinoma. Approximately 17% of gastric cancer cases and 10% of colorectal cancer cases have peritoneal metastases at the time of presentation (25). Once tumor cells spread within the peritoneal cavity, metastatic involvement of the ovaries may occur and could potentially be mistaken for a primary ovarian tumor. The gastrointestinal tract should be carefully reviewed as a potential site of primary tumor in patients with peritoneal metastases. Mesothelioma and papillary serous carcinoma of the peritoneum may also have a similar appearance (5). Benign mimics of peritoneal carcinomatosis are rare, but in the right clinical setting infectious or inflammatory processes should be considered, particularly tuberculous peritonitis (25).
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Imaging: Goals, Techniques, and Accuracy
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The goals of imaging that are critical to patient management are (a) detection of metastatic disease to prevent understaging and (b) identification of disease that can complicate primary surgical debulking or is unresectable. Although variations between institutions exist, factors that generally indicate inoperable disease include the following: (a) invasion of the pelvic sidewall, rectum, sigmoid colon, or bladder; (b) tumor deposits greater than 1–2 cm in the porta hepatis, intersegmental fissure of the liver, lesser sac, gastrosplenic ligament, gastrohepatic ligament, subphrenic space, root of mesentery, and presacral space; (c) suprarenal adenopathy; and (d) hepatic (parenchymal), pleural, or pulmonary metastases (26,37–39). Patients with bulky, unresectable disease may benefit from chemotherapy before cytoreductive surgery.
Ultrasonography
US has a well-defined, important role in the initial evaluation of a suspected adnexal mass (40,41). Its use in evaluating peritoneal implants has been described, but its role in staging ovarian cancer is limited. US is operator dependent, and a thorough search of all peritoneal surfaces requires meticulous technique (42,43). Bowel gas, poor soft-tissue contrast, and other technical factors make a complete evaluation of all possible areas of involvement difficult, even when meticulous technique is used. Tempany et al (28) found that in patients with advanced cancer (stages III and IV), the sensitivity of Doppler US in the detection of peritoneal metastases was 69%, compared with 95% for MR imaging, and 92% for spiral CT. MR imaging and CT were superior to US, especially in evaluation of the subdiaphragmatic and hepatic surfaces. Although US demonstrated high specificity, CT and MR imaging were equally accurate and recommended for the staging of ovarian cancer.
Computed Tomography
CT is the primary modality used for staging ovarian cancer. The CT examination should be tailored to evaluate the primary tumor site, potential sites of peritoneal implants, lymphadenopathy, and solid organs. Several early studies have addressed the value of CT in preoperative staging of ovarian cancer with reported accuracies of 70%–90% (26,44–47).
Intraperitoneal dissemination is the most common route of spread in ovarian carcinoma, and an assessment of peritoneal involvement is a critical part of the imaging examination. In studies of conventional (not spiral) contrast material–enhanced CT, CT had sensitivities of 63%–79% in the detection of peritoneal involvement (17, 48,49). In the largest study to date, the Radiology Diagnostic Oncology Group performed a 3-year, five-institution prospective study of 280 patients with ovarian masses. The authors examined the group of patients with advanced disease (stages III and IV) and reported that CT had a sensitivity of 92% and specificity of 82% in the detection of peritoneal metastases (28). All examinations were performed with spiral CT technique and included 5-mm-thick sections at 8–10-mm intervals.
A more recent study in which 64 patients were examined with spiral CT demonstrated that CT had an overall sensitivity of 85%–93% and specificity of 91%–96% in the detection of peritoneal metastasis outside the pelvis (25). All scans were performed spirally, with section collimation ranging from 5 to 10 mm, with 10-mm collimation used in 34% of patients. The improved detection of peritoneal implants is related to increasing use of thinner sections and absence of section misregistration artifact. However, implants less than 1 cm were difficult to detect, and the reader sensitivity in the detection of implants ranged from 25% to 50%. It is important to note that a positive imaging-based diagnosis of peritoneal metastases remains clinically more useful than a negative result.
The use of orally administered contrast agents is generally recommended. Opacification of the gastrointestinal tract helps one differentiate bowel from serosal and mesenteric implants, which is a major advantage of CT over MR imaging and US (Fig 20). Use of contrast material also allows differentiation of fluid-filled bowel from cystic ovarian masses. It is important to note, however, that calcified metastases may potentially be obscured by contrast enhancement (Fig 21). Some authors have suggested that water be used as a contrast agent (50). Ideally, one should tailor the examination to the individual patient.
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Figure 20. Metastatic mucinous cystadenocarcinoma. Axial CT image obtained after administration of intravenous and oral contrast material shows a low-attenuation mass on the serosal surface of the ileum (arrowhead) as well as thickening along the peritoneal surface (arrows). Without adequate bowel opacification, the serosal implant could be easily missed.
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Figure 21. Metastatic serous adenocarcinoma. Unenhanced axial CT image shows calcified serosal (arrows) and mesenteric (arrowhead) implants. These metastases could be potentially obscured if an oral contrast agent had been given.
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In most patients, imaging of the abdomen is performed before that of the pelvis, which will optimize enhancement of the solid organs. Early spiral imaging can be initiated through the abdomen after intravenous bolus administration of contrast material to optimize imaging dynamics of the liver and other solid organs; after a delay of 90–120 seconds (to optimize venous enhancement to differentiate lymph nodes from iliac vessels), imaging is performed through the pelvis (21). De
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Abstract
LEARNING OBJECTIVES FOR TEST...
