Abstract
Adnexal masses may present as symptomatic lesions or be discovered incidentally during radiological examinations. The questions asked of radiologists are firstly, what is the nature of the mass and secondly, does it need to be removed and if so, how? Multidisciplinary discussion is to plan patient management and aim to avoid the two scenarios of simple resection of an ovarian cancer and major debulking surgery for benign disease.
Ultrasound (US) is excellent for characterisation of many common benign pathologies, but benign disease can present with complex appearances that are sonographically indeterminate. The widespread use of computed tomography (CT) as first-line investigation in many clinical settings has resulted in diagnosis but limited characterisation of adnexal lesions.
Magnetic Resonance Imaging (MRI) has a crucial role to play as a problem-solving tool. The ability to confirm the organ of origin and give information on the nature of contents of a lesion allows confident diagnoses to be made, and an algorithmic approach to this has been described in the Ovarian-Adnexal Reporting and Data System (O-RADS) MRI scoring system.
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Keywords
FormalPara Learning Points-
1.
To recognise common benign adnexal pathologies
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2.
To appreciate the limitations of US and CT for the assessment of adnexal masses
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3.
To understand when MRI is indicated and how it is performed
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To become familiar with the O-RADS MRI scoring system
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5.
To be aware of and recognise non-gynaecological adnexal pathologies
15.1 Introduction
Adnexal lesions are common. In premenopausal women the majority of these are detected by Ultrasound and are benign lesions such as physiological cysts, endometriomas, mature ovarian teratomas (dermoid cysts), cyst adenomas or lesions of the fibroma lineage. In postmenopausal women adnexal masses are also likely to be benign.
The rapid expansion in the use of computed tomography (CT) for first-line assessment of the urinary and gastrointestinal tracts, investigation of patients presenting with non-specific symptoms, with an acute abdomen or following trauma has resulted in many adnexal masses being diagnosed but not characterised. Incidental adnexal masses are reported in approximately 5% of CT studies [1]. Of incidentally detected adnexal cysts at CT, the ovarian cancer rate is approximately 0.7% [2].
Whilst ultrasound is the initial imaging modality of choice in young women and those of any age presenting with pelvic symptoms and is excellent for characterisation of many lesions, benign diseases such as endometriosis, teratomas and adenofibromas can look complex with mixed cystic and solid components. The clinical presentation of the patient and ancillary information such as inflammatory indices and tumour markers are crucial in aiding interpretation of radiological findings and when there is a mismatch between the clinical picture and the level of radiological concern, additional imaging is then needed. This is also crucial for incidental CT findings. The role of additional imaging is to confirm benign diagnoses and to detect those lesions that are borderline or malignant in nature in order to ensure the patients are managed by the appropriate gynaecological oncology teams.
15.2 Imaging Modalities for Assessment of Adnexal Masses
15.2.1 Ultrasound
Ultrasound is considered the first-line imaging modality to characterise adnexal masses as benign or malignant. By using transvaginal and transabdominal approaches, in many cases not only determining the likelihood of malignancy but also predicting specific differential diagnoses is possible, with examples including simple or haemorrhagic cysts, endometriomas and mature cystic teratomas. In such cases management recommendations can often be made solely by ultrasound findings without the need for further imaging. However, when the adnexal mass remains indeterminate by ultrasound owing to factors of lesion complexity or limitations of the study due to patient characteristics, MRI can be helpful for further characterisation [3].
15.2.2 Magnetic Resonance Imaging (MRI)
The usage of MRI is widely adopted by many national guidelines for characterisation of sonographically indeterminate adnexal masses [4]. Advantages of MRI include exquisite soft tissue resolution and lack of ionising radiation, in comparison with CT. Numerous studies have shown that MRI has the highest diagnostic accuracy among imaging modalities with pooled sensitivity of 0.94 (95% CI 0.91–0.95) and specificity of 0.91 (95% CI, 0.90–0.93) for differentiating malignant from benign adnexal tumours [5].
