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The British Journal of Radiology logoLink to The British Journal of Radiology
. 2021 Jul 21;94(1125):20210091. doi: 10.1259/bjr.20210091

Ovarian cancer staging: What the surgeon needs to know

Lucas Roberto Lelis Botelho de Oliveira 1,✉, Natally Horvat 2, Pamela Ines Causa Andrieu 2, Pedro Sergio Brito Panizza 1, Giovanni Guido Cerri 1,3, Publio Cesar Cavalcante Viana 1,3,4,5
PMCID: PMC9327759  PMID: 34289310

Abstract

Ovarian cancer (OC) is the leading cause of gynecological cancer death, and most cases are diagnosed at advanced stages due to a nonspecific and insidious clinical presentation. Radiologists play a critical role in the decision of which patients are candidates for primary debulking surgery and who may benefit from neoadjuvant chemotherapy. This pictorial review summarizes the dissemination patterns of OC, main imaging findings of metastatic disease, and which findings may alter the treatment plan or predict suboptimal tumor resection.

Introduction

Ovarian cancer (OC) is associated with the highest mortality among all gynecological cancers. These tumors may originate from the ovarian surface epithelium, sex-cord stroma, or germ cells. Epithelial tumors are the most frequent subtype, representing around 90% of all cases. In the early stages, OC is often clinically silent, contributing to 70% of all cases being diagnosed at advanced stages.1

OC is staged surgically, but the radiologist must be familiar with clinical staging systems (Figure 1) as the stage at diagnosis is a fundamental parameter to guide management and predict outcomes. Particularly, the survival is significantly worse for patients with advanced disease, with survival rates of 41 to 20% for stages III and IV, compared with 89 to 71% for stages I and II.2–5

Figure 1.

Figure 1.

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FIGO and TNM Staging. Schematics summarizing the International Federation of Gynecology and Obstetrics (FIGO) and Union for International Cancer Control (UICC) TNM ovarian cancer staging systems.

However, studies investigating the feasibility of populational screening as a tool to make earlier diagnoses have not proven a decrease in OC mortality. The screening strategy was even associated with a higher number of unnecessary surgeries. Thus, no populational screening is currently recommended.6

The options for primary management of OC include either primary debulking surgery (PDS) followed by platinum-based adjuvant chemotherapy or neoadjuvant chemotherapy (NACT) followed by interval debulking surgery (IDS). Patients in good medical condition with no imaging findings that predict suboptimal resection should typically undergo PDS consisting of total abdominal hysterectomy and bilateral salpingo-oophorectomy, omentectomy, and a maximal effort to achieve complete resection. Patients considered as poor surgical candidates are typically managed with NACT and IDS.5,7

The extent of residual disease (RD) after surgery is an important prognostic factor. Patients with complete cytoreduction, defined as no visible RD, have the longest survival. If complete resection is not possible, those with RD ≤1 cm (optimal cytoreduction) have a better prognosis than those with RD >1 cm (suboptimal cytoreduction).5,7,8

Dissemination patterns

OC may spread by intraperitoneal seeding, direct invasion, or through lymphatic or vascular dissemination.

Peritoneal dissemination

Intraperitoneal dissemination is the most usual form of OC spread, with the distribution of metastasis following the preferential flow of peritoneal fluid. After the detachment of cells from the primary tumors, cancer cells spread into the ascitic fluid due to gravity in the rectouterine pouch and paravesical recesses. Then, due to diaphragmatic movement during respiration, peritoneal fluid is pulled upwards, preferentially via the right paracolic gutter into the right subdiaphragmatic and perihepatic spaces, followed by caudal reflow into the inframesocolic compartment (Figure 2).9

Figure 2.

Figure 2.

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Peritoneal Dissemination Pattern. A: Illustration of the posterior peritoneal reflections showing the transverse mesocolon (arrow), which separates the peritoneal cavity into supramesocolic and inframesocolic compartments. The root of the small bowel mesentery divides the inframesocolic compartment into right and left infracolic spaces. The sigmoid mesocolon (white arrowhead) channels peritoneal fluid preferentially into the pelvis and right paracolic gutter. (B:) Illustration shows the preferential pattern of intraperitoneal fluid flow and ovarian cancer spread through the peritoneal cavity.

