Benign and Suspicious Ovarian Masses—MR Imaging Criteria for Characterization: Pictorial Review

Ovarian masses present a special diagnostic challenge when imaging findings cannot be categorized into benign or malignant pathology. Ultrasonography (US), Computed Tomography (CT), and Magnetic Resonance Imaging (MRI) are currently used to evaluate ovarian tumors. US is the first-line imaging investigation for suspected adnexal masses. Color Doppler US helps the diagnosis identifying vascularized components within the mass. CT is commonly performed in preoperative evaluation of a suspected ovarian malignancy, but it exposes patients to radiation. When US findings are nondiagnostic or equivocal, MRI can be a valuable problem solving tool, useful to give also surgical planning information. MRI is well known to provide accurate information about hemorrhage, fat, and collagen. It is able to identify different types of tissue contained in pelvic masses, distinguishing benign from malignant ovarian tumors. The knowledge of clinical syndromes and MRI features of these conditions is crucial in establishing an accurate diagnosis and determining appropriate treatment. The purpose of this paper is to illustrate MRI findings in neoplastic and non-neoplastic ovarian masses, which were assessed into three groups: cystic, solid, and solid/cystic lesions. MRI criteria for the correct diagnosis and characteristics for differentiating benign from malignant conditions are shown in this paper.


Introduction
Ovarian masses present a special diagnostic challenge when imaging findings cannot be categorized into benign or malignant pathology. Ultrasonography (US), Computed Tomography (CT), and Magnetic Resonance Imaging (MRI) are currently used to evaluate ovarian tumors. US is the first-line imaging investigation for suspected adnexal masses helping in detection and characterization of ovarian tumors [1]. US morphological analysis of adnexal masses is usually accurate for identifying low risk or high risk lesions [2]. The most important morphological features for high risk ovarian masses include (a) solid/cystic or solid lesions with a maximum diameter greater than 4 cm; (b) the presence of irregular, nonfatty, solid vascularized areas greater than 28 mm in diameter [3]; (c) the presence of papillary projection (vegetation) and thick wall and septa greater than 3 mm in a cystic lesion [4]. Color Doppler US helps the diagnosis identifying vascularized components within the mass [5].
Though US can be inconclusive. An adnexal mass is defined as indeterminate on US when it cannot be confidently placed into either the benign or malignant category, even after thorough interrogation including Doppler assessment, or for which the site of origin, from the ovary, uterus or another pelvic structure, remains to be established [6]. CT is commonly performed in preoperative evaluation of a suspected ovarian malignancy, but it exposes patients to radiation. When US findings are nondiagnostic or equivocal, MRI can be a valuable problem solving tool, an adjunctive modality for evaluating adnexal lesions, useful to give also surgical planning information without radiation exposure [7]. MRI is well known to provide accurate information about hemorrhage, fat, and collagen [6]. It is able to identify different types of tissue contained in pelvic masses, distinguishing benign from malignant ovarian tumors, with an overall accuracy of 88% to 93% [8]. Benign ovarian diseases can simulate malignancies. The knowledge of clinical syndromes and MRI features of these conditions is crucial in establishing an accurate diagnosis and determining appropriate treatment. The purpose of this paper is to illustrate MRI findings in neoplastic and nonneoplastic ovarian masses, separated into three groups: cystic, solid, and solid/cystic lesions. MRI criteria for the correct diagnosis and characteristics for differentiating benign from suspicious conditions are shown in this paper.