In order to achieve such high diagnostic accuracies as shown in the literature, guidelines recommend that certain protocols be followed when performing pelvic MRI for assessing adnexal lesions [6]. For preparation, fasting (e.g., 4 h), intravenous smooth muscle relaxants (e.g., glucagon), and partially filling the urinary bladder are recommended. MRI sequences should include (a) T2-weighted imaging (T2WI) in at least 2 planes—most commonly sagittal for orientation of the uterus and axial in high-resolution for analyzing the ovaries and (b) axial T1-weighted imaging (T1WI). Additional sequences for problem solving include (a) T2-weighted imaging in the plane along the long axis of the uterus (i.e., oblique axial) when ovaries are not seen well or when needing to evaluate for the presence of ‘bridging vessels’ to the uterus to determine organ of origin (i.e., adnexal vs. uterine); (b) fat-saturated T1-weighted imaging to differentiate fat vs. haemorrhagic cystic contents; (c) diffusion-weighted imaging (DWI) with b-values of 0–50 and ≥ 1000 s/mm2 and (d) dynamic contrast-enhanced (DCE) MRI up to 4 min post-gadolinium-based contrast agent injection with temporal resolution of ≤15 s with derived subtraction images (especially for haemorrhagic lesions).
15.2.3 O-RADS MRI Scoring System for Risk Stratification of Adnexal Masses
It is recommended that risk stratification of sonographically indeterminate adnexal masses be done using an algorithmic approach. Recently the Ovarian-Adnexal Reporting and Data System (O-RADS) MRI scoring system was established by an international committee of multidisciplinary experts [7]. This was developed based on the ADNEX MR scoring system that incorporates assessment of fluid and solid components using anatomical and functional MRI which had been validated prospectively in multiple centres with a sensitivity and specificity of 0.93 and 0.91, respectively [8, 9]. O-RADS MRI risk stratification system allows assignment of 6 scores as follows:
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O-RADS MRI score 0 (incomplete exam). Sometimes, adnexal lesions cannot fully be characterised due to incomplete coverage or technical issues (e.g., artifacts).
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O-RADS MRI score 1 (normal ovaries). This score is given when there are only normal or physiological findings in the ovaries. This includes follicles, haemorrhagic cysts and corpus luteal cysts that are ≤3 cm in size in premenopausal women and small residua of follicles in postmenopausal women at the radiologist’s discretion. A key tip to identifying the ovary (and in turn assessing whether the finding is adnexal or not) is to trace the gonadal veins. Of note, if the findings are not ovarian or adnexal origin, O-RADS MRI risk score is not applicable.
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3.
O-RADS MRI score 2 (almost certainly benign; positive predictive value [PPV] of cancer <0.5%). This category includes findings that are almost certainly benign. Examples are unilocular cyst with either simple or endometriotic fluid regardless of wall enhancement, proteinaceous haemorrhagic cysts without wall enhancement, simple hydrosalpinx, peritoneal inclusion cyst. Mature teratoma can have small amount of solid tissue, commonly in the form of a Rokitansky nodule [10]. Only solid masses that demonstrate very low signal on both T2-weighted imaging and DWI, known as the “dark/dark” pattern are also included.
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O-RADS MRI score 3 (low risk for malignancy [PPV around 5%]). Unilocular cysts containing proteinaceous, haemorrhagic, or mucinous fluid with a smooth enhancing wall, or multilocular cysts with any type of fluid with smooth enhancing wall/septa. In the presence of solid tissue not showing ‘dark/dark’ pattern, the tissue should enhance slower than the uterine myometrium without a shoulder or plateau (low risk time intensity curve [TIC]). Dilated fallopian tubes showing thick/smooth walls/folds or containing non-simple fluid are also included here.
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O-RADS MRI score 4 (intermediate risk for malignancy [PPV around 50%]). This category includes lesions with solid tissue that are not ‘dark/dark’ and demonstrate moderate enhancement less than or equal to myometrium, with a shoulder and plateau (intermediate risk TIC). Additionally, lesions with fat-containing large volume of enhancing solid tissue are considered O-RADS MRI score or 4.