As the disease progresses, secretion of vascular endothelial growth factor (VEGF) – causing vascular hyperpermeability and obstruction of lymphatic vessels by cancer cells – leads to accumulation of progressively larger ascites, thus allowing further disease dissemination in the peritoneal cavity.10

Lymphatic dissemination

Lymphatic dissemination of OC is most likely to occur to paraaortic and paracaval nodes due to lymphatic vessels that follow the ovarian veins. The involvement of these chains is detected in 70–75% of patients in stages III–IV. Other common sites of lymph node disease are along with the external iliac and obturator lymph nodes that follow the broad ligament and inguinal lymph nodes following the round ligament. Lymph node disease increases the risk of disease recurrence and is an independent factor associated with poor prognosis.10

Hematogenous dissemination

It is traditionally believed that the hematogenous route plays a smaller role in the dissemination of OC and tends to occur at advanced stages. However, Pradeep et al used a parabiosis mouse model to demonstrate a more critical contribution of hematogenous metastasis to the omentum than previously thought.11

Role of the radiologist in preoperative imaging

There is no definitive consensus on criteria to define the inoperable disease, and the definition of the unresectable disease may also vary according to surgeon expertise. Therefore, the radiologist’s role in preoperative imaging is not to determine if the disease is resectable or not but to report lesions that may increase the likelihood of suboptimal debulking and discuss such findings with clinicians to aid decision-making on whether to perform primary surgery or neoadjuvant chemotherapy.12,13

It is also critical to report disease on locations inaccessible or not easily accessed at laparoscopy, such as disease in the falciform ligament, mesenteric root, subdiaphragmatic spaces, intraparenchymal liver, or splenic metastasis, intraluminal gastrointestinal tract lesions, and pleural metastasis.9,12

Findings that indicate potentially unresectable disease or increased surgical complexity are summarized in box 1.

Box 1. Relevant imaging findings of ovarian cancer.

Potentially nonresectable disease

  • Invasion of pelvic side-wall

  • Bladder trigone infiltration

  • Extensive small bowel disease or mesenteric root involvement

  • Involvement of lymph nodes superior to the celiac axis

  • Hepatic parenchymal metastases, particularly near the hepatic veins, inferior vena cava

  • Implants larger than 1 cm in diameter in the diaphragm, porta hepatis, falciform ligamentfissure, gallbladder fossa, lesser sac, or lesser omentum (*)

Disease that increases surgical complexity

  • Limited or solitary hepatic metastasis

  • Subdiaphragmatic or subcapsular hepatic implants smaller than 1 cm

  • Splenic hilum involvement

  • Bowel implants

  • Bowel disease with contiguous transverse mesocolon invasion

  • Bladder or ureteral invasion

  • Solitary implants smaller than 1 cm on the same locations previously described above (*)

In the first evaluation of patients with signs of peritoneal carcinomatosis, it is also critical to attempt to identify the primary lesion. Peritoneal carcinomatosis also commonly arises from gastrointestinal malignancies, which must be suspected in the presence of normal ovaries and signs of peritoneal seeding. Less commonly, primary peritoneal tumors or other mimics may occur.14

Key imaging findings

The most important findings for each anatomical location are summarized as follows:

  • Pelvic Disease – location, size, and characteristics of pelvic masses must be reported. Evidence of ureteral, bladder, or rectal invasion should be carefully evaluated and documented. Ureteral invasion may require surgical subspecialty assistance, and invasion of the bladder trigone is potentially unresectable. Pelvic sidewall invasion is also unresectable and must be suspected when the primary tumor is within 3 mm of the pelvic sidewall or encases iliac vessels (Figure 3).9

  • Greater Omentum – the greater omentum is routinely removed during surgery, but the presence of contiguous invasion of the transverse mesocolon must be detailed, as it modifies the surgical plan (Figure 4).9,15

