Epithelial ovarian cancer: a review of preoperative imaging features indicating suboptimal surgery

Abstract

Epithelial ovarian cancer has been traditionally treated with cytoreductive surgery and chemotherapy. Optimal surgery is the key to improving the prognosis, and, thus, preoperative imaging should be carefully assessed to determine if the involvement of gastrointestinal, vascular, or thoracic surgeons is necessary to achieve this. Consequently, gynecologists should be able to recognize which imaging features suggest optimal or suboptimal resection. The aim of this review was to present the preoperative imaging features indicating suboptimal resection of epithelial ovarian cancer.

INTRODUCTION

Epithelial ovarian cancer is the second most common gynecologic cancer in the USA and has the highest mortality rate [1]. This tumor is frequently detected in advanced stages because the patients are asymptomatic in the early stage [2,3,4,5]. Accordingly, tumor prognosis depends on the use of cytoreductive surgery and chemotherapy [6,7]. To achieve optimal cytoreductive surgery, it is crucial for gynecologists to assess and recognize preoperative imaging features [8] so that they can identify not only metastasis but also adhesion or invasion, which could influence optimal resection. The recent development of imaging modalities enables gynecologists to easily understand anatomical and functional information for the detection and determination of the extent of the tumor [9,10,11].

If gynecologists cannot recognize the imaging features suggesting incomplete resection preoperatively, they end up doing nothing but keeping the patient's abdomen open until gastrointestinal surgeons, vascular surgeons, or urologists come to intervene. Therefore, identifying tumor adhesion or invasion is crucial so that they can know which other surgeons will be involved in the procedure. However, most radiologic reports that illustrate imaging features of ovarian cancer mainly focus on the differential diagnoses [12,13,14,15,16], and very few reports illustrate computed tomography (CT) or magnetic resonance imaging (MRI) features suggesting incomplete resection.

The aim of this review was to present preoperative imaging features that indicates suboptimal resection of epithelial ovarian cancer.

IMAGING FEATURES INDICATIVE OF INCOMPLETE RESECTION

1. Bowel adhesion or invasion

The obliteration of a fat layer between a tumor and the bowel is a common imaging finding that suggests adhesion (Fig. 1). Fat tissue is hypoattenuating on a CT scan and is hyperintense on T1- and T2-weighted images. Previous surgical treatment, radiation therapy, and pelvic inflammation frequently obliterate the fat plane between the tumor and the bowel.

Fig. 1. Bowel adhesion and invasion in a 58-year-old woman.

(A) Contrast-enhanced axial CT image shows recurrent ovarian cancer (arrow) in the sigmoid mesocolon. Arrowheads indicate a preserved fat plane between the tumor and the sigmoid colon. (B) A contrast-enhanced axial CT image taken 3 months later shows the fat plane (arrowheads) obliterated or hyperattenuating, suggesting tumor adhesion to the bowel. An arrow indicates the recurrent ovarian tumor. (C) A contrast-enhanced axial CT image taken 3 months later shows the tumor invading the muscular layer (arrowheads) of the sigmoid colon. An arrow indicates the recurrent ovarian tumor.

CT, computed tomography.

Radiation therapy or post-surgical inflammation may increase the attenuation of fat tissue, suggesting that it becomes hard due to the accumulation of inflammatory cells, such as neutrophils, lymphocytes, and fibroblasts. Accordingly, adhesion may exist even if the fat plane is not obliterated between the tumor and the bowel. Radiologists may frequently miss this imaging feature because the tissue plane still remains between the bowel and the tumor.

A disruption of the bowel layers is a direct sign of tumor invasion (Fig. 1). International Federation of Gynecology and Obstetrics staging only accepts bowel invasion in cases where mucosa involvement is identified by endoscopy. However, although serosa or muscular layers are invaded, an ovarian tumor may not be entirely removed. Thus, gastrointestinal surgeons should be involved to achieve optimal resection and to avoid bowel perforation. Some investigators have reported that deeper bowel wall invasion is not associated with a worse surgical outcome if all tumors are clearly removed and that serosa or muscular involvement is not significantly different from mucosa involvement [17,18,19]. Other studies have reported that mucosal invasion provides poorer prognosis or disease-free survival than invasion into other layers [20,21].

A tumor projecting into the bowel lumen on CT images or MRI indicates mucosa involvement, and this is the most significant finding to diagnose bowel invasion. In cases of mucosal involvement on CT images or MRI, an endoscopy is definitely unnecessary in patients who have gastrointestinal bleeding, such as hematemesis, melena, or hematochezia.