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O-RADS MRI score 5 (high risk for malignancy [PPV around 90%]). This category is assigned to adnexal lesions with non- ‘dark/dark’ solid tissue showing brisk enhancement greater than myometrium (high-risk TIC) or when definite signs of malignancy such as peritoneal or omental deposits are present.
Although using TIC pattern analysis has been recommended, it is acceptable to base the degree of enhancement at 30–40 s if DCE MRI is not available [11].
15.2.4 Computed Tomography (CT)
CT has become the first-line imaging modality for assessment of the urinary tract for calculi and other causes of haematuria, for assessing the colon and in the investigation of patients who present with non-specific symptoms and those who prevent emergently to the Accident & Emergency Department with acute abdominal pain or following trauma. It is the modality of choice for staging of many cancers, and it is therefore not surprising, given the volume of CT performed, that a significant number of adnexal masses are discovered. CT is poor for characterisation of an isolated adnexal mass. On single-phase CT of the pelvis, it cannot differentiate between cystic lesions containing non-simple fluid and homogeneous poorly enhancing solid masses such as fibromas. Adenofibromas may appear cystic and solid, and masses of the fibroma lineage can be associated with ascites in the setting of Meigs syndrome. Foci of calcification may suggest fibroma or Brenner tumour but can also be seen in low-grade serous carcinoma and some borderline tumours. A pelvic mass on CT in the absence of secondary signs of malignancy such as peritoneal disease or adenopathy is often indeterminate. Low volume free fluid and streaky change in the peri-lesional fat may be due to an inflammatory process such as a tubo-ovarian abscess or torsion of a lesion, and knowledge of the presenting clinical symptoms is crucial for correct interpretation. CA 125 may be elevated by any process which causes peritoneal irritation and biochemical and imaging findings need to be interpreted in the relevant clinical setting to avoid over diagnosis of malignancy.
Once a diagnosis of ovarian cancer is made, however, CT is the modality of choice to stage disease and provide information needed in the MDT meeting to make decisions regarding the likelihood of successful primary surgery versus primary chemotherapy followed by interval debulking surgery [12].
15.2.5 Positron Emission Tomography/Computed Tomography (PET/CT)
Fluorodeoxyglucose (FDG) activity can be seen in response to physiological change in the ovaries and in benign adnexal diseases such as endometriomas, teratomas and fibroids. Conversely malignant lesions such as necrotic, mucinous and low-grade tumours can be FDG negative or show only low level activity. Consequently, FDG PET/CT is not recommended for the characterisation of adnexal masses nor is it used routinely in the management of patients with ovarian cancer. It can have a role in the assessment of patients with an elevated CA 125 who have no visible disease or only equivocal findings on CT and MRI [13, 14].
15.3 Benign Adnexal Masses
15.3.1 Benign Adnexal Masses and Ultrasound
Most adnexal masses discovered incidentally in pre- and postmenopausal women will be benign. Characterisation of a lesion as benign allows the managing clinician to decide whether intervention is needed based upon the imaging findings, the mode of presentation and the patient’s overall health status.
Simple cysts are one of the most common adnexal findings and often visualised using ultrasound. These mostly represent follicles or follicular cysts in premenopausal women and para-ovarian cysts in postmenopausal women. On ultrasound they are seen as round or oval anechoic fluid that is contained by smooth and thin walls without internal septations, solid areas, nor flow on colour Doppler studies. It has been well documented that simple cysts in asymptomatic women have no difference in cancer risk compared with women without such findings, regardless of menopausal status and size of the lesion [15]. Multidisciplinary consensus guidelines recommend that most simple cysts do not require follow-up, but this should be reserved for larger cysts of >3–5 cm in pre- and > 5–7 cm in postmenopausal women, or for less well-defined cysts where follow-up may be helpful to ensure that no suspicious findings were missed on initial imaging. Follow-up to 2 years could be done for simple cysts that have not decreased in size initially, to ensure stability and to identify development of suspicious areas such as papillary projections. Haemorrhagic cysts may have more variable appearance depending on the stage of the blood products and the presence of clot. These latter can also be typically characterised on ultrasound as showing reticular or fishnet pattern of internal echoes or having a retracting clot, which can be differentiated from a mural nodule by identifying sharp and concave margins and lack of flow on Doppler studies. In cases where ultrasound is indeterminate, MRI can be used to further determine its nature. On MRI, haemorrhagic cysts show T1 hyperintense fluid that remains high despite fat suppression and variable T2 signal with lack of enhancing solid tissue.
