RadioGraphics
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


DOI: 10.1148/rg.241035178
This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow CME Test (opens in a new window)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Woodward, P. J.
Right arrow Articles by Saenger, J. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Woodward, P. J.
Right arrow Articles by Saenger, J. S.
Related Collections
Right arrow Obstetric/Gynecologic Radiology
Right arrow Genitourinary Radiology
(Radiographics. 2004;24:225-246.)


AFIP ARCHIVES

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).


    Abstract
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
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


    LEARNING OBJECTIVES FOR TEST 6
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
After reading this article and taking the test, the reader will be able to:


    Introduction
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
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.


    Staging System
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
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).


View this table:
[in this window]
[in a new window]

 
TABLE 1. FIGO Staging of Ovarian Carcinoma

 
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 (2224). 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 (2224).

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.



View larger version (95K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 1a.  Diagrams illustrate stage IA (a) and stage IB (b) ovarian carcinoma. (Adapted from reference 12.)

 


View larger version (94K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 1b.  Diagrams illustrate stage IA (a) and stage IB (b) ovarian carcinoma. (Adapted from reference 12.)

 


View larger version (163K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (124K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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.



View larger version (158K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (82K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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 57). Direct invasion is often easier to identify with MR imaging than with either CT or US because of its superior soft-tissue contrast (26).



View larger version (95K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 4a.  Drawings illustrate stage IIA (a) and stage IIB (b) ovarian cancer. (Adapted from reference 12.)

 


View larger version (88K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 4b.  Drawings illustrate stage IIA (a) and stage IIB (b) ovarian cancer. (Adapted from reference 12.)

 


View larger version (167K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (157K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (114K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (152K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (153K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (150K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (116K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (128K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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.



View larger version (64K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.)

 


View larger version (143K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (115K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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).



View larger version (130K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (132K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (124K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (151K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (134K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (60K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (163K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 
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).



View larger version (68K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 13.  Drawing illustrates stage IV ovarian carcinoma. There are distant metastases present, including in the hepatic parenchyma. (Adapted from reference 12.)

 


View larger version (107K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (116K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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).



View larger version (164K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (141K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (151K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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.



View larger version (152K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (169K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (154K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 


View larger version (195K):
[in this window]
[in a new window]
[Download PPT slide]
 
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).

 
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.



View larger version (140K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (127K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (120K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (136K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (116K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (157K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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).



View larger version (158K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (163K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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).


    Imaging: Goals, Techniques, and Accuracy
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
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 (26,3739). 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% (26,4447).

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.



View larger version (162K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 


View larger version (145K):
[in this window]
[in a new window]
[Download PPT slide]
 
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.

 
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). Delayed imaging after bladder enhancement will avoid the pitfall of mistaking a fluid collection or cystic ovarian mass from an unenhanced fluid-filled bladder (51,52). Thinner (3–5 mm) collimation is useful for accurate staging.

A challenging area to evaluate with CT is along the hemidiaphragms, where the deposits may be plaquelike or of minimal nodularity and parallel to the axial plane. The advent of multidetector CT has allowed the routine acquisition of 1–3-mm-thick sections over large volumes. These data can then be manipulated in an interactive display of data in multiple planes. Use of this technique has the potential to improve CT evaluation of local extension of disease. Small lesions are more easily detected with coronal or sagittal reformatted images, which are obtained with fewer artifacts with multidetector CT (50).

MR Imaging
Although CT is the primary modality used in the evaluation of ovarian cancer metastasis, MR imaging has staging accuracy similar to that of both conventional (26) and spiral (53) CT. The literature has well established that MR imaging provides excellent tissue characterization, and MR imaging has demonstrated superiority to both Doppler US and contrast-enhanced CT in accurate characterization of adnexal masses (53). Because of the superior soft-tissue contrast available with MR imaging, invasion of pelvic organs is often more easily evaluated with MR imaging than with CT (cf Fig 5 and Fig 6) (26).

In patients with advanced disease (stages III and IV), there is no statistical difference in accuracy between MR imaging and spiral CT in the determination of the location, distribution, and size of peritoneal implants (28). In a small-scale study, MR imaging demonstrated improved visualization of small or equivocal peritoneal implants compared with spiral CT (54). MR imaging is often helpful in cases without ascites, when detection with CT is difficult (Fig 22). These studies illustrate the ability of MR imaging to demonstrate peritoneal disease even without use of an orally administered contrast agent. Oral contrast material composed of dilute barium can be administered, providing negative intraluminal contrast on T1-weighted images. Preliminary work in which use of dilute barium and intravenous contrast-enhanced MR imaging were compared with conventional and spiral CT showed that use of MR imaging resulted in improved detection of serosal and omental implants (55,56). Tumors less than 1 cm in diameter were better detected with double-contrast MR imaging than with CT (55,56).