  • Subphrenic Space – subdiaphragmatic lesions are common in patients with peritoneal carcinomatosis, especially on the right side, because of the preferential flow of peritoneal fluid. Early signs of subphrenic involvement include nodules, abnormal thickening, and enhancement. Peritonectomy may be performed for small solitary lesions, but lesions greater than 1 cm or extensive subdiaphragmatic disease usually preclude surgery. Small lesions are easily missed on axial imaging and are better visualized on coronal or sagittal reformatted images (Figure 5).9,12

  • Liver – implants on the liver surface are far more common than intraparenchymal metastasis but these surface implants may secondarily invade the parenchyma. Surgeons may resect small localized capsular implants but extensive capsular disease and intraparenchymal metastasis are often unresectable. Of special significance are the implants near the porta hepatis, hepatic veins, or inferior vena cava due to a higher risk of surgical bleeding (Figure 6).9

  • Perihepatic Space – the gallbladder fossa and the fissure for the falciform ligament are the main structures of the perihepatic space. They communicate with the periportal space and are commonly involved. Lesions greater than 1 cm are potentially unresectable (Figure 6).9,12,15

  • Lesser Omentum – the lesser omentum is composed of the gastrohepatic and hepatoduodenal ligaments. The gastrohepatic ligament contains the left gastric artery, vein, and gastrohepatic lymph nodes. The hepatoduodenal ligament has the portal vein, common bile duct, hepatic artery, and portocaval lymph nodes. Due to the anatomical complexity, the involvement of the lesser omentum usually precludes surgery. Some institutions may perform lesser omentectomy for lesions smaller than 1 cm (Figure 7).9,12

  • Lesser Sac – the lesser sac is a potential space between the stomach and the pancreas. On the right side, it communicates with the greater sac via the foramen of Winslow. On the left side, its limits are the splenorenal and the gastrosplenic ligaments. Metastasis to the lesser sac or its associated ligaments may preclude surgery, particularly when > 1 cm. The presence of fluid distending the lesser sac is a sign of its involvement.16,17

  • Spleen – the presence or absence of splenic lesions should be documented for the surgeon to decide between splenectomy or spleen sparing surgery. Disease in the splenic hilum must be specified due to higher technical challenges during surgery. Intraparenchymal splenic metastasis is classified as stage IVB disease (Figure 8).9

  • Bowel – Imaging findings of secondary disease to the bowel include nodules, masses, or focal thickening. Detection of parietal or intraluminal intestinal implants is difficult, particularly when smaller than 5 mm. The use of positive oral contrast makes such lesions more conspicuous, and water as negative oral contrast facilitates detection of small calcifications. Partial or complete bowel obstruction are frequent complications. The diffuse disease of the small bowel in which resection would lead to short bowel syndrome (remaining bowel <1.5 m) is unresectable (Figure 9).18,19

  • Mesentery – An area of special concern is the small bowel mesentery near the terminal ileum in the right lower quadrant due to the preferential flow of peritoneal fluid to this area. Involvement of the mesenteric root is unresectable (Figure 10).9

  • Pleural Cavity – the presence of pleural effusion is suspicious for distant metastasis, but stage IV disease is only confirmed after identification of cancer cells in cytologic analysis.20

  • Lymph Nodes – paraaortic lymph nodes are the most frequently involved. Lymph node disease at or above the level of the celiac axis, porta hepatis, and cardiophrenic lymph nodes are predictors of suboptimal resection.16,17

Figure 3.

Figure 3.

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Pelvic Disease. A and B: High-grade serous ovarian carcinoma on a 60-year-old female. Axial and Coronal T2-weighted MRI reveals a right ovarian mass abutting the sigmoid colon (white arrow), iliac vessels (black arrows), and the right distal ureter (arrowhead). C: High-grade serous ovarian carcinoma in a 33-year-old female. Noncontrast CT reveals infiltrative calcified lesions within the presacral space and left pelvic sidewall (arrows). D: High-grade serous ovarian carcinoma in a 72-year-old female. Axial T2-weighted MRI shows a right ovarian complex cystic lesion with thickened septa. The lesion is abutting the sigmoid colon (arrowhead) and close to the external iliac vessels (white arrows).