MRI Technical Suggestions
Patients undergoing MRI examination for evaluating an ovarian mass must fast for 3-4 hours and receive an antispasmodic drug, intramuscularly, 10 minutes before MRI, in order to reduce bowel peristalsis, also to improve visualization of the adnexa and peritoneal surfaces. For an adequate pelvic MRI evaluation, images must be obtained minimum in two planes. T1-weighted spin-echo images in the axial plane and T2-weighted fast spin-echo images obtained in the axial, sagittal, and coronal planes are usually employed to evaluate uterus, adjacent organs, pelvic floor, and broad ligaments, providing panoramic "morphological" view of the pelvis. Acquisition of T1-and T2-weighted images is fundamental for pelvic anatomy and tissue characterization [9][10][11].
T1-weighted images with a selective chemical fatsuppression technique in the axial plane are useful to identify blood and fat tissue [11][12][13][14]. T2-weighted images with a selective chemical fat-suppression technique can be usefully employed to better identify inflammation changes or edema. 3D fat-saturated T1-weighted Spoiled Gradient Echo (SPGR) images after intravenous contrast material help detection of solid components into the mass, also improving detection of peritoneal and omental implants [15,16]. The use of small fields of view (20 cm), high-resolution matrixes (256 × 256), and thin sections (4 mm) improves the delineation of papillary projections into cystic lesions. A body axial T2weighted sequence for evaluating retroperitoneal space can also be used to complete the pelvis evaluation [8].
Several types of tissue and fluid characterizing an ovarian mass can be distinguished at MRI on the basis of their signal intensity [17]. Cystic lesions demonstrate low signal intensity on T1-weighted images and very high signal intensity on T2-weighted images. Solid portions are characterized by relative high hyperintensity on T2-weighted images. Fat, hemorrhage, and some high-viscosity, mucin-containing lesions have high signal intensity on T1-weighted MRI. Fibrosis or smooth muscle has low or intermediate signal intensity on T1-weighted MRI and low signal intensity on T2-weighted images [6].

Cystic Lesions
3.1.1. Polycystic Ovary Syndrome. Polycystic ovary syndrome (PCOS) affects approximately 20% of premenopausal women and is one of the most common endocrinopathies of women [18]. The follicles in PCOS are typically smaller in size than those in normal ovaries. US imaging features include 10 or more follicles with a diameter of 2 to 8 mm, arranged around an echo dense central stroma, with a threshold stroma/area (S/A) ratio of 0.34 (calculated as ovarian stromal area to the total area of the ovary). This S/A ratio has been described as having sensitivity and a specificity of 100% [19]. Typical MRI features include enlarged ovaries, with a central stroma and multiple small follicles located peripherally [20,21]. Enlargement of the central ovarian stroma usually shows low intensity on T2-weighted images. The role of MRI in this condition is excluding other hormonestimulating ovarian disorders (like Granulosa cell tumor, Sclerosing stromal tumor, and Sertoli-Leydig cell tumor, Steroid cell tumor) by carefully evaluating the presence of solid lesions within the mass [7]. These conditions generally appear as a well-defined, heterogeneous enhancing solid mass with internal cyst or areas of intracellular lipids; they can be associated with endometrial abnormalities [4].

Endometrioma.
Endometrioma occur as a result of extrauterine implantation of endometrial epithelium. The typical US appearance is a complex cystic ovarian mass with homogenous low-level internal echoes and thick wall which is usually hypovascular at color Doppler evaluation. US sensitivity (90.4%) in diagnosing endometrioma is as high as MRI sensitivity (90%); however MRI is usually performed after the US because other foci of endometriosis located in the pelvis and subpelvic spaces can be associated and for excluding malignant degeneration [22,23]. MRI is able to differentiate endometrioma from endometrioid adenocarcinoma and clear-cell adenocarcinoma that can develop within endometrial cysts, with an incidence of 0.6-1.0% [24]. In these cases, MRI demonstrates solid components in the cystic wall clearly enhancing in postcontrast images. Subtraction images of precontrast and postcontrast sequences are useful when the enhancement evaluation is difficult due to the hyperintensity of endometrial cysts on T1-weighted images ( Figure 1). Endometrioma appears on MRI images as high intensity on T1-weighted images and relatively low intensity lesions on T2-weighted images ("shading" effect) manifesting as gradual loss of signal of dependent layering contents [13,25]. MRI has been reported to have a sensitivity of 68-90% and specificity of 83-98% for the diagnosis of endometrial cysts [13,26]. The presence of multiple, bilateral lesions add specificity to the diagnosis of endometriosis [19]. Fat saturation technique is highly used to differentiate endometrioma from fatty lesions, also showing   [7]. Presence of normal ovary entrapped centrally within the lesion creating a "spider in a web" appearance is a suggestive finding. No mural nodules or enhancing solid components are seen [19].

