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Abdominal Imaging |
1 Department of Diagnostic and Interventional Radiology, Gunma University School
of Medicine, 3-39-15 Showa-machi, Maebashi, Gunma 371-0034, Japan.
2 Department of Nuclear Medicine, Gunma University School of Medicine, Gunma
371-0034, Japan.
Received December 2, 2003;
accepted after revision March 16, 2004.
Address correspondence to H. Morita
(moritahideomh{at}yahoo.co.jp).
Abstract
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CONCLUSION. Serous surface papillary carcinoma of the peritoneum should be included in the differential diagnosis when ascites, omental caking, and peritoneal nodules or enhancement are observed in a postmenopausal woman with or without ovarian enlargement.
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CT of the whole abdomen was performed in all patients, and nine patients underwent MRI. One patient underwent unenhanced studies because she had asthma. CT was performed with a LightSpeed QX/i unit (GE Healthcare) in seven patients, a HiSpeed Advantage unit (GE Healthcare) in two, or an X-force unit (Toshiba Medical Systems) in two. Enhanced CT was performed using a standard protocol with IV contrast material (300 mg I/mL), including a power-injected bolus of 50 mL given at 1.5 mL/sec followed by an additional 50 mL at a rate of 0.7 mL/sec. Continuous 7-mm-thick (HiSpeed Advantage), 7.5-mm-thick (LightSpeed QX/i), or 10-mm-thick (X-force) slices were taken from the diaphragm through the pubic symphysis.
MRI was performed with a high-field (1.5-T) unit (Signa Horizon, GE Healthcare) in seven patients and with a low-field (0.5-T) unit (Flexart, Toshiba Medical Systems) in two, using a body coil. All MRI examinations included conventional spin-echo T1-weighted, fast spin-echo T2-weighted, and contrast-enhanced T1-weighted fat-saturation images. For T1-weighted MR images, the TR range/TE range was 400–620/10–20; for fast spin-echo T2-weighted MR images, 4,800–6,316/97–120; and for contrast-enhanced T1-weighted images with fat saturation, 400–600/10–14.
On CT and MRI, we evaluated the abdominal organs for ascites, peritoneal thickening, peritoneal metastases, omental changes, lymphadenopathy, ovarian changes, and other changes.
Parietal peritoneal thickening on CT and MRI was defined in cases of smooth or irregular enhancement of the peritoneum with a thickness greater than 5 mm on two or more continuous slices. Peritoneal metastases were defined as localized nodules on the peritoneum that were more than 1 cm in diameter. Omental change (diffuse enlargement and enhancement of the greater sac) was assessed. Lymph nodes of more than 1 cm in diameter with obvious enhancement or necrosis were regarded as lymphadenopathy.
All patients underwent laparotomy, including optimal debulking surgery performed in five patients and biopsy in six patients. Radiologic findings were compared with surgical findings of omental and peritoneal abnormalities, lymph nodes, ascites, ovaries, and other abdominal organ changes.
The final diagnosis was made according to the Gynecologic Oncology Group's 1993 inclusion criteria for serous surface papillary carcinoma [1], as follows: First, both ovaries must be either physiologically normal in size or enlarged by a benign process. Second, involvement at the extraovarian sites must be greater than the involvement on the surface of either ovary. Third, microscopically, the ovarian component must be either nonexistent, confined to ovarian surface epithelium with no evidence of cortical invasion, involving ovarian surface epithelium and underlying cortical stroma but with any given tumor smaller than 5 x 5 mm, or a tumor smaller than 5 x 5 mm in the ovary with or without surface disease. Finally, the histologic and cytologic characteristics of the tumor must be predominantly of the serous type that is similar or identical to any grade of ovarian serous papillary adenocarcinoma.
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All patients underwent gastrointestinal and colorectal endoscopies, and all but one had no malignancy. In the one patient, serous surface papillary carcinoma and stage II sigmoid colon cancer were detected and resected at the same time; the final pathologic diagnosis of colon cancer was moderately differentiated adenocarcinoma with involvement of the muscularis propria.
CT and MRI Findings
The frequency of the radiologic findings in 11 patients with serous surface
papillary carcinoma is summarized in Table
1.
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Nine patients had ascites (Fig. 1A, 1B). Seven patients had peritoneal thickening and nodules (Fig. 1A, 1B), three had only peritoneal nodules, and one had neither on unenhanced studies. Peritoneal thickening or nodules showed low signal intensity on T1-weighted images and high signal intensity on T2-weighted images (Fig. 2). Diffuse peritoneal enhancement was seen on contrast-enhanced T1-weighted images with fat saturation. No patient had peritoneal calcification.
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Omental caking (diffuse enlargement) was detected in eight patients (Fig. 3). On MRI, these omental lesions showed low signal intensity on T1-weighted images and high signal intensity on T2-weighted images.