View larger version (114K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 22a.  Implant on the liver capsule. (a) Axial CT scan shows a subtle low-attenuation area along the liver capsule (arrow). This finding could not be differentiated from a prominent diaphragmatic slip. (b) Axial T2-weighted, fat-suppressed MR image of the same area shows an obvious high-signal-intensity mass (arrow). (c) Axial gadolinium-enhanced, T1-weighted, fat-suppressed MR image demonstrates enhancement of the mass (arrow). (d) FDG PET images in the axial, sagittal, and coronal planes show uptake within the metastatic implant (arrow).

 


View larger version (137K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 22b.  Implant on the liver capsule. (a) Axial CT scan shows a subtle low-attenuation area along the liver capsule (arrow). This finding could not be differentiated from a prominent diaphragmatic slip. (b) Axial T2-weighted, fat-suppressed MR image of the same area shows an obvious high-signal-intensity mass (arrow). (c) Axial gadolinium-enhanced, T1-weighted, fat-suppressed MR image demonstrates enhancement of the mass (arrow). (d) FDG PET images in the axial, sagittal, and coronal planes show uptake within the metastatic implant (arrow).

 


View larger version (121K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 22c.  Implant on the liver capsule. (a) Axial CT scan shows a subtle low-attenuation area along the liver capsule (arrow). This finding could not be differentiated from a prominent diaphragmatic slip. (b) Axial T2-weighted, fat-suppressed MR image of the same area shows an obvious high-signal-intensity mass (arrow). (c) Axial gadolinium-enhanced, T1-weighted, fat-suppressed MR image demonstrates enhancement of the mass (arrow). (d) FDG PET images in the axial, sagittal, and coronal planes show uptake within the metastatic implant (arrow).

 


View larger version (23K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 22d.  Implant on the liver capsule. (a) Axial CT scan shows a subtle low-attenuation area along the liver capsule (arrow). This finding could not be differentiated from a prominent diaphragmatic slip. (b) Axial T2-weighted, fat-suppressed MR image of the same area shows an obvious high-signal-intensity mass (arrow). (c) Axial gadolinium-enhanced, T1-weighted, fat-suppressed MR image demonstrates enhancement of the mass (arrow). (d) FDG PET images in the axial, sagittal, and coronal planes show uptake within the metastatic implant (arrow).

 
All patients should undergo imaging of both the pelvis and abdomen. Use of a high-field-strength magnet and a phased-array coil is recommended whenever possible for imaging of the pelvis to maximize signal-to-noise and in-plane image resolution. Fasting for 3 hours before the study has been recommended (28,53), together with use of an antiperistaltic agent immediately before the study, to help suppress bowel motion and to aid in visualization of the bowel surface, peritoneum, and adnexa. Given the range of pulse sequences available for MR imaging of the abdomen and pelvis, a structured protocol that combines the various described techniques is provided (Table 2).


View this table:
[in this window]
[in a new window]

 
TABLE 2. MR Imaging Sequences for Ovarian Cancer Staging

 
Delineation of pelvic anatomy and tissue characterization requires fast spin-echo T2-weighted imaging, with a similar sequence used to image the abdomen. Breath-hold T1-weighted fat-suppressed imaging through the abdomen and pelvis before and after intravenous bolus administration of gadolinium chelate is recommended in all cases. The contrast-enhanced study not only helps characterize the tumor but improves detection of peritoneal and omental implants (5659). Marked enhancement of small peritoneal tumors on contrast-enhanced fat-suppressed T1-weighted images facilitates the detection of metastases to the free peritoneal surface and bowel serosa, and the technique is superior to the use of unenhanced T1- and T2-weighted sequences (Fig 23) (56,57). The ability to suppress the high signal of adjacent fat optimizes visualization of small tumor volumes. Enhancement of ascites 15–20 minutes after administration of contrast material has been reported with peritoneal carcinomatosis (60).



View larger version (147K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 23a.  Diffuse peritoneal carcinomatosis from ovarian carcinoma. Axial T1-weighted (a), T2-weighted (b), and breath-hold contrast-enhanced T1-weighted, fat-suppressed (c) images demonstrate that the degree of peritoneal involvement is much better demonstrated on images obtained with fat suppression and after the administration of gadolinium (arrows in c).

 


View larger version (145K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 23b.  Diffuse peritoneal carcinomatosis from ovarian carcinoma. Axial T1-weighted (a), T2-weighted (b), and breath-hold contrast-enhanced T1-weighted, fat-suppressed (c) images demonstrate that the degree of peritoneal involvement is much better demonstrated on images obtained with fat suppression and after the administration of gadolinium (arrows in c).