Adnexal Torsion.
Ovarian torsion most commonly occurs in the first 3 decades of life and frequently involves the ovary and corresponding fallopian tube. It is more often associated with an ovarian cyst or mass (approximately in 50% of cases) [27]. US usually shows an enlarged ovary with follicles distributed peripherally [28]. Doppler US improves diagnostic possibilities of US showing the lack of flow in the twisted ovary. However, torsion may occur with incomplete vascular obstruction. MRI can achieve a more adequate diagnosis showing typical findings as the ovary drawn to the uterus, deviation of the uterus to the side of torsion, straight vessels draping around the lesion, absence of enhancement or massive ovarian edema in the case of intermittent torsion, which is shown as diffuse high signal intensity on T2weighted images. When hemorrhagic necrosis occurs, the lesion may exhibit high intensity on T1-weighted images [29,30] (Figure 2).

Pelvic Inflammatory Disease (PID).
Pelvic Inflammatory Disease (PID) is a common condition among women in reproductive age and sexual activity. PID is usually clinically and laboratory diagnosed (pain, fever, and leukocytosis), but imaging studies are performed in patients with uncertain diagnosis, or whose not responding to therapy. Hydrosalpinx is most often seen on US images as a hypoechoic adnexal mass, with a thick vascularized wall ring, associated with free fluid in the "cul-de-sac". In emergency, CT is usually requested when US findings are indeterminate [31,32]. However MRI can be used in mediate urgency showing 95% sensitivity and 89% specificity in the tuboovarian abscess diagnosis [33]. On MRI, a tubo-ovarian abscess is characterized by mild signal intensity on T1-weighted and high signal intensity on T2-weighted images. An irregular thick wall, markedly enhancing after contrast medium administration, and stranding in the surrounding fat planes are characteristic easy to be recognized. In patients with longterm use of intrauterine devices, actinomycetes are a frequent cause of chronic inflammation. On MRI, an ill-defined lesion border resulting from trans fascial inflammatory spread may simulate a malignancy involving the ovary. Relatively low intensity on T2-weighted images representative of fibrosis may be an important tool in the accurate diagnosis of this condition [33,34] (Figure 3).

Mature Cystic Teratoma (Dermoid Cyst).
Mature cystic teratoma is the most common ovarian tumor (26-44% of all ovarian masses). Incidence picks at 30 years old, generally is found in asymptomatic patients, 90% unilaterally. This benign tumor consists of ectodermal tissue predominantly and is lined with keratinized squamous epithelium and skin appendages. MRI affords a specific diagnosis by demonstrating fat tissue signal which is usually demonstrated as high intensity, the same as subcutaneous fat, on T1-weighted and T2-weighted images. A selective T1-weighted fat suppression technique enables differentiation of cystic teratoma from hemorrhagic adnexal processes such as endometrial cyst. In cases of atypical dermoid cysts with scarce lipid components, chemical shift sequence has been reported to be useful to detect intracellular or microscopic lipid. Other MRI findings for cystic teratomas includes layering or floating debris, softtissue protuberances (Rokitansky nodules or dermoid plugs), and low-signal-intensity teeth. MRI is also collaborative in identifying complications associated with dermoid cysts, such as torsion, rupture, and malignant transformation [35].
Malignant transformation is rare and occurs in approximately 2% of mature cystic teratoma. Invasive squamous carcinomas are the most common malignancy arising in cystic teratoma. The age of patients has a wide range; however, postmenopausal women are most predominantly affected. The tumor tends to spread by direct invasion. The use of intravenous contrast material may be helpful in assessing the malignant solid components (Figure 4).