An ovarian tumor that obstructs the bowel loop is also suggestive of bowel invasion. In most cases, tumors surround bowel loops circumferentially. However, it should be kept in mind that bowel obstruction may also be caused by many kinds of benign conditions, such as adhesion, ischemia, infarct, or inflammation.

2. Vascular adhesion or invasion

Obliteration of a fat layer is also a common imaging finding suggesting vascular adhesion. In these cases, a hypoattenuating or hyperintense fat layer on CT imaging or MRI is not observed between the tumor and the vessels. Previous histories of lymph node dissection, radiation therapy, and retroperitoneal fibrosis increase the likelihood of vascular adhesion. Because radiation therapy decreases the thickness of the fat layer or increases fat attenuation, ovarian tumors frequently stick to the vessels. Moreover, a progressed tumor becomes rock hard after metastatic lymph nodes are irradiated. For this reason, even vascular surgeons experience difficulty in peeling out a recurrent tumor following radiation therapy. A large tumor makes a fat layer very thin, giving the appearance of vascular adhesion or invasion. Extraluminal encasement or abutment of the major vessels is one of the patterns that suggest vascular invasion [22]. Disruption or thickening of a pelvic peritoneal layer helps to diagnose vascular adhesion or invasion (Fig. 2). Normal pelvic peritoneal layer is difficult to see on CT. However, it becomes thick by seeding cancers and then easily visible on CT images. Moreover, vessel distortion or collapse and tumor encasement are good signs suggestive of vascular invasion (Fig. 2) [22,23]. Tumor-to-vessel angle is also an important factor to determine whether there is vascular invasion. Generally, more than 180° indicates vascular invasion, but we need to concern another factors such as surgeon skill, tumor hardness, inflammatory change, contact length, and so on.

Fig. 2. Vascular invasion in a 48-year-woman.

Contrast-enhanced axial CT image showing metastatic cancer (arrow) in the pelvic cavity. The smaller tumor (arrowheads) is encasing the right external iliac vessels, suggesting vascular invasion. A laterally-pointed arrowhead also indicates that peritoneum becomes thick by cancer spread.

CT, computed tomography.

The presence of tumor thrombi is the most significant finding indicating venous invasion [24,25], and enhancement is the key finding to differentiate between malignant and benign thrombi. Malignant thrombi tend to enhance well, whereas benign thrombi do not. Circumferential encasement or vascular collapse also indicate vascular invasion.

3. Bladder adhesion or invasion

It is not uncommon for seeding ovarian tumors to invade the urinary bladder, which has a relatively thick muscle layer. When bladder layers are obliterated by adjacent tumors, bladder invasion is strongly suggested (Fig. 3). Disruption of the normal bladder wall architecture is a characteristic sign of bladder invasion [26], and, thus, endoscopy is unnecessary because the urothelium is intact. Therefore, preoperative CT or MRI is important to avoid bladder injury during the surgery. Muscular layer is best depicted on T2-weighted images and shows intermediate signal intensity. Accordingly, obliterated or thin muscle layer is one of imaging features suggesting suboptimal resection.

Fig. 3. Bladder invasion in a 48-year-old woman.

T2-weighted coronal MRI showing a seeding cancer (arrow) invading the bladder dome in which the low signal intensity (arrowheads) of the wall is disrupted.

MRI, magnetic resonance imaging.

Preservation of the normal fat plane between the tumor and bladder excludes stage IVA cancer [27]. Appropriate preparation is important since this anatomic plane is difficult to assess in patients with an overdistended bladder. The presence of bladder mucosa edema does not indicate mucosal involvement [28,29,30,31].

When a focal mass projects into the bladder lumen, it is a definite sign of bladder invasion. This situation does not require an endoscopy to confirm the bladder invasion, especially in patients who have hematuria.

MRI is superior to CT in assessing bladder invasion because of high soft-tissue contrast. T2-weighted imaging is the best MRI sequence to delineate bladder wall architecture, and the axial or sagittal planes are good to detect bladder invasion.

4. Diffuse thickening of the small bowel

Serosal deposits are difficult to detect on CT or MRI, particularly if bowel distention is inadequate. However, diffuse serosal infiltration, focal nodules, segmental mural thickening, and a well-defined mass are imaging features indicating the involvement of both the serosa and the adjacent mesentery [32]. Bowel obstruction is a final sign of carcinomatous involvement and precludes optimal debulking [33,34]. Therefore, it is one of the indications for neoadjuvant chemotherapy [35].