Figure 4.

Figure 4.

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Greater Omentum. A: High-grade serous ovarian carcinoma on a 74-year-old female. Axial contrast-enhanced T1-weighted MRI reveals the presence of multiple peritoneal metastatic nodules (arrows). B: High-grade serous ovarian carcinoma on a 72-year-old female. Axial noncontrast CT shows thickening of the greater omentum (arrow) and a small volume of ascites (arrowhead). C: Photograph showing the intraoperative aspect of diffuse malignant infiltration of the greater omentum (“omental cake”). D: Photograph of the same patient showing peritoneal cavity aspect after greater omentectomy.

Figure 5.

Figure 5.

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Subphrenic Space. A: Ovarian sero-mucinous carcinoma on a 28-year-old female. Coronal contrast-enhanced CT shows subtle thickening of the hepatic capsule, suspicious for metastasis (arrow). B: Follow-up of the same patient after four months reveals increased loculated fluid on the right subphrenic space consistent with metastasis (arrow). C: High-grade serous ovarian carcinoma on a 65-year-old female. Coronal noncontrast CT shows a small subcapsular calcified nodule on the right liver lobe (arrow). D: High-grade serous ovarian carcinoma on a 24-year-old female. Reformatted coronal noncontrast CT reveals linear calcified metastatic lesions on the hepatic (arrows) and splenic capsules (arrowhead), as well as right-sided pleural effusion.

Figure 6.

Figure 6.

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Liver and Perihepatic Space. A: High-grade serous ovarian carcinoma on a 61-year-old-woman. Axial contrast-enhanced CT reveals a hypovascular lesion within the falciform ligament fissure (arrow). B: High-grade serous ovarian carcinoma on a 49-year-old female. Axial contrast-enhanced CT shows ill-defined infiltrative tissue in the porta hepatis (arrow). C: High-grade serous ovarian carcinoma on a 62-year-old female. Contrast-enhanced CT reveals multiple intraparenchymal liver metastases due to hematogenous dissemination (arrow). These are rarely seen at diagnosis and tend to occur at more advanced stages. There is also ascites. (D): Ovarian serous papillary carcinoma on a 61-year-old female. Coronal contrast-enhanced CT shows a subcapsular hepatic implant invading the subjacent parenchyma (arrow).

Figure 7.

Figure 7.

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Lesser Omentum. A: Ovarian sero-mucinous carcinoma on a 28-year-old female. Contrast-enhanced CT reveals a secondary nodule in the hepatoduodenal ligament (arrow). B: High-grade serous ovarian carcinoma on a 33-year-old female. Axial noncontrast CT shows a calcified lesion on the hepatoduodenal ligament (arrow). There is another lesion on the hepatorenal space infiltrating the lateral abdominal wall (arrowhead).

Figure 8.

Figure 8.

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Spleen. A: High-grade serous ovarian carcinoma on a 77-year-old female. Axial contrast-enhanced CT reveals a large cystic lesion with a solid mural component in contact with splenic hilum, increasing surgical difficulty (arrow). B: High-grade serous ovarian carcinoma on a 63-year-old female. Axial contrast-enhanced CT shows both splenic capsular implants and intraparenchymal metastases (arrows). There are also multiple intraparenchymal hepatic metastases (arrowheads).

Figure 9.

Figure 9.

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Bowel. A: High-grade serous ovarian carcinoma on a 71-year-old female. Axial contrast-enhanced CT shows nodular thickening on the ascending colon wall (arrow). B: Ovarian serous papillary carcinoma on a 43-year-old female. Axial-contrast enhanced CT reveals diffuse malignant infiltration of the small bowel (arrow). C: High-grade serous ovarian carcinoma on a 44-year-old female. Contrast-enhanced CT shows nodular thickening of a segment of jejunum, with moderate upstream bowel obstruction (arrow). D: Laparoscopy image showing multiple small nodules adhered to small bowel segment. CT has low sensitivity for the detection of nodules smaller than 5 mm.

Figure 10.

Figure 10.