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Four patients had lymphadenopathy (Fig. 4A, 4B) located in the left paraaortic region in two patients, in the left internal iliac and left paraaortic regions in one, and in the bilateral iliac and paraaortic regions in one.
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The ovaries were not identified in six patients on either CT or MRI, were unilaterally enlarged in two patients, and were bilaterally enlarged in three patients. All depicted ovaries were enlarged and showed heterogeneous high intensity on T2-weighted images of MRI and heterogeneous enhancement on both CT and MRI (Fig. 5A, 5B).
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One patient had multiple solid tumors in the liver (Fig. 6). Although a pathologic specimen of these tumors was not obtained, only serous surface papillary carcinoma was detected in her screening study for primary malignancy.
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One patient, who had asthma and underwent only unenhanced studies, had no abnormal findings on either CT or MRI, but a minimal amount of ascites was detected in the Douglas pouch on transvaginal echography. Her initial diagnosis was made by cytologic examination of this ascites; the specimen was obtained by transvaginal sonographically guided aspiration. MRI did not add any information that CT did not identify.
Gross Surgical and Pathologic Observations
All patients underwent laparotomy, and the diagnosis was confirmed
according to the Gynecologic Oncology Group's inclusion criteria
[1] for serous surface
papillary carcinoma. Intraoperative evaluation showed peritoneal tumors
without other primary tumors. Clear or hemorrhagic ascites was present in all
11 patients.
Diffuse abdominopelvic tumor metastases on both the parietal and visceral peritoneum, including the omentum, were noted in 10 patients. A dominant extraovarian mass was seen in eight patients, and all involved the omentum. Two patients had lymphadenopathy: one in the bilateral internal iliac region and the other in the bilateral internal iliac and paraaortic regions. The ovaries were of a normal size and had a smooth surface in six patients, who did not show any ovarian abnormality on CT or MRI. The other five patients had unilateral or bilateral ovarian enlargement that showed heterogeneous enhancement in CT and MRI studies. One patient had multiple solid tumors of the liver that showed heterogeneous and poor enhancement on CT and MRI studies.
Microscopic Observations
Pathologic examination revealed four well-differentiated, one moderately
differentiated, five poorly differentiated, and one un-differentiated
adenocarcinomas. Psammoma bodies were found in five patients with well- or
moderately differentiated adenocarcinoma. The microscopic features of serous
surface papillary carcinoma were almost identical to those of serous ovarian
papillary carcinoma. No evidence was seen of a tumor in the fallopian tubes or
uterus. Microscopic tumor invasion to the superficial ovarian parenchyma was
found in all five patients with enlarged ovaries.
Treatment
Five patients were treated with debulking surgery that included
hysterectomy, salpingooophorectomy, omentectomy, and resection of the
peritoneal tumor. After the first debulking surgery, two patients received
five to seven courses of a chemotherapy combination of Taxol (paclitaxel,
Bristol-Myers Squibb) plus carboplatin, or docetaxel plus carboplatin, and
three patients received five courses of a regimen of cisplatin, Adriamycin
(doxorubicin, Farmitalia), and cyclophosphamide (CAP), which is regarded as a
standard treatment for ovarian cancer.
In the other six patients with advanced peritoneal carcinomatosis, sampling surgery was followed by the first chemotherapy of five to seven courses of paclitaxel plus cisplatin or five to 11 courses of CAP. Three of the patients underwent a second-look operation within 4 weeks after the first chemotherapy, followed by the second chemotherapy of several courses of paclitaxel plus carboplatin or docetaxel plus carboplatin.
Prognosis
The median follow-up time for all patients was 28 months (range,
11–44 months). Seven patients died of their disease, and four were alive
with disease as of February 2004. Five patients underwent second-look
laparotomies that found variously sized residual tumors, and they went on to
receive second-line chemotherapy. The median survival time was 22 months.
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Serous ovarian papillary carcinoma is a common subtype of ovarian epithelial carcinoma. Clinical features of stages III and IV serous ovarian papillary carcinoma closely resemble those of serous surface papillary carcinoma, including peritoneal carcinomatosis and an elevated level of CA 125 [1, 2, 5]. In recent matched-case studies comparing serous surface papillary carcinoma and serous ovarian papillary carcinoma, when the same treatment was performed, such as combining optimal debulking surgery with platinum-based chemotherapy, the prognosis of serous surface papillary carcinoma was similar to that of stage III or IV serous ovarian papillary carcinoma. For example, the median survival time of serous surface papillary carcinoma ranges from 11.3 to 24 months [2, 5, 6, 12, 13, 15], whereas that of serous ovarian papillary carcinoma ranges from 13.5 to 31 months [2, 5, 6, 15]. The mean survival time of our 11 patients was also in this range. Ordonez [16] concluded that, pathologically, both serous surface papillary carcinoma and serous ovarian papillary carcinoma have a similar immunophenotype, and so immunohistochemical studies are not useful in separating these entities.