Ovarian cancer may seed along the small bowel wall, making if diffusely thick (Fig. 4). A segmental involvement can be treated with resection and anastomosis by gastrointestinal surgeons, but surgical correction of long or multifocal involvement is impossible. Extensive small bowel resections lead to a high risk of postoperative functional complications [36]. Great care should be taken not to miss this finding because bowel wall thickening is frequently undetected when it is equivocal. The obliteration of the serosa line and a thick wall is the most frequent finding suggestive of diffuse thickening of the small bowel.

Fig. 4. Diffuse small bowel thickening in a 55-year-old woman.

(A) Contrast-enhanced coronal CT image shows multiple seeding tumors along the small bowel loops, in which the walls are diffusely thick (arrowheads). (B) Contrast-enhanced axial CT image shows a seeding cancer (white arrowhead) adjacent the superior mesenteric vein (black arrowhead).

CT, computed tomography.

MRI is reported to be superior to CT in assessing small bowel or mesenteric involvement because of superior soft-tissue contrast [37]. However, active peristalsis may result in motion artifacts in the MRI, making CT is superior to MRI in patients with active peristalsis. CT or MRI frequently underestimates bowel or mesenteric involvement compared with surgical exploration [38].

Three imaging planes according to axial, coronal, and sagittal dimensions should be carefully evaluated to reduce misinterpretation errors resulting from false negative or positive findings. Multi-detector CT scans are now more available and can provide thee imaging planes with data set obtained from a single-phase CT scan. Therefore, gynecologists need to ask radiologists to make sagittal and coronal reformat images on every CT scan.

5. Poorly-accessible tumor locations

Recent studies have reported that a threshold diameter of 1 cm is most commonly used for acceptable residual disease because it is well correlated with good prognosis and long-term survival [39,40]. If a lesion diameter of <1 cm remains, it is considered acceptable residual disease, defined as optimal cytoreduction. Some surgeons routinely perform aggressive resections of metastatic ovarian cancer in the liver, spleen, and bowel [36,39,41]. Others have reported that this approach is associated with high morbidity, delayed chemotherapy, and poor life quality [42]. Reportedly, neoadjuvant chemotherapy and debulking surgery are not inferior to debulking surgery and adjuvant chemotherapy in terms of disease-free survival [43,44,45,46]. However, this debate is still ongoing, and preoperative selection is important in advanced ovarian cancer with a substantial tumor burden. As a result, preoperative imaging provides gynecologists with useful features to determine what is and is not resectable [47].

Poorly-accessible tumor locations are mainly determined by surgical skill and experience. Therefore, there are no clearly established surgical criteria for indicating inoperable disease and no generally accepted consensus of optimal cytoreduction. Many papers have reported tumor locations such as the mediastinum, lesser sac (Fig. 5), mesentery root (Fig. 4), pleura, porta hepatis (Fig. 6), and fissure for ligamentum venosum or ligamentum teres (Fig. 7) [32,47,48,49]. If ovarian tumors metastasize to these locations, it is difficult for gynecologists alone to perform optimal cytoreductive surgery, and thoracic or general surgery is necessary to determine that the tumors have been completely resected. Therefore, preoperatively assessing CT imaging or MRI is crucial to formulate a surgical plan with other surgeons.

Fig. 5. Lesser sac metastasis in a 62-year-old woman.

Contrast-enhanced axial CT image shows a metastatic cancer (arrowhead) in the lesser sac. A large amount of ascites (asterisk) is seen in the upper abdomen.

CT, computed tomography.

Fig. 6. Porta hepatis metastasis in a 61-year-old woman.

Contrast-enhanced axial CT image shows a metastatic cancer (arrowhead) in the porta hepatis. The tumor is invading the caudate lobe of the liver. Because it was not surgically correctable, it was treated with percutaneous radiofrequency ablation.

CT, computed tomography.

Fig. 7. Liver fissure metastases in a 66-year-old woman.

Contrast-enhanced axial CT image shows two metastatic cancers in the major liver fissures. Black and white arrowheads indicates cancer foci in the fissures for ligamentum teres and venosum, respectively.

CT, computed tomography.

CONCLUSION

In patients with epithelial ovarian cancer, preoperative imaging examinations can provide important radiologic features to show tumor adhesion or invasion to critical organs and poorly-accessible tumor locations in which there is a high risk of suboptimal debulking. Therefore, careful evaluation of imaging features is a key to determine whether or not the involvement of other surgeons is necessary to achieve optimal resection. Furthermore, due to improvements and new developments in imaging tools and software, radiologists need to report any imaging features that indicate suboptimal resection.