Key Point
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Adnexal masses are common in pre- and postmenopausal women and are most often benign. Ultrasound can characterise many benign lesions.
15.3.2 Benign Adnexal Masses and MRI
MRI can make confident benign diagnoses in simple and non-simple fluid-containing cystadenomas, ovarian teratomas, endometriomas, solid and mixed cystic and solid lesions of the fibroma/adenofibroma lineage.
The demonstration of gross fat using T1-weighted sequences with and without fat saturation, with attention to using the same plane of imaging, makes the diagnosis of a teratoma (Fig. 15.1).
Teratomas can show complex internal architecture depending on the content of the lesion, which may include enamel, glial and thyroid tissue in addition to fat, but it is scrutiny of the wall of the lesion that is crucial to identify rare but poor prognosis malignant teratomas. The malignant elements are usually squamous carcinomas that arise within skin elements. These are usually located in the wall of the lesion and can be seen as solid enhancing mural nodules that may demonstrate transmural extension (Fig. 15.2).
Endometriomas reflect episodes of repeated haemorrhage due to endometrial tissue in an ectopic location, usually in the ovary or Fallopian tube. This pathophysiology results in a cystic mass containing blood of differing ages and gives the pathognomonic finding of ‘shading’ of contents on T2-weighted imaging and this is seen as the gradation of signal from high T2 signal intensity (SI) non-dependently to lower T2 signal in the dependent portion of a lesion (Fig. 15.3).
Small low T2 signal foci reflecting haemosiderin may also be apparent. Endometriomas are of high SI on T1 weighted sequences without signal loss post fat saturation and display restricted diffusion. Ancillary signs of endometriosis may be present elsewhere with thickening of the junctional zone of the uterine body due to ectopic endometrial glands within the myometrium reflecting adenomyosis, haematosalpinges and low T2 signal fibrotic endometriosis commonly seen between the posterior uterine serosa and the undersurface of the recto-sigmoid and related to the vaginal fornices in the Pouch of Douglas. The ovaries may lie medially in the pelvis, often tethered to the posterior uterine serosa—‘kissing ovaries’—due to adhesions. Malignant change can occur in endometriomas, most commonly to clear cell carcinoma and suspicious features are mural thickening and solid components (Fig. 15.4).
Solid adnexal masses cause significant diagnostic challenges on CT. The first question is where do they arise from? The excellent soft tissue contrast of T2-weighted MRI may allow identification of normal ovaries separate to the lesion and its relationship to the uterus. Tortuous vessels seen as signal void within a mass, within a vascularised pedicle or in the para-uterine region are a feature of fibroid disease and suggest the lesion may be uterine rather than adnexal in origin. This should prompt search for separate ovaries.
Ovarian fibromas are typically low signal intensity on T2-weighted imaging, do not show restricted diffusion and display minimal enhancement post-Gadolinium (Fig. 15.5).
Adenofibromas may show variable cystic change which accounts for diagnostic difficulty on US or CT, but the T2 dark solid areas which are low signal on high b value diffusion-weighted imaging (DWI) allow MRI to make the correct diagnosis [16].
Ascites is commonly seen when fibromas are present in the setting of Meigs syndrome (Fig. 15.6). This causes further diagnostic difficulty with US and CT and if the clinical picture is not one of malignancy and the CA 125 level is not particularly raised, this diagnosis should be considered, and MRI is again of use to characterise the lesion.
Granulosa cell tumours may display avid enhancement on both CT and MRI and give an intermediate to high risk of malignancy O-RADS score of 4 or 5, although clinically they are considered of low malignant potential. Due to their hormonal activity, they may present with vaginal bleeding and be associated with ancillary MRI signs such as preservation of zonal anatomy and uterine size in a postmenopausal woman and these findings should prompt consideration of such tumours as a differential diagnosis (Fig. 15.7).