 


View larger version (165K):
[in this window]
[in a new window]
[Download PPT slide]
 
Figure 23c.  Diffuse peritoneal carcinomatosis from ovarian carcinoma. Axial T1-weighted (a), T2-weighted (b), and breath-hold contrast-enhanced T1-weighted, fat-suppressed (c) images demonstrate that the degree of peritoneal involvement is much better demonstrated on images obtained with fat suppression and after the administration of gadolinium (arrows in c).

 
Further improvements in technology with respect to design of phased-array coils and the advent of parallel imaging have dramatically improved the efficiency of MR imaging. The ability to acquire multiple lines of data simultaneously for each application of a phase-encoding gradient can be put to use in a number of ways, including reduction in breath-hold times, reduction in overall duration of image acquisition, improvement in temporal resolution, improvement in spatial resolution that can be acquired in a given imaging time, and improvement in image quality from a reduction in time-dependent artifacts.

Positron Emission Tomography
Positron emission tomography (PET), performed with 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG), is an advanced, noninvasive imaging tool that allows identification of metabolic and physiologic alterations in tumors. Malignant cells demonstrate increased glycolytic activity, as glucose is preferentially concentrated because of an increase in membrane glucose transporters as well as some of the principle enzymes responsible for phosphorylation. FDG, a glucose analogue, is preferentially transported into cells via glucose transporter proteins, where it undergoes phosphorylation by hexokinase, and is converted to FDG-6-phosphate. However, unlike gluocose-6-phosphate, FDG-6-phosphate is not further metabolized, does not cross the cell membrane, and becomes metabolically trapped in cancer cells (61,62). The ability of cancer cells to trap the FDG metabolite forms the basis for imaging the in vivo distribution of the tracer with FDG PET (Fig 22).

The role of whole-body FDG PET in the diagnosis and staging of primary ovarian tumors is controversial. Early studies showed sensitivities and specificities of 83%–86% and 54%–86%, respectively (6365). In a more recent study, Rieber et al (66) examined the role of FDG PET in the preoperative diagnosis of 103 suspicious adnexal masses (12 malignant and 91 benign, as proved by histologic analysis) found with US in asymptomatic patients. Comparison of the diagnoses made with gadolinium-enhanced MR imaging, transvaginal Doppler imaging, FDG PET, and consensus diagnosis yielded the following calculated data: sensitivity, 83%, 92%, 58%, and 92%; specificity, 84%, 59%, 78%, and 84%; and diagnostic accuracy, 83%, 63%, 76%, and 85%; respectively. Rieber et al (66) concluded that the low sensitivity (58%) of FDG PET in their study was the result of a higher percentage of tumors of low malignant potential and early stage ovarian cancer, in contrast to the higher sensitivities in earlier studies, which had a greater proportion of advanced stage tumors (6365). Borderline tumors and early stage carcinomas pose a dilemma in imaging because there is only a small amount of transformed tissue for glucose uptake. In addition, the limited resolution of FDG PET may prevent visualization of small (<1 cm) tumor deposits, despite the accumulation of FDG. In the study of Rieber et al (66), false-positive findings were noted in inflammatory processes; histologically benign tumors; and gastrointestinal activity, which can accumulate FDG to the same intensity as glucose metabolism in malignant tissue. The authors concluded that routine use of FDG PET is unsuitable as a diagnostic imaging procedure for lesion characterization, evaluation of extent of disease, and relationship to adjacent organs (66). The more valuable role for PET imaging may be in the setting of recurrent disease, when results of CT and MR imaging are negative but tumor markers are increasing, although this use too has not been convincingly proved (67,68).

Imaging Summary
It is important to acknowledge differences in MR and CT imaging techniques, which can vary widely between published studies and which can result in discrepancies in data. CT is the primary modality for staging ovarian cancer, given its widespread availability and general use. Review of the literature indicates that MR imaging is equally or more accurate than CT in the detection of small or equivocal implants and localized extension of disease. However, MR imaging is currently limited by availability, duration of examination, lack of widespread reader experience, and expense. Competing techniques in MR imaging and multidetector CT should be evaluated in an environment of increasing cost awareness. This evaluation is best accomplished by outcomes analysis to determine not only the most cost-effective method of assessing patients with ovarian cancer but to establish the appropriate treatment or referral pattern.


    Treatment
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
Surgery is the cornerstone of treatment for ovarian carcinoma. The goal of surgery is threefold: resection of the primary tumor with histologic confirmation of malignancy, accurate and complete staging, and optimal cytoreductive surgery (debulking) (13). The amount of residual tumor after the initial debulking procedure is an important prognostic indicator for survival. In addition, debulking may greatly improve the patient’s quality of life.