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Mesentery. A: High-grade serous ovarian carcinoma on a 63-year-old female. Axial contrast-enhanced CT shows multiple small nodules on the mesenteric root (arrow). There is also moderate right hydronephrosis and ureteral dilation (arrowhead) due to ureteral infiltration by the pelvic lesion (not shown). B: High-grade serous ovarian carcinoma a 49-year-old female. Axial contrast-enhanced CT shows diffuse parietal thickening of the small bowel and a metastatic implant within the mesenteric fat (arrow).

Peritoneal Carcinomatosis Index

The Peritoneal Carcinomatosis Index (PCI) quantifies the extent of peritoneal disease. The score is ultimately determined at laparoscopy, although it may also be evaluated in CT or MRI by dividing the abdomen into nine quadrants and the small bowel into four segments (Figure 11). Each of these locations receives a score based on the size of lesions (Table 1). The final score is then calculated by adding the score for each of those 13 anatomical locations, reaching a final number between 0 and 39.21

Figure 11.

Figure 11.

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Peritoneal Carcinomatosis Index.

Table 1.

Peritoneal Carcinomatosis Index.

LS Score Lesion Size
LS 0 No lesions seen
LS 1 Lesions smaller than 0.5 cm
LS 2 Lesions of 0.5 to 5 cm
LS 3 Lesions greater than 5 cm or confluent
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Each anatomical location (Figure 11) receives a score based on the size of lesions. The final score is the sum of all scores, reaching a final number between 0 and 39.

PCI should not be used alone to determine resectability, given that patients with metastasis to critical locations, such as the mesenteric root or lesser sac, could have a low PCI and still have an inoperable disease. Nevertheless, PCI is another tool to aid preoperative decision-making. Although the cutoff may vary among different institutions, recently Jónsdóttir et al found that a PCI of 24 or higher was associated with lower rates of complete resection and higher risk of postoperative complications.22

Figures 12 and 13 summarize the suggested structured analysis of patients with OC.

Figure 12.

Figure 12.

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Structured Analysis. A summary of important aspects of ovarian cancer imaging evaluation

Figure 13.

Figure 13.

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Structured Analysis. A summary of important aspects of ovarian cancer imaging evaluation.

Role of the radiologist in postoperative imaging

Assess Residual Disease

Postoperative imaging has an important role as a prognostic marker by accurately quantifying the extent of residual disease. Historically, the determination of postoperative RD has been based on the surgeon’s intraoperative assessment. Still, studies have shown that such assessment is prone to errors. In almost half of the patients deemed to have optimal resections at primary cytoreduction, postoperative imaging revealed the presence of RD >1 cm, which is associated with a significant decrease in progression-free and overall survival.23,24

In a recent study, Manning-Geist et al found that among a group of 270 patients, 97 (35.9%) had residual disease after surgery. The most common locations were diaphragm (41.2%), mesentery (20.6%), pelvic region (17.6%), bowel serosa (11.8%), peritoneum (5.9%), and pelvic or paraaortic lymph nodes (2.9%) (Figure 14).25

Figure 14.

Figure 14.

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Residual Disease. Illustration demonstrating common locations of residual disease (arrows), such as diaphragm (41.2%), mesentery (20.6%), pelvic region (17.6%), bowel serosa (11.8%), peritoneum (5.9%), and pelvic or paraaortic lymph nodes (2.9%). Most patients with residual disease have implants in more than one anatomical location.

Assess complications

Radiologists must also evaluate the presence of surgical complications. Clark et al reported perioperative complications in 32% of patients after surgical debulking of ovarian carcinoma. The most common complications are wound infections and/or intraabdominal collections, small bowel obstruction and ileus, pleural effusion, and pulmonary embolism.26

Evaluating treatment response

The effectiveness of chemotherapy may be assessed via analysis of serum CA-125, or measurements of tumor size on CT or MR images, or FDG uptake on Positron Emission Tomography (PET).