Granulosa cell tumour. A predominantly solid left adnexal mass in a postmenopausal woman (arrowhead). The T2-weighted sequence shows preserved uterine zonal anatomy and cystic adenomyosis (arrow) which is abnormal in a patient of this age (a) and there is an avid enhancement of the lesion post-gadolinium (b)
Key Point
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MRI should be used to characterise lesions that are indeterminate on Ultrasound and CT, and where the clinical picture does not reflect the initial imaging findings.
15.4 Borderline Adnexal Masses
Borderline ovarian tumours occur in younger patients and have a better prognosis. This is an important diagnosis to make pre-operatively as fertility-sparing surgery is then considered as a treatment option. Serous borderline ovarian tumours have pathognomonic imaging features on MRI with papillary projections related to the internal aspect of the wall of the lesion in the cystic form or related exophytically to the lesion wall in the surface form (Fig. 15.8a) [17]. These distinctive findings are not readily apparent on CT or US.
Borderline ovarian tumours. Papillary projections both within the lumen (white arrow) and related to the surface (black arrowhead) of a serous borderline tumour on T2-weighted imaging (a). Borderline mucinous tumours typically display locules of differing signal intensities on T2 and T1-weighted sequences (b, c)
Borderline ovarian tumours may also be mucinous in nature and appear as multiloculated cystic masses with locules containing fluid of differing signal intensities on T1-weighted MRI sequences (Fig. 15.8b, c). The wall and internal septations are thin and no solid foci are apparent [18].
Key Point
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Adnexal lesions with mucinous features on MRI should prompt scrutiny of the GI tract including the appendix for a possible primary tumour site.
15.5 Malignant Adnexal Masses
A complex adnexal mass on ultrasound or CT which is then shown to have intermediate T2 signal intensity solid areas which display restricted diffusion and contrast enhancement on MRI, i.e. O-RADS score 4 or 5, is considered malignant and these patients need further management by specialist Gynaecology oncology teams (Fig. 15.9).
Additional imaging may be needed to determine the extent and spread of disease within the abdomen and pelvis. This can be performed with MRI at the time of the pelvic characterisation study or by CT (Fig. 15.10).
Primary ovarian cancer spreads primarily by peritoneal dissemination of disease causing ascites, omental disease, serosal disease often involving the undersurface of the diaphragm, the surface of the liver, spleen and bowel. Nodal disease may be present in the abdomen and pelvis, and the presence of anterior paracardiac and diaphragmatic nodes implies diaphragmatic involvement. Stage IV involvement of the thorax is often reflected by pleural disease with pleural fluid positive for malignant cells and adenopathy spreading through the mediastinum to the supraclavicular fossae. Multidisciplinary discussion is then needed to determine whether primary surgery will achieve optimal debulking or whether the extent of disease combined with the patients’ clinical status suggests primary chemotherapy followed by interval debulking surgery (IDS) is more appropriate.
Knowledge of tumour markers in addition to the pattern of disease spread is crucial as the radiological features of metastatic ovarian cancer may be identical to those of metastatic non-ovarian cancer [19]. Metastatic disease to the ovaries is not always solid nor bilateral as originally described by Friedrich Ernst Krukenberg in 1896. The term Krukenberg tumour refers to metastatic mucin-rich signet-ring adenocarcinoma to the ovary from a gastrointestinal primary site. Gastric cancer accounts for approximately 70% of ovarian metastases, with a combination of gastric and colorectal metastases making up 90%. Other tumour sites may also metastasise to the ovaries and primary ovarian cancer may be associated with other non-ovarian malignancies such as breast cancer in those with BRCA gene mutations. The finding of abnormal tumour markers other than CA 125 should prompt detailed scrutiny of the GI tract, including the appendix, the solid upper abdominal organs and the breasts (Fig. 15.11).