Debulking is considered optimal when residual tumor is less than 1.5–2.0 cm (4). The 4-year survival rate is 30% for patients whose residual tumor is less than 2 cm, compared with only 10% if the remaining tumor is greater than 2 cm (69). Further debulking below 1.5–2.0 cm has not generally been thought to be useful; however, some authors have advocated complete resection of all macroscopic disease (4,70). Larger, randomized, prospective studies would be needed to see if patients truly benefit from a more aggressive surgical approach.

Cytoreductive surgery does not, by itself, improve patient outcome. The major benefit obtained from optimal debulking is improved response to chemotherapy (13,30). The improved tumor response is thought to be secondary to a number of factors based on tumor growth kinetics. An obvious advantage of debulking is that fewer tumor cells remain to be eradicated. The remaining malignant cells are often better vascularized and metabolically more active, thus increasing their susceptibility to the cytotoxic effects of chemotherapy. Chemotherapy usually consists of a platinum-based regimen with cisplatin combined with adriamycin and cyclophophamide; more recently, paclitaxel has been used (13,30).

The importance of having an experienced subspecialist perform the initial cytoreductive surgery cannot be overemphasized (71), but even in the best of hands the optimal debulking cannot be achieved in some cases. Generally, optimal resection of macroscopic disease is not possible in patients who have bulky disease in difficult-to-reach areas (porta hepatis, lesser sac, gastrosplenic and gastrohepatic ligaments, root of mesentery); extensive bladder, bowel, or sidewall invasion; or stage IV disease. Failure to achieve an optimal macroscopic tumor reduction confers no survival benefit to the patient (4). Patients with unresectable disease may benefit from neoadjuvant (preoperative) chemotherapy before cytoreductive surgery. More controlled randomized studies are needed, but results of preliminary investigations suggest that overall survival is equivalent to, or better than, that of patients who undergo cytoreductive surgery before chemotherapy (13,72,73). In addition, quality-of-life issues were considered superior in the neoadjuvant group. Radiologic imaging has an important role in the identification of this group of patients, with accuracies of 93%–95% for both CT and MR imaging in the detection of unresectable disease (26).


    Conclusions
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 
It is important to recognize the role and limitations that radiology has in the staging of ovarian carcinoma. Despite rapid technologic advances, no imaging modality can demonstrate clinically important microscopic disease. Therefore, negative imaging findings do not obviate complete surgical staging. Some have argued, because peritoneal spread can never be excluded, that imaging is an unnecessary expense and that once a suspicious mass is identified, the patient should go directly to surgery, which accomplishes both staging and debulking in a single procedure. There are, however, several compelling arguments in favor of preoperative radiologic staging. Radiologic staging provides an evaluation of the extent of disease (both bulk and location), which aids in preoperative planning and patient counseling. In addition, radiologic staging often guides subspecialty referral. If stage III disease is shown on an imaging study, there is a greater likelihood that the patient will be referred directly to a gynecologic oncologist so that optimal cytoreductive surgery can be performed. Finally, imaging can help identify that very important group of patients for whom optimal debulking is not possible and who may be more optimally treated with preoperative chemotherapy. We therefore believe the radiologist plays an important role and can have a significant impact directing the appropriate care of ovarian cancer patients.


    Acknowledgments
 
The authors thank Brent J. Wagner, MD, for his work at the AFIP in the area of ovarian cancer imaging and for his contribution of cases to this review. We also thank Dianne Engelby, MAMS, for her wonderful illustrations, which added greatly to the manuscript.


    Footnotes
 
The opinions and assertions contained herein are the private views of the authors and are not to be construed as official nor as representing the views of the Departments of the Army or Defense.

Abbreviation: FDG = fluoro-2-deoxy-D-glucose


    References
 Top
 Abstract
 LEARNING OBJECTIVES FOR TEST...
 Introduction
 Staging System
 Imaging: Goals, Techniques, and...
 Treatment
 Conclusions
 References
 