Lauchlan [11] first discussed the secondary müllerian system in association with serous surface papillary carcinoma and serous ovarian papillary carcinoma. According to that author's theory, serous surface papillary carcinoma probably arises from embryonic nests of the müllerian cells that are present in the peritoneum. These cells also are present on the surface and in the stroma of the ovary and may give rise to serous carcinoma. This theory would explain why serous surface papillary carcinoma behaves like serous ovarian papillary carcinoma in many ways, with similar clinical, radiologic, and immunohistochemical findings and similar sensitivity to chemotherapy.
From the viewpoints of treatment and prognosis, it may not be important to differentiate serous surface papillary carcinoma from serous ovarian papillary carcinoma. However, we consider it important to differentiate serous surface papillary carcinoma from other peritoneal disorders such as peritoneal carcinomatosis due to other cancers, mesothelioma, lymphomatosis, or tuberculous peritonitis because they need different treatment protocols.
Diffuse peritoneal mesothelioma is one of the diseases that mimics serous surface papillary carcinoma most closely. Mesothelioma is known to occur in persons with a history of asbestos exposure. Whitely et al. [18] described the CT findings of peritoneal mesothelioma, which included thickening of the peritoneum, mesentery, and pleura; ascites; bone destruction; a peritoneal mass; and retroperitoneal lymphadenopathy. These findings are almost identical to those of peritoneal carcinomatosis except for bone destruction. Because of this, electron microscopy or an immunohistochemical procedure is necessary to make a definitive diagnosis of mesothelioma from serous surface papillary carcinoma or serous ovarian papillary carcinoma [10, 16].
The radiologic findings of peritoneal lymphomatosis mimic those of peritoneal carcinomatosis [19, 20]. Ascites, omental masses, peritoneal nodules or thickening, infiltration of the mesentery, and retroperitoneal lymphadenopathy were frequently observed. Lynch et al. [20] documented the final diagnosis, which was established by autopsy, laparotomy, or guided needle aspiration.
Tuberculous peritonitis resembles peritoneal carcinomatosis, because patients with abdominal tuberculosis frequently do not have a thoracic examination [21]. Ha et al. [21] reported that the common radiologic findings of tuberculous peritonitis and peritoneal carcinomatosis were ascites, mesenteric changes, omental changes, and lymphadenopathy of the celiac axis or paraaortic region. However, in patients with tuberculous peritonitis, a low-density center (43%) or calcification (14%) was seen in peritoneal masses or lymph nodes [21]. Other common findings of peritoneal tuberculosis were splenic abnormalities and lymphadenopathy in unusual sites such as the pericardial or paravertebral regions [21]. Ha et al. calculated the sensitivity of CT for diagnosing tuberculous peritonitis and peritoneal carcinomatosis to be 69% and 91%, respectively.
Consequently, it may not be easy to differentiate serous surface papillary carcinoma from peritoneal mesothelioma, lymphomatosis, or tuberculosis on CT and MRI. Laparotomy is usually required to make the final diagnosis of serous surface papillary carcinoma.
In the reports by Furukawa et al. [4] and Zissin et al. [14], all patients with serous surface papillary carcinoma had high levels of serum CA 125. In our patients, serum CA 125 levels were variously elevated (55–14,307 U/mL) in all patients. CA 125 is a sensitive tumor marker used mainly in the follow-up of ovarian cancer, for monitoring the efficacy of therapy, and for early detection of recurrence [22]. However, because serum CA 125 can be elevated in any serositis, we should consider various conditions such as pleuritis, peritonitis, pancreatitis, endometriosis, uterine leiomyomas, hemodialysis, and benign ovarian cysts as other causes of elevated values [22].
In summary, we described the CT and MRI findings in 11 patients with serous surface papillary carcinoma. Ascites, omental caking, and peritoneal nodules or enhancement were the dominant imaging features, with or without ovarian enlargement. Because serous surface papillary carcinoma and serous ovarian papillary carcinoma show similar clinical, radiologic, and histopathologic findings and are treated using the same protocol, serous surface papillary carcinoma may be regarded as a variant of serous ovarian papillary carcinoma. However, radiologists should be familiar with serous surface papillary carcinoma because the treatment and prognosis differ from those of other peritoneal disorders such as mesothelioma, lymphomatosis, and tuberculosis. Laparotomy is required to make a definitive diagnosis of serous surface papillary carcinoma.
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  A. D. Levy, J. Arnaiz, J. C. Shaw, and L. H. Sobin From the Archives of the AFIP: Primary Peritoneal Tumors: Imaging Features with Pathologic Correlation RadioGraphics, March 1, 2008; 28(2): 583 - 607. [Abstract] [Full Text] [PDF]
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