Ovarian cancer is recognised as the ‘silent killer’, patients having advanced disease by the time they present with abdominal swelling or other non-specific symptoms. An acute presentation with abdominal pain is atypical for malignant disease and patients with such symptoms are usually assessed in the emergency department by general surgeons, unless they are known to have a pre-existing adnexal lesion, and initial investigation is invariably CT. The presence of an adnexal mass with low volume free fluid and streaky change within the pelvic fat could be interpreted as cancer with early peritoneal disease. CA 125 is non-specific and invariably elevated in acute abdominal conditions that cause peritoneal irritation, however, torsion of an adnexal mass must be considered and then a search made for relevant radiological signs including a thickened, twisted vascular pedicle and deviation of the uterus to the side of the lesion [20]. Masses may appear as low attenuation on CT due to lack of contrast enhancement if they are already infarcted or they may appear of high attenuation due to intralesional haemorrhage. If the diagnosis of torsion is considered, assessment with MRI—if it can be performed in a timely fashion—can confirm the diagnosis. The twisted vascular pedicle is more readily apparent and intramural haemorrhage related to the lesion or the pedicle is a pathognomonic finding (Fig. 15.12) [21].
Torsion of a benign fibroma in a patient presenting with abdominal pain. The lesion is seen to be oedematous with a thickened vascular pedicle on the T2-weighted image (a), intramural haemorrhage which is high SI on T1 and high b value DWI (b, c) is seen related to the lesion (arrow head) and the pedicle (arrow)
Key Point
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Clinical presentation with pain suggests an ‘accident’ to an adnexal mass, commonly torsion or haemorrhage. Most lesions that present acutely are benign.
Women with inflammatory adnexal disease may also present generally unwell and with non-specific symptoms. Ascending infection should be considered in sexually active women and uncommon infections such as actinomycosis remembered as a potential diagnosis if there is a long history of an IUD in situ.
It should be remembered that non-gynaecological structures can also present as an adnexal mass. Mucocoele of the appendix may appear as a tubular adnexal structure on all imaging modalities suggesting it is of tubal origin; however, its relationship to the caecal pole and identification of distant normal ovaries allow the correct diagnosis to be made. These lesions may display calcification on CT (Fig. 15.13).
Gastrointestinal Stromal Tumours (GISTs) are a rare type of sarcoma found in the wall of the digestive system and can occur anywhere from the oesophagus to the rectum [22]. Although most commonly located in the stomach, approximately 55%, they can rarely occur in the colon or rectum 3%, and are an uncommon but important differential diagnosis for an adnexal mass with otherwise normal gynaecological structures (Fig. 15.14).
15.6 Concluding Remarks
Adnexal masses are common in pre- and postmenopausal women, and many are discovered as incidental findings, particularly on CT scans performed for a wide variety of indications. The role of imaging is to characterise the lesions and identify those with borderline or malignant features in order to ensure that patients are managed by appropriate specialist gynaecological oncology teams. Where initial imaging findings on US or CT are indeterminate, or their findings do not correlate with the clinical picture or presentation, MRI is an excellent problem-solving modality and allows confident benign and malignant diagnoses to be made and this has been supported by the developed MRI scoring systems, ADNEX MR and subsequently O-RADS MRI.
Take-Home Messages
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1.
Radiological findings of an adnexal mass need to be interpreted in the knowledge of the mode of presentation, the patient’s clinical status and tumour markers.
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2.
Whilst Ultrasound is an excellent initial imaging modality and may make confident diagnoses, CT is poor for characterisation of adnexal masses particularly in the absence of secondary signs of malignancy.
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3.
MRI is an excellent problem-solving modality, allows correct benign and malignant diagnoses to be made and therefore ensure patients are managed by the appropriate specialist teams.
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4.
Radiologists should be aware of the range of differential diagnoses and the pathognomonic MRI findings of common benign lesions, which may be indeterminate on CT and Ultrasound.
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Swift, S., Woo, S. (2023). Adnexal Diseases. In: Hodler, J., Kubik-Huch, R.A., Roos, J.E., von Schulthess, G.K. (eds) Diseases of the Abdomen and Pelvis 2023-2026. IDKD Springer Series. Springer, Cham. https://doi.org/10.1007/978-3-031-27355-1_15
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