  1. Jemal A, Murray T, Samuels A, Ghafoor A, Ward E, Thun MJ. Cancer statistics, 2003. CA Cancer J Clin 2003; 53:5-26.[Abstract/Free Full Text]
  2. Scully RE. Tumors of the ovary and maldeveloped gonads. Atlas of tumor pathology, fasc 16, ser 2. Washington, DC: Armed Forces Institute of Pathology, 1979; 1-44.
  3. Wagner BJ, Buck JL, Seidman JD, McCabe KM. Ovarian epithelial neoplasms: radiologic-pathologic correlation. RadioGraphics 1994; 14:1351-1374.[Abstract]
  4. Friedlander ML. Prognostic factors in ovarian cancer. Semin Oncol 1998; 25:305-314.[Medline]
  5. Coakley FV. Staging ovarian cancer: role of imaging. Radiol Clin North Am 2002; 40:609-636.[CrossRef][Medline]
  6. Holschneider CH, Berek JS. Ovarian cancer: epidemiology, biology, and prognostic factors. Semin Surg Oncol 2000; 19:3-10.[CrossRef][Medline]
  7. Berchuck A, Schildkraut JM, Marks JR, Futreal PA. Managing hereditary ovarian cancer risk. Cancer 1999; 86:2517-2524.[CrossRef][Medline]
  8. NIH Consensus Development Panel on Ovarian Cancer. NIH consensus conference: ovarian cancer—screening, treatment, and follow-up. JAMA 1995; 273:491-497.[Abstract/Free Full Text]
  9. Fathalla MF. Incessant ovulation: a factor in ovarian neoplasia? Lancet 1971; 2:163.[CrossRef][Medline]
  10. Daly MB. The epidemiology of ovarian cancer. Hematol Oncol Clin North Am 1992; 6:729-738.
  11. Ovary. In: Fleming ID, Cooper JS, Henson DE, et al., eds. AJCC cancer staging manual. 5th ed. Philadelphia, Pa: Lippincott, Williams & Wilkins, 1998; 188-190.
  12. Spiessl B, Beahrs OH, Hermanek P, et al. eds. Ovary. TNM atlas. 3rd ed. Berlin, Germany: Springer-Verlag, 1989; 198-206.
  13. Marsden DE, Friedlander M, Hacker NF. Current management of epithelial ovarian carcinoma: a review. Semin Surg Oncol 2000; 19:11-19.[CrossRef][Medline]
  14. Hoskins WJ, Bundy BN, Thigpen JT, Omura GA. The influence of cytoreductive surgery on recurrence-free interval and survival in small-volume stage III epithelial ovarian cancer: a Gynecologic Oncology Group study. Gynecol Oncol 1992; 47:159-166.[CrossRef][Medline]
  15. Young RC, Decker DG, Wharton JT, et al. Staging laparotomy in early ovarian cancer. JAMA 1983; 250:3072-3076.[Abstract/Free Full Text]
  16. McGowan L, Lesher LP, Norris HJ, Barnett M. Misstaging of ovarian cancer. Obstet Gynecol 1985; 65:568-572.[Medline]
  17. Buy JN, Moss AA, Ghossain MA, et al. Peritoneal implants from ovarian tumors: CT findings. Radiology 1988; 169:691-694.[Abstract/Free Full Text]
  18. Meyers MA, Oliphant M, Berne AS, Feldberg MA. The peritoneal ligaments and mesenteries: pathways of intraabdominal spread of disease. Radiology 1987; 163:593-604.[Abstract/Free Full Text]
  19. Coakley FV, Hricak H. Imaging of peritoneal and mesenteric disease: key concepts for the clinical radiologist. Clin Radiol 1999; 54:563-574.[CrossRef][Medline]
  20. Feldman GB, Knapp RC. Lymphatic drainage of the peritoneal cavity and its significance in ovarian cancer. Am J Obstet Gynecol 1974; 119:991-994.[Medline]
  21. Kawamoto S, Urban BA, Fishman EK. CT of epithelial ovarian tumors. RadioGraphics 1999; 19:S85-S102.
  22. Rose PG, Piver MS, Tsukada Y, Lau TS. Metastatic patterns in histologic variants of ovarian cancer: an autopsy study. Cancer 1989; 64:1508-1513.[CrossRef][Medline]
  23. Dvoretsky PM, Richards KA, Angel C, et al. Distribution of disease at autopsy in 100 women with ovarian cancer. Hum Pathol 1988; 19:57-63.[CrossRef][Medline]
  24. Dauplat J, Hacker NF, Nieberg RK, Berek JS, Rose TP, Sagae S. Distant metastases in epithelial ovarian carcinoma. Cancer 1987; 60:1561-1566.[CrossRef][Medline]
  25. Coakley FV, Choi PH, Gougoutas CA, et al. Peritoneal metastases: detection with spiral CT in patients with ovarian cancer. Radiology 2002; 223:495-499.[Abstract/Free Full Text]
  26. Forstner R, Hricak H, Occhipinti KA, Powell CB, Frankel SD, Stern JL. Ovarian cancer: staging with CT and MR imaging. Radiology 1995; 197:619-626.[Abstract/Free Full Text]
  27. Walkey MM, Friedman AC, Sohotra P, Radecki PD. CT manifestations of peritoneal carcinomatosis. AJR Am J Roentgenol 1988; 150:1035-1041.[Abstract/Free Full Text]
  28. Tempany CM, Zou KH, Silverman SG, Brown DL, Kurtz AB, McNeil BJ. Staging of advanced ovarian cancer: comparison of imaging modalities—report from the Radiological Diagnostic Oncology Group. Radiology 2000; 215:761-767.[Abstract/Free Full Text]