Cystadenomas.
Cystadenomas are true cystic epithelial ovarian neoplasm. Serous cystadenomas are common and account for approximately 25% of benign ovarian neoplasm. Incident picks between 20 and 50 years old, bilaterally in 12-23% of cases. The lining of the cyst is flat or may have small papillary projections. The typical MRI appearance of serous cystadenoma is a unilocular cyst with a thin wall ( Figure 5). The presence of blood can vary to heterogeneous signal intensity. Mucinous cystadenomas are common and account for approximately 41% of benign ovarian neoplasms. In contrast to serous tumors, only 2%-5% of cases are bilateral [35]. Mucinous cystadenomas are multilocular cysts, larger than serous, containing gelatinous material or fluid of various viscosities. Therefore, the loculi of the tumors often show various signal intensities on both T1-and T2-weighted images ("stained-glass appearance") ( Figure 6). They rarely appear as unilocular cysts. Presence of thick wall or septa may suggest borderline lesions while the presence of solid components suggests carcinoma ( Figure 5(c)).  [19]. This tumor can be associated with other cystic ovarian neoplasms, such as cystadenomas, in 30% of cases ( Figure 6). On MRI Brenner tumor typically exhibits distinct low intensity on T2-weighted images due to solid components. It is possible to find a characteristic amorphous calcification within the solid components. If present, it is characteristic. However MRI may be limited for detection of calcifications. In these cases, the combination of calcifications demonstrated by ultrasonography or computed tomography and low intensity on T2-weighted MRI strongly suggests the diagnosis of Brenner tumor [35].

Cystadenofibroma.
Cystadenofibroma is an uncommon epithelial tumor, which is pathologically characterized by dense fibrous tissue in association with one or many locules. On MRI, these tumors typically manifest as a complex cystic mass associated with solid components of distinct low intensity on T2-weighted images [5,7,19].

Struma
Ovarii. If the dermoid cyst is composed only of mature thyroid tissue received the name of "struma ovarii." Typically presented as a multilocular cyst with heterogeneous signal intensity in the locules also known as "stained-glass appearance" on MRI. Thyroid colloid in the cystic space exhibits low intensity on both T1-and T2-weighted images.
Most of the cases present fat tissue component being helpful in the final diagnosis [7].

Discussion and Conclusion
When an adnexal mass is observed on US examination, MRI can be usefully employed to confirm or refute the benign nature of the lesion because the property of tissue characterization. MRI is an effective second confirmatory test also helpful for problem solving since MRI criteria for ovarian malignancy are clearly established. Features suggestive of malignancy ( Table 1) include demonstration of solid, solid/cystic enhancing masses (greater than 4 cm in maximum diameter) with papillary projections and irregular thick wall and septa (greater 3 mm) into a cystic lesion (the number of septa and the number and dimension of the vegetations can be suggestive of malignancy). Secondary feature includes the presence of necrosis in a solid mass and intratumoral hemorrhage. Heterogeneous and early enhancement pattern can be suggestive of malignancy. Finally, the ancillary criteria of involvement of pelvic organs or the sidewall, ascites, and lymphadenopathy should be carefully evaluated to distinguish benign from malignant disease [5]. US is an operator-dependent technique, less panoramic than MRI which better identify fat tissue and blood products, that are the main components of most frequent ovarian masses. In addition, MRI dynamic imaging with gadolinium chelates appears promising for problem solving [36]. Combination of US and MRI minimizes the risk of misdiagnosing a malignant mass as benign. Especially in younger women, in whom exposure to ionizing radiation should be as low as possible to preserve fertility. US remains the primary imaging modality in ovarian masses but MRI enables a specific diagnosis to be made for certain pathologic types and has greater specificity in the diagnosis of malignancy with 91-95% accuracy from differentiating benign from malignant adnexal tumors [2,35]. MRI should be used for characterization of ovarian masses when US results are indeterminate or equivocal, especially when tumor markers are normal or in young patients when conservative surgery is suggestive.