CA-125

Serum CA-125 analysis has an important role in treatment follow-up. CA-125 response is when there is at least a 50% decrease compared to pretreatment levels, and when CA-125 levels drop within the reference range (<35 U ml−1), patients are considered complete responders. However, normal CA-125 levels cannot entirely exclude the presence of residual disease or recurrence. High CA-125 levels after surgery or chemotherapy suggest residual disease after surgery or insensitivity to chemotherapy, indicating poor prognosis.27

Conventional imaging

The Response Evaluation Criteria in Solid Tumors (RECIST) are used as a standard way of measuring treatment response. Lesions are classified in either target or nontarget lesions. The criteria for the progressive disease are the appearance of any new lesion, a 20% increase in the sum of the longest diameters (SLD) of target lesions, or progression of nontarget lesions. Partial response is defined as a decrease >30% in the SLD of target lesions. Complete response is the disappearance of all lesions and decrease of all pathologic lymph nodes to <10 mm in their short axis. Unfortunately, the application of RECIST has limitations in OC evaluation, as the disease frequently consists of ill-defined confluent lesions or multiple subcentimeter peritoneal nodules.28

Functional imaging

Functional imaging techniques help to evaluate the treatment response because they better reflect tumor metabolism since metabolic response occurs earlier than morphological changes in lesions.

In positron emission tomography performed with F-18-fluorodeoxyglucose (FDG-PET), the metabolic response is defined as an SUV decrease of 20 and 55% from baseline after the first and third treatment cycles. Thus, FDG-PET may predict early treatment response. PETCT is also superior to conventional imaging in the early detection of recurrence, which may guide subsequent treatment.29,30

Diffusion-weighted imaging (DWI) may also predict treatment response by analyzing changes in Apparent Diffusion Coefficient (ADC) values. An increase in ADC after the first and third treatment cycles characterizes response. DWI is also superior to CT and PET/CT in the detection of peritoneal metastasis.31,32

Radiomics in Ovarian Cancer imaging

Radiomics is a rapidly evolving and potentially disruptive field in radiology. Several recent studies have shown that radiomics may predict characteristics such as tumor aggressiveness, response to therapy, and prognosis.33–36

For instance, Vargas et al have shown an association between quantitative metrics capturing intersite heterogeneity (heterogeneity between different metastatic sites in the same patient) with shorter overall survival and incomplete surgical resection.37 In a recent study, the same group demonstrated that a model incorporating analysis of both intrasite and intersite heterogeneity with clinical and genomic variables is effective at stratifying patients by risk of outcome.38

Radiomics may also help predict BRCA mutation status in patients with High-grade serous ovarian cancer (HGSOC) as Nougaret et al found that the qualitative CT features such as the pattern of peritoneal disease (PD), presence of PD in the gastrohepatic ligament, mesenteric involvement, and supradiaphragmatic lymphadenopathy were associated with BRCA mutation status. This carries prognostic implications as patients with BRCA-mutant HGSOC have a better prognosis due to differences in tumor biology and greater platinum sensitivity.39 Meier et al also demonstrated an association between high intersite heterogeneity and incomplete surgical resection in BRCA-negative patients, but not in BRCA-positive patients.40

Radiomics is still an emerging field, and several improvements are needed to bring it closer to the day-to-day work of radiologists. But research is evolving rapidly, and these are just a few examples of how radiomics could impact patient care in the recent future.

Conclusion

The main role of radiologists in OC staging relies on identifying findings that predict suboptimal resection, guiding the therapeutic plan, and helping to avoid ineffective surgery that would postpone chemotherapy. Understanding the patterns of disease dissemination, associated imaging findings, and evaluating them in a structured manner may improve the accuracy of OC imaging evaluation and enhance patient care.

Footnotes

The authors Lucas Roberto Lelis Botelho de Oliveira and Natally Horvat contributed equally to the work.

Contributor Information

Lucas Roberto Lelis Botelho de Oliveira, Email: lucasrlelis@gmail.com.

Natally Horvat, Email: natallymaciel@gmail.com.

Pamela Ines Causa Andrieu, Email: causapamela@gmail.com.

Pedro Sergio Brito Panizza, Email: pedropanizza@gmail.com.

Giovanni Guido Cerri, Email: giovanni_cerri@uol.com.br.

Publio Cesar Cavalcante Viana, Email: publioviana@gmail.com.

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