  29. Steinberg JJ, Demopoulos RI, Bigelow B. The evaluation of the omentum in ovarian cancer. Gynecol Oncol 1986; 24:327-330.[CrossRef][Medline]
  30. Hoskins WJ. Surgical staging and cytoreductive surgery of epithelial ovarian cancer. Cancer 1993; 71:1534-1540.[Medline]
  31. Jung SE, Lee JM, Rha SE, Byun JY, Jung JI, Hahn ST. CT and MR imaging of ovarian tumors with emphasis on differential diagnosis. RadioGraphics 2002; 22:1305-1325.
  32. Mitchell DG, Hill MC, Hill S, Zaloudek C. Serous carcinoma of the ovary: CT identification of metastatic calcified implants. Radiology 1986; 158:649-652.[Abstract/Free Full Text]
  33. Ronnett BM, Zahn CM, Kurman RJ, Kass ME, Sugarbaker PH, Shmookler BM. Disseminated peritoneal adenomucinosis and peritoneal mucinous carcinomatosis: a clinicopathologic analysis of 109 cases with emphasis on distinguishing pathologic features, site of origin, prognosis, and relationship to "pseudomyxoma peritonei". Am J Surg Pathol 1995; 19:1390-1408.[Medline]
  34. Ronnett BM, Kurman RJ, Zahn CM, et al. Pseudomyxoma peritonei in women: a clinicopathologic analysis of 30 cases with emphasis on site of origin, prognosis, and relationship to ovarian mucinous tumors of low malignant potential. Hum Pathol 1995; 26:509-524.[CrossRef][Medline]
  35. Carnino F, Fuda G, Ciccone G, et al. Significance of lymph node sampling in epithelial carcinoma of the ovary. Gynecol Oncol 1997; 65:467-472.[CrossRef][Medline]
  36. Sakai K, Kamura T, Hirakawa T, Saito T, Kaku T, Nakano H. Relationship between pelvic lymph node involvement and other disease sites in patients with ovarian cancer. Gynecol Oncol 1997; 65:164-168.[CrossRef][Medline]
  37. Meyer JI, Kennedy AW, Friedman R, Ayoub A, Zepp RC. Ovarian carcinoma: value of CT in predicting success of debulking surgery. AJR Am J Roentgenol 1995; 165:875-878.[Abstract/Free Full Text]
  38. Nelson BE, Rosenfield AT, Schwartz PE. Preoperative abdominopelvic computed tomographic prediction of optimal cytoreduction in epithelial ovarian carcinoma. J Clin Oncol 1993; 11:166-172.[Abstract]
  39. Heintz AP, Hacker NF, Berek JS, Rose TP, Munoz AK, Lagasse LD. Cytoreductive surgery in ovarian carcinoma: feasibility and morbidity. Obstet Gynecol 1986; 67:783-788.[Medline]
  40. Brown DL, Doubilet PM, Miller FH, et al. Benign and malignant ovarian masses: selection of the most discriminating gray-scale and Doppler sonographic features. Radiology 1998; 208:103-110.[Abstract/Free Full Text]
  41. Kinkel K, Hricak H, Lu Y, Tsuda K, Filly RA. US characterization of ovarian masses: a meta-analysis. Radiology 2000; 217:803-811.[Abstract/Free Full Text]
  42. Goerg C, Schwerk WB. Peritoneal carcinomatosis with ascites. AJR Am J Roentgenol 1991; 156:1185-1187.[Free Full Text]
  43. Hanbidge AE, Lynch D, Wilson SR. US of the peritoneum. RadioGraphics 2003; 23:663-685.[Abstract/Free Full Text]
  44. Amendola MA. The role of CT in the evaluation of ovarian malignancy. Crit Rev Diagn Imaging 1985; 24:329-368.[Medline]
  45. Kalovidouris A, Gouliamos A, Pontifex G, Gennatas K, Dardoufas K, Papavasiliou C. Computed tomography of ovarian carcinoma. Acta Radiol Diagn (Stockh) 1984; 25:203-208.[Medline]
  46. Sanders RC, McNeil BJ, Finberg HJ, et al. A prospective study of computed tomography and ultrasound in the detection and staging of pelvic masses. Radiology 1983; 146:439-442.[Abstract/Free Full Text]
  47. Shiels RA, Peel KR, MacDonald HN, Thorogood J, Robinson PJ. A prospective trial of computed tomography in the staging of ovarian malignancy. Br J Obstet Gynaecol 1985; 92:407-412.[Medline]
  48. Halvorsen RA, Jr, Panushka C, Oakley GJ, Letourneau JG, Adcock LL. Intraperitoneal contrast material improves the CT detection of peritoneal metastases. AJR Am J Roentgenol 1991; 157:37-40.[Abstract/Free Full Text]
  49. Jacquet P, Jelinek JS, Steves MA, Sugarbaker PH. Evaluation of computed tomography in patients with peritoneal carcinomatosis. Cancer 1993; 72:1631-1636.[CrossRef][Medline]
  50. Pannu HK, Bristow RE, Montz FJ, Fishman EK. Multidetector CT of peritoneal carcinomatosis from ovarian cancer. RadioGraphics 2003; 23:687-701.[Abstract/Free Full Text]
  51. Urban BA, Fishman EK. Spiral CT of the female pelvis: clinical applications. Abdom Imaging 1995; 20:9-14.[CrossRef][Medline]
  52. Urban BA, Fishman EK. Helical (spiral) CT of the female pelvis. Radiol Clin North Am 1995; 33:933-948.[Medline]
  53. Kurtz AB, Tsimikas JV, Tempany CM, et al. Diagnosis and staging of ovarian cancer: comparative values of Doppler and conventional US, CT, and MR imaging correlated with surgery and histopathologic analysis—report of the Radiology Diagnostic Oncology Group. Radiology 1999; 212:19-27.[Abstract/Free Full Text]
  54. Low RN, Semelka RC, Worawattanakul S, Alzate GD, Sigeti JS. Extrahepatic abdominal imaging in patients with malignancy: comparison of MR imaging and helical CT, with subsequent surgical correlation. Radiology 1999; 210:625-632.[Abstract/Free Full Text]
  55. Low RN, Francis IR. MR imaging of the gastrointestinal tract with i. v., gadolinium and diluted barium oral contrast media compared with unenhanced MR imaging and CT. AJR Am J Roentgenol 1997; 169:1051-1059.
  56. Low RN, Barone RM, Lacey C, Sigeti JS, Alzate GD, Sebrechts CP. Peritoneal tumor: MR imaging with dilute oral barium and intravenous gadolinium-containing contrast agents compared with unenhanced MR imaging and CT. Radiology 1997; 204:513-520.[Abstract/Free Full Text]
  57. Low RN, Carter WD, Saleh F, Sigeti JS. Ovarian cancer: comparison of findings with perfluorocarbon-enhanced MR imaging, In-111-CYT-103 immunoscintigraphy, and CT. Radiology 1995; 195:391-400.[Abstract/Free Full Text]
  58. Semelka RC, Lawrence PH, Shoenut JP, Heywood M, Kroeker MA, Lotocki R. Primary ovarian cancer: prospective comparison of contrast-enhanced CT and pre- and postcontrast, fat-suppressed MR imaging, with histologic correlation. J Magn Reson Imaging 1993; 3:99-106.[Medline]
  59. Outwater EK, Siegelman ES, Wilson KM, Mitchell DG. Benign and malignant gynecologic disease: clinical importance of fluid and peritoneal enhancement in the pelvis at MR imaging. Radiology 1996; 200:483-488.[Abstract/Free Full Text]
  60. Arai K, Makino H, Morioka T, et al. Enhancement of ascites on MRI following intravenous administration of Gd-DTPA. J Comput Assist Tomogr 1993; 17:617-622.[Medline]
  61. Wahl RL. Targeting glucose transporters for tumor imaging: "sweet" idea, "sour" result. J Nucl Med 1996; 37:1038-1041.[Free Full Text]
  62. Kostakoglu L, Agress H, Jr, Goldsmith SJ. Clinical role of FDG PET in evaluation of cancer patients. RadioGraphics 2003; 23:315-340.[Abstract/Free Full Text]
  63. Romer W, Avril N, Dose J, et al. Metabolic characterization of ovarian tumors with positron-emission tomography and F-18 fluorodeoxyglucose. Rofo Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr 1997; 166:62-68.[Medline]
  64. Hubner KF, McDonald TW, Niethammer JG, Smith GT, Gould HR, Buonocore E. Assessment of primary and metastatic ovarian cancer by positron emission tomography (PET) using 2-[18F]deoxyglucose (2-[18F]FDG). Gynecol Oncol 1993; 51:197-204.[CrossRef][Medline]
  65. Zimny M, Schroder W, Wolters S, Cremerius U, Rath W, Bull U. 18F-fluorodeoxyglucose PET in ovarian carcinoma: methodology and preliminary results. Nuklearmedizin 1997; 36:228-233.[Medline]
  66. Rieber A, Nussle K, Stohr I, et al. Preoperative diagnosis of ovarian tumors with MR imaging: comparison with transvaginal sonography, positron emission tomography, and histologic findings. AJR Am J Roentgenol 2001; 177:123-129.[Abstract/Free Full Text]
  67. Cho SM, Ha HK, Byun JY, Lee JM, Kim CJ, Nam-Koong SE. Usefulness of FDG PET for assessment of early recurrent epithelial ovarian cancer. AJR Am J Roentgenol 2002; 179:391-395.[Abstract/Free Full Text]
  68. Nakamoto Y, Saga T, Ishimori T, et al. Clinical value of positron emission tomography with FDG for recurrent ovarian cancer. AJR Am J Roentgenol 2001; 176:1449-1454.[Abstract/Free Full Text]
  69. Cannistra SA. Cancer of the ovary. N Engl J Med 1993; 329:1550-1559.[Free Full Text]
  70. Eisenkop SM, Nalick RH, Wang HJ, Teng NN. Peritoneal implant elimination during cytoreductive surgery for ovarian cancer: impact on survival. Gynecol Oncol 1993; 51:224-229.[CrossRef][Medline]
  71. Eisenkop SM, Spirtos NM, Montag TW, Nalick RH, Wang HJ. The impact of subspecialty training on the management of advanced ovarian cancer. Gynecol Oncol 1992; 47:203-209.[CrossRef][Medline]
  72. Vergote I, De Wever I, Tjalma W, Van Gramberen M, Decloedt J, van Dam P. Neoadjuvant chemotherapy or primary debulking surgery in advanced ovarian carcinoma: a retrospective analysis of 285 patients. Gynecol Oncol 1998; 71:431-436.[CrossRef][Medline]
  73. Schwartz PE, Chambers JT, Makuch R. Neoadjuvant chemotherapy for advanced ovarian cancer. Gynecol Oncol 1994; 53:33-37.[CrossRef][Medline]



This article has been cited by other articles:


Home page
RadioGraphicsHome page
J. W. Lee, S. Kim, S. W. Kwack, C. W. Kim, T. Y. Moon, S. H. Lee, M. Cho, D. H. Kang, and G. H. Kim
Hepatic Capsular and Subcapsular Pathologic Conditions: Demonstration with CT and MR Imaging
RadioGraphics, September 1, 2008; 28(5): 1307 - 1323.
[Abstract] [Full Text] [PDF]


Home page
RadioGraphicsHome page
A. N. Viswanathan, B. M. Buttin, and A. M. Kennedy
Oncodiagnosis Panel: 2006: Ovarian, Cervical, and Endometrial Cancer
RadioGraphics, January 1, 2008; 28(1): 289 - 307.
[Full Text] [PDF]


Home page
Journal of the American Animal Hospital AssociationHome page
G. E. Pastore, C. R. Lamb, and V. Lipscomb
Comparison of the Results of Abdominal Ultrasonography and Exploratory Laparotomy in the Dog and Cat
J. Am. Anim. Hosp. Assoc., September 1, 2007; 43(5): 264 - 269.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Roentgenol.Home page
S. G. Yarram, H. V. Nghiem, E. Higgins, G. Fox, B. Nan, and I. R. Francis
Evaluation of Imaging-Guided Core Biopsy of Pelvic Masses
Am. J. Roentgenol., May 1, 2007; 188(5): 1208 - 1211.
[Abstract] [Full Text] [PDF]


Home page
ImagingHome page
M V Pakkal and M Balogun
Imaging of ovarian cancer
Imaging, August 1, 2006; 18(1): 20 - 27.
[Abstract] [Full Text] [PDF]


Home page
RadioGraphicsHome page
K. J. Burkholz, B. P. Wood, and C. Zuppan
Best Cases from the AFIP: Borderline Papillary Serous Tumor of the Right Ovary
RadioGraphics, November 1, 2005; 25(6): 1689 - 1692.
[Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow CME Test (opens in a new window)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Woodward, P. J.
Right arrow Articles by Saenger, J. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Woodward, P. J.
Right arrow Articles by Saenger, J. S.
Related Collections
Right arrow Obstetric/Gynecologic Radiology
Right arrow Genitourinary Radiology


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
RADIOGRAPHICS RADIOLOGY RSNA JOURNALS ONLINE